Genomic Designing for Biotic Stress Resistant Fruit Crops 3030918017, 9783030918019

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Chittaranjan Kole   Editor

Genomic Designing for Biotic Stress Resistant Fruit Crops

Genomic Designing for Biotic Stress Resistant Fruit Crops

Chittaranjan Kole Editor

Genomic Designing for Biotic Stress Resistant Fruit Crops

123

Editor Chittaranjan Kole Raja Ramanna Fellow Department of Atomic Energy Government of India ICAR-National Institute for Plant Biotechnology New Delhi, India

ISBN 978-3-030-91801-9 ISBN 978-3-030-91802-6 https://doi.org/10.1007/978-3-030-91802-6

(eBook)

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Dedicated to

Prof. Roger D. Kornberg Nobel Laureate in Chemistry 2006 Professor of structural biology at Stanford University School of Medicine With regards & gratitude for his generous appreciations of my scientific contributions and service to the academic community, and constant support and encouragement during my professional journey!

Preface

Crop production is drastically affected due to external or environmental stresses. The biotic stresses cause significant yield losses in the range of 31–42% together with 6–20% loss during the post-harvest stage. The abiotic stresses also aggravate the situation with crop damage in the range of 6–20%. Understanding the mechanisms of interaction of plants with the biotic stresses caused by insects, bacteria, fungi, viruses, oomycetes, etc., and abiotic stresses due to heat, cold, drought, flooding, submergence, salinity, acidity, etc., is critical to develop resilient crop varieties. Global warming and climate change are also causing emergence of new diseases and insects together with newer biotypes and physiological races of the causal agents on the one hand and aggravating the abiotic stress problems with additional extremes and unpredictability. Development of crop varieties resistant and/or adaptive to these stresses is highly important. The future mission of crop improvement should, therefore, lay emphasis on the development of crop varieties with optimum genome plasticity by possessing resistance or tolerance to multiple biotic and abiotic stresses simultaneously. A moderate estimation of world population by 2050 is about 9.3 billion that would necessitate an increase of crop production by about 70%. On the other hand, the additional losses due to climate change and global warming somewhere in the range of 10–15% should be minimized. Therefore, increase in the crop yield as well as minimization of its loss should be practiced simultaneously focusing on both ‘adaptation’ and ‘mitigation.’ Traditional plant breeding practiced in the last century contributed a lot to the science of crop genetic improvement. Classical plant breeding methods including selection, hybridization, polyploidy and mutation effectively catered to the basic F5 needs—food, feed, fiber, fuel and furniture. The advent of molecular breeding and genetic engineering in the latter part of twentieth century complimented classical breeding that addressed the increasing needs of the world. The twenty-first century came with a gift to the geneticists and plant breeders with the strategy of genome sequencing in Arabidopsis and rice followed by the tools of genomics-aided breeding. More recently, another revolutionary technique, genome or gene editing, became available for genetic correction of crop genomes! The travel from ‘plant breeding’ based on visual or perceivable selection to ‘molecular breeding’ assisted vii

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Preface

by linked markers to ‘transgenic breeding’ using genetic transformation with alien genes to ‘genomics-aided breeding’ facilitated by known gene sequences has now arrived at the age of ‘genetic rectification’ employing genome or gene editing. Knowledge on the advanced genetic and genomic crop improvement strategies including molecular breeding, transgenics, genomic-assisted breeding and the recently emerged genome editing for developing resistant, tolerant and/or adaptive crop varieties is useful to students, faculties and scientists in the public and private universities and organizations. Whole-genome sequencing of most of the major crop plants followed by genotyping-by-sequencing has facilitated identification of exactly the genes conferring resistance, tolerance or adaptability leading to gene discovery, allele mining and shuttle breeding which in turn opened up the scope for ‘designing’ or ‘tailoring’ crop genomes with resistance/tolerance to biotic and abiotic stresses. To my mind, the mission of agriculture in this century is FHNEE security meaning food, health, nutrition, energy and environment security. Hence, genome designing of crops should focus on breeding of varieties with higher yields and improved qualities of the five basic F5 utilities; nutritional and neutraceutical compounds; and other industrially and aesthetically important products and possibility of multiple utilities. For this purpose of ‘precise’ breeding, employment of the genetic and genomic techniques individually or in combination as and when required will play a crucial role. The chapters of the 12 volumes of this twin book series entitled Genomic Designing for Biotic Stress Resistant Crops and Genomic Designing for Abiotic Stress Resistant Crops will deliberate on different types of biotic and abiotic stresses and their effects on and interaction with crop plants; will enumerate the available genetic diversity with regard to biotic or abiotic stress resistance among cultivars; will illuminate on the potential gene pools for utilization in interspecific gene transfer; will brief on the classical genetics of stress resistance and traditional breeding for transferring them to their cultivated counterparts; will discuss on molecular mapping of genes and QTLs underlying stress resistance and their marker-assisted introgression into elite crop varieties; will enunciate different emerging genomics-aided techniques including genomic selection, allele mining, gene discovery and gene pyramiding for developing smart crop varieties with genetic potential to produce F5 of higher quantity and quality; and also will elaborate the case studies on genome editing focusing on specific genes. Most of these chapters will discuss on the success stories of genetic engineering in the relevant crops specifically for generating crops with resistance and/or adaptability to diseases, insects and abiotic stresses. There are obviously a number of reviews and books on the individual aspects of plant molecular breeding, genetic engineering and genomics-aided breeding on crops or on agro-economic traits which includes the 100-plus books edited by me. However, there is no comprehensive reviews or books available that has coverage on crop commodity groups including cereals and millets, oilseeds, pulses, fruits and nuts, vegetables and technical or industrial crops, and modern strategies in single

Preface

ix

volumes with precise focuses on biotic and abiotic stresses. The present volumes will fill this gap with deliberations on about 120 important crops or their groups. This volume on “Genomic Designing for Biotic Stress Resistant Fruit Crops” includes nine chapters contributed by 63 scientists from 11 countries including Austria, Chile, France, Germany, Greece, India, Italy, Lithuania, Spain, UK and USA. I remain immensely thankful for their highly useful contributions. I am indebted to my wife Phullara who as always has assisted me directly in editing these books and indirectly through maintaining an academic ambience to pursue my efforts for science and society pleasantly and peacefully. New Delhi, India

Chittaranjan Kole

Contents

1 Genomics of Biotic Stress Resistance in Malus Domestica . . . . . . . . . Surender Kumar, Tanuja Rana, Karnika Thakur, Reenu Kumari, and Vipin Hallan

1

2 Genomic Designing for Biotic Stress Resistant Banana . . . . . . . . . . . S. Backiyarani, C. Anuradha, and S. Uma

25

3 Genetic Improvement of Citrus Limon (L. Burm f.) for Resistance to Mal Secco Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Catalano, M. Di Guardo, G. Distefano, A. Gentile, and S. La Malfa 4 Genomic Designing for Biotic Stress Resistant Grapevine . . . . . . . . . Silvia Vezzulli, David Gramaje, Javier Tello, Giorgio Gambino, Paola Bettinelli, Carlotta Pirrello, Anna Schwandner, Paola Barba, Elisa Angelini, Gianfranco Anfora, Valerio Mazzoni, Alberto Pozzebon, Juan Emilio Palomares-Rius, Maria Pilar Martínez-Diz, Silvia Laura Toffolatti, Gabriella De Lorenzis, Emanuele De Paoli, Irene Perrone, Erica D’Incà, Sara Zenoni, Jurrian Wilmink, Thierry Lacombe, Manna Crespan, M. Andrew Walker, Luigi Bavaresco, Mario De la Fuente, Anne Fennell, Giovanni Battista Tornielli, Astrid Forneck, Javier Ibáñez, Ludger Hausmann, and Bruce I. Reisch

75 87

5 Wild and Related Species as a Breeding Source for Biotic Stress Resistance of Peach Cultivars and Rootstocks . . . . . . . . . . . . . . . . . 257 Thomas M. Gradziel 6 Genomic Designing of New Almond-Peach Rootstock-Variety Combinations Resistant to Plum Pox Virus (Sharka) . . . . . . . . . . . . 275 Manuel Rubio, Federico Dicenta, and Pedro Martínez-Gómez

xi

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Contents

7 Genomic Designing of New Plum Pox Virus Resistant Plumcot [Prunus Salicina Lindl. x Prunus Armeniaca L.] Varieties Through Interspecific Hybridization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287 María Nicolás-Almansa, D. Ruiz, A. Guevara, J. Cos, Pedro Martínez-Gómez, and Manuel Rubio 8 Integrated Genomic Designing and Insights for Disease Resistance and Crop Protection Against Pathogens in Cherry . . . . . . . . . . . . . . 305 Antonios Zambounis, Dimitrios Valasiadis, and Anastasia Boutsika 9 Development of Biotic Stress Tolerant Berries . . . . . . . . . . . . . . . . . 331 Birutė Frercks, Dalia Gelvonauskienė, Ana D. Juškytė, Sidona Sikorskaitė-Gudžiūnienė, Ingrida Mažeikienė, Vidmantas Bendokas, and Julie Graham

Contributors

Gianfranco Anfora Center Agriculture Food Environment (C3A), University of Trento/Fondazione Edmund Mach, San Michele all’Adige (TN), Italy Elisa Angelini CREA Council for Agriculture Research and Economics, Research Center for Viticulture and Enology, Conegliano (TV), Italy C. Anuradha ICAR-National Research Centre for Banana, Tiruchirappalli, Tamil Nadu, India S. Backiyarani ICAR-National Research Centre for Banana, Tiruchirappalli, Tamil Nadu, India Paola Barba Instituto de Investigaciones Agropecuarias, INIA La Platina, Santiago, Chile Luigi Bavaresco Dept. Sustainable Crop Production, Università Cattolica del Sacro Cuore, Piacenza, Italy Vidmantas Bendokas Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania Paola Bettinelli Center Agriculture Food Environment (C3A), University of Trento/Fondazione Edmund Mach, San Michele all’Adige (TN), Italy Anastasia Boutsika Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization ‘Demeter’ (ELGO-Demeter), Thessaloniki-Thermi, Greece C. Catalano Department of Agriculture, Food and Environment, University of Catania, Catania, Italy J. Cos Department of Hortofruticulture, IMIDA, Murcia, Spain Manna Crespan CREA Council for Agriculture Research and Economics, Research Center for Viticulture and Enology, Conegliano (TV), Italy

xiii

xiv

Contributors

G. Distefano Department of Agriculture, Food and Environment, University of Catania, Catania, Italy Mario De la Fuente Viticulture Research Department, UPM-Polytechnic University of Madrid, Madrid, Spain Gabriella De Lorenzis Department of Agricultural and Environmental Sciences, University of Milan, Milan, Italy Emanuele De Paoli Department of Agricultural and Environmental Sciences, University of Udine, Udine, Italy Federico Dicenta Departament of Plant Breeding, CEBAS-CSIC, Espinardo, Murcia, Spain M. Di Guardo Department of Agriculture, Food and Environment, University of Catania, Catania, Italy Erica D’Incà Department of Biotechnology, University of Verona, Verona, Italy Anne Fennell Agronomy, Horticulture, and Plant Science Department, South Dakota State University, Brookings, South Dakota, USA Astrid Forneck Department of Crop Sciences, Institute of Viticulture and Pomology, University of Natural Resources and Life Sciences Vienna, Tulln, Austria Birutė Frercks Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania Giorgio Gambino Institute for Sustainable Plant Protection, National Research Council of Italy (IPSP-CNR), Torino, Italy Dalia Gelvonauskienė Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania A. Gentile Department of Agriculture, Food and Environment, University of Catania, Catania, Italy Thomas M. Gradziel University of California-Davis, Davis, USA Julie Graham James Hutton Institute, Dundee Scotland, UK David Gramaje Instituto de Ciencias de la Vid y del Vino (ICVV), Consejo Superior de Investigaciones Científicas – Universidad de la Rioja – Gobierno de La Rioja, Logroño, Spain A. Guevara Department of Hortofruticulture, IMIDA, Murcia, Spain Vipin Hallan Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur, India

Contributors

xv

Ludger Hausmann Institute for Grapevine Breeding Geilweilerhof, Julius Kuhn Institute (JKI), Siebeldingen, Germany Javier Ibáñez Instituto de Ciencias de la Vid y del Vino (ICVV), Consejo Superior de Investigaciones Científicas – Universidad de la Rioja – Gobierno de La Rioja, Logroño, Spain Ana D. Juškytė Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania Surender Kumar Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur, India Reenu Kumari Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur, India; College of Horticulture and Forestry, Dr YS Parmar University of Horticulture and Forestry Thunag Mandi, Nauni, HP, India Thierry Lacombe AGAP, Univ Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France S. La Malfa Department of Agriculture, Food and Environment, University of Catania, Catania, Italy Maria Pilar Martínez-Diz Estación de Viticultura y Enología de Galicia (AGACAL-EVEGA), Leiro-Ourense, Spain Pedro Martínez-Gómez Departament Espinardo, Murcia, Spain

of

Plant

Breeding,

CEBAS-CSIC,

Ingrida Mažeikienė Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania Valerio Mazzoni Research and Innovation Center, Fondazione Edmund Mach, San Michele all’Adige (TN), Italy María Nicolás-Almansa Departament Espinardo, Murcia, Spain

of Plant

Breeding, CEBAS-CSIC,

Juan Emilio Palomares-Rius Instituto de Agricultura Sostenible (IAS), Consejo Superior de Investigaciones Científicas (CSIC), Avenida Menéndez Pidal s/n, Córdoba, Spain Irene Perrone Institute for Sustainable Plant Protection, National Research Council of Italy (IPSP-CNR), Torino, Italy Carlotta Pirrello Department of Agronomy, Food, Natural resources, Animals and Environment, University of Padua, Padua, Italy Alberto Pozzebon Department of Agronomy, Food, Natural resources, Animals and Environment, University of Padua, Padua, Italy

xvi

Contributors

Tanuja Rana Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur, India; Department of Agricultural Biotechnology, CSK HPKV, Palampur, India Bruce I. Reisch Horticulture and Plant Breeding Sections, School of Integrative Plant Science, Cornell University, Geneva, NY, USA Manuel Rubio Departament of Plant Breeding, CEBAS-CSIC, Espinardo, Murcia, Spain D. Ruiz Departament of Plant Breeding, CEBAS-CSIC, Espinardo, Murcia, Spain Anna Schwandner Institute for Grapevine Breeding Geilweilerhof, Julius Kuhn Institute (JKI), Siebeldingen, Germany Sidona Sikorskaitė-Gudžiūnienė Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, Akademija, LTKedainiai distr., Lithuania Javier Tello Instituto de Ciencias de la Vid y del Vino (ICVV), Consejo Superior de Investigaciones Científicas – Universidad de la Rioja – Gobierno de La Rioja, Logroño, Spain Karnika Thakur Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur, India Silvia Laura Toffolatti Department of Agricultural and Environmental Sciences, University of Milan, Milan, Italy Giovanni Battista Tornielli Department of Biotechnology, University of Verona, San Pietro in Cariano (VR), Italy S. Uma ICAR-National Research Centre for Banana, Tiruchirappalli, Tamil Nadu, India Dimitrios Valasiadis Laboratory of Pomology, Department of Agriculture, Aristotle University of Thessaloniki, Thessaloniki, Greece Silvia Vezzulli Research and Innovation Center, Fondazione Edmund Mach, San Michele all’Adige (TN), Italy M. Andrew Walker Viticulture and Enology Department, North Davis, CA, USA Jurrian Wilmink Department of Crop Sciences, Institute of Viticulture and Pomology, University of Natural Resources and Life Sciences Vienna, Tulln, Austria Antonios Zambounis Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization ‘Demeter’ (ELGO-Demeter), Thessaloniki-Thermi, Greece Sara Zenoni Department of Biotechnology, University of Verona, Verona, Italy

Abbreviations

2-DE 6mA ABA ABF ABRE ADH AF AFLP AFP AGPase ALA AMFs AP AP2/EREBP APEDA APX AQP ARF ASR ATAF ATG8f BAC BSA bZIP CAGR CAPS Cas9 CAT CBD

Two-dimensional electrophoresis N6-methyladenine Abscisic acid ABRE binding factor ABA-responsive element Alcohol dehydrogenase Annual-fruiting Amplified fragment length polymorphism Antifreeze protein (from Antarctic fish) ADP-glucose pyrophosphorylase 5-aminolevulinic acid Arbuscular mycorrhizal fungi Apetala gene AP2/ethylene-responsive Agricultural and Processed Food Products Export Development Authority Ascorbate peroxidase Aquaporin Auxin response factor Abscisic acid-stress and ripening-inducer Arabidopsis transcription activation factor Autophagy-related protein 8f Bacterial artificial chromosome Bulk segregant analysis Basic leucine zipper Compound annual growth rate Cleaved amplified polymorphic sequences CRISPR-associated protein 9 Catalase Convention on Biological Diversity

xvii

xviii

CBF CCS cDNA CDPK CEBAS CG CIB CIRAD CMT COR CQD CR CRISPR CRT CS CSIC CUC DAM DEG DHAR DHN DI DM DNMT DRE DRE(B) DREB DRM DSB EBI ECe ECs ECw EMS EPA ERD ERF ESP EST ET F1 F3H FAO FAOSTAT

Abbreviations

C-repeat binding factor Copper chaperone for superoxide dismutase Complementary DNA Calcium-dependent protein kinase Centro Edafología y Biología Aplicada del Segura Candidate gene Cold-induced gene Centre de cooperation International en Recherché Agronomique pour le Développement Chromomethylase Cold responsive Carbon quantum dot Chilling requirement Clustered regularly interspaced short palindromic repeats C-repeat Cabernet sauvignon Consejo Superior de Investigaciones Científicas Cup-shaped cotyledon Dormancy associated MADS-box Differentially expressed gene Dehydroascorbate reductase Dehydrin Deficit irrigation Downey mildew DNA methyltransferase Drought-responsive element Drought-responsive element binding Dehydration responsive element binding protein Domain-rearranged methyltransferase Double-strand break European Bioinformatics Institute Electrical conductivity of equivalent Electrical conductivity for soil Electrical conductivity for water Ethylmethyl sulphonate Environmental Protection Agency Early response to dehydration Ethylene response factor Exchangeable sodium percentage Expressed sequence tag Evapotranspiration First filial generation Flavanone 3-hydroxylase Food and Agriculture Organization FAO Corporate Statistical Database

Abbreviations

FDA FLS FPP GA GBS GES GM GMO GolS GP GPCR GS GTPases GWA GWAS HK HR HR HS Hsf HSF HsfA2 HSP HT ICE1 ICE1 IGG InDel INIBAP IPCC IPGRI ISSR ITC JA K+/Na+ KASP Lb LD LEA LG LOD LT LT LTR(E/B) Ma

xix

Food and Drug Administration Flavonol synthase Farnesyl diphosphate Gibberellic acid Genotyping by sequencing Geraniol synthase Genetically modified Genetically modified organism Galactinol synthase1 Guaiacol peroxidase G protein-coupled receptors Genomic selection Guanosine triphosphatase Genome-wide association Genome-wide association study/ studies Histidine kinase Heat requirement Homologous recombination Heat stress Heat shock factor Heat shock transcription factor Heat stress factor A2 Heat shock protein High tolerance Inducer of CBF expression Little elongation complex subunit 1 Intergovernmental Group Insertion/deletion International Network for the Improvement of Banana and Plantain Intergovernmental Panel on Climate Change International Plant Genetic Resources Institute Inter-simple-sequence repeat Indian Tobacco Company Jasmonic acid Potassium/sodium ratio Kompetitive allele amplification Late blooming Linkage disequilibrium Late embryogenesis abundant protein Linkage group Logarithm of odds Low temperature Low tolerance Low-temperature-responsive (element/binding) Musa acuminata

xx

MABCB MANT MAPK MAPKK MAPKKK MAS MASS Mb MDA miRNA MSAP MT MTP MYB MYC NAC042 NAC68 NAM NCBI NGS NHB NHEJ NIP NIR NMU NOS NP NPBT NPC NR NRCB NSP O•−2 OE OIV PA PAC PCD PDS PGIP PIP PIP1; 1 PIP1; 2 PIR PM

Abbreviations

Marker assisted backcross breeding Methyl anthranilate Mitogen-activated protein kinase Mitogen-activated protein kinase kinase Mitogen-activated protein kinase kinase kinase Marker assisted selection Marker-assisted seedling selection Musa balbisiana Malondialdehyde MicroRNA Methylation sensitive amplified polymorphism Medium tolerance Metal tolerance protein Myeloblastosis Myelocytomatosis NAC domain-containing protein 42 NAC domain-containing protein 68 No apical meristem National Center for Biotechnology Information Next generation sequencing National Horticultural Board Non-homologous end-joining Nodulin-like plasma membrane intrinsic protein Near-infrared spectrometry N-nitroso-methyl urethane Nitric oxide synthase Nanoparticle New plant breeding techniques Nuclear pore complex Nitrate reductase National Research Center for Banana Nanoscale particle Superoxide radical Overexpression International Organization of Vine and Wine Proanthocyanidin P1-derived artificial chromosome Programmed cell death Phytoene desaturase Polygalacturonase-inhibiting protein Plasma membrane intrinsic protein Aquaporin PIP1-1 Aquaporin PIP1-2 Protein information resource Powdery mildew

Abbreviations

PN POD PP2C PRD PRP PS I/II PSY PTM Put QD QD qPCR QTL QTLs RAD RAPD RdDM RDI REMAP RFLP RIP RLK RNAi RNA-Seq RNP ROP ROS RT-PCR SAP SAR SCAR sgRNA sHSF sHSP SIB SiNP SIP siRNA SLAF-seq SNP SnRK2 SOD SPL SRAP SSN

xxi

Photosynthetic rate Peroxidase C-type protein phosphatase partial root drying Plant proline-rich protein Photosystem I and II Phytoene synthase Post-translational modification Putrescine Quantum dot Quarentadias (Name of a banana variety in Portuguese language) Quantitative PCR Quantitative trait locus Quantitative trait loci Restriction site associated DNA Random amplified polymorphic DNA RNA-directed DNA methylation Regulated deficit irrigation Retrotransposon-microsatellite amplified polymorphism Restriction fragment length polymorphism Ribosome inactivating protein Receptor-like kinases RNA interference RNA Sequencing Ribonucleoproteins Repressor of primer protein Reactive oxygen species Real time–PCR Switch-activating protein Sodium absorption ratio Sequence-characterized amplified region Single guide RNA Small heat stress transcription factor Small heat shock protein Swiss Institute of Bioinformatics Silicon nanoparticle Small intrinsic protein Small interfering RNA Specific length amplified fragment sequencing Single nucleotide polymorphism SNF1-related protein kinases2 Superoxide dismutase Squamosa promoter binding protein-like Sequence-related amplification polymorphism Site-specific nuclease

xxii

SSR SWEETs TA TAC TALE TALEN TE TF TGE TIP TK TSS UNDESA UniProtKB UPOV USDA VLT VNTRS Vv WBF WGS WL WT YAC ZFN ZIP

Abbreviations

Simple sequence repeat Sugars will eventually be exported transporters Tartaric acid Transformation-competent artificial chromosome Transcription activator-like effector Transcription activator-like effector nuclease Transposable element Transcription factor Targeted genome editing Tonoplast intrinsic protein Traditional knowledge Total soluble sugars United Nations Department of Economic and Social Affairs UniProt Knowledgebase International Union for the Protection of New Varieties of Plants United States Department of Agriculture Very low tolerance Variable number of tandem repeats Vitis vinifera World Banana Forum Whole-genome shotgun Waterlogging Wild type Yeast artificial chromosomes Zinc-finger nuclease Zipper protein

Chapter 1

Genomics of Biotic Stress Resistance in Malus Domestica Surender Kumar, Tanuja Rana, Karnika Thakur, Reenu Kumari, and Vipin Hallan

1.1 Introduction Apple (Malus x domestica Borkh.) is an important temperate fruit crop of the world. A large number of environmental and biological factors affect the productivity and sustainability of the apple orchards. Apple plants are susceptible to several pathogens viz. fungus, bacteria, viruses etc. (Kumar et al. 2011). A number of methods (serological, biological and molecular) for early detection of these pathogens were developed, however it is not practically possible to analyze each plant in field (Kumar et al. 2014). Therefore, understanding the plant disease resistance is prerequisite and this knowledge can be implemented for generation of disease resistance plants. The Malus genus and its pathogens have coevolved in nature and some accessions may harbor resistance genes that can be targeted for breeding programs (Kumar et al. 2010; Laurens et al. 2011). Resistance in crops has been produced successfully by both conventional and molecular breeding techniques for many years. The recent advent of molecular biology coupled with genome sequence information has enabled the identification of dominant and recessive resistance genes. This knowledge is providing novel insights into the intricacies of plant defence and host–pathogen interactions. Based on insights achieved, more sophisticated molecular breeding strategies can be employed for crop protection.

S. Kumar · T. Rana · K. Thakur · R. Kumari · V. Hallan (B) Plant virus lab, Biotechnology division, CSIR-IHBT, Palampur 176062, India T. Rana Department of Agricultural Biotechnology, CSK HPKV, Palampur 176062, India R. Kumari College of Horticulture and Forestry, Dr YS Parmar University of Horticulture and Forestry Thunag Mandi, Nauni, HP 175048, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_1

1

2

S. Kumar et al.

1.2 Fungal Diseases and Their Resistance in Apple The major fungal diseases that affect apple production are fire blight, powdery mildew, apple scab, and juniper rusts (which includes cedar quince rust, cedar-apple rust, and cedar-hawthorn rust). These diseases were detailed in Table 1.1. Fungal diseases are controlled mainly through chemicals (Sutton 1996; Igarashi et al. 2016). The genome-based resistance breeding strategies of apples against many of these pathogens is opted in recent past. There is a huge demand of apple cultivars with high productivity and good fruit quality in the market. One of the major challenges in increasing the apple productivity is the fact that apple hosts a wide range of diseases caused by fungus. Apple scab (Venturia inaequalis), powdery mildew (Podosphaera leucotricha), Alternaria leaf and fruit blotch (A. aborescens, A. tenuissima and A. alternata), bitter rot (Glomerella cingulata), cedar-apple rust (Gymnosporangium juniperi-virginianae), and black rot (Botryosphaeria obtusa) are few fungal diseases of apple. Apple scab and powdery mildew (PM) are two most important fungal diseases of apple which cause huge economic losses by damaging leaves and young fruits (Jha et al. 2009; Qu et al. 2009; Bus et al. 2010, 1996). Resistance breeding, fungicide spray, biological control measures and good sanitary practices are commonly used to combat fungal diseases of apple (MacHardy ). For years, resistance breeding has been exploited extensively and is being regarded as the preferred eco-friendly sustainable alternative to chemical control in order to combat these diseases. Most of the efforts have been directed towards breeding apple resistance against the scab (Venturia inaequalis), powdery mildew (Podosphaera leucotricha) diseases of apple (Laurens 1998). The availability of a range of resistance genes in apple enables breeders to develop new cultivars with durable disease resistances. However, there are reports that different strains of pathogens have breached several resistance genes (R genes) and have made them ineffective for imparting disease resistance (Parlevliet 1993; Gessler et al. 2006). Exploring new resistance genes and pyramiding of more than one major R genes or combination of major R genes and disease resistance quantitative trait loci (QTLs) are being explored for effective and sustainable disease resistance. The availability of apple genome and extensive evaluation of germplasm has led to the identification of many useful sources of resistance that could be exploited in resistance breeding (MacHardy 1996; Giovannoni 2010; Velasco et al. 2010). A number of dominant R-genes had been identified in apple and approximately 868 R-genes have been identified to impart resistance against pathogens (Perazzolli et al. 2014). These genes encode for proteins that are able to recognize pathogen effectors and activate the defense response (Dodds and Rathjen 2010; Pavan et al. 2010). Resistance against apple fungal pathogens is derived from both monogenic and polygenic loci. Several monogenic and polygenic genetic loci have been identified from wild cultivars of apple that are capable of imparting resistance against particular races of V. inaequalis (MacHardy 1996; Gessler et al. 2006). Till date 17 monogenic R genes (Rvi1, Rvi2, Rvi3, Rvi4, Rvi5, Rvi6, Rvi7, Rvi8, Rvi9, Rvi10, Rvi11, Rvi12,

Fire Blight (Erwinia amylovora)

Gram Negative bacterium

Ascomycota

Black rot (Botryosphaeria obtusa)

Bacterial diseases

Basidiomycota

Cedar-apple rust (Gymnosporangium juniperi-virginianae)

Wilting, Browning/blackening of young shoots

Purple spots on leaves surface, fruit rot

Lesions on fruit

Fruit rot

Ascomycota

Bitter rot (Colletotrichum acutatum, Colletotrichum gloeosporioides and Glomerella cingulata)

(continued)

Baker (1971), Mikicinski et al. (2016)

Brown-Rytlewski et al. (2000)

Crowell (1934)

Sutton (1990), González et al. (2006), Munir et al. (2016), Jayawardena et al. (2016)

Filajdic et al. (1995), Madhu et al. (2020)

Purple to black spots on leaves which later on turn into frog eye spots, premature defoliation, dark and sunken spots on fruits

Ascomycota

McHardy (1996), Gladieux et al. (2008), Jha et al. (2009) Gauthier (2018)

Alternaria leaf and fruit blotch (Alternaria. aborescens, A. tenuissima and A. alternata)

Olive colored spots on early vegetative leaves and fruits, heavily infested leaves with spores, grey to black spots on the fruit

References

Leaves covered with grey to white fungal Butt et al. (1983), Yodder (2000), spores, curled leaves, webbed russeting Gañán et al. (2020) on fruits

Ascomycota

Apple scab (Venturia inaequalis)

Symptoms

Powdery mildew (Podosphaera leucotricha) Ascomycota

Taxonomic group/division

Disease name/causal agent

Fungal diseases

Table 1.1 Major apple tree’s fungi, bacterial and viral diseases enlisted with taxonomic groups, and some of their characteristic disease symptoms

1 Genomics of Biotic Stress Resistance in Malus Domestica 3

Gram Negative bacterium Gram Negative bacterium Gram Negative bacterium

Apple blister spot or blister canker (Pseudomonas syringae pv. papulans)

Crown gall (Agrobacterium tumefaciens)

Hairy roots (Rhizobium rhizogenes)

Ilarvirus

Capillovirus

Trichovirus

Foveavirus

Apple mosaic virus (ApMV)

Apple stem grooving virus (ASGV)

Apple chlorotic leaf spot virus (ACLSV)

Apple stem pitting virus (ASPV)

Viral diseases

Taxonomic group/division

Disease name/causal agent

Fungal diseases

Table 1.1 (continued) References

Die back, inner bark necrosis, decline, severe pitting and grooving in xylem, vein yellowing, latent infection, graft incompatibility and epinasty

Chlorotic leaf spots or rings, chlorosis, line patterns, stem pitting and severe graft incompatibilities in some Prunus combinations

Severe pitting and grooving in xylem, graft union abnormalities, reduced vigor and decline in susceptible Malus species

Mosaic, necrotic ring spots, mottling, tree decline, decreased ascorbic acid content of the fruit, reduced shoot growth, fruit set, fruit weight and yield per tree

Site of infection shows overabundant growth of hairy roots

(continued)

Fridlund and Aichele (1987), Kogenezawa and Yanase (1990), Brakta et al. (2015)

Chairez and Lister (1973), Dunez et al. (1975, 1988)

Uyemoto and Gilmer (1971), Plese et al. (1975), van Oosten et al. (1982)

Gotlieb and Berbee (1973), Wood et al. (1975), Desvignes (1999), Singh et al. (1979)

Riker et al. (1930)

Gall formation on the roots/at the base of Kado (2002) crown

Vein necrosis, rough papery bark, lesions Burr and Hurwitz (1979), Kerkoud on fruits et al. (2002, 2011)

Symptoms

4 S. Kumar et al.

Sobemovirus

Apple latent virus (ALV)

Tomato ringspot virus (apple union necrosis) Nepovirus (ToRSV)

Taxonomic group/division

Disease name/causal agent

Fungal diseases

Table 1.1 (continued)

Mosaic, rasp leaf, yellow bud or vein, ringspots and chlorosis

Latent infection

Symptoms

Stouffer et al. (1977), Parish and Converse (1981)

Franki and Miles (1985)

References

1 Genomics of Biotic Stress Resistance in Malus Domestica 5

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Rvi13, Rvi14, Rvi15, Rvi16 and Rvi17) imparting resistance against various races of Venturia have been characterized in apple (Bowen et al. 2009; Bus et al. 2009). Among various R genes, Rvi6 previously known, as Vf is the most studied gene of apple and had been extensively used in various resistance breeding programs (Crosby et al. 1992; MacHardy 1996; King et al. 1999; Gessler et al. 2006). Extensive efforts have been done to isolate, clone and characterize the Rvi6 gene, which have led to full length cloning of the gene (Vinatzer et al. 2001; Xu and Korban 2002; Belfanti et al. 2004; Gessler et al. 2006; Szankowski et al. 2009). Rvi6, also known as HcrVf2 (Homologous to C. fulvus R genes of the Vf region) is constitutively expressed gene and encodes an extracellular leucine-rich repeat containing membrane bound glycoproteins having domain architecture similar to that of Cf protein, a receptor like protein (Belfanti et al. 2004; Gessler et al. 2006; Szankowski et al. 2009). Several other paralogs of Rvi6 have been identified from apple. They are speculated to act as reservoirs that apple might be using to develop resistance against constantly evolving pathogen (Xu and Korban 2004; Gessler et al. 2006). Three members of TNL (toll/interleukin-1 receptor (TIR)- nucleotide binding site (NBS)- leucine rich repeat (LRR)) like resistance genes are found to be present at the Rvi15 (Vr2) resistance gene locus in apple (Galli et al. 2010). However, which of them impart Rvi15 (Vr2) mediated resistance is not known. The Rvi16, a new scab resistance gene has been mapped on the lower end of linkage group (LG) 3 (Bus et al. 2011). Interestingly the gene seems unique as it segregates independently from all the known scab resistance genes and impart resistance symptoms that are very distinct from that imparted by other known R genes and disease resistance QTLs. This suggests that Rvi16 gene employs different resistance mechanisms against scab pathogen. Recently, another major scab resistance gene Rvi17 (V a1 ) from the Russian apple cultivar ‘Antonovoka’ accession APF22 has been identified (Bus et al. 2011). The gene is closely linked to the simple sequence repeat (SSR) marker CH-Vf1 which happens to co-segregate with the Vf gene. This SSR analysis revealed that Rvi17 is present close to the Rvi6 gene at apple LG 1 (Dunemann and Egerer 2010). The proximity of these two major R genes on the same linkage group could prove beneficial and could be further exploited in pyramiding major resistance genes for durable resistance against scab. Resistance to powdery mildew in apple is derived from both monogenic and polygenic resistance derived from the wild or ornamental crab apples and from the domesticated Malus x domestica. Five major genes Pl-1, Pl-2, Pl-w, Pl-d and Pl-m have been known to date for resistance against P. leucotricha (Knight and Alston 1968; Dayton 1977; Visser and Verhaegh 1976, 1979; Gallott et al. 1985; Simon and Weeden 1991; James et al. 2004; Calenge and Durel 2006) and SSRs or easy to use sequence characterized amplified region (SCAR) markers are available for all of them (Markussen et al. 1995; Seglias and Gessler 1997; Dunemann et al. 1999; Gardiner et al. 1999, 2003; James et al. 2004; James and Evans 2003). Availability of these markers has enabled mapping of these genes on apple genome. Pl2 and Plm are reported to be linked with SCAR marker N18-SCAR (Gradiner et al. 2003) and had been mapped on the LG11 (Seglias and Gessler 1997), Plw has been mapped at the top of LG8 (James and Evans 2003) while Pld has been mapped at the bottom of LG12 (James et al. 2004). Although the markers of Pl1 gene were available

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7

but the gene was not mapped until recently when the Dunemann et al. (2007) have mapped this gene on LG12 of apple genome (Fig. 1.1). Beside monogenic R genes, family of resistance gene analogs (RGAs) with a NBS domain and several QTLs either broad-spectrum or isolate specific have been identified in different apple cultivars which impart resistance against pathogens (Gessler et al. 2006; Soufflet-Freslon et al. 2008; Perazzolli et al. 2014; Caffier et al. 2016). As the pathogens have breached several R genes, resistance imparted by them is not durable. Resistance imparted by QTL is frequently assumed to be more durable as various mechanisms such as basal defense, chemical warfare, defense signal transduction etc. underlie quantitative resistance (Poland et al. 2009). Quantitative resistance could be broad spectrum i.e., it provides resistance against all isolates of pathogen or isolate specific. Several resistance QTLs imparting resistance against apple scab have been identified and mapped across 11 apple LGs (Durel et al. 2003; Liebhard et al. 2003; Calenge et al. 2004; Gessler et al. 2006; Soufflet-Freslon et al.

(a) 0

6

9

19

(b)

(c)

CH01g12

0

CH04d02

7

CH01f02

16

CH03c02

CH01g12

CH01g12

0

8

CH01f02

17

CH03c02

CH01f02

CH03c02

26

28

Hi07f01 Pl1-Gh RGA-15G11

29

Hi07f01

28

AT20-SCAR

30

RGA-15G11

33

CH01d03z

36

Pl1-F

AT20-SCAR

AT20-SCAR 33

26

33

CH01d03z

Hi07f01

Fig. 1.1 Genetic maps depicting Pl1-carrying linkage group LG12 adapted from Dunemann et al. (2007) a markers for 154 individuals of population 04/208 (‘Idared’x Robusta 5), b161 individuals of population 99/2-Gh (‘Idared’ × 78/18–4, locus Pl1-Gh, mildew scored in a greenhouse) and c 125 individuals of population 99/2-F (‘Idared’ × 78/18–4, locus Pl1-F, mildew scored in the field)

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2008; Bus et al. 2011). Interestingly, the phenomenon of erosion of quantitative resistance over the years has been observed in the case of scab pathogen due to pathogen adaptation. In a study, it was observed that the two broad-spectrum QTLs (QTLs F11 and F17) which provide resistance against scab pathogen have been breached (Caffier et al. 2014). At least four or five QTLs according to the season have been identified in apple as polygenic determinant of resistance against powdery mildew. Out of these, two QTLs on LG2 and LG13 appear to be stable as they were consistently identified through five seasons, while five QTLs on LG1, LG8, LG10, LG14 and LG17 were identified in only one, two or three seasons. Dominance effect in some of the QTLs (LG2) was also observed apart from the known additive effect of these QTLs in conferring disease resistance (Calenge and Durel 2006). Mutations in susceptibility genes (S-genes) are also being explored for ability to impart disease resistance against fungal pathogens. It has been reported that some S-genes function as negative regulator of plant immunity system, which when impaired prevents the suppression of plant defense thus providing resistance against the pathogen (Pavan et al. 2010). The MLO gene from barley is an example of such Sgene which causes powdery mildew (PM) susceptibility. Loss of function mutations in MLOs-gene have been shown to reduce the susceptibility to PM in various plants such as barley (Büschges et al. 1997), Arabidopsis thaliana (Consonni et al. 2006), pea (Pavan et al. 2011), tomato (Bai et al. 2008) and pepper (Zheng et al. 2013). In apple, three MLO genes (MdMLO11, MdMLO18 and MdMLO19) were found to be upregulated during the early stages of PM infection (Pessina et al. 2014). Out of these three genes, MdMLO11and MdMLO19 genes were knocked down/suppressed using RNA interference (RNAi) to assess their possible role in powdery mildew susceptibility in apple. Authors found that knocking MdMLO11 down did not result in reduction of susceptibility. Knocking down MdMLO11 with MdMLO19 does not result into any additional reduction in susceptibility, leading to conclusion that MdMLO19 is the only functional S-gene in apple that plays an important role in powdery mildew susceptibility in apple (Pessina et al. 2016). MicroRNAs (miRNAs) have emerged as key regulators of gene expression in plants that control the expression of transcription factors involved in various physiological activities (Ma et al. 2014; Zhang et al. 2017). These are noncoding RNA molecules (20–24 nt) which binds to the complementary sequences of mRNA, to either inhibit their expression or induce their degradation, leading to the silencing of targeted gene. They are crucial regulatory factors that control most of the biological processes including abiotic stresses. Their role in regulating transcription factors involved in biotic stress pathways in plants is relatively less explored. A total of 146 miRNAs have been identified from apple cultivar Golden Delicious from which 11 miRNAs were found to be novel (Ma et al. 2014). MdmiRLn11, one of the novel miRNAs, was shown to suppress the expression levels of Md-NBS (an NBS–LRR protein) gene and decreased the resistance to apple leaf spot pathogen (Ma et al. 2014). NBS–LRR has a NBS and a LRR domain which encodes for an intracellular innate protein and specific expression imparts plant resistance against broad spectrum resistance to fungal pathogens (Yang et al. 2008). Recently, Zhang and group, explored the possible role of MicroRNAs (miRNAs) in regulating the WRKY transcription factors of apple against leaf spot fungal pathogen, Alternaria

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alternaria f. sp. Mali (ALT1) (Zhang et al. 2017). They identified 58 miRNAs that showed two-fold upregulation upon ALT1 infection in Golden Delicious (GD). A pair of miRNAs, Md-miRNA156ab and Md-miRNA395 was identified which targeted novel WRKY transcription factors MdWRKYN1 and MdWRKY26, respectively. They observed increased expression levels of miRNA156ab and Md-miRNA395 and decreased expression levels of MdWRKYN1 and MdWRKY26 during susceptible interaction between GD and ALT1. To establish the possible role of these two miRNAs in imparting resistance against leaf spot pathogen, authors upregulated the expression levels of MdWRKYN1 and MdWRKY26 or suppressed the expression of miRNA156ab and Md-miRNA395. This resulted in the increased expression of WRKY-regulated pathogenesis related (PR) protein encoding genes enhancing disease resistance in plants. This study showed that ALT1-induced miRNA156ab and Md-miRNA395 results in susceptibility to ALT1 in GD by suppressing MdWRKYN1 and MdWRKY26 thereby decreasing the expression levels of PR genes. To resist fungal pathogens, plants rely on its innate immunity and have well developed strategies to perceive the pathogen and mount a very strong defense response to combat diseases. Plant pattern recognition receptors or R genes mediate the perception of various pathogens. Diverse categories of domain architecture and functions have been assigned to these receptors. However, fungal pathogens are evolving to break down the plant immunity. Efforts are being made to understand the mechanism adopted by different pathogens to breach the plant immunity and characterize the virulence strategies adopted by these pathogens to cause disease. After decades of efforts a scab (fungus) resistance trait was successfully introgressed into a commercial cultivar (crab apple) (Gessler and Pertot 2012). In apple most resistance genes identified have been linked with fungal resistance (Xu and Korban 2002; Kumar et al. 2010; Laurens et al. 2011). With reduced cost of genome sequencing due to various next generation sequencing technologies, the complete genome sequencing of apple varieties and re-sequencing of several different accessions/cultivars of apple should be extremely useful in this regard.

1.3 Bacterial Diseases and Their Control Apple blister spot or blister canker (Pseudomonas syringae pv. papulans), crown gall (Agrobacterium tumefaciens), and fire blight (Erwinia amylovora) are considered as major disease of apple tree (Table 1.1).

1.3.1 Blister Spot/Canker Disease Blister spot/canker disease is caused by Pseudomonas syringae pv. papulans, is a gram-negative bacterium and this disease is considered as one of the major economical hurdles in apple fruit marketing. The disease was first reported in USA by Rose

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(1917) and more than 20 different cultivars of apple was known to be susceptible for this with varied susceptibility (Burr and Hurwitz 1979; Van Hall 1981; Sholberg and Bedford 1997). The disease was reported from almost all major apple growing countries (Bazzi and Calzolari 1983; Kerkoud et al. 2002, 2011). The symptoms associated with this includes mid vein necrosis on leaf blades and rough papery bark on branches (Bonn and Bedford 1986). As the disease progress there appears blisters or brown lesions on fruits (10–200), rendering them unmarketable (Bazzi and Calzolari 1983). The major entry route for this pathogen is through stomata (Tetley 1930). Based on symptoms, host preference, biochemical and immonological characters P. syringae has been divided into many pathovars (Kerkoud et al. 2002). During winter, bacteria survive in weeds, fruit buds, leaf scars and infected left-over fruits, which become as reservoir of infection in the next vegetative season. Warm and humid conditions of early spring provide a favorable environment for multiplication of the pathogen whereas late spring season when rains are abundant helps in its dispersal from one plant to another. If left unattended it can infect 80% of apple crop in an orchard. To control the pathogen spread, good agricultural practices and disease-free planting material are important. Apart from these, a number of chemicals/ antibiotics are available for its control; however, growing resistance against chemicals reduces their use (Jones et al. 1991). Molecular means of resistance in this disease are not yet identified.

1.3.2 Fire Blight Disease It is a type of canker disease which infects mainly members of the Rosaceae family and is the first known disease caused by bacteria (Baker 1971; Johnson and Stockwell 1998). The disease is caused by erwinia amylovora, a rod-shaped, gram-negative bacterium, belonging to family Enterobacteriacae (Johnson 2000). Some of the infected cankers present on twigs or trunk region where bacteria survive during winters, acts as reservoir for pathogen. During favorable conditions it spreads from infected to healthy twigs and plants respectively (Johnson and Stockwell 1998). Pathogen enters inside the host plants through natural openings (like stigmas, stomata, nectaries of flowers etc.) and wounds. It infects almost all the above ground parts of plants and its symptoms include burn like symptoms on flowers, fruits, leaves, terminal shoots (as per disease name), canker on trunks and braches, finally leading to plant dieback/mortality (Johnson and Stockwell 1998; Thompson 2000; Mikicinski et al. 2016). Humidity and warm conditions of summer helps in rapid proliferation of pathogen. Fire blight is considered as one of the most devastating bacterial diseases of apple causing huge economical loss for e. g. in USA losses and its control costs 100 million dollars per year (Norelli et al. 2003) and this cost is increasing with time. Limitation of synthetic compounds and development of resistance to commonly used antibiotics pose serious hurdle in management of fire blight disease. However, many

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innovative ways to target the pathogen have been used, which showed promising results. Epiphytic population can be controlled by contact bactericides compounds like cooper and strepomycin but pathogen inside the host cell escape from this. E. amylovora uses xylem and cortical parenchyma system for systemic spread and at this stage many of the available synthetic compounds and traditional ways of spray fails. To overcome this, Acimovic et al. (2015) uses trunk injection approach to control pathogen; this allows the systemic transfer of compounds through vascular system. Application of streptomycin and oxytetracycline showed significant control of blossom and shoot blight phases of disease, respectively. Similarly, application of plant resistance inducers like potassium phosphites (PH), oracibenzolar-S-methyl (ASM) lead to increase in expression of defense related proteins (PR-1, PR-2 and PR8). This method presents advantages over traditional ones as it uses less antibiotics, is ecofriendly and increase the effectiveness of drugs/compounds against pathogen. Apart from synthetic compounds a number of biological agents were also used against fire blight (Mikicinski et al. 2016) which are commercially available for e. g. Bloomtime (Pantoea agglomernas E325, USA), Blossom Bless (P. agglomerans P10c, New Zeland), Blight Ban C9-1 (P. vagans C9-1, USA), Blight Ban A506 (P. fluorescens A506, USA) and Serenade (Bacillus subtilis QST713, USA). To study the host response to disease, high throughput sequencing of RNA extracted from inoculated flowers (48 h) was carried out (Kamber et al. 2016). In this study, 1,080 transcripts were found differentially regulated as compared to mock sample. Most of these transcripts belong to putative disease resistance, stress, pathogen related, general metabolic, and phytohormone related genes. This study showed the early molecular events within the host and understanding these events surely can lead to generation of fire blight disease resistance.

1.3.3 Crown Gall Disease This disease is caused by A. tumefaciens and is a major problem in several plant species including apple. It is a very unique disease in which Agrobacterium transfers its tumor inducing (Ti) plasmid into the host genome. The Ti plasmid encodes for iaaM (tryptophan monooxygenase), iaaH (indole-3-acetamide hydrolase), and ipt (AMP isopentenyl transferase) genes and their expression leads to overproduction of auxin and cytokinin, leading to formation of galls in roots (Garfinkel et al. 1981; Ream et al. 1983). Mutation in these genes leads to abolishment of disease (Ream et al. 1983). In order to develop resistance against crown gall disease in apple RNA interference (RNAi) approach has been used (Viss et al. 2003). In this study, iaaM and ipt genes were targeted for silencing by expressing their dsRNA. Inactivation of these genes leads to development of resistance against crown gall disease.

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1.4 Viral Diseases of Apple Plant viruses are the most underestimated but significant plant pathogens that not only compromise the quantity but also the quality of the produce. Apple trees worldwide are susceptible to four major viruses viz.: apple mosaic virus (ApMV, genus Ilarvirus), apple chlorotic leaf spot virus (ACLSV, genus Trichovirus), apple stem grooving virus (ASGV, genus Capillovirus) and apple stem pitting virus (ASPV, genus Foveavirus) (Desvignes 1999). Of these ASGV, ASPV and ACLSV are often symptomless when present alone and thus are also referred as latent apple viruses. However, in orchards mostly these viruses occur as mixed infection with other viruses and pathogens causing severe losses to apple production worldwide. Apple necrotic mosaic virus (ApNMV) (Noda et al. 2017), Apple latent virus (ALV) and Tomato ringspot virus (apple union necrosis disease) (ToRSV) are considered as minor apple viruses (Table 1.1). The latent viruses result in reduction of yield and plant vigor (Table 1.2) (Cembali et al. 2003; Hadidi et al. 2011). The yield losses recorded owing to virus infections range from less than 10% to greater than 80–90% (Hadidi et al. 2016). The knowledge of viral epidemiology and effect on host plant is crucial for developing effective and sustainable plant virus resistance strategies. Apple viral diseases spread mainly thorough vegetative propagation though incidences of seed, pollen, insects and nematode transmission are also reported for ToRSV, ALV and ApMV (Hadidi et al. 2011). Molecular characterization of ACLSV, ASGV and ASPV from different countries and hosts revealed the presence of significant diversity at molecular level (Magome et al. 1997; Mathioudakis et al. 2010; Rana et al. 2010; Ferretti et al. 2010; Dhir et al. 2011; Komorowska et al. 2011; Song et al. 2011; Liebenberg et al. 2012; Chen et al. 2014; Yao et al. 2014) attributing to differential biological and serological properties among viral isolates. Table 1.2 Effects of viral diseases on apple yield Apple cultivars

Virus(es)

Golden delicious Apple mosaic virus (AMV)

Reduction in apple yield References (%) 46

Baumann and Bonn (1988), Cembali et al. (2003)

Golden delicious Apple stem grooving 12 virus (ASGV), Apple stem pitting virus (ASPV), Apple chlorotic leaf spot virus (ACLSV)

Meijnske et al. (1975)

Golden delicious ASGV, ASPV, ACLSV

30

van Oosten et al. (1982)

McIntosh

ApMV

9

Zawadzka (1983)

Red delicious

ApMV

Golden delicious ACLSV

42

Zawadzka (1983)

30–40%

Nemchinov et al. (1995), Wu et al. (1998), Cembali et al. (2003)

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As more viral genome sequences are being determined, variations in viral genomic sequences and their effects on pathogenicity need to be investigated. A number of phylogenetic analyses of ACLSV-coat protein isolates revealed high molecular variability among isolates at several positions (Candresse et al. 1995; Pasquini et al. 1998; Krizbai et al. 2001; Al Rwahnih et al. 2004; Rana et al. 2010). In ACLSV isolates sequence variability was generally not dependent on the geographical origin or host of the isolates (Rana et al. 2010; Ferretti et al. 2010; Chen et al. 2014). ACLSV isolates clustered into four groups (Chen et al. 2014) based on phylogenetic variability thus pointing to an infrequent gene flow in absence of a known transmission vector. The exchange of propagative plant material between different countries could be a plausible reason for this. The phylogenetic analysis also revealed large inter-cluster genetic divergence accompanied by very low intra-cluster variation thus, indicating close relatedness of phylogenetic placements of isolates to their genetic differentiation (Chen et al. 2014 regions, also reported by Nickel et al. (2001). Such detailed analysis of variability could be exploited for various pathogen derived resistance (PDR) strategies. For ASGV, two sequence variable regions (V1 and V2) and several recombinants have been identified among various isolates from the world (Chen et al. 2014). ASPV (Nemchinov et al. 1998) recorded greatest genetic diversity among isolates and is the most variable among the three viruses and only for ASPV a possible correlation with the geographical origin could be predicted. Nevertheless, no correlation based on host plant was shown by the phylogenetic analyses for all these latent viruses (Ferretti et al. 2010). Management of plant viruses is a critical problem and a foremost challenge in apple cultivation. Such information about variability and phylogeny of viruses could be used to develop effective control and management strategies using biotechnology and bioinformatic tools. Currently there are two strategies for developing virus resistance: (a) using available natural resistance and using it for resistance breeding (b) developing engineered virus-resistance (i.e., PDR). For long-term, sustainable management strategies for controlling these viruses the knowledge of host, environment and vector generated selection pressure on viral genome is important. The mutant generated due to the changed environment would harbor the heritable variations. Similar studies on selection pressures on various ACLSV genes were tested and the result pointed towards the negative selection pressure on the ACLSV genome (Chen et al. 2019).

1.5 Natural Resistance and Breeding for Resistance The M. domestica (also designated M. x domestica Borkh.) resulted from initial domestication and subsequent interspecific hybridization (Hancock et al. 2008; Qian et al. 2010). The primary center of diversity extends from Asia Minor to the western provinces of China (Juniper et al. 1999). The cultivation history of M. domestica reports more than ten thousand cultivars although many of these are now lost

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(Way et al. 1990; Qian et al. 2010; Velasco et al. 2010). Hancock et al. (2008) reported that most of the apple species are diploid (2n = 2x = 34) though, higher somatic numbers (e.g., 51, 68, 85) have been recorded and several cultivated ones are triploid. Apple flowers are self-incompatible and therefore need to be crosspollinated for fruit development. The taxonomy database of the U.S. Department of Agriculture Germplasm Resources Information Network (GRIN) has recorded a list of 58 species and hybrids. The various apple databases classify apple germplasm based on fruit and growth characteristics. The use of virus-resistance present in germplasm is an effective and inexpensive approach to decrease the economic losses due to the plant viruses (Cerqueira-Silva et al. 2008). Few records for biotic (fungi, bacteria) and abiotic (cold, drought) stress tolerance in apple are available. However, no information for virus resistance apple cultivar is recorded. Thus, there is a limited gene pool for tapping natural resistance. Also, comparatively breeding for resistance is a time-consuming, laborious and an expensive process (Borém and Milach 1998). Genetic improvement of M. domestica cultivars is bottlenecked due to selfincompatibility, along with high allelic heterozygosity, a long juvenile period, and inbreeding depression (Brown and Maloney 2003). Marker-assisted selection (MAS) is an effective strategy used in recent breeding programs. In MAS, genetic markers associated to a specific trait is used for integrating that particular marker/trait into the new cultivars. MAS has been shown to be very effective in integrating large-effect loci (e.g., red-fleshed fruit) into apple breeding programs (Chagné et al. 2007). With the sequencing of M. domestica genome (Velasco et al. 2010) there is an increase in efforts towards trait-marker linkage analysis. To bridge the gap between breeding and molecular genetic research work (e.g., RosBREED, Fruit Breedomics Consortium 2012; Iezzoni et al. 2010) towards large-scale, multi-year projects were undertaken. Slow germplasm characterization and annotation have resulted in limited utility of genetic information stored in gene banks by breeding programs. A need for high throughput genotyping of germplasm accessions and intensive phenotypic evaluation of agronomic traits of importance along with the re-sequencing of candidate genes linked with their control could provide new leap for resistance breeding. Molecular marker technology also offers opportunities to decrease this disparity. Thus, for the sustainable conservation and increasing the use of crop genetic resources an amalgamation of genomic technology and the characterization of germplasm banks would have an important role. Chagné et al. (2012) used genomic sequence data of 27 globally important apple cultivars to develop of a broad coverage single nucleotide polymorphism (SNP) array (produced by RosBREED). Similarly, Khan et al. (2012) reported the assembly of other SNP arrays. Genomic selection is effective in directing breeding for complex polygenic traits (Jannink et al. 2010) and was successfully used to direct fruit quality trait breeding in apple (Kumar et al. 2012a). Very limited work has been done for virus resistance breeding in apples and not much information for stable and durable source of virus resistance is reported or characterized till date. A review by Rodrigues et al. (2009) detailed the initiation of virus infection, spread in susceptible plants, plant response to infection and virus counter action. The plant immune system comprises dominant (R) and recessive resistance

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(r) genes. There is an allele-specific interaction between the dominant resistance genes (R) with pathogen avirulence (Avr) genes. “Hypersensitive response” (HR), is defined as a localized programmed cell death, frequently observed in R and Avr interactions. It is a preventive response for limiting the extent of pathogen invasion (Ritzenthaler 2005). The R genes that trigger HR identify viral coat proteins (CP), movement proteins (MP), RNA polymerase subunits and genomic segments as avirulence factors (Rodrigues et al. 2009). The recessive resistance-based breeding is one of the best suited practices for development of resistance against pathogens (Cavatorta et al. 2008). It offers better durability as compared to the dominant gene-based resistance. The mutations in viral genome can easily suppress the interaction between the plant resistance factors and virus avirulance factors and could break a dominant resistance (Lecoq et al. 2004). For decades the dominant I gene is used to confer protection to Phaseolus vulgaris against bean common mosaic virus (BCMV) and others viruses (Keller et al. 1996). Dominant resistance has been recorded that thye can stay effective for many years (Kang et al. 2005a, b). Resistance breeding for dominant gene is preferred as it targets the exact pairs of host genes facilitating plant selection (Ritzenthaler 2005). Most of the R genes that confer resistance to viral infection belong to the NBS-LRR class (Martin et al. 2003). Another orthodox option is the use of attenuated or weakened virus strains to prime the resistance response against related pathogenic viral strain (Ichiki et al. 2005).

1.6 Engineered Virus-Resistance Most of the engineered resistance in plants is pathogen derived and achieved by expression of viral protein/sequences in plant cells leading to plant protection without interference with essential host functions (Prins et al. 2008). The RNA mediated pathogen-derived resistance (PDR) against virus in plants is also known as post-transcriptional gene silencing (PTGS) (Prins et al. 2008). Baulcombe (2004) described three RNA silencing (RNAi) pathways: (i) Cytoplasmic small interfering RNA (siRNA) silencing, important in virus infected cell; (ii) Silencing of endogenous mRNAs by miRNAs and (iii) DNA methylation and the suppression of transcription (Rodrigues et al. 2009). PDR can be classified as protein-mediated and nucleic acid-mediated resistance. Protein mediated resistance has been reported for ACLSV. Viral movement proteins (MPs) have important role in virus transport between the adjacent cells as well as systemically (i.e., long distance). Nicotiana occidentalis plants expressing ACLSV movement protein (P50) and partially functional MP deletion mutants (Delta A and Delta C) of ACLSV recorded resistance to grapevine berry inner necrosis virus (GINV) (Yoshikawa et al. 2006). Thus, the mutated MPs for transgenic plant development could be efficient in inhibiting the local and systemic spread of many different viruses.

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For the plum pox virus (PPV), an important virus of pome and stone fruits, constructs for intron-spliced hairpin RNAs (ihpRNAs) able to produce dsRNAs, were introduced in the ‘Startovaja’ (Prunus domestica L.) commercial plum cultivar (Sidorova et al. 2016). The resulting transgenic plum trees were asymptomatic for five years, despite the long-term systemic PPV infection (sharka disease) caused by the infected scions implanted onto the transgenic shoots (Sidorova et al. 2017, 2018). A non-transgenic based approach of exogenously applying dsRNA to combat virus infestation in plants is being utilized to manage plant production losses due to viruses. This could be a simple, economic, environmentally safe, new biotechnological tool against plant virus diseases and could be an effective application of RNA silencing technology. Tenllado et al. (2003, 2004) used E. coli for producing large amounts of dsRNA coding for partial sequences of pepper mild mottle virus (PMMoV) and PPV. Simultaneous injection of dsRNA with purified virus particles inhibited both viruses. Also, resistance to virus infection was observed when the recombinant bacterial preparations harbouring dsRNA producing construct were sprayed onto the N. benthamiana leaves. Plant virus vectors are another alternative to the genetic transformation for trait delivery. Apple latent spherical virus (ALSV) is an infectious plant virus which spreads through infected cells without inducing any diseases. Igarashi et al. (2009) designed ALSV as VIGS (virus-induced gene silencing) vector. This ALSV vector was capable of sustaining uniform silencing phenotypes in herbaceous plants persisting for several months. Apple seedlings inoculated with rbcS-ALSV developed systemic silencing phenotype which persisted for about three months in the infected plants (Sasaki et al. 2011). Although apple is the natural host, ALSV infects usually asymptomatically members of family Cucurbitaceae, Fabaceae, Solanaceae and fruit trees in the Rosaceae (including apple). ALSV VIGS vector system was shown to induce both VIGS and gene overexpression efficiently and persistently in both apple seedlings and herbaceous plants. The ALSV vector is confirmed as not transmissible to most of the successive progenies (Yamagishi et al. 2014, 2016). This technique can accelerate breeding programs, as the host plant is not modified genetically. The ALSV vector is thus an innovative tool for genetic manipulations, allowing overexpression or suppression of a target gene in plants. The ALSV vector system has been used for inducing foreign gene expression, virus-induced gene silencing, and virusinduced transcriptional gene silencing over a long period of time and in various plant species (Igarashi et al. 2009; Taki et al. 2013; Satoh et al. 2014). However, a major drawback to this is the use of a full-length infectious virus which is to be maintained and propagated in host plants. The small insert size carrying capacity of the viral vector and dependence on biolistics method for administration of the mature viral RNA, could be laborious (Cusin et al. 2017). Apple is a vegetatively propagated crop. Commercial cultivars are grafted onto a rootstock and therefore the development of virus resistant rootstocks would be an effective disease-control strategy. Among rootstocks available for commercial plantation M.7 is reported to be Tomato ring spot virus resistant and M.9 is considered to be tolerant to latent viruses (Cummins and Aldwinckle 1995). Moreover, nongenetically modified scion grafted onto the genetically modified (GM) transgenic

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rootstock is another innovative strategy that could be exploited for resistance, and would have fewer biosafety concerns (Lemgo et al. 2013; Sidorova et al. 2018). This approach produces non-transgenic fruit and ensures the overall resistance to virus infection by transgenic RNAi inducing genetically modified (GM) rootstock. The success depends on the plant species, the expression and the interactions of the small interfering RNA (siRNA) with the target gene (Limera et al. 2017). It has been reported that the movement of transgene-derived siRNAs signals from the GM cherry rootstocks to the non-GM scions in grafted trees was effective in inducing protection against PNRSV, a minor apple virus (Chandel et al. 2008; Zhao et al. 2014). However, the silencing signal movement from transgenic rootstock to non-transgenic scion in apples was not observed (Flachowsky et al. 2012). More trials for rootstock-to-scion delivery are required to ascertain the efficiency of the trans-grafting technology for individual species. New and improved methods for stable genetic transformation in Malus need to be standardized.

1.7 Genome Editing—A New Means for Crop Improvement and Development of Resistance For the crop improvement, targeted genome engineering has emerged as favorite alternate than classical breeding. CRISPR (Clustered regularly interspaced palindromic repeat)/Cas9 gene editing tool has been exploited for mutation, repression, activation and epigenome editing in the plants/protoplast system of Arabidopsis, tomato, rice, tobacco, maize, poplar, Citrus, petunia and grape (Jiang et al. 2013; Wang et al. 2014; Subburaj et al. 2016). As fruit trees have longer breeding cycles, production of varieties with desired traits requires lots of efforts. Most of the fruit trees are produced by clonal propagation and specific traits transfer via backcross breeding is difficult (Nishitani et al. 2016). Therefore, mutants can be generated directly via genome editing and desired traits can be introgressed into elite lines without any compromise with other properties. The wild species of cultivated crops with unique traits also acts as potential candidates for genome editing (Xu et al. 2019). Erwinia amylovora causes fire blight in apple and many other commercial important plants of Rosaceae family. Candidate genes have been identified for generating resistance against fire blight through genetic engineering but due to regulation hurdles till now no resistant GM plants have been developed. DIPM gene family show interaction with effector protein DspA/E of E. amylovora and act as fire blight susceptibility genes and their inactivation can help to generate tolerance (BorejszaWysocka et al. 2004, 2006; Pompili et al. 2020; Tegtmeier et al. 2020). DIPMs (DspA/E-interacting proteins from Malus) gene family is encoded by four genes (DIPM 1–4) and show close matching to transmembrane LRR receptor-like kinases. They express in young shoots and except DIPM1, others show induction upon E. amylovora infection (Meng et al. 2006). A recent study demonstrated the targeted

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mutagenesis of DIPM-1, 2 and 4 in the protoplast of apple cultivar GD using CRISPRribonucleoprotein (RNP) (Malnoy et al. 2016). Osakabe et al. (2018) developed a protocol for the genome editing to alter the traits of interest via plasmid mediated as well as direct delivery of CRISPR-Cas9 (CRISPR-associated protein 9) ribonucleoproteins in the apple protoplast. Pompili et al. (2020) also demonstrated the use of CRISPR/Cas9-system for the development of genome edited apple plants against fire blight with reduced susceptibility by targeting MdDIPM4. The edited plants displayed 75% editing efficiency. Recently, Zhang et al. (2021) successfully demonstrated the use of CRISPR/Cas9 system for the genome editing in wild apple (Malus sieversii) by targeting MsPDS gene. Mildew-resistance locus O (MLO) have been identified against powdery mildew resistance in 1940s. Podosphaera leucotricha causes the powdery mildew in apple (Turecheck 2004) and MLO19 gene have been reported to generate resistance against disease (Pessina et al. 2017) but it needs to be investigated by CRISPR/Cas9 technology. The knowledge obtained from above studies can help to overcome challenges and utilize this technique to target the various susceptibility factors.

1.8 Conclusion There is a need to collate widespread information on apple origin, dispersal, and cultivars; germplasm resources; molecular markers, QTL analysis and physical mapping; transposable elements and transcription factors; whole genome sequencing; molecular databases, transcriptome analysis; small RNA databases, expressed sequence tags, gene editing and trait dissection; gene prediction and characterization etc. to identify the challenges and to generate opportunities for genetic improvement of the apple. Developing pathogen resistance in apple is area white space where various biotechnological tools like CRISPR-Cas9 system can decrease the laborious and time-consuming aspects. However, the foremost need is to characterize and annotate the available molecular data followed by validation of the functional aspect using wet lab experiments and on-field trials. This is CSIR-IHBT publication number.

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Visser T, Verhaegh JJ (1979) Resistance to powdery mildew (Podosphaera leucotricha) of apple seedlings growing under glasshouse and nursery conditions. In: Proceedings of Eucarpia fruit section symposium, tree fruit breeding. Angers, France, pp 111–120 Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32(9):947–951 Xu J, Hua K, Lang Z (2019) Genome editing for horticultural crop improvement. Hortic Res 6(1):1–16 Xu M, Korban SS (2004) Somatic variation plays a key role in the evolution of the Vf gene family residing in the Vf locus that confers resistance to apple scab disease. Mol Phylogenet Evol 32(1):57–65 Xu M, Korban SS (2002) A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162(4):1995–2006 Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280(3):187–198 Yoder KS (2000) Effect of powdery mildew on apple yield and economic benefits of its management in Virginia. Plant Dis 84(11):1171–1176 Zhang Q, Li Y, Zhang Y, Wu C, Wang S, Hao L, Wang S, Li T (2017) Md-miR156ab and MdmiR395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Front Plant Sci 8:526 Zhang Y, Zhou P, Bozorov TA, Zhang D (2021) Application of CRISPR/Cas9 technology in wild apple (Malus sieverii) for paired sites gene editing. Plant Methods 17(1):1–9 Zheng Z, Nonomura T, Bóka K, Matsuda Y, Visser RG, Toyoda H, Kiss L, Bai Y (2013) Detection and quantification of Leveillula taurica growth in pepper leaves. Phytopathology 103(6):623–632

Chapter 2

Genomic Designing for Biotic Stress Resistant Banana S. Backiyarani, C. Anuradha, and S. Uma

2.1 Introduction Banana (Musa spp.), one of the most important fruit crops, is a widely consumed fruit for its flavor, nutritional value, and availability throughout the year. It is a staple food in many developing countries as well as an important cash crop for export. Based on the purpose of consumption, bananas are classified as dessert and cooking bananas or plantains. All the parts of banana plant such as the corm, roots, pseudostem, leaves, leaf sheath, inflorescence and fruits are used for human needs and also as cattle feed. It is considered as a perfect functional food as it contains important health benefitting bioactive compounds such as flavonoids, carotenoids, phenolics, sterols, antimicrobial compounds and also a major source of potassium, resistant starch and total dietary fibers. As it contains fructo-oligosaccharides, inulin (oligosaccharides), catechin, epicatechin, epigallocatechin, and gallic acid (polyphenols), it has high nutraceutical values and intake of the fruits results in the prevention of muscular contractions and colon cancer, regulation of blood pressure, and in the cure of intestinal disorders. Banana needs a uniform warm and rainy climate year round and is grown in the tropical and subtropical regions. South East Asia, especially from Assam (India) to the Western Pacific is considered to be the center of origin of bananas (Horry et al. 1997) and now cultivated throughout the tropics and in selected areas in the subtropical regions of South Africa, Brazil, India, China, Spain, Israel, Australia, the Caribbean and Latin America. It is one of the top ten crops globally in area and

S. Backiyarani (B) · C. Anuradha · S. Uma ICAR-National Research Centre for Banana, Thogamalai Road, Thayanur Post, Tiruchirappalli, Tamil Nadu 620 102, India e-mail: [email protected] S. Uma e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_2

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contributes 37% of total fruit production. The annual production of banana is approximately 116 million tons (http://www.fao.org/) with an approximate value of 31 billion USD from 5.6 million hectares of land, of which 26 million tons are exported annually (International Trade Statistics 2019). The international banana trade of more than USD 45 billion has a huge impact on the economy of many countries (FAO 2019). Among the continents, 60% of the global production is contributed by Asia. A changing climate since 1961 has increased the annual banana production with an average of 1.37 tons/ha (Varma and Bebber 2019). It is also expected that by 2070 land suitable for bananas will increase by 50% as the annual temperature increases by 3 °C (Calberto et al. 2015). But, by 2050, 50% yield reduction is predicted owing to climate change which resulted in increase in spread of pest and diseases as the result of change in the distribution, population dynamics and development of new isolates/strains/races. It is estimated that the impact of climate change causes severe spread of black sigatoka leaf disease which results in an average 3% reduction in global annual production, i.e., a loss of yearly revenue of about USD 1.6 billion (Strobl and Mohan 2020). In recent past, mono-culturing of Cavendish types, which is occupying more than 60% banana growing area, favors various pests, resulting in higher pesticide usage and rapid evolution of pests. This emphasizes the cultivation of diverse varieties to overcome the problems of pest and diseases. The list of pest and diseases that affects the banana production is given in Tables 2.1 and 2.2. Being a vegetatively propagated crop, clonal variation, occurring at an average frequency of 6%, can be exploited to develop new resistant varieties (Deepthi 2018) but, the possibility of reverting back to their original phenotype within 2–3 vegetative propogations limit their exploitation (Biswas et al. 2009). The naturally available genetic resources harboring resistant genes can be used in many genetic backgrounds through conventional and/or non-conventional breeding approaches. But reproductive barriers such as female and male sterility, poor germination percentage limit the development of many recombinant events through conventional breeding approaches in developing resistant varieties. In spite of the fertility constraints, hybridization was first attempted to improve Fusarium wilt resistance in the commercial triploid variety (Shepherd 1974). Later, attempts have been made to develop triploids by crossing the fertile tetraploid with diploid (Tenkouano and Swennen 2004). Though the yield potential of newly developed hybrids are high, the success of banana breeding in terms of reaching the farming community is very limited owing to lesser acceptance by the consumers as it is not possible to incorporate the specific trait alone in the desirable background (Dzomeku et al. 2007). The gene modification techniques open up new avenues to improve the desirable trait without changing the background of commercial cultivars. But unlike other seeded crops, elimination of T-DNA and selectable markers from the transgenic plant is tedious in this polyploid crop. The recent genome editing techniques (e.g. CRISPR/Cas9) are the possible approach that has tremendous opportunities to improve the polyploid, parthenocarpic and vegetative crop like banana.

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Table.2.1 Major pest and diseases of banana Name of the disease/pest Causal organism

% yield loss

References

Fungal diseases Fusarium wilt

Fusarium oxysporum f.sp cubense (Foc)

100

Thangavelu et al. (2020)

Black sigatoka

Pseudocercospora fijiensis

33–76

Eric and Mohan (2020)

Yellow sigatoka

P. musicola

50

Musa fact sheet, INIBAP

Septoria leaf spot

P. eumusae

20–50

Crous and Mourichon (2002)

Erwinia carotovora, E. chrysanthemi

100

Ambachew Zerfu Geberewold (2019)

Bunchy top disease

Banana bunchy top virus

70–90

Kumar et al. (2015)

Banana streak disease

Banana streak virus

6–15

Daniells et al. (2001)

Bract mosaic disease

Banana bract mosaic virus

30–70

Selvarajan and Jeyabaskaran (2006)

Mosaic / Heart rot

Cucumber mosaic virus

40

Yohanis Kebede and Majumder (2020)

Odiporus longicollis

10–90

Padmanaban et al. (2020)

Corm Weevil

Cosmopolites sordidus

42

Gold et al. (2005)

Banana skipper

Erionota torus

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www.pestnet.org/ fact_sheets

Fruit and leaf scarring beetles

Basilepta spp.

12–96

Choudhary et al. (2010)

Burrowing nematode

Radopholus similis

31–41

Nair (1979)

Spiral nematode

Helicotylenchus multicinctus

30–60

Davide (1995)

Root lesion nematode

Pratylenchus spp.

44

Sundararaju and Cannayane (2003)

Root knot nematodes

Meloidogyne spp.

57

Musa pest fact sheet, INIBAP

Bacterial diseases Rhizome rot Viral diseases

Insect Pests Pseudostem Weevil

Nematodes

2.2 Descriptions on Different Biotic Stresses The occurrence, distribution, causal organism, symptoms and favorable conditions for pest/disease development, spread and crop losses of the major fungal, bacterial,

28 Table.2.2 Minor diseases and pests of banana

S. Backiyarani et al. Disease/pest

Scientific name

Tip over or rhizome rot

Erwinia caratovora

Anthracnose

Colletotrichum musarum

Crown rot

C. musae, Fusarium spp. and Botryodiplodia theobromae

Cigar end rot

Verticilium theobromae, V. staphylidium, Trachysphaera

Botryodiplodia black tip disease

B.theobromoece

Pitting disease

Pyricularia grisea

Peduncle rot

C. gloeosporioides and B. theobromae

Deightoniella leaf and Fruit spot

Deightoniella torulosa (Syd.)

Bacterial wilt

Pseudomonas solanacearum (race 1)

Blood disease

Ralstonia syzigii subsp. celebensis

Bugtok

Ralstonia solanacearum (race 2)

Finger tip rot (gumming)

Pseudomonas spp.

Moko

R.solanacearum (race 2)

Rhizome rot

E. carotovora, E. chrysanthemi

Javanese vascular wilt

Pseudomonas spp.

Xanthomonas wilt (BXW)/Banana bacterial wilt/enset wilt,

Xanthomonas campestris pv. musacearum

Small banana weevil

Polytus mellerborgii

Aphids

Pentalonia nigronervosa f. typica

Banana flower thrips

Thrips hawaiiensis

Banana leaf thrips

Helionothrips kadaliphilus

Banana lacewing bug

Stephanitis typical

Banana silvering thrips

Hercinothrips bicinctus

Root mealybug

Geococcus sp. nr. johorensis

Fruit mealybug,

Rastrococcus iceryoides

Spiralling whitefly

Aleurodicus disperses

Rugose spiralling whitefly

A. rugioperculatus

Leaf caterpillar

Spodoptera litura

Fall armyworm

S. frugiperda

Banana bagworm

Kophene cuprea

Hairy caterpillar

Olepa ricini (continued)

2 Genomic Designing for Biotic Stress Resistant Banana Table.2.2 (continued)

Disease/pest

29 Scientific name

Spider mite

Oligonychus indicus

Hairy caterpillar

Olene mendosa

Red spider mites

Tetranychus spp.

Oriental red mite

Eutetranychus orientalis

Red mite

Raoiella indica

viral diseases, pest and (Include, after viral disease) occurring in banana are described below.

2.2.1 Panama Wilt of Banana/Fusarium Wilt Fusarium wilt (FW), a soil-borne pathogen, caused by Foc was first reported in Australia (Bancroft 1876; Ploetz and Pegg 1997). Based on the pathogenicity to reference host cultivars Foc is classified in to four races. Race 1 (R1) affects Gros Michel (AAA) and Manzano/Apple/Latundan (Silk, AAB); race 2 (R2) affects cooking bananas of the Bluggoe (ABB) subgroup and race 4 (R4) is pathogenic to all cultivars in the Cavendish (AAA) subgroup in addition to those susceptible to R1 and R2 (Stover et al. 1961; Su 1986). Race 4 is further divided into two sub groups: tropical (TR4) and subtropical (STR4) race 4. Foc STR4 isolates cause disease under subtropical conditions in Cavendish cultivars, whereas FocTR4 isolates attack Cavendish under both tropical and subtropical conditions (Buddenhagen 2009). Race 3 infect only Heliconia spp., hence it is no longer considered as part of Foc (Ploetz 2005). FW spread through the infected planting material, contaminated soil, surface irrigation, root-pathogens like nematodes, farm implements and machinery, host weed species. The fungus enters into the root system and invades via water conducting tissues of the corm and pseudostem. The pathogen develops in the vascular system of the host plant by producing numerous micro, macro conidia and chalmydospores. FW, a typical vascular disease, causes systemic foliage symptoms, by disturbances of translocation which eventually lead to collapse of the crown and pseudostem. The symptom appears around 5th to 8th month after planting as a premature yellowing of the oldest leaves followed by necrosis. Typically, diseased plants have few erect leaves with an increasing number hanging down beside the pseudostem. The unfurled heartleaf dies and only the pseudostem remains standing, which also collapse, in due course. When an infected plants’ pseudostem and rhizome are cut longitudinally the vascular tissue shows reddish to purplish brown discoloration. Pseudostem splitting at the base is a common symptom in Rasthali, Karpuravalli and Ney Poovan. In Monthan, conspicuous bright orange color of older leaves is observed in severely affected plants. The affected plant will not yield bunch, however if the infection starts at the later stage of the crop, it throw bunch, but there will not be any bunch development.

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This disease is being managed by various management strategies such as floodfallowing, application of organic amendments, planting of resistant banana varieties, crop rotation, fungicidal treatment, use of disinfected farm implements and soil fumigation. Usage of fungicides such as cyproconazole, propiconazole prochloraz, benomyl, carbendazim and thiabendazole showed disease reduction up to 80% and at present the carbendazim is widely used for managing this disease. Usage of antagonistic microbes such as Bacillus strain KY-21 (Sun et al. 2010) and biocontrol agents such as Pseudomonas spp, endophytes and Trichoderma spp. strains have been used to control Foc. Lower biocontrol efficacy has also been obtained with arbuscular mycorrhizal fungi, Bacillus spp., and non-pathogenic Fusarium strains (Bubici et al. 2019).

2.2.2 Leaf Spot Disease Banana leaf spot diseases are the second most devastating disease, caused by P. fijiensis (black Sigatoka), P. musicola (yellow Sigatoka) and P. eumusae (eumusae leaf spot) (Marin et al. 2003; Cordeiro et al. 2004; Conde-Ferráez et al. 2007). Black Sigatoka develops more rapidly and causes more damage which makes it more difficult to control (Simmonds 1986; Johanson and Jeger 1993). Black and yellow Sigatoka can cause indistinguishable symptoms depending on the cultivar infected, stage of the disease and season (Johanson and Jeger 1993). The symptoms appear as dark brown specks on the lower surface of the leaf and causes reddish-brown streaks running parallel to the leaf veins, which aggregate to form larger, dark-brown to black compound streaks. These streaks eventually form uniform or elliptical lesions which merge to cause extensive leaf necrosis. Adjacent tissue often has a water-soaked appearance, especially under conditions of high humidity. This disease decreases the photosynthetic capacity of leaves, causing a reduction in the quantity and quality of fruits, and inducing the premature ripening (Stover and Simmonds 1987). In case of black Sigatoka, conidiophores are formed singly or in small groups (2–5) on lower leaf surface and the conidiophores are straight or bent, 0–3 septate and occasionally branched, slightly thickened spore scars. The conidia are tapered from base to apex with 1–6 septate and a distinct basal scar. In yellow Sigatoka, conidiophores are formed in dense clusters (sporodochia) on both the leaf surfaces. The conidiophores are straight, usually non-septate and unbranched, no spore scars. Sigatoka leaf spot on bananas decreases somewhat during the dry season but otherwise produces more or less continuously repeated cycles of infection. Monocropping of banana for long time and planting banana round the year may lead to leaf spot incidence in the region. This disease can be managed by timely removal of weeds and suckers, and burning of affected leaves. Waterlogging and closer spacing should be avoided. Management of Sigatoka complex in general is currently almost completely dependent on frequent (weekly) fungicide treatments throughout the growing season.

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Spraying of carbendazim, propicanozole or mancozeb, dithiocarbamates, benzimidazoles, azoles and strobilurins and teepol (sticking agent) three times at 10–15 days interval with the appearance of the leaf spot will reduce the spread of the disease.

2.2.3 Viral Diseases There are about 20 viruses infecting banana globally, of which four viruses namely Banana bunchy top virus (BBTV, genus Babuvirus, family Nanoviridae), Banana streak virus (BSV, genus Badnavirus, family Caulimoviridae), Banana bract mosaic virus (BBrMV, genus Potyvirus, family Potyviridae) and Cucumber mosaic virus (CMV, genus Cucumovirus, family Bromoviridae) are the most significant. Among them, BSV, BBrMV, and CMV are known to occur in all banana producing countries, whereas BBTV spread is limited to a few countries.

2.2.3.1

Banana Bunchy Top Disease (BBTD)

BBTD, caused by Banana bunchy top virus BBTV, is the most important viral disease responsible for the significant adverse economic impact on banana production. It is a single-stranded DNA (ssDNA) virus with a multipartite genome comprising of six circular components with an approximate size of 1.1 kb each (Harding et al. 1993; Burns et al. 1995). The six components, named DNA-R, -U3, -S, -M, -C, and -N (previously known as DNA 1–6), are encapsulated within separate virions, each about 18–20 nm in diameter (Harding et al. 1993). BBTV is transmitted by the banana aphid (Pentalonia nigronervosa) and infected planting materials. Fruit production in infected plants reduces by 70–100% within one season, and plantations cannot be recovered from infections. The affected plants show intermittent dark green dots, dash, streaks of variable length like ‘Morse code’ pattern on leaf sheath, midrib, leaf veins and petioles of infected plants. Leaves produced are progressively shorter, brittle in texture, narrow and gives the appearance of bunchyness at the top. In case of late infection plant can throw bunch but the fingers will not develop. Fruits of infected plants are malformed.

2.2.3.2

Banana Streak Disease

Banana streak virus (BSV) disease, the most widely distributed disease, is caused by a pararetrovirus. BSV is a bacilliform double-stranded DNA (dsDNA) virus with a monopartite genome of 7–8 Kb long with three open reading frames (ORFs). It occurs in the replicative form in the cell known as episomal form and the one which is integrated in the genome is called as endogenous forms (Harper et al. 1999). Multiple copies of episomal form of BSV (eBSV) sequences are integrated as direct and inverted tandem repeats at a single locus in the host B genome (Chabannes and Iskra-Caruana 2013). The integrated form of eBSV remains dormant and develops

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no symptom. Environmental stress, micro-propagation, and interspecific crossing trigger the integrated eBSV to form episomal infectious viral particles, leading to disease symptoms in banana (Tripathi et al. 2019). The most characteristic symptoms of BSV disease are chlorotic and necrotic streaks on leaves, later it extends to form long streaks. The chlorotic streaks become necrotic giving a blackish appearance on lamina (Selvarajan et al. 2011). Necrotic streaks are also observed on midrib, petiole and pseudostem. Bunch choking, abortion of bunch and seediness in fingers are observed in infected plants. It is transmitted through mealybugs or through the use of infected planting materials, but the epidemics mostly occur due to the activation of eBSV. Control of BSV is difficult due to genomic integration and clonal propagation.

2.2.3.3

Banana Bract Mosaic Disease (BBrMD)

BBrMD caused by banana bract mosaic virus (BBrMV) has flexuous filamentous particles (660–760 × 12 nm) with a single stranded positive sense RNA genome (Balasubramanian and Selvarajan 2012). The infected plants show distinct, dark coloured, broad streaks on the bracts of the inflorescence; necrotic streaks on fingers, leaf, pseudostem and mid rib; bunches are unusually very long or very short peduncle, chocking of bunches, raised corky growth on peduncle (Selvarajan and Jeyabaskaran 2006). Dark red to purple mosaic streaks will be observed on the pseudostem after the removal of leaf sheath but, deep pigmentation will be there in the newly emerging suckers. Foliar symptoms appeared as chlorotic streaks parallel to veins and petioles. BBrMV is primarily transmitted through planting materials and non–persistently transmitted through several aphid species viz., P.nigronervosa, Rhopalosiphum maidis, Aphis gossypii and A. craccivora (Magnaye and Espino 1990; Munez 1992; Selvarajan and Jeyabaskaran 2006).

2.2.3.4

Banana Mosaic Disease

Banana mosaic caused by Cucumber mosaic virus (CMV) is one of the common viral diseases affecting the bananas and plantains and occurs throughout the world (Lockhart and Jones 2000). CMV is a positive-sense RNA virus with a tripartite genome infecting many plant species. Banana mosaic or infectious chlorosis is characterized by a range of symptoms from diffused foliar mosaic severe chlorosis, chlorotic streaking or flecking, stripes, line patterns, ring spots, leaf curling, distortion, rosette appearance of leaf arrangement to stunting of plant. Symptoms have often been confused with those of BSV, as happen with BSV infection in banana, CMV infected plant also show symptoms sporadically on few leaves. Primarily this virus is transmitted through infected suckers and it is also acquired from a wide range of host plants growing near banana fields through aphid vectors. The aphids, A. gossypii, A.craccivora, R. maidis, R. purnifolia, Myzus persicae and Macrosiphum pisi have been reported to carry and spread this virus disease (Magee 1940; Capoor and Varma 1968; Mali and Rajagore 1980; Rao 1980). Depending upon the virus strain and

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temperature the symptom will change. In some varieties, high temperature may suppress symptoms and it will be more severe when temperature falls below 24 ºC. All the viral diseases combat by identifying and killing the infected plants by injecting either Fernoxone 80WP (2, 4-D) or Gramaxone 20 EC and eradicating the affected mats. Planting of virus indexed tissue cultured plants is the best approach. Removal of alternate hosts, weeds and unwanted suckers reduce the aphid population. Injection or foliar application of systemic insecticides like monocrotophos or methyl dematon and imidacloprid reduce the vector population. Doubling the fertilizer dose has found to compensate the yield loss (Selvarajan and Balasubramanian 2008).

2.2.4 Nematodes More than 150 species of nematodes belonging to 54 genera are reported to be associated with banana. Important nematode species causing economic damage are burrowing nematode (Radopholus similis); root-lesion nematodes (P. coffeae; P. thornei and P. brachyurus); root-knot nematodes (M. incognita and M. javanica); spiral nematodes (H. multicinctus and H. dihystera). In case of burrowing nematode initial damage is on roots as small dark purplish-red lesions, it also enters the corms and causes reddish brown cortical lesions which are characteristic feature of the disease. These symptoms result in retarded growth, leaf yellowing and falling of mature plants. Lesion nematode symptom is similar to burrowing nematode and in severe case the cortical region of the root is completely damaged and turns black in colour. Spiral nematode feeds on the cortical cells close to the epidermis, root lesions are relatively shallow and superficial necrotic lesions on banana roots and corms. The infected plant root and corm are reddish brown/ black in colour. Existence of synergistic interaction among root-lesion and root-knot nematodes and Fusarium wilt pathogen and aggravation of wilt disease in association with nematodes were also reported (Sundararaju and Thangavelu 2009). Various nematode management measures were developed using cultural, physical, biological, host plant resistance and chemical means. Prevention of transportation of suckers from infested fields to newer areas through quarantine measures is the best prophylactic measure. Hot water treatment of suckers is a simple and economic prophylactic measure. Management of nematodes by cultural means such as crop rotation / fallowing are promising technique as they are simple, easy to adopt and economic. Organic amendments such as green manures, cakes of various oilseeds are effective in managing nematodes. Biocontrol agents such as Pochonia chlamydosporia, Purpureocillium lilacinum (Paecilomyces lilacinus), Trichoderma spp., Bacillus spp. etc. are promising in nematode management. Chemical nematicides are excellent option to manage the nematodes as they are effective in killing nematode population present in both soil and root system (Fogain 2000).

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2.2.5 Insect Pests 2.2.5.1

Banana Corm Weevil

Corm weevil, C. sordidus is distributed in all banana growing areas and affects both desert and plantains. Both the grubs and the larvae bore into the corm and form tunnels. The female weevil lays 1–3 eggs near the corm just above the ground level and they hatch in 5–7 days. The grubs emerge and enter the corm, after 20 days they form oval chambers and pupate near the corm surface and adults emerge after 8 days. The adults are 12 mm long, reddish brown color and later turn into black. The weevils live up to 2 years. The larvae cause rot and arrest the flow of the nutrients and the leaf appears unhealthy. The suckers will wither and die and they will topple easily. The infected plants produces small bunches of undersize fruit. Before planting, the material should be checked carefully for the presence of any weevils, ideal is to use tissue culture plants. Hot water treatment of the corm for the control of nematode will likely destroy the weevil eggs and grubs. Chlorpyrifos, fipronil, bifenthrin and imidacloprid can be used for the control of this pest. An aggregation pheromone (sordidin) that attracts both sexes is available and used for monitoring (4 traps/ha) and mass trapping (20 traps/ha).

2.2.5.2

Banana Pseudostem Weevil

O. longicollis adult lives for one year and its pre-oviposition period is 15–30 days. Upto nine eggs are laid at the rate of one egg per day. Oviposition takes place only in the leaf sheaths and the incubation period ranges from 3 to 8 days. The emerging larvae are fleshy, yellowish white and apodous. The larvae feed on tissues of the succulent sheath by tunnelling extensively and reach the true stem. The depth of the tunnels made by the larvae ranges from 8 to 10 cm. The tunnels are widespread and may go as high as the fruit peduncle or to the lowermost collar region near the rhizome. Infestation of the weevil normally starts in 5-month-old plants. Early symptoms of the infestation are the presence of small pinhead-sized holes on the stem, fibrous extrusions from bases of leaf petioles, adult weevils and exudation of a gummy substance from the holes on the pseudostem. Rotting occurs due to secondary infection of pathogens and a foul odour is emitted. Stem weevil infestation interferes with the translocation of nutrients and water, retards growth and development and increases susceptibility to wind lodging, which is more commonly associated with nematode infestation. Stem injection with a systemic organophosphorus compound is extensively used in controlling this pest. Along with stem injection, swabbing with surfactants, mud slurry containing the candidate insecticide, spraying and fumigation of the spaces between the leaf sheaths in the pseudostem are carried out to manage this pest. Field sanitation is imperative in the control of this pest. Dried old leaves must be removed to allow the detection of early symptoms of weevil infestation and to increase the efficacy of chemical application. Banana stumps kept in the field

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after harvest must be removed and destroyed as they serve as weevil refuges and breeding site. Two species of earwigs feeding on larvae and pupae are reported from China. There is a report of an acarid mite parasitizing larvae and adults. Release of an ectoparasitic mite, Uropodia sp. on adult had been tried for its control with limited success. Metarhizium anisopliae, an entomopathogenic fungus, causes more than 90% mortality.

2.2.5.3

Scarring Beetle

Besides weevils, leaf and fruit and scarring beetles are major seasonal pests of bananas and plantains in many states of northern, eastern, and northeastern India, Bangladesh, and parts of Southeast Asia (Prathapan et al. 2019). The extent of damage to banana bunches by this pest has been estimated at 30% (Ahmad et al. 2003) and 11.47–95.68% (Choudhary et al. 2010) in Bihar, north India respectively and is as high as 80% in Assam, northeastern India in the rainy and post-rainy seasons. M. sapientum and M. acuminata are principal hosts and ginger, Canna indica L., taro and turmeric are other hosts (Prathapan et al. 2019). The adult beetles are most active during the monsoon and post-monsoon seasons and summer. They are nocturnal and usually found hiding inside the leaf whorls and come out only when disturbed. They feed on the young unfurled leaves, leaf petioles and stems of banana and the emerging leaves are badly scarred. Feeding damage was also observed on flowers and bracts, as well as young, developing fruits. In severe cases, the developing bunches and fruits are so badly scarred that they lose their market value. Eggs are laid in the soil and the larvae feed on the roots of grasses and other weeds. Pupation takes place in the soil. Emerging adults feed on young leaves and fruits. Adults hibernate during winter. In Uttar Pradesh, North India, adults of the predatory beetle, Paederus fuscipes Curtis (Coleoptera, Staphylinidae), were found to be commonly associated with B. subcostata. Natural epizootics of entomofungal pathogens, such as Beauveria bassiana, are commonly observed on B. subcostata in the northeastern region of India and exert some control in the post-monsoon months. Chemical control is not possible as the adult is an active flyer and the larvae are buried in the ground.

2.2.5.4

Banana Skipper

E. thrax, is an emerging important pest in banana. The caterpillars cause damage by shredding the leaves and making numerous rolls on the leaf blade for safe feeding. Eggs are laid in single or in clusters (upto 25) and they are, 2 mm diameter. The eggs hatch in 5–8 days. Caterpillars are pale green with a distinctive shiny black head and grow upto 6 cm. They make their way to the edge of the leaf to feed and to make the characteristic rolls. There are five larval stages and all except the first stage is covered in a white waxy powder; the fact that older caterpillars close their rolls more securely than younger ones, allows them to survive heavy rains. Pupation occurs inside the leaf roll, and takes about 10 days. The moth is brown with three yellow spots on the forewings.

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The egg parasite, Ooencyrtus erionotae, and the larval parasite Apanteles erionotae are used to manage this pest. Heavy rains also bring about death of the young caterpillars, and wind reduces populations by shredding the banana leaves so that the caterpillars cannot make their protective rolls. Neem, derris, pyrethrum or chillies are used along with soap solution as organic control measures. Biopesticides, like spinosad, Bacillus thuringiensis var. kurstaki can be used for controlling this pest.

2.3 Genetic Resources of Resistant Genes The ancestors of the present day seedless commercial cultivars are seeded diploid Musa species. The spontaneous occurrence of structural changes and the recombination in the M.acuminata chromosomes resulted in the development of natural reproductive barriers and broadening its diversity at subspecies level namely M. ac ssp. banksii, M. ac ssp. errans, M. ac ssp. burmannica, M. ac ssp. malaccensis, M. ac ssp. siamea, M. ac ssp. microcarpa, M. ac ssp. truncata and M. ac ssp. zebrina (Jones 2000). The natural intra- and inter-subspecies hybridization of these M. acuminata produced plants with various levels of female sterile fruits. It has been estimated that at least four subspecies of M. acuminata contributed to the origin of cultivated bananas. It is assumed that the cross between the partly sterile edible diploids with fertile plants produced triploid cultivars with high vigor and yield, seedlessness with good fruit quality. Unlike M. acuminata, hardy natured M. balbisiana possesses only less variability (Uma et al. 2005; Wang et al. 2007) and has no such classification at subspecies level (Wang et al. 2008). But it has high potential value in breeding program as it is reported as tolerant to abiotic stresses like drought (Daniells et al. 2001), osmotic and cold stresses (Thomas et al. 1998) and biotic stresses like BBTV (Hapsari and Masrum 2012), FW and leaf spot diseases (Singh et al. 2001). In spite of the broad range of genetic resources, their utilization in breeding program is very limited owing to its inherent problem of male and female sterility, poor seed set, germination and poor survival rate of hybrid progenies. This issue has been addressed by conducting pre-breeding program by hybridizing the diploid accession with the wild species to develop fertile improved progenies having resistant genes. Many reports evidenced that M.balbisiana and M. nagensium are the sources of resistance to drought, M. sikkimensis, M.basjoo and M.thomsonii are resistant to cold and M. itinerans is for waterlogging, and FW (MusaNet 2016; García-Bastidas et al. 2019). M. balbisiana is tolerant to both biotic and abiotic stresses (Uma et al. 2005), M. ac. ssp. zebrina is resistant to race 1 (Arinaitwe et al. 2019). Vakili (1965) reported that M.ac. ssp. malaccensis, M.ac. ssp. burmannica, M.ac. ssp. microcarpa and M.ac. ssp. siamea as the resistant sources for Foc race 1. M. laterita, a resistant source to Foc TR 4, belongs to section Rhodochlamys, is more compatible with section Eumusa (Shepherd 1968) and also being used as one of the male parents for transferring the resistant genes to the edible banana cultivars through introgression. Based on the in vitro and field screening of wild banana species against Foc-TR4

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wild relatives M. basjoo and M. itinerans were found to be highly resistant whereas M. nagensium, M. ruiliensis, M. velutina and M. yunnanensis showed some degree of infection against Foc TR 4 in the greenhouse but they were found to be resistant in the field (Li et al. 2014). Some of the wild Musa species, such as M. ac. ssp. burmanicca, malaccensis, and siamea are found to be resistant to black Sigatoka (Jones 2000). Two wild accessions Tuu Gia and Birmanie were found to be resistant to P. fijiensis (Ortiz-Vázquez et al. 2005; Rebouças et al. 2018; Nascimento et al. 2020) whereas M.ac. ssp. malaccensis and M.ac. ssp. microcarpa are considered under moderately resistant category (Nascimento et al. 2020). M.ac. ssp. burmaniccoides (Calcutta 4), is considered as one of the best multiple resistant source to many biotic stresses namely Foc, corm weevil and nematodes and being used in resistant breeding programme (Thangavelu et al. 2020). Integration of eBSV in the M.balbisiana accessions restricted its utilization in interspecific breeding program. To exploit the breeding potential of M.balbisiana, research activities are being carried out at global level for developing B genome accessions devoid of eBSV either through selfing and/or double haploid lines (https:// agritrop.cirad.fr/561237/) or inactivating the eBSV through genome editing (Tripathi et al. 2019). List of primary, secondary and tertiary resistant sources are given in Table 2.3.

2.4 Glimpses on Classical Genetics and Traditional Breeding Genetic improvement of banana is mainly focused on creating hybrids with good agronomic traits such as high yield with resistance/tolerance to biotic (FW, bacterial wilt, leaf spot disease, pseudo stem weevil, nematodes) and abiotic stresses (drought, cold, high temperature). Viral diseases caused by BSV, CMV, BBrMV and BBTV are also receiving increased attention (Kumar et al. 2015). Next to this, other desirable traits like, short duration, dwarf, fruit quality, cylindrical bunches with uniform size fruits, high photosynthetic efficiency (Pillay et al. 2002; Bakry et al. 2009) are the other traits to be improved. To safeguard the dessert banana industry from the devastating disease caused by Foc during 1950s and outbreak of Sigatoka diseases during 1970s forced to focus on banana improvement program to reduce the usage of chemical pesticide. Effort towards developing resistant varieties are being taken in the research centers of banana growing countries (Table 2.4) through identification of resistant cultivars by screening the existing germplasm accessions and, somaclonal variation in the hot spot area, creating genetic diversity through induced mutagenesis, hybridization program and manipulation of genes through overexpression of resistant genes and silencing of susceptibility factors. Buddenhagen (1987) reported that breeder should focus on selection of resistance with high yielding per unit area and time while developing resistant hybrids. Elite hybrid lines should be selected for

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high photosynthetic efficiency, early maturity, and minimum delay between consecutive harvests Eckstein and Robinson (1996). Somaclonal variation existing in the commercial tissue culture plantation can be explored for variability in desirable traits. Though, two Foc TR 4 resistant clones, GCTCV-215-1 and 217 were identified (Hwang 1999), Formosona (GCTCV-218), a Cavendish tissue culture variant was selected for its resistance to Foc TR4 and commercialized by Taiwan Banana Research Institute (TBRI) which eventually rescued the banana industry (Hwang and Ko 2004). More somaclonal variants were identified through in vitro and field selection for various biotic stresses and promising lines are under commercial cultivation. FWresistant somaclonal variants have been developed in Rasthali (Ghag et al. 2014; Table.2.3 Resistant sources of Musa for various biotic stresses Trait

Primary gene pool Secondary gene pool

Fusarium wilt M. ac. ssp. zebrina Foc race 1 ssp. malaccensis, ssp. burmannica, ssp. microcarpa, ssp. siamea, ssp. burmannicoides, M. ac. Assam Wild, M. ac. Arunachal Pradesh, M. balbisiana M. balbisiana (A&N) Pagalapahad wild II Jungle Kela II Jungle Kela I Bhimkol

Red banana, Hatidat Pisang Jari Buaya Cv. Rose, Pisang Berlin Tongat, Kanai bansi Balukpong wild, H-201, Karthobiumtham, Chengalikodan, Nendran, Nedu Nendran, PeddaPacha Williams, Jahaji, Kaveri Sugantham, Cheeni Champa, Karpura Chakkarakeli, Kottavazhai, Terabun Poovan, Soneri, Mottapoovan, Mysorebale Borchampa, Alpon, Ladies Finger, Padathi Ladan Small, Pacha Ladan Pointed, Matti Manohar, Sasrabale Shrimanti, Manjahaji Singapur, Borjahaji

Tertiary gene pool

References

Cavendish cultivars, GCTCV-119 Co-1, H-3 Popoulu, FHIA-01

Thangavelu et al. (2021)

(continued)

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Table.2.3 (continued) Trait

Primary gene pool Secondary gene pool

Tertiary gene pool

References

Foc TR4

M. itinerans M. laterita M. basjoo M. nagensium M. ruiliensis M. velutina M. yunnanensis M. ac.ssp. zebrine M. ac. ssp. burmonicoides M. balbisiana type.Tani M. beccarii M. laterita M. maclayi

GCTCV-215 GCTCV-247 Sk5 mutant FHIA-25 FHIA-21

Zuo et al. (2018) Li et al. (2014)

Igitsiri, Ingagara Inkira, Intokatoke Kazirakwe, Mbwazirume, Akpakpak, Curare enano, Obino l’Ewai, Obubit Ntanga, Orishele False Horn, Pisang Ceylan, Pisang Rajah, CCIRAD930, Tuu Gia, Pisang Lilin NBA, Banksii Maia Oa, Pisang Jari Buaya, Pa, Figue Rose Borneo Microcarpa Pisang Berlin, Khai, Pisang Klutuk Wulung, Blue Java Namwa Khom, Kamaramasenge, Rukumamb, Thap Maeo„ Foconah Poingo Maia, LW 142 Khai Thong Ruang

Black M. Sigatoka Leaf acuminata subsp. spot disease burmanicca, ssp. malaccensis, ssp. Siamea ssp. Microcarpa, ssp. burmaniccoides

Tuu Gia and Birmanie

Banana Most of the M. bunchy top balbisiana virus (BBTV)

Kayinja FHIA-03’ Prata, Gisandugu, Pisang Awak, Saba, Highgate, Gros Michel subgroup

Niyongere et al. (2011)

(continued)

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Table.2.3 (continued) Trait

Primary gene pool Secondary gene pool

Tertiary gene pool

Nematodes Root lesion

M. ac. ssp. burmaniccoides

YKM5, Pisang lilin Hybrid E.A. Karthobiantham, 0322, FHIA 0, Singlal, Sakkarachayna, Malai kali, Manik champa, Madavazhai, Karthobiumtham, Marabale, Karpuravalli Kunnan, Paka, Vennettu kunnan, Burrow cemsa

Vadivelu et al. (1987), Collingborn and Gowen (1997), Sundararaju (2010), Sundararaju and Uma (1998)

Burrowing nematode

M. ac. ssp. burmaniccoides

PJB, YKM5, Pisang mass, Prata enana

Viaene et al. (2003), Suganthagunthalam et al. (2010)

Root knot nematode

M. ac. ssp. burmaniccoides

Pisang Mass, Singlal, Manik champa, Sabri, Wather, Vudu papau

Banana corm weevil

M. ac. ssp. burmaniccoides

Pisang Awak, Bluggoe, Njeru, Muraru, YKM-5, Sannachenkadali Sakkali Senkadali Elacazha Njalipoovan (Padmanaban et al.2001) Long Tavoy (Ortiz et al. 1995)

FHIA03 TMBx612-74 TMB2 × 6142–1 TMB2 × 8075–7 TMB2 × 7197–2 (Kiggundu et al. 2003)

Kiggundu et al. (2003), Musabyimana et al. (2000)

Banana pseudostem weevil

M. ac. ssp. burmaniccoides

–

–

Padmanaban et al. (2020)

SH 3142, 3362, 3648, 3723 SH 2095, 3624, FHIA-01

References

Suganthagunthalam et al. (2010)

Saraswathi et al. 2016) and in Cavendish sub group, TC1-229 (Tang et al. 2000) and TC2-425 (Hwang 2002). Lee et al. (2011) developed a high yielding Foc resistant Cavendish variant, Tai-Chiao No. 5. Similarly Giménez et al. (2001) identified Cavendish variant, Var. CIEN-BTA-03 for yellow Sigatoka resistance. The success of the banana improvement program through conventional breeding approach mainly depends on the seed set and development of enough number of parthenocarpic progenies. Understanding the pollen fertility and its compatibility to

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Table.2.4 Institutes involved in banana genetic improvement program Name of the institute

Place

ICTA—Imperial College of Tropical Agriculture

Trinidad, South America

FHIA—FundaciónHondureña de InvestigaciónAgrícola

Honduras

CIRAD—Centre de Coopération Internationaleen Recherche Agronomique pour le Développement (French Agricultural Research Centre for International Development)

France

CARBAP—Centre Africain de Recherches sur Bananiers et Plantain

Cameroon, Africa

IITA—International Institute for Tropical Agriculture

Nigeria, Africa

IAEA—International Atomic Energy Agency

Austria

EMBRAPA—Empresa Brasileira de Pesquisa Agropecuaria

Brazil, South America

NRCB - National Research Centre for Banana

Tamil Nadu, India

TNAU—Tamil Nadu Agricultural University

Tamil Nadu, India

KAU—Kerala Agricultural University

Kerala, India

TBRI—Taiwan Banana Research Institute

Taiwan

NARO—National Research Organization

Uganda, Africa

CNRA—Centre National de Recherches Agronomiques

Cote d’Ivoire

INIBAP—International Network for Improvement of Banana and Plantains

France, Africa, Asia, and Latin America

INIBAP International Transit Center

KULeuven, Belgium

Bioversity International

Italy

set viable seeds, seed setting behavior, its germination ability in commercial varieties are the major criteria in the banana breeding program. Exploitation of residual female fertility of the commercial varieties gives scope for hybridization approach. Many triploid and diploid commercial varieties of AAA (Gros Michel, Red banana, Manoranjitham), AAB (Plantains-Nendran), ABB (Blugo, Pisang Awak) and AB (Kunnan) genome were found to seed set upon artificial pollination, while some of AAA (Cavendish type-Grand Naine) and AB (Ney Poovan) genome are female sterile. Among the seeded accessions of AA genome, Calcutta 4 is highly polleniferous with resistance to sigatoka leaf spot, nematodes and FW. The parthenocarpic AA polleniferous diploid accessions such as Pisang Lilin (resistant to Sigatoka leaf spot) and cv. Rose (resistant to Foc and nematodes) are being used as universal male parents in banana resistance breeding program. Tjau Lagada, a moderate female and male fertile accession, is categorized as incomplete resistance to sigatoka leaf spot and used in diploid breeding.

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Tenkouano et al. (1998) reported that most of the economic important traits are inherited from the diploid parents than triploid or tetraploid parents. The limited source of polleniferous resistant natural diploids hinders the selection of compatible male parents for improving commercial varieties. Broadening the genetic base of the diploid genome by incorporating the resistant traits and / or more than two economically important traits will favour the banana breeding program. This emphasised that development of diploid stocks in various genetic backgrounds becomes imperative in banana breeding. Intermediate diploid accessions belonging to different M. acuminata subspecies have to be developed to diversify and broaden the resistance base as pre- breeding materials. Calcutta 4, morpho-taxonomically close to plantain banana, is used at IITA as one of the diploid resistant source to improve plantains which resulted in development of plantain-derived diploids, TMP2 × −Tropical Musa plantain-derived diploid series (Vuylsteke and Ortiz 1995) and it also focus on the production of banana diploid series [TMB2 × −Tropical Musa banana-derived diploid). By crossing among the diploid accessions the resistant genes present in the different background are being stocked in the improved diploid banana hybrids and being used as breeding stocks. Tenkouano et al. (2003) developed promising diploid stocks ‘TMB2 × 5105–1’·and ‘TMB2 × 9128–3’·are now routinely used as progenitors in IITA crossing programs to generate superior secondary triploid or diploid stocks. ICAR-NRCB has also developed many polleniferous diploids under various genetic background with resistant to Foc race 1, nematodes e.g. Progeny No. 207 (Matti × cv. Rose), Progeny No. 429 (cv. Rose × Pisang Lilin) etc. are used in resistant breeding program. The occurrence of chromosomal imbalances during meiosis resulted in production of n, 2n and 3n gametes in triploid bananas make it possible to develop progenies with various ploidy. In banana breeding program, developing tetraploid is the foremost important step to breed resistant triploid accessions. The tetraploid can be developed by crossing the triploid accessions which need to be improved with the diploid resistant accessions through the fusion of unreduced and reduced gametes of female and male parent, respectively. These tetraploids are generally inferior in fruit quality with male and female fertility along with resistance. Through this approach, many tetraploids (BITA03, PITA14) and triploids (PITA16, −21, 23) with improved traits have been developed at IITA. ICAR-NRCB has developed 16 Pisang Awak based tetraploids of which two were found to be resistant to Foc race 1 with average yield and these promising hybrids are being used in breeding program to improve their yield traits.

2.5 Brief on Diversity Analysis Conservation and utilization of Musa genetic diversity are the important criteria for the sustainable banana production. This genetic diversity includes wild species, native landraces, elite cultivars, released varieties and breeding materials. Nearly 70–85% of the gene pool of the domesticated banana is available in Asia and the Pacific regions.

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Banana and plantains belong to the genus Musa under the family Musaceae. The genus Musa includes four sections—Callimusa, Rhodochlamys, Australimusa and Eumusa. The major diversity and distribution of the genus Musa lies in the South East Asia, except for Australimusa. Of which, most of the edible bananas are coming under the section Eumusa and rarely under the section Australimusa. Callimusa constitutes non-domesticated and wild species and is found in Indo-China and Indonesia and its utilization is limited to its ornamental values. Species belonging to Rhodochlamys section are mostly ornamental with small plant size erect to semi-erect bright colour inflorescences and are distributed in India, Indo-China, the Philippines, Thailand and Malaysia (Horry 2000; Valmayor 2000). The major regions of diversity, distribution and commercial utilization of Australimusa are the Philippines and Australia. Musa textilis and Musa Fehi belong to the section Australimusa and is present in the Philippines which is used in the commercial production of textile fibres whereas the later is grown for its edible fruits in south pacific and Indonesia. The section Eumusa has ten species and distributed in India, South East Asia, Papua New Guinea, to South Pacific and Japan. M. acuminata and M. balbisiana are two very wide spread species across the centre of origin and diversity among the Eumusa. M. balbisiana is less extensively distributed than M. acuminate and the origin was limited to India and Myanmar (Carreel 1994; Horry 2000). Based on molecular studies, Horry (2000) classified M. acuminate into six subspecies ie., M. ac. ssp. burmannica/burmannicoides/siamea, M. ac. ssp. truncate, M. ac. ssp. malaccensis, M. ac. ssp. microcarpa, M. ac. ssp. banksii/errans, M. ac. ssp. zebrine. However, Perrier et al. (2009) differentiated M. acuminata seeded diploids into four basic clusters based on RFLP and SSR as (i) M. ac. ssp. banksii cluster from New Guinea, (ii) M. ac. ssp. malaccensis cluster from Malayan Peninsula, (iii) M. ac. ssp. burmanica, burmanicoides, siamea from northeast India, Burma, southern China and Thailand and (iv) M. ac. ssp. Zebrine cluster from Java (Tables 2.5 and 2.6). Vast diversity was observed among the edible bananas for many traits such as plant height, architecture, pigmentation, suckering ability, size, shape and orientation of the bunches, size, shape, colour, falvour and taste of the fruits. Nearly 300–1200 numbers of cultivars are available worldwide in various banana growing countries. Based on consumption of fruits, the edible cultivars are classified as four types namely dessert, cooking, plantains and dual purpose. Plantains bear long and slender fruits with high starch content even when fully ripe are cooked to make it palatable. The cultivars with short, stout and angular fruits with high starch content are considered as cooking bananas. The dessert banana bears sweet fruits that are eaten fresh upon ripening. The cultivars which are consumed both as fresh and cooked are classified as dual purpose. The present day cultivated bananas is diverse in nature with respect to morphology, genome and ploidy level such as AA, AB, AAA, AAB, ABB, AAAA AAAB, AABB and ABBB (Daniells et al. 2001). Though the ancestors of these intra and interspecfic hybrids is still unresolved based on the morphological features and molecular characterization, it is hypothesized that one or more backcrosses might occur naturally among the ancestors of the allopolyploid cultivars (De Langhe et al. 2010). Based on the molecular characterization, it is suggested that the popular dessert banana

M. coccinea M. violascens M. gracilis

M. ornate M. velutina M. laterita M. sanguinea M. mannii M. aurantiaca M. rosea M. rubra

M. textilis M.maclayi M. lolodensis M. peekelii M. fehi

Callimusa

Rhodochlamys

Australimusa

Queensland, New Caledonia Philippines Australia

India to Indo-China Philippines Thailand Malaysia

Indo-China, Thailand, Malaysia and Indonesia

Distribution

Musa

Selected species West Africa to Papua New Guinea

Section

Ensete

Genus

Table.2.5 Diversity and distribution of species under different sections of the genus Musa

Fibre, fruit, vegetable

Ornamental

Ornamental

Vegetable, fibre

Uses

10

11

10

9

(continued)

Chromosome

44 S. Backiyarani et al.

Genus

Selected species

M. acuminate M. acuminate ssp. burmannica/burmannicoides/siamea M. acuminate ssp. malaccensis M. acuminate ssp. truncate M. acuminate ssp. microcarpa M. acuminate ssp. banksii/errans M. acuminate ssp. zebrina M. balbisiana M. schizocarpa M. itinerans M. flaviflora M. sikkimensis M. cheesmani M. nagensium M. halabanensis M. ochracea

Section

Eumusa

Table.2.5 (continued) India, South East Asia, Papua New Guinea, to South Pacific and Japan

Distribution Fruit, fibre, Vegetable and medicinal

Uses 11

Chromosome

2 Genomic Designing for Biotic Stress Resistant Banana 45

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Table.2.6 Diversity and distribution of diploid and triploid subgroups of cultivated banana and plantains Ploidy

Group

Geographical distribution

Diploids

AA

The ‘Indonesia-Philippines-Melanesian’ region, with exceptional AA density in New Guinea and India

Triploids

AB

South India

BB

Northeastern India, Myanmar

AAA—Cavendish The Highland AAA bananas (East African Highland bananas, EA-AAA)

Humid tropical regions between 20°N and 20°S also extended to 20° and 30° latitude of both hemispheres The Great Lakes region in East Africa

AAB—Plantain

Mainly found in hillsides of humid tropics to the lowland humid tropical forest of Americas, West Africa and South India

AAB—Silk, Mysore and Pome

Mysore can be found in Southern states of India, Brazil, few restricted areas of Mexico and Venezuela Pome type can be found in Australia Silk type is grown in the Caribbean and South East Asia

ABB—Bluggoe and Pisang Awak

Bluggoe found in South America, especially indigenous people of Savannahs and Amazon basin Pisang Awak is popular in the backyard garden of Asia and grown on small to medium scale

AAB—Maia Maoli /Popoulu

Pacific Island, west coast of South America

AAA—Mutika/Lujugira

East African Highland banana, grown between higher altitudes of 1000–2000 m. Major food crop of Uganda

such as Cavendish as well as other important dessert bananas having AAA genome are originated from the diploid accession subgroup “Mchare which is having the ancestor of M. ac. ssp. zebrina/microcarpa and banksii, and the unreduced gamete of this, fused with the reduced gamete of ssp malaccensis (Martin et al. 2020). The other edible triploid bananas having the genomic group of AAB or ABB might originate by the fusion of an unreduced gamete of interspecfic hybrid of AB genome with the haploid gamete of M. ac. ssp. banksii or M. balbisiana (Baurens et al. 2019). The presence of enormous variation in the AAB and ABB cultivated banana is mainly due to the occurrence of pairing and recombination between homeologous chromosomes of A and B genome (Jeridi et al. 2011) and the exchange of chromosomal segments between the genomes (Perrier et al. 2009). Irrespective of these natural variations, only 2% of the diversity is being cultivated for their fruit quality

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and their natural resistance mechanisms have been lost during the process of domestication (Carlini and Grossi-de-Sa 2001). The remaining untapped banana diversity has to be utilized for the banana improvement program by conserving and characterizing this wealth. Field gene bank of banana germplasm are available in at least 60 centers worldwide which comprises more than 6000 accessions. At present, the CGIAR genebank International Musa Germplasm Transit Centre (ITC) conserves 1617 accessions from 38 countries to safeguard global Musa diversity (Van den Houwe et al. 2020). The problem of ex situ conservation of this diversity is solved by maintaining under field, in vitro and cryo conditions. The phenotypic and genotypic characterization of these conserved diversity are being documented and the information is available in the public domain. The centre shares the Musa diversity to several international and national breeding programs either in the form of lyophilized leaves, seeds and propagules. Based on the ploidy and morpho-taxonomic scoring, the edible bananas are classified as various genomic groups. The cultivars showing predominant morphotaxonomic characters of M.acuminata with a score of 15–25 are classified as AA/AAA genomic groups, while cultivars with morphotaxonomic characters of M.balbisiana with a score of 70–75 are classified as BB/BBB genomic groups. The cultivars possessing the morphotaxonomic characters of both the species are considered as natural hybrids of M.acuminata and M.balbisiana and further classified as AAB for the cultivars having the score of 26–46, AB/AABB for the score of 47–49, ABB for 59–63 and as ABBB for the score of 67–69 (Simmonds and Shepherd 1955). Cultivars with diploid A genome are most abundant in Malaysia, Indonesia, India, and Papua New Guinea (the only place where AA clones are common). They are cultivated due to their extraordinarily sweet, fine quality fruits. In general, they are less hardy than triploid cultivars. They are again subgrouped into Inarnibal subgroup, Lakatan subgroup, Pisang Lilin subgroup and Sucrier subgroup. Some unique AA cultivars namely Chingan, Hapai and Tuu ghia are originated from India, Hawai and pacific islands, respectively. Diploid AB cultivars are very rare and sub grouped into Kamarangasenge, Ney Poovan and Kunnan. Kamarangasenge is cultivated only in Uganda while Ney Poovan has unique flavor and is cultivated in India, Sri Lanka, West Indies, Uganda and Kunnan sub group is cultivated only in India. AAA genomic cultivars are further subgrouped into Cavendish, Gros Michel, Ibota, Mutika/Lujugira and Red. Worldwide, Cavendish sub group cultivars are grown in large area (>40%), they are major export commodities in Central and South America, the Caribbean, West Africa, and the Philippines. Pisang Masak Hijau (Malaysis), Giant Cavendish, Grand Naine, Dwarf Cavendish, Double and Extra Dwarf Cavendish are some of the commonly grown cultivars in many banana growing countries. Gros Michel subgroup has three members namely Gros Michel, High Gate and Honduros (lowgate). The members of these sub groups are used in the breeding programs as they set seeds upon pollination. Many hybrids having disease resistance, high yield with acceptable taste are being developed in Honduras in the FHIA program. Ibota subgroup has only one member, Yangambi KM 5, is resistant to nematode and used in nematode resistance breeding. East African Highland Bananas,

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coming under the Mutika/Lujugira sub group, are staple foods of East Africa, especially in Burundi, Rwanda, and Uganda. This sub group is an example of secondary diversity in the bananas developing outside Southeast Asia and being diversely used. Red sub group banana are classified for it deep red pigmentation in pesudostem and peel. Fruits are light orange pulp. AAB genomic group has five sub groups namely ‘Mysore’, ‘Pisang Raja’, ‘Plantain’, ‘Pome’ and ‘Silk’. Of which, all are dessert types, except plantains. ABB genomic group are generally starchy and used as cooking bananas whereas Pisang Awak sub group are dessert types. and theyare tolerant to drought and resistant to Sigatoka leaf spot diseases. They are grouped under seven sub groups namely ‘Bluggoe’, ‘Monthan’(India), ‘Klue Teparod’, ‘Ney Mannan’ (India), ‘Pelipita’(Central America), ‘Pisang Awak’(Malaysia) and ‘Saba’(Philippines). Tetraploid genomes such as AAAA, AAAB, AABB and ABBB are rarely cultivated. Except some of the hybrids developed in Honduras are dessert type bananas of AAAA (‘FHIA-02’,‘FHIA-17’ ‘FHIA-23’), AAAB (‘FHIA 1’), dual purpose hybrid of AAAB (‘FHIA-18’), plantain type of AAAB (‘FHIA-20’ and ‘FHIA-21’) and dual type AABB (‘FHIA-03’). Singh et al. (2014) tried to confirm the genome of banana accessions using the modified genome score card developed by Singh and Uma (1996) using 15 important characters of banana. It was observed that the accessions showed variation in the morphological and floral characters had the same genome score whereas the same genome type had different genome scores and some of the cultivars have overlapping scores between the genome types which suggested that further characterization has to done at molecular level. The morphotaxonomic and molecular characterisation of the sections Eumusa and Rhodochlamys revealed that it exhibited higher genetic relatedness at molecular level, in spite of high difference at morphological level (Durai et al. 2011). This genetic proximity of Rhodochlamys and Eumusa suggested that this section could be successfully exploited in a gene pyramiding programme through intersectional hybrids. Different markers like restriction fragment length polymorphism (RFLP), random amplified polymorphic DNA (RAPD), amplified fragment length polymorphism (AFLP) have been used for diversity analysis of banana accessions involving different genomic groups (Bhat and Jarret 1995; Kaemmer et al. 1997; Bhat et al. 2004). Ning et al. (2007) and Rout et al. (2009) reported that ISSR markers produced high polymorphic bands and able to group morphologically similar types in a cluster more efficiently and considered as the best for diversity analysis than RAPD and RFLP. Visser (1996) was able to distinguish AAB and ABB group genotypes using random primers (RAPD). Ning et al. (2007) proved that microsatellite or simple sequence repeat (SSR) markers are the best one to study the genomic diversity as it could separate the banana accessions based on their genomic groups. Ravishankar et al. (2017) clustered the AAB genomic group into their sub group classification using SSR markers which distinctly separate the Pome types from other three subgroups. It also separated the cultivars of two sub-groups Mysore and Pome based on geographical locations. Biswas et al. (2020) estimated the phylogenetic relationships among 50 banana accessions using novel functionally relevant

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SSR markers and demonstrated the utility of these markers for germplasm characterization, comparative mapping and genomic-associated studies among Musa and non-Musa spp. DNA barcoding analysis was performed for the banana cultivars and wild Musa accessions using the internal transcribed spacer region (ITS2) for a better understanding of the origin and domestication of cultivated banana and to clear the confusions that exist in the nomenclature and varietal synonyms. PCR–RFLP of the ITS region using RsaI restriction endonuclease on banana accessions showed consistent and distinguishing polymorphic DNA patterns between the wild species and cultivars of M. acuminata (Bhat and Jarret 1995; Hapsari and Lestari 2016). Among the various species of Musaceae, an acceptable structural diversity and molecular phylogeny were obtained using an ITS1, 5.8S and ITS2 region (Hapsari and Lestari 2016). Dhivya et al. (2020) reported that ITS2 is an ideal DNA barcode candidate for Musa sp. owing to its discriminating power in firmly assigning the identification and nomenclature of the members of the Musaceae. Isozymes profile was used as biochemical marker for identification of banana cultivars. Isozyme namely acid phosphatase, catalase, esterase and peroxidase are the best markers to differentiate the banana genotypes differing in their doses of ‘A’ and ‘B’ genomes. (Espino and Pascua 1992; Suman et al. 2015). Mandal et al. (2001) proved that peroxidase, esterase, superoxide dismutase and malate dehydrogenase profiling distinguish the cultivars, of which esterase was found to be most efficient. The isozyme variation observed among the various genomic groups of Musa germplasm revealed that pacific plantains had close relationship with acuminata/banksii complex of Papua New Guinea (Lebot et al. 1993). A high degree of polymorphism for esterase was observed among the various genomic groups of banana accessions (Liyanage et al.1998). Jarret and Litz (1986) reported that isozymes of glutamate oxaloacetate transaminase could be used to differentiate the clones of cavendish sub group. Mendioro et al. (2007) reported that the isozymes of malate dehydrogenase (MDH), 6-phosphogluco dehydrogenase, phosphogluco isomerase and phosphogluco mutase could be used for identification of dessert and cooking types. Kavino et al. (2008) proved that peroxidase (PO) and polyphenol oxidase (PPO) are induced upon challenge inoculation with Foc only in resistant hybrids, and suggested that this could be used as a tool for early identification of resistance banana clones. Jarret and Litz (1986) reported shikimic acid dehydrogenose (SKDH), malate dehydrogenase (MDH), phosphoglucomutase (PGM), and peroxidase (PRX) could differentiate only at subspecies level of M. acuminata but not within AAA genomic group. Espino and Pimental (1988) reported that SKDH, and GOT (glutamate oxaloacetate transaminase) were of little use in differentiating AAB and ABB genotypes from BB/BBB genotypes.

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2.6 Association Mapping Studies Genome-wide association studies (GWAS) is becoming widely used for the identification of candidate genes for various agronomic, biotic and abiotic stresses. But in case of banana, application of GWAS is difficult due to various ploidy level, and presence of many interspecific hybrids which complicates single nucleotide polymorphism (SNP) mapping in banana (Sardos et al. 2016). Apart from that developing parthenocarphic variety with improved resistance through conventional breeding using the wild sources is another important task as the inferior fruit characteristics are often inherited through linkage drag along with the desired traits (Swennen and Vuylsteke 1993). It has also been reported that seedlessness in banana is a complex character either due to combination of structural and genetic factors (Dodds and Simmonds 1948). Similarly the trait bunch weight is governed by more number of genes as they are dependent on many yield related attributes such as number of hands and fruits, pulp filling, length and circumference of the fruits (Nyine et al. 2017). It emphasis that banana improvement program is not only based on the discovery of resistant genes, but focus should also be given to discover the candidate genes for traits related to yield and seedlessness. Earlier findings proved that the trait parthenocarpy is governed by three genes (Simmonds 1962) whereas the bunch weight is governed by quantitative trait loci (QTLs) (Turner and Gibbs 2018). Based on GWAS in the breeding population of banana, Nyine et al. (2019) identified the clustering of SNPs in the transcription factors and genes involved in cell cycle regulation mainly governing the trait fruit filling. This is in concordance with the earlier findings of D’Hont et al. (2012) and Liu et al. (2017) who reported that subfamily of MADs (MCM1, agamous, defensins, SRF), MYB and AP2/ERF transcription factors are involved in fruit architecture, development and ripening. Similarly, twenty-one SNPs associated with the seedlessness corresponding to 13 candidate genomic regions were identified and reported that one putative orthologous gene to Histidine Kinase CKI1 is the strong candidate gene for female sterility (Sardos et al. 2018). Utilization of the molecular tools in banana breeding program is highly appropriate to simplify the selection of genotypes for a complex and low heritable traits as these traits are highly influenced by environment (Tuberosa 2012). But detection of QTLs through linkage mapping and GWAS is often biased as most of the quantitative traits are governed by large number of minor QTLs (Zhao et al. 2014). This limitation can be overcome by using a large set of marker information distributed across the whole genome. This can be achieved through Genomic selection (GS), a breeding approach which exploits high-density DNA markers distributed across the genome to facilitate the rapid selection of the best candidates and it will increase genetic gain per unit time (Meuwissen et al. 2001). This GS approach exploits different prediction models by combining the datasets of genotype and phenotype of the training population (TP) to determine genomic-estimated breeding values (GEBVs). GEBVs allow breeders to predict the superior genotypes for selection of parent in hybridization and/or for advancement of the breeding program. The basic principle is that

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the information derived from several markers widely distributed over the genome, having the potential to reveal genetic variations in the genome, can evaluate breeding values without prior information of where the selected genes are located (Crossa et al. 2017). The success of the GS depends on the selection of training populations with maximum genomic prediction accuracy. Hence to confirm the efficiency of the training population developed using EAHB breeding material, the population was phenotyped in two contrasting conditions and their genetic diversity was assessed using SSR markers. A high level of correlation between vegetative and yield related traits in the training population and concluded that the complex traits can be selected based on the simple traits which are having correlation with that (Nyine et al. 2017).

2.7 Molecular Mapping of Resistant Genes and QTLs Understanding of the inheritance of resistance is the foremost important criteria for the successful durable resistance breeding. Screening of a hybrid population and determination of the segregation ratios can provide information on the inheritance and number of alleles controlling this trait.Unlike other seeded crops, mapping of genes for a specific trait is cumbersome in banana because of its female and male sterility, structural heterozygosity, ploidy and different genomic combinations (Gonzalez de Leon and Fauré 1993). It has also been reported that frequent occurrence of inversion and translocation of chromosomes further limit the mapping of Musa genome (Shepherd 1999; Vilarinhos et al. 2006). With great effort, the first linkage map was developed in F2 population of a diploid M. acuminata accessions using 90 markers (Fauré et al. 1992). Subsequently Lagoda et al. (1998) and Vilarinhos et al. (2006) tried to develop linkage map with more number of markers. Then, Kayat et al. (2009) developed linkage maps from M. ac ssp. malaccensis population segregating for Foc resistance. Hippolyte et al. (2010) constructed genetic map with 11 linkage groups covering 1197 cM with an average density of one marker for 2.8 cm using the segregating population (F1) of M.ac. ssp microcarpa and Pisang Lilin. Construction of saturated linkage map in banana is not possible due to the occurrence of segregation distortions and the risk of pseudo linkages. The magnitude of distortions from expected Mendelian segregation was varied in the population obtained from interspecific and intraspecific combination as they are having different originators which resulted in structural rearrangements (Pardo-Manuel de Villena and Sapienza 2001). Mapping population was developed by selfing of wild banana accession M. ac. ssp. malaccensis (AA, 2n = 22) to investigate the inheritance of resistance to Race 1 and TR4 that cause FW. Genetic mapping was done using 2802 high-quality SNPs and phenotyping for FW segregation which resulted in identification of a single dominant resistant locus for Race 1 at the distal part of chromosome 10. At the same position QTLs for TR4 resistance was identified showing partial resistance to TR4 (Ahmad et al. 2020). Arinaitwe et al. (2019) generate 142 F1 genotypes by crossing Monyet, resistant to Foc race 1 and Kokopo, susceptible and challenged with Foc race 1. The results suggest that resistance to Foc race 1 in banana is controlled by at

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least two dominant genes with epistatic interaction and that heritability of resistance to Foc race 1 is low in Musa spp. Ssali et al. (2013) reported resistance to Fusarium wilt in Musa is conditioned by a single recessive gene by studying the inheritance of resistance in Musa to Foc race 1 which was investigated in F2 populations derived from a cross between ‘Sukali Ndizi’ and ‘TMB2X8075-7’. Fraser-Smith et al. (2016) studied the genetic resistance to TR4 in diploid wild banana M. ac ssp. malaccensis, a potential source of Fusarium resistance genes. The F1 progeny of self-fertilized malaccensis plants challenged with STR4 and TR4 segregated for resistance according to a Mendelian ratio of 3:1 which is consistent with a single dominant gene hypothesis. Dochez et al. (2009) studied the genetics of resistance to R. similis in a diploid banana hybrid population derived from crossing the diploid hybrids TMB2 × 6142– 1 and TMB2 × 8075–7 and the results indicated that resistance to R. similis is controlled by two dominant genes. Rowe and Rosales (1996) indicated that one or more dominant alleles control genetic resistance to burrowing nematode. Vakili (1968) concluded that factors conditioning resistance to yellow sigatoka in M. acuminata ssp. zebrina were partially dominant and that multiple genes were involved and Shepherd (1990), reported that the resistance in M. accuminata was homozygous recessive. Black sigatoka resistance in plantain hybrids using M. ac. ssp. burmannica as a resistant parent has been shown to be controlled by a single major recessive allele and two independent recessive alleles with additive effects (Ortiz and Vuylsteke 1992; Anonymous 1993). The inheritance/gene action for various pest and disease resistance is given in Table 2.7.

2.8 Genomics-Aided Breeding for Resistance Traits The success of the resistant breeding through conventional approach depends on the phenotypic selection. It is highly time consuming process, labour intensive and less efficient as the scoring data is highly environment dependent which hamper the resistant breeding program. Marker assisted breeding has improved the efficiency to some extent especially for the traits which are governed by major genes through various strategies such as introgression of major genes through back crossing. This facilitates the breeder to switch from phenotype selection to genotype-based selection. But, it has been reported that different resistant mechanism might be involved in various resistant genotypes and the resistance may be governed by the QTLs with major and minor alleles. Thus, discovery of QTLs is of great importance to marker-assisted breeding. Recently, the advancement in next generation and third generation sequencing technologies facilitate the whole genome sequencing, resequencing and transcriptome sequencing with less cost. This genomic information integrates the genotype and phenotype, and leads to a new revolution in breeding, especially for complex traits. Integration of genomic tools and conventional breeding makes it possible for the genomic aided breeding (GAB) which is a powerful strategy for gene pyramiding and genome selection (GS) especially for the improvement of

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Table.2.7 Inheritance/gene action for various pest and disease resistance Pest/disease

Gene action

References

Foc race 1

Single dominant gene

Larter (1947) Vakili (1965) Ahmad et al. (2020)

Two dominant genes with epistatic interaction

Arinaitwe et al. (2019)

Recessive gene

Ssali et al. (2013)

Foc TR 4

Polygene

Li et al. (2013)

Single dominant gene

Smith and Hamill (1999) Fraser-Smith et al. (2016)

Polygene

Rowe (1991)

Two dominant genes

Dochez et al. (2009)

Polygene

Damodaran (2004)

Burrowing nematode

One or more dominant genes

Rowe (1984) Rowe and Rosales (1996)

Yellow Sigatoka

Recessive genes in M. acuminata ssp. resistance

Shepherd (1990)

Dominant genes in M. acuminata ssp. malaccensis

Shepherd (1990)

Radopholus similis

Polygene in M. acuminata ssp. Rowe (1984) microcarpa e ssp. errans Black Sigatoka resistance

one major recessive allele and two independent alleles with additive effects

Ortiz and Vulsteke (1994)

Bactertial wilt (moko Several and Rowe and disease) resistance

Recessive genes

Vakili (1965)

Cosmopolites sordidus

Partial dominance

Ortiz et al. (1995)

complex traits. The whole-genome re-sequencing of various cultivars, landraces, and wild accessions provide an unlimited resource for high-throughput SNP genotyping. The availability of high-density SNP markers in natural/ germplasm population has opened a way for genome wide association study (GWAS). This strategy will overcome constraints of conventional linkage mapping in vegetatively propagated crop like banana. Advancement of next generation sequencing (NGS) facilitate the development of large number of genetic markers including SSRs, SNPs. Construction of genetic map and detection of QTLs through bi-parental and/or association mapping populations have accelerated to reveal the genetics of important traits. NGS coupled with GWAS increases the mapping resolution for precise location of genes/alleles/QTL (Varshney et al. 2014). A draft genome sequence assembly of doubled-haploid plant of Musa acuminata represented a major step forward in understanding the structure and evolution of the banana genome (D’Hont et al. 2012). As, it is the first monocotyledon

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genome sequence outside the Poales, this sequence information is highly useful as an essential bridge for comparative genome analysis among monocotyledones (Cenci et al. 2014). Banana has the highest number of transcription factors (TFs) (3,155) among the all sequenced plants. Of which, 759 TFs to banana belonged to MYB and AP2/ERF transcription factor families that plays a role in fruit architecture and ripening were unique to banana (D’Hont et al. 2012). A total of 36,542 and 36,638 protein coding genes were identified in M. acuminata and M. balbisiana respectively (D’hont et al. 2012). The phylogenomic analyses of 3,553 gene families of Musa genome revealed that three rounds of palaeopolyploidization has occurred; two might have occurred independently after Poales and Zingiberales divergence. A total of 37 families of microRNAs with 235 members were predicted in A genome whereas only 270 members were predicted in 42 miRNAs families of B genome (D’Hont et al. 2012; Davey et al. 2013). Wang et al. (2019) reported that B genome had less expansion and more contraction of gene families. And the analysis of expansion and contraction of gene families in the M. acuminata and M. balbisiana showed that A and B genomes are functionally diverged at the genome level during their respective genome evolution. Substantial sequence divergence between B and A genome was noticed at a frequency of 1 homozygous SNP per 23.1 bp, and one heterozygous SNP per 55.9 bp (Davey et al. 2013). The significant improvements made on the banana reference genome sequence will have important impact on the quality of future genetic and comparative genomic analysis. Martin et al. (2016) developed a modular bioinformatics pipeline comprises several semi-automated tools to improve genome sequence assemblies. This module identify and split misassembled contigs / scaffolds using a combination of GBS genetic mapping data and Large insert size Paired Reads (LPR) data. Till date, genome of three sub species of M.acuminata ssp.banksii, burmannica, zebrina have been sequenced by Rouard et al. (2018); .the genome of other Musa species, M.balbisiana (Davey et al. 2013), M. itinerans (Wu et al. 2016), and M. schizocarpa (Belser et al. 2018) and their information were made available in the public domain. Whole genome sequencing for 19 different genotypes which includes various Musa species namely M.acuminata, M.balbisiana, M.textilies, M. velutina, M.acuminata sub species namely malaccensis, zebrina, each seven accessions of intra specific hybrids of M.acuminata (AA, AAA, AAAA) interspefic hybrids of M.acuminata and M.balbisnana (AB, AAB, ABB), Fe’i and pink banana was performed by Sambles et al. (2020). The sequence reads were aligned to the reference genome sequences of M. acuminata and M.balbisiana which provides important quality-assurance data about the taxonomic identities of the sequenced plant material. Several research groups have provided evidence for pairing and recombination between homeologous A- and B- chromosomes during hybridization. The commercial interspecific triploids have arisen from one or more steps of (re) combination and exchange of chromosomal segments between the A- and B-genomes. As a result, most if not all Musa cultivars probably have genomes consisting of different proportions of the A- and B-genome. A similar process of hybridization between subspecies of M. acuminata probably also underlines the evolution of the edible AA and AAA

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types. A consequence of these recombination events is that the hybrid genomes contain an unbalanced number of A- and B-genome alleles (Davey et al. 2013). This clearly complicates genetic studies of trait inheritance, as well as the development and application of molecular marker technologies in banana. Genome sequence of M. acuminata Dwarf Cavendish was compared with the Pahang reference genome assembly and numerous small sequence variants were detected which determined its triploid nature. It also revealed the presence of duplication of a large segment on the long arm of chromosome 2 which is unique to Dwarf Cavendish. Although no functional relevance of this duplication was identified, this example shows the potential of plants to tolerate such aneuploidies (Busche et al. 2020). NGS based transcriptome analysis have also been successfully applied to gene expression profiling by sequencing different mRNA species that measure the activity of thousands of genes in parallel and also quantify transcripts (Voelkerding et al. 2009). The comparative RNAseq of FocTR4 resistant wild relative M.ac ssp. burmonicoides with the susceptible cultivar Brazilian during the FocTR4 infection revealed that high resistance of burmonicoides is quantitatively driven with the high expression level of large number of defense related genes (Li et al. 2020). The advances in genome sequencing, along with high-resolution genetic mapping and precise phenotyping will accelerate the discovery of functional alleles and allelic variations that are associated with traits of interest for perennial fruit crop breeding.

2.9 Recent Concepts and Strategies Developed The issues and limitations of conventional genetic engineering strategy is the complexity associated with the manipulation of large genomes of higher plants. This can be overcome by editing of target genes in plants through “zinc fingers” coupled with FokI endonuclease domains which act as site-specific nucleases (zinc finger nucleases (ZFNs), TALENs (transcription activator-like effector nucleases) and CRISPR/Cas (clustered regularly interspaced short palindromic repeats). Genomeediting was first demonstrated in the cultivar “Rasthali” (AAB genome) by creating mutation in the PDS gene using single gRNA (Kaur et al. 2017). Later, Naim et al. (2018) and Ntui et al. (2020) demonstrated that the editing efficiency can be improved up to 100% in different genomic group of banana using polycistronic gRNAs. It has been already demonstrated using Agrobacterium-mediated stable genetic integration of a Cas9-containing transgene in the genome of sterile triploid banana varieties (Shao et al. 2020; Ntui et al. 2020). In banana, somatic embrygenesis is highly genotypic dependent (Strosse et al. 2006) which hampers the implementation of CRISPR technology in all the commercial varieties. Resistance for Foc TR4 can be enhanced through editing the promoter of RGA which is found to be a resistant gene for FocTR4 (Dale et al. 2017) for developing transgene free Foc TR4 resistance banana varieties. Targeting either single gene conferring resistance to different races (race 1, TR4 and STR4)/isolates of Foc or

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multiple genes (for each race separately) using multiple gRNAs by following monocistronic or polycistronic strategies is the best approach. The endogenous banana streak virus (eBSV), which is integrated in the banana Bgenome was inactivated using multiple gRNAs (Tripathi et al. 2021). Developing resistance to plant RNA viruses through CRISPR/Cas- based on editing of host plant factors influencing viral infection rather than the viral genes is the best strategy. Several eIF such as eIF4E and eIF (iso) 4E, have been identified as recessive resistance alleles to confer resistance against several potyviruses (Anuradha et al. 2021). For further improving commercial cultivars through hybridization approaches, CRISPR technique should be employed in the universal diploid male parents (Zorrilla-Fontanesi et al. 2020).

2.9.1 Challenges in Genome Editing of Banana The success of genome editing in banana depends on targeting the multiple alleles and gene copies simultaneously as it has a high number of multigene families with paralogs (Cenci et al. 2014). The guide RNA (gRNA) needs to be designed to target all the copies and alleles of the gene, since editing of a particular gene through knockdown or knockout does not result in any phenotypic change which may be due to the dose–effect of other paralogous copies of genes. Selection of an edited line with multiallelic mutations should be carried out while screening mutant. To target more number of genes of interest in banana, multiplexed genome-editing using multiple gRNAs targeting several genes and their paralogs in a gene family is an efficient tool for improving polyploid crops (Ansari et al. 2020). Plasmid-based delivery through protoplast transfection and stable transformation through Agrobacterium overcomes the major challenges of genome editing in banana (Ntui et al. 2020) Other transient delivery systems like agro-infiltration or protoplast fusion are not successful in banana. The edited plants developed through stable are considered GMOs due to transgene integration and had to go through regulatory approvals. Removal of Cas9, marker gene, and Agrobacterium–derived DNA sequences through backcrossing is not practicable in banana unlike seeded crops (Tripathi et al. 2020). To overcome these, delivering preassembled Cas9gRNA ribonucleoproteins (RNP) directly into plant cells lead to development of transgene free genome-edited banana plants (Liang et al. 2018; Tripathi et al. 2020). To avoid off target effects and unwanted integration of DNA segments derived from plasmids encoding Cas9 and guide RNA at both on-target and off-target sites in the genome, RNA-guided engineered nucleases (RGENs) enable genome editing is being followed in plants (Kim and Kim 2014). In this approach, the RGENs-RNPs edit the target sites immediately and are rapidly degraded by endogenous proteases in cells, leaving no traces of foreign DNA elements and might not require GMO regulatory approval (Kanchiswamy et al. 2015).The major problem in selection of genome edited events is the lack of high throughput screening methods. Screening of edited plants through PCR and target sequencing are expensive and time-consuming. Thus,

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high-throughput phenotyping for the desired trait, followed by target sequencing of the selected events will be more cost-efficient (Tripathi et al. 2020).

2.9.2 Application of Nanotechnology in Banana In the integrated pest and disease management strategies, application of chemical pesticides is one of the control measures. In this approach only a minimum quantity of chemical reach the target site and the actual utilization of biological target is only 20%) are indicated in bold parental genotype responsible of the source of resistance in each detected QTL is indicated in bold

a Major

Pathogen/Pest

Table 4.2 (continued)

135

13.4

Population Trait size variance (%) –

Candidate gene/s

Rubio et al. (2020)

References

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(RAD-seq) for genetic map construction. QTL mapping detected one stable QTL of minor effect (ca. 13% of phenotypic variance) on chromosome 14, which carries a series of R-genes containing NB and LRR domains (Table 4.2). As indicated before, the genetic basis of DM resistance is a relevant topic in grapevine research (Buonassisi et al. 2017; Vezzulli et al. 2019b). Only in the last two years, seven novel Rpv loci (Rpv22–Rpv27) have been identified by QTL mapping (Lin et al. 2019; Sapkota et al. 2019a; Fu et al. 2020; Bhattarai et al. 2021), which add complexity to the already known complex architecture of the grapevine resistance mechanisms against P. viticola (Table 4.2). Rpv22, Rpv23, Rpv24, Rpv25 and Rpv26 loci are suggested to derive from V. amurensis. The first three loci were detected using the same population described for Cgr1 (Fu et al. 2019, 2020), whereas the last two loci were identified in a biparental population derived from the susceptible V. vinifera cv. ‘Red Globe’ and the resistant V. amurensis cv. ‘Shuangyou’ (Lin et al. 2019). Rpv22, Rpv23, Rpv24 were detected via genotyping-by-sequencing (GBS)-based QTL analysis, and they were mapped on chromosomes 2, 15 and 18, respectively. The range of phenotypic variance explained by these three QTLs varied from 26 to 30%, and results indicated a total of seven candidate resistance genes associated with these loci. Besides, Rpv25 and Rpv26 have been mapped on different genomic regions of chromosome 15, using a high-density specific length amplified fragment (SLAF)marker genetic map. Rpv25 explained less than 20% of total phenotypic variance, whilst Rpv26 can be included in the list of major QTLs, due to the high percentage of variability explained, ca. 64%. Candidate genes responsible for these loci include three cysteine-rich receptor protein kinases (in the Rpv25 region) and a gene encoding a LRR-RLK (receptor-like protein kinases) family protein (in the Rpv26 region). On chromosome 18, Sapkota et al. (2019a) mapped a new resistance locus for P. viticola (Rpv27) in a population originated from a cross between the resistant V. aestivalis × V. vinifera-derived cv. ‘Norton’ and the susceptible V. vinifera cv. ‘CabernetSauvignon’, based on a high-resolution linkage map obtained with SNP and SSR markers. Rpv27 can be considered a major QTL, because it can explain around 34% of the phenotypic variance (Table 4.2). Lastly, Rpv28 was mapped on chromosome 10 of V. rupestris, and it explained up to 67% of the phenotypic variance (Bhattarai et al. 2021). Regarding the genetic determinants of resistance to root-feeding forms of grape phylloxera (D. vitifoliae), three new loci (Rdv6, Rdv7 and Rdv8) have been recently identified in a progeny between the resistant hybrid VRH8771 (V. vinifera × M. rotundifolia) and the susceptible V. vinifera cv. ‘Cabernet-Sauvignon’ (Rubio et al. 2020). Rdv6, identified on chromosome 7, is a major QTL because of the high trait variance it explains. The other two QTLs, mapped on chromosome 3 and 10, explain less phenotypic variance. These results indicate that various QTLs influence grapevine resistance to D. vitifoliae attack. The same population has been used to characterize the genetic determinants of grapevine resistance to the dagger nematode X. index (Rubio et al. 2020). Three new loci were mapped on chromosome 9 (XiR2), 10 (XiR3) and 18 (XiR4), explaining around 23, 21 and 13% of the total phenotypic variance, respectively (Table 4.2).

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4.8.4 Association Mapping for QTL Detection: Benefits and Drawbacks Linkage disequilibrium (LD)-based association mapping (AM) is a complementary approach to the conventional QTL mapping performed in biparental mapping populations to understand the global genetic architecture of complex traits. In contrast to QTL mapping, AM searches for functional variation in a broader context, using an association panel of diverse genotypes derived from germplasm collections and/or breeding programs, which are selected by carrying most of the genetic variability available for the trait of interest (Zhu et al. 2008). The genetic diversity analysed in the association panel is the result of numerous historical and evolutionary recombination events happening across generations, so AM provides higher resolution during QTL mapping than conventional approaches under an adequate marker density (Myles et al. 2009). As a result, whilst findings from biparental crosses tend to be specific to the same or closely related populations, results from AM are more applicable to a much wider level (Zhu et al. 2008). As in other species with long generation cycles, AM is of special interest in grapevine genetics since it reduces research time by not requiring the generation of new mapping populations (Myles et al. 2009). Despite its multiple advantages, AM also presents a series of drawbacks, including the risk of spurious marker-trait associations due to population genetic structure and family relatedness effects. Association panels often are a compendium of non-independent genotypes with varying levels of pedigree relationships, common geographical origin and local adaptation and breeding history (Zhu et al. 2008). As a result, any phenotypic trait that correlates with the underlying population structure or pedigree relatedness at neutral loci will show an inflated number of spurious associations (Balding 2006). This problem is widely known, and many statistical methods have been developed to reduce the confounding effect of these two factors on AM (Tibbs Cortes et al. 2021). For instance, the popular unified mixed linear model (MLM) proposed by Yu et al. (2006) simultaneously controls for both population structure and kinship effects, providing a powerful solution for trait dissection. Nonetheless, correcting for population structure (and kinship) might increase the number of false negatives (Tibbs Cortes et al. 2021). The presence of high LD between genotyped markers is another factor that might reduce the potential of AM to detect true biological signals (Gao et al. 2010). Therefore, determining an adequate statistical significance threshold is fundamental to identify markers truly associated with the target trait. This is commonly done by Bonferroni correction and false discovery rate (FDR) approaches, which assume independence between association tests. Nevertheless, it is not habitual in AM studies (Tibbs Cortes et al. 2021), resulting in the use of overly stringent thresholds that increase the number of false negatives. Among others, alternative approaches based on the dependency among markers (Duggal et al. 2008; Gao et al. 2010) or marker-based heritability values (Kaler and Purcell 2019) have been proposed to calculate more appropriate significance thresholds for AM.

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4.8.5 Extent of Linkage Disequilibrium in Grapevine The degree of non-random association between alleles at two genetic loci within a population is known as LD (Zhu et al. 2008). AM performance relies on the LD between the genotyped markers and the functional polymorphism in the causative gene, and on the rate of LD decay over a specific genetic distance. In general, markers near the causative locus used to be in high LD with the functional polymorphism, and thus associate with the phenotype of interest. AM detects these associations and marks up the genomic regions harboring these significant markers and the potentially implicated genes (Myles et al. 2009). Therefore, LD is an important factor to determine the number and density of genetic markers needed to reach an adequate statistical power at the whole-genome level. In particular, marker density needs to overcome the underlying LD structure to ensure that all responsible polymorphisms are in linkage with (at least) one genotyped marker. Studies describing patterns of LD in grapevine indicate a fast decay in the sativa subspecies, reaching r 2 values below 0.2 within short physical distances. To cite some examples, Nicolas et al. (2016) observed a LD decay below r 2 = 0.2 at 43 kbp in a diversity panel of 279 grape cultivars, whilst Marrano et al. (2017) reported a LD extent of 20 kbp to reach the same LD decay through the analysis of 14 k RAD-seq-derived SNPs screened in 51 grapevine cultivars. These estimates are comparable to those indicated by Laucou et al. (2018) through the analysis of 10 k SNPs in 783 genotypes (LD decay below r 2 = 0.2 at 29–58 kbp). These short LD values suggest the need of genotyping a very high number of well-scattered markers to have a proper genome-wide statistical power. In fact, Nicolas et al. (2016) suggested the need of genotyping (at least) one marker per kbp, which undoubtedly implies the use of high-throughput genotyping methods like reduced representation sequencing (using technologies like GBS, RAD-seq and double-digested (dd) RAD-seq), or whole genome resequencing to reach such marker densities (Pavan et al. 2020). More recently, the whole genome resequencing of a panel of table, wine and multi-purpose cultivars has suggested that the rate of LD decay in the cultivated grapevine might be faster than previously reported (Kui et al. 2020; Liang et al. 2019), entailing the need of using an even higher number of markers for an adequate genome-wide coverage.

4.8.6 Association Mapping Software and Statistical Models As stated before, the need to control for population structure and kinship effects in AM studies led to the development of multiple statistical models, and this continues to be an important research topic (see Tibbs Cortes et al. (2021) for a recent review). Nowadays, there is a trend through the development of multi-locus models, which improve mapping resolution compared to single-locus methods by the simultaneous incorporation of multiple markers in the model as covariates. This approach was firstly implemented in the multi-locus mixed model (MLMM) developed by Segura

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et al. (2012), which paved the way to other derived models, like FarmCPU (Liu et al. 2016b), mrMLM (Wang et al. 2016a) or ISIS EM-BLASSO (Tamba et al. 2017), already tested or with great potential for AM studies in grapevine. More recently, different multi-trait multi-locus models capable of dealing with complex underlying associations between markers and traits have been developed too, such as the penalized MTMM (Liu et al. 2016c) or the mtmlSEM (Igolkina et al. 2020) models. Many mixed linear models and multi-locus models have been progressively incorporated into common software packages like TASSEL (Bradbury et al. 2007), PLINK (Purcell et al. 2007), GAPIT (Lipka et al. 2012) and GEMMA (Zhou and Stephens 2014) to ease data processing and results interpretation. As a result, these packages now implement multiple statistical models to allow a direct comparison between AM solutions. Nevertheless, the development of new methods and tools for AM continues, and, attending to the many works posted as preprints in open-access servers, many more will be released soon, providing a new framework for AM studies in the next few years.

4.8.7 Candidate-Gene and Genome-Wide Association Studies of Grapevine Resistance For AM studies, two widely used approaches are used: genome-wide and candidategene association studies (GWAS and CGAS, respectively). GWAS are mostly used as exploratory analyses to examine the genetic architecture of the trait of interest. On the contrary, CGAS assumes some previous understanding of the genetics of the trait, and commonly the candidate gene derives from a QTL identified through a previous GWAS (Zhu et al. 2008). In other cases, candidate gene selection is based on information obtained from genetic, biochemical or physiological studies in related or model crop species. CGAS are ultimately used to move from QTLs to quantitative trait nucleotides (QTNs), to ideally identify the functional genetic variant responsible for phenotypic variation (Myles et al. 2009). Different CGAS are available exploring relevant traits for grape breeding like muscat flavor, berry colour, or cluster characteristics (see Vezzulli et al. 2019b and references therein). Nevertheless, this approach has not been applied yet to the analysis of disease resistance in grapevines. On the contrary, several works dealing with this issue via GWAS can already be found in the literature. Zhang et al. (2020) examined the genetic architecture of grapevine white rot disease resistance caused by C. diplodiella through the analysis of 386 genotypes and 88.877 SNPs detected by RAD-seq. MLM results indicated six SNPs located on chromosomes 1, 2, 4, 13, 16 and 17 significantly associated with disease symptoms. The analysis of the neighbouring regions derived in the detection of eight candidate genes, five on them with putative functions related to plant resistance mechanisms. Through a GWAS using 350 cultivars and 77,126 SNPs detected by GBS, Jang et al. (2020) explored the ripe rot disease resistance mechanisms caused by the fungal pathogens C. acutatum and

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C. gloeosporiodes. Results identified 26 and 44 SNPs significantly associated with C. acutatum and C. gloeosporiodes disease symptoms respectively, which subsequently led to the identification of two genes that code for two coiled coil (CC)–NBS–LRR proteins capable to recognize specific pathogen-derived products to start a complex resistance response. Lastly, after testing both single- and multi-locus GWA models, Sargolzaei et al. (2020) identified three new genomic loci associated with grapevine resistance to P. viticola (Rpv29, Rpv30, and Rpv31, in chromosomes 14, 3, and 16, respectively) coupling information from a breeding population obtained by selfpollination of ‘Mgaloblishvili’ (a V. vinifera cultivar resistant to DM (Toffolatti et al. 2018)) and a series of Georgian cultivars, genotyped with the Vitis18K SNP-chip array (Laucou et al. 2018). These three new loci co-localize in genomic regions enriched of genes associated with plant defense mechanisms against biotic stress, including receptors of pathogen effectors, signaling mechanisms mediated by protein ubiquitination, and a cluster of Lr10-like (NB-LRR) effector receptors.

4.8.8 Potential Application of QTL Results for Assisted Germplasm Enhancement Decades of research support the usefulness of genetic mapping to detect QTLs and underlying genes involved in grapevine biotic resistance mechanisms, results that have been eventually used as a starting point to guide MAB and germplasm enhancement programs and pyramid breeding. In general, to avoid the resistance breakdown risk that is associated with monogenic and oligogenic resistance, breeding programs aim at pyramiding different QTLs in single prebreeding varieties, used as donors of traits in breeding programs (Zini et al. 2019). Indeed, durability of resistance to the nematode X. index (vector of GFLV ) was confirmed in grapevine rootstocks possessing three QTLs (XiR2, XiR3 and XiR4) (Nguyen et al. 2020). In contrast, P. viticola strains that are able to overcome resistance due to a single QTL (Rpv3 and its allelic variants Rpv3.1 and Rpv3.2) have been isolated in Czechia, Italy and Germany (Eisenmann et al. 2019; Peressotti et al. 2010; Toffolatti et al. 2012). The recent discovery that resistance traits can also be found in V. vinifera cultivars (as observed with DM (Toffolatti et al. 2016)) opens the way to new breeding perspectives within this species. Now, AM potentially allows discovering the QTNs responsible for phenotypic variation, which enables the development of highly efficient functional markers to track relevant traits in grapevine breeding (Emanuelli et al. 2014). Nevertheless, and even under strong statistical evidence and/or theoretical support, the risk of false positive associations is still present, which calls for an independent validation process of the candidate gene/s. This stage could be approached through a cross validation in different populations, as the potential usefulness of an association would be higher if it is found in independent genetic backgrounds. Alternatively, laboratory experiments (like candidate gene knock-out or overexpression studies) could be

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determinant to bind a candidate gene or candidate mutation to a trait of interest, as proved for the grapevine mlo genes and PM susceptibility (Pessina et al. 2016). In this regard, emerging genome editing technologies such as the CRISPR/Cas9 system are suggested to speed up this process, as they are expected to provide determinant functional information to validate the role of a candidate gene (or mutation) on a specific trait (see Sect. 4.13.2).

4.9 Hints About Map-Based Cloning of Resistance Genes 4.9.1 Genomic DNA Libraries and Physical Mapping Unlike the plethora of genetic loci identified in grapevine, single genes controlling important agronomic traits–such as biotic stress resistance–are barely unknown. A physical map is essential to positionally clone such genes and instrumental in a genome sequencing project. Bacterial artificial chromosome (BAC) libraries are the large DNA insert libraries of choice and an indispensable tool for mapbased cloning, physical mapping, molecular cytogenetics, comparative genomics and genome sequencing. In contrast to their name, BACs are not artificial chromosomes per se, but rather are artificial bacterial F factor derived constructs (Ren et al. 2005). Based on an automated protocol, an initial physical map was constructed based on 29,727 BAC clones derived from the cultivar ’Cabernet Sauvignon’. Despite some limitations that interfere with the correct assembly of heterozygous clones into contigs, this physical map is a useful and reliable intermediary step between a genetic map and the genome sequence. This tool was successfully exploited for a quick mapping of complex families of genes, and it strengthened previous clues of co-localisation of major NBS-LRR clusters and R-loci in grapevine (Moroldo et al. 2008). Then, the first whole genome physical map of grapevine was built using high information content fingerprinting of 49,104 BAC clones from the cultivar Pinot Noir. Prior computer simulations, the experimental assembly results were in full agreement with the theoretical expectations, given the heterozygosity levels reported for grape (Scalabrin et al. 2010). The physical map was anchored to a dense linkage map based also on BAC-end sequence (BES) markers (Troggio et al. 2007), paving the way to a new era in both grapevine genetics and GAB.

4.9.2 Positional Cloning of R-Genes The ultimate goal of mapping agronomical traits is the identification and isolation of the underlying genes. This approach aiming to associate a phenotype with a genotype is known as “forward genetics”. In forward genetics, map-based cloning (or positional

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cloning) is a commonly used strategy to isolate genes governing major traits. Initially, molecular markers physically linked to the trait of interest have to be identified through whole genome or local genetic mapping. Traditionally, a local fine map is constructed with the aim to assign the trait to the smallest possible genetic region, thus reducing subsequent sequencing efforts. This means that the region of interest will be targeted and densely covered by molecular markers in order to detect markers flanking the gene of interest as closely as possible. When a marker is closely related to a gene, low recombination frequency is expected and large segregating populations are required to detect the rare recombinant (Welter et al. 2011). This strategy was successfully used to physically map the resistance locus Run1. At first, a local map around the Run1 locus was constructed employing the BSA strategy (Pauquet et al. 2001). Secondly, using the same strategy, resistance gene analog (RGA)-based markers tightly linked to the Run1 locus were detected (Donald et al. 2002). For fine mapping, three independent populations segregating for the resistance locus Run1, in total 996 recombinant individuals, were employed (Barker et al. 2005). Fine mapping allowed the identification of two flanking microsatellite markers showing a very low recombination frequency (tight linkage) with the Run1 locus, thus defining a short genetic interval for the locus. These two flanking markers were used together with three markers that co-segregated with Run1, to screen a BAClibrary constructed from the genomic DNA of a plant carrying Run1. In this way the physical mapping of the region spanning the resistance locus was performed. Markercarrying BAC clones were end-sequenced and assembled into extended contigs after identification of overlapping BACs. This allowed an overall coverage of the region spanning the locus Run1. After the sequencing of the contig spanning the genomic region associated with Run1, positional candidate genes were selected for functional analysis. The identified gene responsible for PM resistance has shown to encode a TIR–NB-LRR domain protein which represents the most important class of R proteins in plants (Feechan et al. 2013). Further examples of map-based cloned genes responsible for biotic stress resistance have concerned the PdR (Riaz et al. 2008a), Ren1 (Hoffmann et al. 2008), and XiR (Hwang et al. 2010) loci. The availability of the grapevine genome sequence opens up new options to accelerate the map-based cloning of genes. Molecular markers surrounding the trait of interest may be anchored to the genome sequence. This genomic region may then be searched for positional candidate genes, based on their predicted functional role. Molecular markers tagging such candidate genes can be developed and tested for their association to the trait. Additionally, markers (e.g. SNPs) with a progressive physical distance from the trait of interest may be developed in both directions and used to estimate their recombination frequencies to the trait. However, it is important to be aware of the fact that specific genes such as resistance genes may not be present in the currently elaborated model genome sequences, as these have been derived from susceptible grapevines. It remains to be seen from further grapevine genome sequencing to what extent the reference genome sequence of ‘PN40024’ are colinear to other grapevine cultivars, breeding material and Vitis wild species accessions on large- andfine scale levels (Anderson et al. 2011). Actually, the milestone of conventional BAC-based physical mapping seems not to be overcome with the

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advent of genome sequencing and the boost in next-generation sequencing technologies. Lately, complementary strategies for assembling the Rpv3.1 haplotype were adopted combining whole genome shotgun (WGS) sequencing of a Vitis accession, homozygous for Rpv3.1, and restriction-based fingerprinting and sequencing of BAC clone inserts across the Rpv3.1 region. This approach allowed for mapping the causal factor for DM resistance to an interval containing a TIR-NB-LRR (TNL) gene pair (Foria et al. 2020). From the applied point of view, positional cloning of the resistance genes provides sequence information that can be used to design perfect genetic markers, which will maximize the efficiency of MAS approaches. In addition, map-based cloning offers the possibility to introduce these genes into existing elite wine grape cultivars, which might not be hybridized, by transgenesis without affecting wine quality.

4.10 Marker-Assisted Breeding for Resistance 4.10.1 Development and Evaluation of Robust Molecular Markers QTL experiments provide relevant information about the genetics of the trait of interest, circumscribed by the experimental design used. Loci obtained from QTL mapping studies differ in percentage of phenotypic variance explained by the locus (r2 ), allele effect, and confidence intervals (see Table 4.2). Although loci with high r2 are preferred, a breeding strategy could use loci explaining different percentages of the phenotypic variance. Before deployment in breeding programs with more diverse genetic background, the effect of the desired alleles requires confirmation, even in the case of a major QTL (Bernardo 2014). In grapevines, a well-documented example of locus validation is the p3-VvAGL11 marker linked to the seedlessness (sdl) locus, which has been successfully adopted by several table grape breeding programs (Bergamini et al. 2013; Ocarez et al. 2020). Biotic resistance is a more complex trait that requires further study. In a recent study, SSR alleles linked to 11 R-loci were investigated among 102 grapevine accessions displaying different levels of PM and DM disease severity over 3 seasons, with only a few of them being further suitable for marker-assisted parent selection (MAPS) or marker-assisted seedling selection (MASS) (Zini et al. 2019). Selection accuracy is related to the genetic distance between the causal polymorphism and the molecular marker selected. Two markers flanking the loci can be used to increase accuracy, as well as haplotypes instead of a single marker, as recently reported for the Rpv3 locus (Wairich et al. 2021). Highly saturated genetic maps and controlled phenotyping assays allow precise loci dissection. Fine mapping of the Ren3 locus narrowed the location to a 7 Mb segment that included both Ren3 and Ren9 (Zendler et al. 2017), and subsequently into separate intervals of 3.1 and 0.6 Mb, respectively (Zendler et al. 2021b). In this study, new molecular markers tightly linked to these two regions were

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described, allowing breeders to track the presence of these two sources of resistance independently. As described in Sect. 4.8, new genotyping technologies based on NGS, such as GBS and RAD-seq, have improved genetic mapping. But the strategy is not well suited for detailed characterization in grapevines, due to the high percentage of missing data, sparse coverage and heterozygote undercalling (Hyma et al. 2015; Barba et al. 2014). For grapevine breeding, loci identified with this strategy have been further studied to: (i) assess the linkage to existing markers located nearby, such as SSRs (Barba et al. 2018), (ii) develop fluorescence hybridization-based genotyping assays, such as kompetitive allele-specific PCR (KASP™) Genotyping (Wairich et al. 2021) or high resolution melting curves (Jang et al. 2020), and (iii) development of genotyping assays based on NGS, such as AmpSeq (Yang et al. 2016) or rhAmpSeq (Zou et al. 2020). Given the high-throughput nature of NGS, these assays allow the screening of up to 2,000 sites in one experiment, but require specific pipelines for data analysis (Fresnedo-Ramírez et al. 2019). Next-generation sequencing technologies have also enabled the study of heterozygous genomes. In a recent study, a partiallyphased reference genome of the resistant interspecific hybrid ‘Börner’ has been developed and utilized for marker discovery (Holtgräwe et al. 2020). Their study found 10,820 putative SSR marker positions, with more than 4,000 tri-allelic SSR candidates. As a proof of concept, 19 single nucleotide variant (SNV) markers were developed around the Rpv14 locus and used to narrow it down to 330 kbp using bulked segregant analysis (BSA) of the V3125 x ‘Börner’ progeny.

4.10.2 Marker-Assisted Selection as a Tool for Marker-Assisted Breeding The use of molecular markers tightly linked to R-loci obtained from QTL studies helps optimize resources, select progeny with several R-loci for durable resistance, and expedite breeding of new resistant grapevine cultivars through MASS (Dry et al. 2019; Vezzulli et al. 2019b). As useful new loci are identified and publication becomes imminent, they are named and listed here for use by the Vitis research community: https://www.vivc.de/index.php?r=loci%2Findex (Table of Loci for Traits of Grapevine; Maul et al. 2021). In recent years, several programs have tested markers linked to Ren/Run and Rpv loci to determine the presence of alleles associated with resistance, using germplasm of diverse origins, such as Russia (Ilnitskaya et al. 2020), Kazakhstan (Pozharskiy et al. 2020) and Italy (Vezzulli et al. 2019c). Beyond PM and DM, breeders have expanded the use of MAS to other pathogens and pests, such as the Mjr1 locus for M. javanica resistance and D. vitifoliae resistance (Table 4.3). In most cases, the R-loci originated in Vitis spp. other than V. vinifera, thus the introgression into the cultivated genetic background is required.

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Table 4.3 Reported loci available to breed for biotic stress resistance through MAPS and MASS. Only works published since 2018 are included Causal agent

Loci

Program location

References

P. viticola

Rpv1, Rpv3, Rpv10

France

Merdinoglu et al. (2018)

Rpv3, Rpv12

Russia

Ilnitskaya et al. (2020)

Rpv1, Rpv3, Rpv10, Rpv12, Rpv14

Italy

Vezzulli et al. (2019c)

Rpv3, Rpv10, Rpv12

Kazakhstan

Pozharskiy et al. (2020)

Run1, Ren3, Ren 3.2

France

Merdinoglu et al. (2018)

Run1, Run2, Ren1, Ren2, Ren3, Ren9

Italy

Vezzulli et al. (2019c)

Run1, Ren1, Ren3

Kazakhstan

Pozharskiy et al. (2020)

M. javanica

Mjr1

Australia

Smith et al. (2019)

D. vitifoliae

Rdv1, Rdv2

Australia

Smith et al. (2019)

E.necator

4.10.3 Marker-Assisted Gene Introgression Marker-assisted seedling backcross and MAPS have been used very effectively for rapid gene introgression. Modified backcross (MBC) breeding is used for Vitis improvement, whereby the recurrent parent is a different unrelated genotype in each generation of crossing. When introgression of a single locus from a wild species is the goal, the trait of interest would normally be assayed prior to crossing to produce the next backcross generation. Where the trait may be expensive to assay or dependent on fruit phenotyping, additional time and funding are required. Yet if tightly linked markers are available, then selections may be made in the weeks following germination, once DNA samples are extracted and analyzed. An excellent example comes from the introgression of PdR1b (encoding PD resistance) on chromosome 14 from V. arizonica into V. vinifera wine grapes (Riaz et al. 2008b). Generation time was reduced to 2 years, or 4 generations in 10 years (Walker and Tenscher 2019) through optimized growing practices. With each generation, presence of the resistance locus was assayed using SSR markers (VVIP26 and CH14-77) soon after seed germination (Riaz et al. 2008b, 2009; Walker et al. 2021a, b). Greenhouse assays were also used to confirm resistance. As a result of this work, the top selections ranging from 88% (MBC2 ) to 97% (MBC4 ) V. vinifera background were field-tested at multiple locations in California and Texas. Evaluations of viticultural traits and enological qualities led to the release of five new cultivars in 2019 (Walker et al. 2021a, b caes.ucdavis.edu). The project took ~20 years, including the time it took for four cycles of backcrossing (Walker and Tenscher 2019).

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V. rotundifolia (selection G52) has strong resistance to PM of grapevine leaves, petioles, canes and fruit. The difficult cross between this muscadine grape (2n = 40) and V. vinifera (2n = 38) was made in North Carolina prior to 1919 (Detjen 1919) and a resulting hybrid (NC 6–15) remained under-utilized for many years. Backcrossing efforts to introgress PM resistance into V. vinifera began in the 1980s (Bouquet 1986), whereupon the single locus for PM resistance, Run1, was first identified. Initially, leaf disc assays and field phenotyping were required to test for the presence of the muscadine resistance source. Later, AFLP markers were established (Pauquet et al. 2001) and proposed for MAS. The causal gene was later identified, and improved, tightly-linked markers were reported (Feechan et al. 2013). As a result of the efforts of Bouquet, along with the teams developing molecular markers for the Run1 locus, it is now used widely by breeders in Hungary (Hajdu 2015), New York (Cadle-Davidson et al. 2011), and elsewhere. In France, the INRAResDur1 breeding program (Merdinoglu et al. 2018) developed and released four cultivars incorporating the Run1 locus along with another locus for PM resistance, and two loci conferring DM resistance. Cornell University test selections with the Run1 locus are currently in field trials in consideration of future release (Reisch, pers. comm.).

4.10.4 Gene Stacking To increase the durability of resistance, gene stacking (“pyramiding”) has been proposed (Mundt 2018; Dry et al. 2019). In grapevines, this approach is enabled by the identification of multiple R-loci for both PM and DM resistance (Dry et al. 2010). However, the race-specificities of the many available loci are only known in a small number of cases, and there are likely more races in situ than have been isolated for laboratory assays. Nevertheless, Stam and McDonald have estimated that four R-genes stacked together would be virtually impossible for cereal PM to overcome (Stam and McDonald 2018). With long-lived perennial crops like grapes, it is prudent to consider measures to make sure that resistance features of new cultivars are not easily overcome. For this reason, some have also proposed combining management strategies (including limited fungicide applications) in combination with deployment of resistant cultivars as a pathway to better assure the durability of resistance over time (Feechan et al. 2015). If left completely uncontrolled, conditions for the pathogen to mutate are optimized. An excellent example of a gene stacking strategy is outlined by Dry et al. (2019) in which the INRA-ResDur program, working with the Julius Kühn-Institut (Germany), Staatliches Weinbauinstitut, (Germany) and Agroscope (Switzlerand) obtained lines with three loci for PM resistance plus three loci for DM resistance. Also in Italy Fondazione Edmund Mach (FEM) obtained stacked (“pyramided”) genotypes carrying two or three loci for DM and/or PM resistance, up to seven combined Rloci in total (Vezzulli et al. 2019c); moreover, Vivai Cooperativi Rauscedo (VCR), along with University of Udine, developed resistant genotypes derived from “elite” cultivars carrying two Rpv loci coupled with two Run/Ren loci (Foria et al. 2019).

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4.10.5 Up-and-Coming Exploitation of Susceptibility Genes Susceptibility genes in plants facilitate infection and compatible interaction with the pathogen (see Sect. 4.13). Development of cultivars homozygous for non-functional alleles has been a successful breeding strategy for durable PM resistance in barley using the MLO gene (Jørgensen 1992), and DM resistance using the DMR and DLO genes, first identified in Arabidopsis thaliana (Van Damme et al. 2008). In grapevines, gene homologues have been studied and described in (Dry et al. 2019). Screening of non-functional mutants among the natural rich diversity of Vitis, or its creation using new breeding techniques such as EcoTILLING or gene editing could be valuable for the development of biotic stress resistant grapevines (Dry et al. 2019; Merdinoglu et al. 2018; Pirrello et al. 2021). Given high heterozygosity and inbreeding depression, the adoption of susceptibility gene strategies in traditional grapevine breeding will require the use of a modified backcross scheme. To this end, use of donors with diverse genetic backgrounds and co-dominant markers linked to the susceptibility loci (to allow selection on the absence of the phenotype among heterozygous seedlings) will expedite the process.

4.10.6 Limitations and Prospects of Molecular-Assisted Breeding Applications To be most useful, genetic markers should be (i) tightly linked, (ii) flanking the locus of interest, (iii) inexpensive, (iv) rapid to assay, and (v) readily transferable between populations. Microsatellite loci have been most widely used (Vezzulli et al. 2019b), but SNP-based assays are compatible with high throughput analyses, automated pipelines, and may increasingly become the system of choice. There are dual roles for MAS: both for selection of desirable seedlings within weeks of germination (MASS), and for selection of parents with desirable traits (MAPS). Both roles present breeders with the potential to reduce phenotyping errors, and to accelerate the identification of desired genotypes. Yet the overall progress in grapevine breeding is not always accelerated by MAB since multi-year field trials are still required to assess the totality of viticultural (and often enological) performance. The best example of accelerated breeding is given in the above discussion of Pdr1b locus introgression from a wild species into cultivated wine grapes at the rate of four generations per 10 years. Marker-assisted breeding is also advantageous for gene stacking approaches where trait phenotyping is unable to determine the marker complement in each seedling (e.g. presence of multiple loci for PM resistance). Yet knowledge of which loci are complementary to each other, and which loci will lead to durable stress resistance, is quite lacking. Marker-assisted breeding is most useful for selection of single loci of moderate to strong effects. It is not useful where traits are under quantitative genetic control, e.g.

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berry weight, cluster size, etc. If minor QTL are selected for MAB, stability should be evaluated across environments prior to use (Vezzulli et al. 2019b). Where the goal is to manipulate polygenic traits, genomic selection (GS) may be the preferred approach but requires further investigation in Vitis. High-density marker sets are available through GBS, RAD-seq, AmpSeq, and rhAmpSeq methods, but the calibration and validation of GS models remains in order to investigate the potential for DNA analyses to inform the breeding for complex, polygenic traits.

4.11 Towards Genomics-Assisted Breeding for Resistance Traits 4.11.1 Excursus in Genome Sequencing The number of grapevine and pathogen/pest genome sequences as well as tools for functional genomics has increased dramatically in the 15 years since the first grapevine sequence assemblies were released. In 2007, two genome assemblies, a descendant of ‘Pinot Noir’ and a heterozygous ‘Pinot Noir’ clone, were the fourth assemblies for flowering plant and first woody fruit crop genome assemblies to be released (Jaillon et al. 2007; Velasco et al. 2007). Grapevine is very heterozygous and the highly homozygous ‘PN40024’ (~7% heterozygosity) made it easier to develop an assembly with haploid consensus sequences (Jaillon et al. 2007). Further sequencing, re-assembly, gene annotation, and an updated genome browser made this a very useful resource in identifying disease related genes and supporting large-scale transcriptomic and proteomic analyses (Canaguier et al. 2017). Subsequently, several short-read assemblies with greater genome coverage were produced for cultivars and species; however, due to the heterozygosity of the grapevine these resulted in fragmented sequences, large number of contigs, large assembly size and inaccuracies in gene models and copy number (e.g. Da Silva et al. 2013; Di Genova et al. 2014; Patel et al. 2020). Regardless, the benefit of these and other newly generated genome sequences was shown in the alignment of multiple species and cultivars that enabled the identification of core sequences and development of a set of universal multiallelic genetic markers (rhAmpSeq) with greater transferability across interspecific grapevine populations (Zou et al. 2020). The divergence of sequences between cultivars and species, which has been acquired during speciation, hybridization and selection, cannot be encapsulated in a few consensus genome assemblies; thus, de novo assemblies conserving the characteristics of both haplotypes for many additional genotypes (including interspecific genotypes) is needed. Several short read and phased long read assemblies are publicly available for 12 V. v. subsp. sativa cultivars (‘Pinot Noir’, ‘Black Corinth’ (seeded and seedless), ‘Cabernet-Sauvignon’, ‘Carménère’, ‘Chardonnay’, ‘Merlot’, ‘Reisling’, ‘Semillion’, ‘Sultanina’, ‘Tannat’, and ‘Zinfandel’), some accessions of V. v. subsp. sylvestris, and six species (V. arizonica, V. cinerea, V. rupestris, V. riparia, V. amurensis

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and M. rotundifolia), providing the opportunity to mine disease resistance genes. The largest single access point for grape and grape pathogen genomes that are browser enabled can be found at the http://grapegenomics.com website (D. Cantu Laboratory, UC-Davis, USA). Recent assemblies using long read sequencing technology have provided the opportunity to assemble the entirety of a genome with both haplotypes, thereby identifying structural variation within coding sequences (Minio et al. 2017). Development of diploid genome assemblies with phased haplotypes for many cultivars and species provides the opportunity to identify unique genes that are important in phenotypic variation in response to biotic stressors in grapevine. It is important to sequence multiple genotypes of each of the 60–70 dioescious wild species, develop diploid genome assemblies and mine structural variation and gene content as the wild species are the primary source of pathogen and pest resistance genes. A survey of common grapevine pathogens indicates a growing number of draft genomes of the major fungal and bacterial pathogens as well as numerous viral and antagonistic pathogens of grapevine pathogens. There are no database resources for these pathogen genomes making it difficult to conduct comparative analysis within a species or between strains. Development of such a resource would provide a greater opportunity to improve detection and understanding of host–pathogen dynamic interactions (Näpflin et al. 2019).

4.11.2 Gene Prediction and Annotation Protein coding gene prediction and annotation are ongoing efforts with new annotation technologies, greater understanding of the structural components within a genome, and new genomes being assembled. Gene prediction using automatic gene annotation has identified 27,000 to 33,568 genes for the ‘PN40024’ 12X.v2 consensus reference genome VCOSTv3 annotation (Canaguier et al. 2017). Transcriptional evidence— expression sequence tags (ESTs)s and cDNA—provides further validation of gene models, emphasizing the importance of paired end and full-length cDNA transcriptomes for identifying novel genes (Minio et al. 2019a). Gene content differences between cultivars and species can be assessed by alignment with well annotated genomes such as ‘PN40024’ and ‘Cabernet-Sauvignon’ (Canaguier et al. 2017; Minio et al. 2017). However, it is important to keep in mind that the inbred ‘PN40024’ likely represents of fraction of the greater diversity of Vitis species and cultivar gene information. Recent comparative analysis of ‘Carménère’ indicated numerous structural variants relative to ‘PN40024’ and ‘Cabernet-Sauvignon’ genomes likely contributed to its differences in gene content (absence 494 and 253; novel 1561 and 449) in ‘Carménère’, respectively to ‘PN40024’ and ‘Cabernet Sauvignon’ (Minio et al. 2019b). Increased availability of annotated phased diploid assemblies, that are more complete than ‘PN40024’, enables identification of homozygous and heterozygous gene regions and gene regions unique to one haplotype allowing the exploration of allelic differences that affect phenotypic differences between genotypes (Smit et al. 2020).

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4.11.3 Updates on Transcriptomics, Proteomics and Metabolomics Databases High-throughput ‘omic technologies are rapidly generating huge datasets (transcriptome, metabolome, proteome, and other components of the grapevine phenome); however, access and utilization of these datasets is limited by the need for searchable databases. Public sequence repositories for RNA and protein sequences provide an important data repository for grapevine information but have limitations in comparative analysis. VitisNet provided a database of gene pathways based on the ‘PN40024’ genome V2 annotation aiding in the functional understanding of gene expression and proteomic studies (Grimplet et al. 2009, 2012). A gene co-expression database utilizing grapevine microarray expression data (~29,000 genes) allowed identification of potential regulatory mechanisms and infer gene function (Wong et al. 2013). Moretto et al. (2016) established the VESPUCCI grapevine gene expression database (http://vespucci.colombos.fmach.it/; 1608 microarray and 135 RNA-seq samples) allowing the user to explore, analyze and visualize the expression data. Grape RNA is a database of RNAseq and microRNA with 25 experimental conditions, assembled transcriptomes, GO, KEGG and NCBI annotations and tools to search, conditions was recently established expanding the RNA-seq data that can be queried using ‘PN40024’ V2 annotation (Wang et al. 2020a). These historical databases provide context for much of the early transcriptomic data; however, strategies for maintaining current and historical data in a useable format is a challenge. Databases quickly become obsolete with the rapid development of genomes and new data acquisition technologies. The heterogenous nature of the phenomic datasets further challenges the grapevine research community to organize, fund, and maintain both historical and new databases. A framework for a distributed grapevine information system has been envisioned, and remains to be implemented with metadata standards for all data types to promote dataset access and organization in future databases (Adam-Blondon et al. 2016).

4.11.4 Methylomics Inspired by seminal studies in Arabidopsis and cereals and enabled by the revolution of NGS in the early 2000s, research in fruit plant science has started investigating chromatin properties and related epigenetic phenomena more deeply, although the discipline is still in its infancy as far as grapevine is concerned. Chromatin modifications, including DNA methylation, histone modifications and nucleosome spatial rearrangements, are deployed by eukaryotic cells to modulate gene expression and maintain genome stability through the control of chromatin tridimensional structure and accessibility. The mode of replication and conservation of such modifications during cell division is well-suited for the potential transmission of gene regulatory information through cell lineages during the development of a plant body plan or through vegetative and sexual reproduction, posing the precondition for long lasting

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memory or even transgenerational inheritance of regulatory setups for gene expression (reviewed in Lämke and Bäurle 2017). The role of chromatin modifications in mediating fundamental genomic functions, recording environmental signals and stabilizing molecular responses and phenotypes over time are all different nuances of a unique body of mechanisms that convey genetic information and elicit genetic differentiation without involving changes in the DNA primary sequence, hence the term epigenetics (literally “beyond genetics”) used to refer to these phenomena. The early steps of epigenetic research in Vitis put a major emphasis on a number of epigenetic features as well as on specific scientific questions raised by the biology of the species and its exploitation, namely (i) the identification of molecular factors known to be responsible for epigenetic modifications and the genetic basis thereof; (ii) the profiling of chromatin modifications at the genome scale (the so called “epigenome”); (iii) the molecular changes triggered by in vitro regeneration as a source for somaclonal variation; (iv) the capability of epigenetic modifications to generate diversity despite an invariable genetic background; and (v) the effects of environmental cues on the epigenome as a molecular foundation for the concept of terroir. In recent studies tackling the above aspects, DNA methylation data have been collected from grapevine samples using NGS approaches, mainly based on the golden standard method of bisulfite sequencing (BS-seq), at the whole genome level or using reduced representation techniques such as reduced representation bisulfite sequencing (RRBS) (Niederhuth et al. 2016; Celii 2016; Xie et al. 2017; Dal Santo et al. 2018; Williams et al. 2020; Varela et al. 2021 and others mentioned hereafter). Some studies also exploited the technique of methylation sensitive amplification polymorphisms (MSAP) (Xie et al. 2017, Valeraet al. 2021) based on methylation sensitive restriction enzymes, which is less informative but suitable for a cheaper prescreening. Compared with DNA methylation, histone modifications and chromatin accessibility have been poorly investigated in grapevine thus far. A notable exception is represented by the fruitENCODE project, which analyzed the regulatory circuits of ripening in different climacteric and non-climacteric fleshy fruit species, including grape, by means of ChIP-seq and DNaseI-seq methods (Lü et al. 2018). To date, this study is the most comprehensive source of information on histone modifications in grapevine with a major focus on the H3K27me3 and H3K43me3 modifications that are associated with gene silencing and active transcription, respectively. Histone modifiers (HMs) involved in the deposition and removal of histone modifications are several and much diversified in plants; a bioinformatic search in the grapevine genome (Wang et al. 2020b) identified 117 HM genes sorted into 11 subfamilies and differentially expressed according to anatomy, hormone treatment and exposure to fungal infection. Tandem and segmental duplications seem to account for 21% of all the HM genes identified, suggesting a possible diversification of functions following species-specific genome rearrangements. The epigenetic regulation of gene expression also involves non-coding RNAs (ncRNA), which comprises ~ 20–24 nt small interfering small RNAs (siRNA) capable of guiding the RNA-induced Silencing Complex (RISC) toward the genomic sites to be epigenetically silenced. The biogenesis and function of siRNAs requires RNA-dependent RNA polymerases (RDR), riboendonucleases of the DICER-like

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(DCL) family and ARGONAUTE (AGO) proteins that are catalytic components of the RISC complex. According to a bioinformatic survey, a total of five VvRDR, four VvDCL and thirteen VvAGO genes are present in the grapevine genome (Zhao et al. 2015), including the peculiar VvAGO10a gene, only expressed in the stem and possibly involved in the systemic movement of siRNAs (Melnyk et al. 2011). Nextgeneration sequencing was used in some studies (Chávez Montes et al. 2014; Zhu et al. 2018) to identify large numbers of endogenous siRNAs from multiple grapevine tissues/organs and provide confirmatory results about the features and genomic distribution of this small RNA category in addition to promising information on their differential expression across developmental stages. Grapevine is one of a few dicot species investigated thus far that stand out for the peculiar DNA methylation pattern observed at the genomic level (Niederhuth et al. 2016). Indeed, DNA methylation in plants occurs by the covalent addition of a methyl group to the 5th carbon position of cytosines in different sequence contexts, namely CG, CHG and CHH (where H represents any base other than G). The three contexts are associated with different DNA methylation pathways and the variation in the amount of average methylation at each context may represent predominance for a specific pathway or the lack of it. The cultivated grapevine is characterized by a lower-than-average level of CHH methylation, which is usually associated with siRNA-mediated RNA-dependent DNA methylation, and it shares this feature with other clonally propagated species (Niederhuth et al. 2016). It is not clear to which extent the mode of reproduction is causally related to CHH methylation, but it has been verified that higher levels of CHH methylation cannot be promptly rescued by a single round of sexual reproduction. As a result, in grapevine, the poor levels of CHH methylation alone can hardly distinguish transcriptionally active regions of the genome from repetitive DNA that is targeted for gene silencing by DNA methylation. However, the meta-analysis of several transposable elements of different families still shows a significant enrichment of CHH methylation, although the effect is much more apparent for the CG and CHG context, suggesting that the underlying function of this pathway may be preserved irrespective of the overall depletion (Celii 2016). Epigenetic marks can add a further level of diversity among individual plants, even if epigenetic changes may be more stochastic and unstable in contrast with strict-sense genetic polymorphisms altering the DNA sequence. The reversibility of DNA methylation changes, for example, is a distinct feature of in vitro propagation, in which epigenetics has long been considered a useful source of phenotypic variability (Schellenbaum 2008; Baránek et al. 2010, 2015). However, it should be noticed that part of the existing epigenetic variation could be ultimately ascribed to genetic variation, such as genomic structural variation caused by transposable element insertions that are target of epigenetic silencing. For instance, spreading of DNA methylation from repetitive DNA into the surrounding regions (up to 2Kbp) has been observed in the grapevine genome by comparing haplotype-specific DNA methylation profiles at sites of hemizygous TE insertions in the ‘Pinot noir’ cultivar (Celii 2016). In these sites, the haplotype presenting the TE insertion displayed higher DNA methylation levels in the flanking regions than in the homologous regions of the parental haplotype. These and similar processes capable of creating obligatory

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epialleles, that is alleles that differ in their epigenetic state because of associated genetic differentiation, may account for some, probably most, of the epigenetic variation observed between grapevine cultivars. Examples of DNA methylation diversity have been observed between ‘Cabernet-Sauvignon’ and ‘Sangiovese’ plants grown in Italy (Dal Santo et al. 2018) and among clones of the ‘Malbec’ cultivar grown in Mendoza, Argentina (Varela et al. 2021). However, the paucity of such studies and the different methodological approaches adopted prevent a systematic evaluation of the phenomenon and its biological consequences. Interestingly, DNA methylation is also a predictor of variation in gene expression between grapevine genotypes, but from a different angle that challenges the traditional view of a negative association between DNA methylation and expression. Indeed, when gene body CG methylation is considered, rather than methylation in promoters or in detrimental repetitive DNA elements, the function of such epigenetic mark does not seem to be linked to silencing and is rather enriched in the transcribed region (gene body) of housekeeping genes that are stably and constitutive expressed in most cultivars (Magris et al. 2019). This observation, which represents an example of a more general phenomenon detected in most plants (Bewick and Schmitz 2017, Zilberman 2017), suggests that the lack of DNA methylation might be the signal to look for when searching for epigenetic marks of potential variability in the molecular phenotype. Whether epigenetic mechanisms can contribute to translate soil physicochemical properties, climate parameters and system of vine management into a chromatin signature that is representative of a specific terroir is a fascinating question that still compels a definitive answer, although promising observations are already available. To date, three major studies addressed this question, namely a comparison of DNA methylation profiling between clones of the ‘Shiraz’ cultivar grown in six wine sub-regions of the Barossa, South Australia (Xie et al. 2017), a multi-omic comparison between clones of ‘Cabernet-Sauvignon’ and ‘Sangiovese’ both grown in three different environments of North Italy (Dal Santo et al. 2018) and an analysis of clones of the ‘Malbec’ cultivar grown in two contrasting vineyards in the area of Mendoza, Argentina (Varela et al. 2021). Except for the second study, which convincingly demonstrated genotype x environment interactions only at the transcriptional level, the other two showed that DNA methylation data could be used to segregate individual plants based on environmental covariates and in two very distinct geographical scenarios.

4.11.5 Integration of Different ‘Omic and Phenomic Data Integration of biotic susceptibility or resistance responses (transcriptomic, proteomic or metabolomic) with population genetic studies provides potential to explore the genetic architecture of the phenotypes and identify candidate genes or infer gene roles in response phenotypes. Metabolic biomarkers have been identified by characterizing metabolic profiles associated with disease resistance (Maia et al. 2020; Viret et al. 2018). Histochemical, transcriptomic, and metabolomic analyses of DM

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response in susceptible and resistant cultivars showed strong correlation between stilbenoid biosysnthesis related genes, stilbene accumulation, and pathogen growth inhibition (Eisenmann et al. 2019). Targeted metabolomic analysis showed a significant induction of stilbenoids in a population segregating for DM resistance (Vezzulli et al. 2019a). Targeted analysis of stilbenoids identified metabolite (m)QTL hotspots with disease-resistance motifs on chromosome 18 and theses mQTLs overlapped a reported PM resistance locus (Riaz et al. 2011; Teh et al. 2019) and the DM resistance region described by Vezzulli et al. (2019b). These complementary studies indicate the power of integrating transcriptomic and metabolomic datasets, collected in conjunction with disease phenotyping in QTL mapping to gain a better understanding of resistance mechanisms. The growing number of genomes and transcriptomic, proteomic, and metabolomic analyses in response to pathogens and pests will increase the opportunity to identify new candidate genes and biomarkers that underly the pathogen and pest response enabling greater understanding of their genetic architecture and development of new cultivar selection and disease/pest control strategies. New initiatives aiming to coordinate Vitis ‘omic data integrations are being funded (see COST CA17111 INTEGRAPE: Data integration to maximize the power of ‘omics for grapevine improvement, http://www.cost.eu/COST_Actions/ca/CA17111 as an example).

4.12 Brief on Genetic Engineering for Resistance Genes 4.12.1 Target Traits and Alien Genes Over time, plants have evolved many responses to the different biotic factors (fungi, bacteria, phytoplasmas, viruses, nematodes, insects, and mites) ranging from the initial recognition of the pathogen/pest to the activation of specific containment mechanisms. The precise knowledge of the molecular pathways underlying defense and/or tolerance responses are essential to identify specific genes involved in these mechanisms for their exploitation through established techniques of genetic modification (ETGMs), i.e. recombinant DNA techniques enabling the insertion of genetic information into an organism regardless of sexual compatibility. The difficulties linked to the genetic transformation process in grapevine, including grapevine regeneration problems, genotype effect and long times to obtain stable transgenesis often led to testing candidate genes in herbaceous model plants or in transient expression approaches before the stable transformation in grapevine (Table 4.4). This section reflects a succession of approaches that has often been observed over the years, namely the identification of gene in different grapevine species and characterization in model herbaceous plants, stable transgenic expression in V. vinifera and finally the last step, the future perspective of cisgenesis, i.e. the use of the most promising genes with their native regulatory sequences.

Gene source

V. quinquangularis ‘Shang-24’

M. rotundifolia ‘Noble’

V. quinquangularis ‘Shang-24’

V. amurensis ‘Shuanghong’

V. amurensis ‘Shuanghong’

V. pseudoreticulata ‘Baihe-35–1’

V. amurensis ‘Shuanghong’

V. quinquangularis ‘Danfeng-2’

Gene name

VqTLP29 (thaumatin-like protein)

MrCBF2 (C-repeat-binding factor dehydration-responsive element-binding factor 1C)

VqJAZ7 (jasmonate ZIM-domain)

VaHAESA (PRR gene)

VaRGA1 (Toll-interleukin1(TIR)-NBS-LRR)

VpTNL1 (TIR-NB-ARC-LRR R)

VaERF20 (ethylene response factor)

VqERF112, VqERF114, VqERF072 (ethylene response factors)

Arabidopsis thaliana

Arabidopsis thaliana

Arabidopsis thaliana Nicotiana tabacum

Arabidopsis thaliana

Arabidopsis thaliana V. vinifera ‘Thompson Seedless’ (transient expression)

Arabidopsis thaliana

Arabidopsis thaliana

Arabidopsis thaliana

Host

References

Liu et al. (2018)

Hanif et al. (2018)

Wu et al. (2017)

(continued)

Botritis cinerea Wang et al. (2020c) Pseudomonas syringae pv. tomato DC3000

Botritis cinerea Wang et al. (2018a) Pseudomonas syringae pv. tomato DC3000

Golovinomyces cichoracearum Wen et al. (2017) Pseudomonas syringae pv. tomato DC3000 Erysiphe cichoacearum DC

Hyaloperonospora arabidopsidis Tian et al. (2020) Pseudomonas syringae pv. tomato DC3000

Hyaloperonospora arabidopsidis Plasmopara viticola

Golovinomyces cichoracearum

Peronospora parasitica isolate BNoco2

Golovinomyces cichoracearum Yan et al. (2017) UCSC1 Pseudomonas syringae pv. tomato DC3000

Induced tolerance/resistance

Table 4.4 Representative examples of functional characterization of grapevine genes and genetic transformation of Vitis species to enhance resistance/tolerance against several pathogens

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V. davidii ‘0940’

V. labrusca x V. vinifera ‘Kyoho’

V. vinifera Arabidopsis thaliana ‘Cabernet-Sauvignon’

V. pseudoreticulata ‘Baihe-35–1’

VdWRKY53 (WRKY transcription factor)

VlWRKY3 (WRKY transcription factor)

VvSNAT2 (serotonin N-acetyltransferase)

VpPR4 (pathogenesis-related protein)

Arabidopsis thaliana

V. pseudoreticulata ‘1058’

Pyrus communis ‘Bartlett’

AtRPW8.2 (resistance to powdery mildew 8)

VpRPW8-d (resistance to powdery mildew 8)

pPGIP (polygalacturonase inhibitory protein)

V. vinifera ‘Thompson Seedless’ ‘Freedom’rootstock

DSF (diffusible signal factor)

V. vinifera ‘Thompson Seedless’, ‘Chardonnay’

Nicotiana benthamiana

CAP (chimeric antimicrobial protein)

Xylella fastidiosa

V. vinifera ‘Thompson Seedless’

V. amurensis ‘Zhuoshan-1’

VaTLP (thaumatin like protein) V. vinifera ‘Thompson Seedless’

V. vinifera ‘Thompson Seedless’

VpPR10.1 (pathogenesis-related V. pseudoreticulata protein) ‘Baihe-35–1’

V. vinifera ‘Red Globe’

Arabidopsis thaliana

Arabidopsis thaliana

Arabidopsis thaliana

V. vinifera ‘Jing Xiu’

VvbZIP60 (bZIP transcription factor)

Host

Gene source

Gene name

Table 4.4 (continued) Induced tolerance/resistance

References Yu et al. (2019a)

Xylella fastidiosa

Xylella fastidiosa

Xylella fastidiosa Botritis cinerea

Phytophthora capsici

Erysiphe necator

Plasmopara viticola

Plasmopara viticola

Erysiphe necator

Golovinomyces cichoracearum

Golovinomyces cichoracearum

(continued)

Lindow et al. (2014) Zeilinger et al. (2018)

Dandekar et al. (2012) Dandekar et al. (2019)

Agüero et al. (2005) Dandekar et al. (2019)

Lai et al. (2018)

Hu et al. (2018a)

He et al. (2017)

Su et al. (2018) Ma et al. (2018)

Dai et al. (2016)

Yu et al. (2019b)

Guo et al. (2018)

Coniella diplodiella Zhang et al. (2019) Golovinomyces cichoracearum UCSC1 Pseudomonas syringae pv. tomato DC3000

Golovinomyces cichoracearum

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V. pseudoreticulata ‘Baihe-35–1’

VpSTS29/STS2 (stilbene synthase)

V. vinifera ‘Thompson Seedless’

V. pseudoreticulata ‘Baihe-35–1’

V. pseudoreticulata ‘Baihe-35–1’

V. pseudoreticulata ‘Baihe-35–1’

VpRH2 (RING-H2-type ubiquitin ligase)

VpCDPK9, VpCDPK13 (calcium-dependent protein kinases)

VpEIFP1 (F-box protein)

V. vinifera ‘Red Globe’ Arabidopsis thaliana

V. vinifera ‘Thompson Seedless’

V. vinifera ‘Shiraz’

VriATL156 (E3 ubiquitin ligase V. riparia ‘Gloire de gene) Montpellier’

V. vinifera ‘Thompson Seedless’ Arabidopsis thaliana

V. vinifera ‘Thompson Seedless’

V. quinquangularis ‘Danfeng-2’

VqSTS6 (stilbene synthase)

V. vinifera ‘Brachetto’

Host

Nicotiana benthamiana ‘41B’ rootstock

Artemisia annua

Aaβ-FS ((E)-β-farnesene synthase)

GFLV Nbs (single-domain antigen-binding fragments of camelid-derived heavy-chain only antibodies)

Gene source

Gene name

Table 4.4 (continued) Induced tolerance/resistance

Erysiphe necator Golovinomyces cichoracearum

Erysiphe necator

Erysiphe necator

Plasmopara viticola

Erysiphe necator Golovinomyces cichoracearum

Erysiphe necator

Grapevine Fanleaf Virus (GFLV )

Lobesia botrana

Wang et al. (2017a)

Hu et al. (2021)

Wang et al. (2017b)

Vandelle et al. (2021)

Xu et al. (2019)

Cheng et al. (2016) Liu et al. (2019)

Hemmer et al. (2018)

Salvagnin et al. (2018)

References

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In the last 25 years the genetic transformation in grapevine has been reported in several works. In this section we will report some of the most significant experiences of the last 5 years related to resistance/tolerance to pathogens, while for a more exhaustive overview of transgenesis in grapevine, different reviews are available (Laimer et al. 2009; Gray et al. 2014; Abu Qamar et al. 2017; Capriotti et al. 2020). In recent years, the search for new traits or alien genes for tolerance and/or resistance to grapevine pathogens have essentially, if not exclusively, focused on the fungus/oomycete responsible of DM and PM for the objective of reducing antifungals treatments in vineyards and for a viticulture with low environmental impact. The search for new sources of resistance/tolerance has been intensified by exploiting wild Chinese grape varieties, a germplasm very interesting for breeding new cultivars and studying special resistance mechanisms. In particular, V. pseudoreticulata ‘Baihe-35–1’, V. quinquangularis and V. amurensis were the species whose resistance mechanisms were most exploited (Table 4.4). V. pseudoreticulata ‘Baihe-35–1’ is a valuable germplasm resource for PM resistance (Yu et al. 2013), as well as for DM, anthracnose (Elsinoe ampelina) and Meloidogyne incognita tolerance; V. quinquangularis with a higher resveratrol content compared to other wild Chinese species showed resistance to PM, anthracnose and M. incognita, while V. amurensis is tolerant to cold, DM and anthracnose (Xu and Wang 2014). Through transcriptomic approaches potential traits involved in the tolerance mechanisms were identified in these species, genes such as pathogenesis-related proteins (PRs), transcriptional factors (WRKYs, DREBs, ERFs), heat shock proteins and stilbene synthases. For example, thaumatin-like protein (TLP) belonging to PR protein family 5 was characterized in Chinese grapevine comparing the expression profiles of this gene in disease resistant and susceptible grape species infected with anthracnose, E. necator or B. cinerea. The expression level of VqTLP29 from V. quinquangularis increased following the pathogen inoculations, and the over-expression in Arabidopsis thaliana enhances resistance to PM and the bacterium Pseudomonas syringae pv. tomato DC3000 suggesting that VqTLP29 may be involved in the SA and JA/ET pathways (Yan et al. 2017). VqJAZ7 gene from V. quinquangularis ‘Shang24’ encodes for a jasmonate ZIM-domain (JAZ) protein, a protein family acting as a negative regulator of JA signalling. In preliminary characterization in Arabidopsis, transgenic lines overexpressing VqJAZ7 enhanced resistance to biotrophic fungus Golovinomyces cichoracearum (responsible of PM in Arabidopsis), but was ineffective against the necrotrophic fungus B. cinerea, and P. syringae pv. tomato DC3000 (Hanif et al. 2018). The results suggested that VqJAZ7 altered the SA-dependent and JA-dependent responses in plants, and it can be useful in grapevine, albeit only against some classes of pathogens. Some ET response factor (ERF) transcription factors play important roles in the regulation of immune responses in plants. VaERF20 isolated from V. amurensis cv. ‘Shuangyou’ (Wang et al. 2018a) and VqERF112, VqERF114 and VqERF072 from V. quinquangularis (Wang et al. 2020c) were induced by fungal infection. Overexpressed in Arabidopsis they increased the resistance to B. cinerea and P. syringae pv. tomato DC3000. The overexpression of these genes induced the activation of

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both SA and JA/ET defense genes, callose accumulation and pattern-triggered immunity (PTI) genes, suggesting that the ERF genes isolated from grapevine resistant genotypes are involved in different signal transduction pathways favouring the plant immune responses (Wang et al. 2018a). Among pattern recognition receptors (PRRs), in V. amurensis cv. ‘Shuanghong’ infected with P. viticola, the VaHAESA gene belonging to the LRR-RLK (leucine-rich repeat receptor-like protein kinase) family was identified through transcriptome analysis. In transient expression in V. vinifera, the gene induced the increase of H2 O2 , NO, and callose levels and the stable expression in Arabidospis confirmed the activation of PAMP-triggered immunity improving the resistance against DM (Liu et al. 2018). From the same grapevine species, a TIR-NBS-LRR gene (VaRGA1) overexpressed in Arabidopsis induced resistance to the biotrofic Hyaloperonospora arabidopsidis (responsible of DM in Arabidopsis) and P. syringae pv. tomato DC3000, while increases the disease induced by the necrotrophic B. cinerea. The resistance mechanisms induced by VaRGA1 involved the activation of SA signaling, while inhibiting the JA pathway (Tian et al. 2020). Another resistance gene from the family TIRNB-ARC-LRR (VpTNL1) from V. pseudoreticulata, identified from a transcriptomic analysis of leaves inoculated with PM was characterized in herbaceous host. In Arabidopsis, it enhanced the tolerance to G. cichoracearum and P. syringae pv. tomato DC3000, and in Nicotiana tabacum was found to confer resistance to tobacco Erysiphe cichoacearum DC. This gene represents an interesting candidate for PM resistance in grapevine (Wen et al. 2017). Among transcription factors, bZIP family plays a crucial role in response to abiotic stress and plant development, however in recent years evidence demonstrates the bZIP can be involved also in plant immune response. VvbZIP60 isolated from V. vinifera cv. ‘Jing Xiu’ was accumulated in leaves in response to pathogens, or to exogenous application of SA and JA. Interestingly, overexpression of VvbZIP60 increased in Arabidopsis the resistance to PM by accumulating PR1 and inducing several genes involved in the SA-signaling pathway (Yu et al. 2019a). WRKY transcription factors are involved with SA in the response against fungi. VvWRKY53 plays a role in the resistance response during the early stage of infection of PM, and other WRKYs isolated from V. pseudoreticulata ‘Baihe-35–1’ and V. labrusca x V. vinifera cv. ‘Kyoho’ improved the resistance to biotic stress (Zhu et al. 2012; Guo et al. 2014, 2018). VdWRKY53 isolated from V. davidii (a wild Chinese grapevine species showing high level of resistance to white rot caused by the fungus Coniella diplodiella (Speg.) Petr. and Syd.) and inserted in Arabidopsis showed greater resistance to C. diplodiella, P. syringae pv. tomato DC3000 and G. cichoracearum (Zhang et al. 2019), confirming that WRKY transcription factors are strong activators of defense-related genes. Melatonin (N-acetyl-5-methoxytryptamine) in plant plays a key role in different developmental processes including responses to biotic and abiotic stresses (Nawaz et al. 2016), and serotonin N-acetyltransferase (SNAT) is one of the key enzymes for melatonin synthesis from L-tryptophan. The expression of VvSNAT2 isolated form V. vinifera cv. ‘Cabernet-Sauvignon’ was induced by pathogen inoculation, and transgenic Arabidopsis overexpressing VvSNAT2 showed high levels of melatonin

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and chlorophyll and improved the resistance to PM through the activation of SA signaling (Yu et al. 2019b). C-repeat-binding factor dehydration-responsive element-binding factor 1C (CBF2/DREB1C) is a transcription factor family well known to play an important role in freezing tolerance and cold acclimation of plants. Recently, its involvement in the early response to DM in grapevine was demonstrated. The gene isolated from M. rotundifolia (MrCBF2) introduced in Arabidopsis showed an increased resistance to DM linked to the accumulation of SA and PR transcripts. However, MrCBF2overexpressing plants exhibited an altered phenotype such as growth retardation, dwarfism, late flowering, and prone rosette leaves (Wu et al. 2017). These are representative examples of functional characterization of candidate genes for tolerance to pathogens in recent years, some of them may be interesting genes to be tested on transgenic grapevines (essentially in V. vinifera) as well as being candidates for future cisgenic approaches.

4.12.2 Genetic Transformation for Biotic Stress Resistance Alongside functional characterization in herbaceous hosts, new resistance or tolerance genes have been characterized directly in V. vinifera. Although fungi are the pathogens on which transgenic research has focused the most efforts in recent years, the fight against other grapevine pathogens has continued (Table 4.4). Grapevine breeding has remained ineffective against viruses due to the absence of confirmed sources of viral resistance or tolerance in the Vitis germplasm (Oliver and Fuchs 2011). For this reason, genetic engineering has played an important role in the attempts to incorporate resistance to grapevine viruses using pathogen-derived resistance and RNA-mediated resistance approaches (Gambino and Gribaudo 2012). Historically the first attempts at engineering in grapevine have been made against grapevine viruses, in particular against GFLV, a nematode-transmitted icosahedral virus and causal agent of fanleaf degeneration. However, only partial successes have been reported (Gambino and Gribaudo 2012) and with the exception of to GFLV-resistant transgenic rootstocks (Vigne et al. 2004), virus-resistant engineered grapevines have rarely been obtained. In recent years, the works in this field have been significantly reduced (Dal Bosco et al. 2018), due to the poor success achieved in the past and to the bad reputation of classic genetically modified organisms (GMOs) among consumers. However, the safety of the classical transgenic approach against viruses has been confirmed recently, indeed no statistically significant differences in the genetic diversity of virus strains and microbiome were associated with GFLV-resistant transgenic rootstocks cultivated in commercial vineyard soil for several years (Hily et al. 2018). Recently Hemmer et al. (2018) proposed an interesting new antiviral approach adopting single-domain antigen-binding fragments of camelid-derived heavy-chain only antibodies, also known as nanobodies (Nbs). Nanobodies specific to GFLV expressed in Nicotiana benthamiana and in grapevine

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41B rootstock, conferred effective resistance against a wide range of GFLV isolates neutralizing the virus at an early step of the life cycle, prior to cell-to-cell movement. In addition to viruses, transgenic grapevines expressing a pear polygalacturonase inhibitory protein (PGIP) (Agüero et al. 2005) or a chimeric antimicrobial protein (CAP) (Dandekar et al. 2012) were previously obtained, and they resulted tolerant to PD, an insect-transmitted bacterial disease caused by X. fastidiosa. Dandekar et al. (2019) tested in field conditions these transgenic lines of V. vinifera cv. ‘Thompson Seedless’, and they demonstrated that PGIP and CAP secreted into the xylem can migrate into scion through the graft union. Interestingly, the tolerance to PD was observed also in the untransformed scion thanks to the transfer from the transgenic rootstock of PGIP or CAP. The trans-graft protection is then effective under field conditions, and this approach could be interesting for further application since the scion would not be transformed. Another approach against PD involved the gene rpfF isolated from both X. fastidiosa and Xanthomonas campestris pv. Campestris, encoding a synthase for diffusible signal factor (DSF). The genes expressed ectopically in ‘Freedom’ rootstock induced a reduced mobility of X. fastidiosa and in field conditions these plants showed a reduction of PD incidence two- to four-fold lower than that of untransformed plants (Lindow et al. 2014). However, Graphocephala atropunctata, one of the leafhopper vector of X. fastidiosa, showed greater colonization efficiency on DSF transgenic grapevines even though DSF plants maintained low levels of X. fastidiosa populations. These contrasting results between insect vector and bacterium suggested that under some conditions DSF transgenic plants could facilitate the X. fastidiosa spread and thus hinder the disease management (Zeilinger et al. 2018). This also highlights the importance of field tests for new genotypes obtained through transgenic and other new breeding techniques, because only in this way it will be possible to correctly evaluate all aspects related to the viticultural ecosystem. An interesting approach has been adopted against the European grapevine moth L. botrana, which is becoming a key pest for grapevine. The insect is attracted to the odour profile of plants characterized by a specific ratio of volatile terpenoids. An (E)-β-farnesene synthase (Aaβ-FS) inserted in V. vinifera cv. ‘Brachetto’modified the emission of (E)-β-caryophyllene and (E)-β-farnesene, transgenic plants showed an alteration of the natural ratio of these compounds and these plants resulted less attractive to insect. The results suggested that the volatile ratio modification might represent a new and effective pest control strategy (Salvagnin et al. 2018). Different genes involved in the response to stress and secondary metabolism have been used against fungi. For example, VpPR4 was strongly induced in V. pseudoreticulata ‘Baihe 35–1’ after 24 h from E. necator inoculation at significantly higher levels in respect to its homologous VvPR4 in V. vinifera. The overexpression of VpPR4 in V. vinifera cv. ‘Red Globe’ under constitutive 35S promoter induced a significant reduction of E. necator hyphal growth, although a complete inhibition was not reached, since the PM resistance is likely regulated by a multi-gene complex (Dai et al. 2016). Other PR proteins isolated from V. pseudoreticulata have been shown to be effective in improving the tolerance to DM. VpPR10.1 inserted in V. vinifera cv. ‘Thompson Seedless’ did not induce macroscopic phenotypic alterations in transgenic lines, but the overexpression of this gene significantly improved DM resistance

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by reducing the spread and intensity of P. viticola sporulation (He et al. 2013; Su et al. 2018). VpPR10.1, interacting with a voltage-dependent anion channel 3 (DAC3), was more active in defense responses than its homologous in V. vinifera. The complex VpPR10.1/VpVDAC3 regulates the defence response to P. viticola through a cell death-related immunity mechanism (Ma et al. 2018). Another PR isolated from V. amurensis cv. ‘Zhuoshan-1’ (VaTLP) and transferred in V. vinifera cv. ‘Thompson Seedless’ under constitutive promoter improved resistance against DM by inhibiting both hyphal growth and asexual reproduction of P. viticola (He et al. 2017). In Arabidopsis, resistance to PM 8 (RPW8) are atypical R genes without NB or LRR domains but able to induce SA-dependent responses and resistance to PM (Wang et al. 2009). RPW8 genes isolated from V. pseudoreticulatawere strongly overexpressed after P. viticola infection, while their homologs in V. vinifera were not activated by the pathogen. In particular, VpRPW8-d overexpressed in N. benthamiana enhanced resistance to Phytophthora capsici (Lai et al. 2018), and the Arabidopsis AtRPW8.2 improved resistance to PM in V. vinifera cv. ‘Thompson Seedless’. The resistance was associated with H2 O2 accumulation, activation of SA signalling and altered expression of other phytohormone-associated genes (Hu et al. 2018a). Stilbene synthases (STSs) codifying for stilbenoids in response to biotic and abiotic stresses in grapevine can increase the resistance or tolerance to different pathogens. Transgenic V. vinifera cv. ‘Thompson Seedless’ plants overexpressing VqSTS6 from V. quinquangularis showed higher stilbenoid content and enhanced resistance to PM (Cheng et al. 2016). Interestingly, if these transgenic lines were used as rootstock, high stilbenoids accumulation was observed in the untransformed scion associated with high callose deposition and increased tolerance to PM (Liu et al. 2019). The results suggested that, in addition to the leaf production, stilbenoids are also root–shoot transported, and this may be useful for inducing resistance/tolerance to wild type scions exploiting the trans-graft protection. Other STS genes VpSTS29/STS2 isolated from V. pseudoreticulata and inserted always in V. vinifera cv. ‘Thompson Seedless’ improved tolerance to E. necator. The overexpression of these genes in V. vinifera reprogrammed the transcriptome and oriented the global gene expression towards the defence, indeed the SA signalling pathway and several endogenous STS genes were transcriptionally activated in leaf-infected tissues inducing programmed cell death (Xu et al. 2019). Calcium ions are ubiquitous second messengers in plants, and calcium-dependent protein kinases (CDPKs) are important signal transmitters of Ca2+ changes in response to environmental stimuli such as biotic ones (Hu et al. 2018b). VpCDPK9 and VpCDPK13 isolated from V. pseudoreticulata induced in overexpressing V. vinifera cv. ‘Thompson Seedless’ an increased resistance to PM involving SA and ET regulation and accumulation of H2 O2 and callose in the cells surrounding the site of infection (Hu et al. 2021). An F-box protein (VpEIFP1) induced by E. necator was isolated from V. pseudoreticulata and inserted in Arabidopisis and V. vinifera cv. ‘Red Globe’. In the transgenic plants, the accumulation of H2 O2 and the increase of NPR1 and PR1 expression levels induced the suppression of E. necator germination and growth. Likely, the mechanism of action induced by VpEIFP1involved the degradation of thioredoxin z (VpTrxz) via the ubiquitin/26S proteasome system (Wang et al. 2017a).

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The ubiquitination plays important roles in disease resistance in plants, and some attempts have been made to exploit this system to improve tolerance to pathogens in grapevine. V. riparia E3 ubiquitin ligase gene (VriATL156), a gene belonging to the ATL subfamily, associated with defense in Arabidopsis, was activated during P. viticola infection as one of the principal signal transduction components of the plant response to the pathogen. Transgenic V. vinifera cv. ‘Shiraz’ overexpressing VriATL156 showed a transcriptional reprogramming of the plant responses in the earliest stages of pathogen infection and provided an effective control of DM (Vandelle et al. 2021). Another example is the VpRH2, a RING-H2-type ubiquitin ligase gene from V. pseudoreticulata inserted in V. vinifera cv. ‘Thompson Seedless’ that induced an increase of PM tolerance. During the infection process, the interaction of VpRH2 with VpGRP2A, a glycine-rich RNA-binding protein, played an important role in PM-resistant gene cascades (Wang et al. 2017b).

4.12.3 Future Challenges The concept of cisgenic plants was introduced in 2006 (Schouten et al. 2006) and refers to genetically modified plants with genes in sense orientation containing their native regulatory sequences (i.e. introns, promoter and terminator) isolated from the same species or species compatible for sexual hybridization. In addition, foreign sequences such as selection genes and vector-backbone sequences must be absent. In parallel with cisgenesis, the concept of intragenesis was also developed, which differ from the first because it allows to use new combination of functional genetic elements (gene, promoter, terminator always from species capable of sexual hybridization) obtained by in vitro cloning (Holme et al. 2013). The cisgenic approach has been taken up in several reviews (Espinoza et al. 2013; Dalla Costa et al. 2017; Limera et al. 2017; Eckerstorfer et al. 2019), although concrete examples in grapevine are almost absent. The first obstacle is to obtain marker-free plants without vector-backbone sequences. While for annual plants these sequences can be eliminated by self-fertilization and segregation in the offspring, in a woody species such as grapevine, approaches involving the use of recombinases have been adopted. The most frequently used recombinase/recognition sites are the Cre/loxP and the yeast Flp/FRT. The bacteriophage P1 Cre recombinase, which specifically recognizes loxP sites, was placed under the control of an estrogen receptor-based fusion transactivator (XVE system) and activated by 17-β-estradiol (Zuo et al. 2001). The excision system was adopted in V. vinifera cv. ‘Brachetto’ with positive results and effective excision of neomycin phosphotransferase (nptII) gene (Dalla Costa et al. 2010). In the same genotype, Flp/FRT system driven by the soybean Gmhsp17.5-E promoter effectively mediated site-specific excision of nptII gene by heat-shock treatment (Dalla Costa et al. 2016). Another obstacle to the development of the cisgenic approach in grapevine is often the lack of knowledge of the regulatory sequences of resistance/tolerance genes. However, in recent years, in addition to the classic functional analysis of the coding sequences, several studies have also been conducted on grapevine promoters (Wen et al. 2017; Tian et al. 2020; Zhang et al. 2019; Wang et al. 2020c; Vandelle

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et al. 2021) improving the basic knowledge in this research field. Although there are still no published articles on cisgenic grapevines for resistance to pathogens, several research groups around the world are working intensively towards this goal and cisgenic plants will be available soon in the near future. Likely, the first plants will be resistant to major fungal and oomycete pathogens (PM and DM) using the classical resistance genes, for example, MrRUN1 and MrRPV1 isolated from M. rotundifolia (Feechan et al. 2013). The future of genetic engineering in grapevine for resistance to pathogens seems to have taken a main road in recent years, that is the study of the resistance mechanisms of grapevine species naturally tolerant to PM and DM in order to insert them in the European grapevine (V. vinifera) which is very sensitive to these diseases. In addition to classic TIR-NB-LRR resistance genes used in the traditional breeding of grapevine (e.g. Run/Ren loci), likely new tolerance genes that act against a broad spectrum of pathogens, and therefore do not confer complete resistance, but different levels of tolerance will be used. This alternative approach to classical resistance can be interesting as it would: (i) in any case reduce the impact of treatments in viticulture, (ii) ensure broad-spectrum protection against multiple pathogens (not only fungi) and (iii) make it more difficult for pathogens to overcome resistance. The road to using these engineered genotypes in the vineyard is still long as it will be necessary to: (i) improve the transformation processes, as few genotypes were currently utilised (e.g. V. vinifera cv. ‘Thompson Seedless’ seem to be the elite genotype to test the effects of transgenes in V. vinifera, Table 4.4); (ii) implement cisgenesis, an approach so far mostly ventilated rather than used in practice, the only approach with genome editing that could be more acceptable to consumers (see Table 4.5); (iii) analyze the new engineered genotypes directly in the vineyard to fully understand the levels of resistance/tolerance, the undesirable effects against the plant microbiome and the effects on the yield and the quality of the productions, aspects almost completely unknown for all transgenic grapevines produced. However, the research progress in recent years suggests a rapid overcoming of many problems related to grapevine transformation and with the support of Government Institutions, the practical use of these new-engineered genotypes might no longer be a utopia.

4.13 Recent Concepts and Strategies Developed 4.13.1 Advent of New Breeding Technologies The term “new breeding technologies” (NBTs) refers to a group of new-generation biotechnological techniques, which resemble traditional breeding techniques but require shorter times, especially at the initial steps, and do not alter the genetic heritage of the cultivar of interest. The best-known NBTs are the “cisgenesis” and the “genome editing through site-directed nucleases”. In a cisgenic plant (see Sect. 4.12.3), only species-specific genes that could also have been transferred

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Table 4.5 Comparison between ETGMs and NBTs Transgenesis

Cisgenesis

Intragenesis

Genome editing

Detectability

PCR and whole genome sequencing (WGS) A suitable reference genome for comparison is available

PCR and whole genome sequencing (WGS) A suitable reference genome for comparison is available

PCR and whole genome sequencing (WGS) A suitable reference genome for comparison is available

PCR and whole genome sequencing (WGS) A suitable reference genome for comparison is available Some modifications cannot be distinguished from naturally occurring mutations

Unintended effects

Random insertion of the transgene may induce insertional mutagenesis and/or influence the expression of other genes Transgene expression pattern dependent from position effect and copy number Integration of marker genes Potential insertion of backbone vector sequences Somaclonal variations

Random insertion of the cisgene may induce insertional mutagenesis and/or influence the expression of other genes Cisgene expression pattern dependent from position effect and copy number Potential insertion of backbone vector sequences Somaclonal variations

Random insertion of the intragene may induce insertional mutagenesis and/or influence the expression of other genes Intragene expression pattern dependent from position effect and copy number Potential insertion of backbone vector sequences Somaclonal variations

Off-target effects Large deletions and insertions at the target site Somaclonal variations

Presence of Exogenous DNA in Exogenous DNA exogenous DNA the form of a in the form of a transgene and cisgene is present marker gene is present

Exogenous No exogenous DNA in the form DNA is present of a intragene is present (continued)

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Table 4.5 (continued) Transgenesis

Cisgenesis

Intragenesis

Genome editing

End product

Plants with genetic material from the same or a sexually compatible or incompatible species and genetic material from other organisms, inserted in a random location

Plants with genetic material (entire gene with its own regulatory elements) from the same or a sexually compatible species, inserted in a random location

Plants with genetic material (new combination of regulatory and coding DNA fragments) from the same or a sexually compatible species, inserted in a random location

Plants without exogenous DNA and with only limited targeted changes of a specific gene

Speed/cost/ease of use

About 1 or 2 years Low-cost Ease of use due to the presence of markers to select transformants The ease of use depends on how amenable the target variety is for in vitro culture

About 1 or 2 years Low-cost The ease of use depends on how amenable the target variety is for in vitro culture

About 1 or 2 years Low-cost The ease of use depends on how amenable the target variety is for in vitro culture

About 1 or 2 years Low-cost The ease of use depends on how amenable the target variety is for in vitro culture and, in case of direct delivery, for regeneration from protoplast

Biosafety concerns

Presence of No foreign genes No foreign antibiotic/herbicide into the plant genes into the resistance markers genome plant genome Foreign genes into the plant genome

Effect of the expression of Cas9 protein specificity and fidelity of Cas9 protein

by traditional breeding are retained (Schouten et al. 2006). In an edited plant, a programmable nuclease will induce a double stranded break which is repaired by the cell natural repair mechanism, either non-homologous end joining (NHEJ), which may introduce nucleotide variation, or homologous direct repair (HDR) when a donor DNA with homologous arms is present (Xiong et al. 2015). The introgression of desired traits through conventional breeding into commercial varieties of woody fruit crops with a long juvenile phase usually requires a lapse of time that can last several decades and the application of ETGM to overcome these constraints has raised a great deal of ethical criticisms. NBTs may represent a valid alternative to these approaches to produce a genetically improved plant without the introgression of foreign DNA. Compared to other woody perennial species, the grapevine features several characteristics that make it a suitable system for the application of NBTs. This holds true

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in particular for genotypes used by the wine industry, represented by elite cultivars selected over the years in the various traditional viticultural areas and vegetatively propagated for decades or centuries. Cultural aspects, varietal traditions and consumer demands hinder the application of genetic engineering to these genotypes, as well as of classical breeding techniques because crossing would alter their peculiar agronomical and qualitative features. Therefore, the genetic improvement of wine grapes may gain a great benefit from NBTs, which require shorter times than traditional breeding techniques and do not alter the genetic heritage of the cultivar (Table 4.5). Grapevine was one of the first plant species included in genome sequencing programs and a well annotated, constantly improved reference genome has been publicly available since 2007 (Jaillon et al. 2007). This important achievement has allowed a large number of transcriptomic and gene functional analyses, which represent a valuable base of knowledge facilitating the selection of candidate genes and the application of NBTs. Indeed, many efforts have already been made to identify interesting genes to be engineered with both ETGM and NBTs (Capriotti et al. 2020). Moreover, protocols for culturing and transforming cell suspensions, hairy roots or embryogenic calli and for regenerating whole plants starting from various explants, including protoplast, have been set up and improved to accomplish the specific requirements of some cultivars (Bertini et al. 2019; Dalla Costa et al. 2019; Scintilla et al. 2021). However, there are still several technical challenges, which may hamper the application of cisgenesis and genome editing to the grapevine. The setting-up of efficient tissue culture procedures requires further development and optimization of several technical aspects, especially for many economically important élite cultivars proved recalcitrant to gene transfer and/or regeneration (Gribaudo et al. 2017). Another limiting factor is the chimerical integration of exogenous DNA and somaclonal variation as an outcome of tissue culture. In grapevine, somaclonal variation is frequently observed among plants regenerated through somatic embryogenesis, resulting in a wide range of traits regarding chlorophyll deficiencies, morphogenetic development, leaf shape and flower type (Martinelli and Gribaudo 2001). An important aspect to take in consideration for the choice of the target sequence is the high heterozygosity of the grapevine genome and the high degree of intraspecific genetic variation among cultivars and accessions. Finally, despite the many efforts made to explore the grapevine genome, the list of interesting candidate genes to be edited is still small and further studies are needed to enlarge the number of candidates, sufficiently characterized to be an object of NBT application. Given the above mentioned limitations, no NBT-derived grapevines have been obtained to date. However, considering the rapid biotechnological advancements achieved in the last few years, the successful production of cisgenic and DNA-free genome edited vines is around the corner. A primary goal for cisgenesis could be the transfer of genes which confer resistance to the major fungal and oomycete pathogens in cultivated grapevine (PM and DM) (Capriotti et al. 2020; Dalla Costa et al. 2019), whereas for the genome editing approach could be the silencing of susceptibility genes, whose knock-down confer resistance to pathogens (Pirrello et al. 2021). An up-to-date overview of the attempts to apply genome editing is presented in the next sections.

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4.13.2 CRISPR/Cas System for Gene Editing Genome editing is carried out using sequence-specific nucleases, including zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs) and, more recently, the CRISPR/Cas9 system (Yin et al. 2017). The doublestranded breaks induced by the sequence-specific nucleases at targeted genome sites are generally repaired by NHEJ or HDR, which lead to gene knockout or gene replacement, respectively. In particular, CRISPR/Cas9 technology is a cutting-edge approach comprising a Cas9 effector protein and a single guide RNA (sgRNA). The Cas9 nuclease is guided to the target DNA by the sgRNA which contains a sequence that matches the sequence to be cleaved. Essential for cleavage is a threenucleotide sequence motif (NGG) immediately downstream on the 3’ end of the target region, known as the protospacer-adjacent motif (PAM). RNA-guided Cas9 creates site-specific double-stranded DNA breaks, which are then repaired by either non-homologous end joining or homologous recombination (Jinek et al. 2012). Prime editing is the most recent CRISPR genome-engineering tool, described as a “search-and-replace” genome editing technology, that represents a novel approach to expand the scope of donor-free precise DNA editing to not only all transition and transversion mutations, but small insertion and deletion mutations as well (Kantor et al. 2020). Prime editing involves a longer-than-usual gRNA, known as pegRNA, and a fusion protein consisting of Cas9 H840A nickase fused to an engineered reverse transcriptase (RT) enzyme. The Cas9 element of the prime editor digests the genomic DNA and the RT element polymerises DNA onto the nicked strand based on the pegRNA sequence (Matsoukas 2020). Genome editing in tree crops by CRISPR/Cas9 is an emerging field and in grapevine very few examples of successful application to dissect gene functions and enhance plant traits have been reported. The first proof-of-concept was provided by Ren et al. (2016) who modified the metabolism of tartaric acid. The mutation of the L-idonate dehydrogenase (IdnDH) enzyme was obtained by stable integration of the genetic components of CRISPR/Cas9 system through A. tumefaciens gene transfer of ‘Chardonnay’ suspension cells. In 2017, ‘Neo Muscat’ somatic embryos were transformed with a CRISPR/Cas9 editing construct targeting the phytoene desaturase gene and plants with albino leaves were produced (Nakajima et al. 2017). In 2020 embryogenic grape cells derived from 41B rootstock were used to knock out CCD8 genes, involved in the control of shoot architecture in grapevine (Ren et al. 2020). Wang et al. (2018b) generated transgenic ‘Thompson Seedless’ lines with biallelic mutation of the WRKY52 transcription factor, with improved resistance to noble rot caused by B. cinerea. The authors therefore provided the first strong evidence in using CRISPR/Cas9 to enhance disease resistance in grapevines. Subsequently, Sunitha and Rock (2020) produced resistant transgenic plants with CRISPR/Cas9 targeting TAS4b, a molecular determinant of GRB virus and PD host susceptibility, and the anthocyanin regulator MYBA7 in the 101–14 rootstock. Wan et al. (2020) showed that CRISPR/Cas9 MLO3-edited grape lines had enhanced resistance to grapevine PM, and Li et al. (2020) reported that PR4b loss-of-function lines had decreased resistance to P. viticola.

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Still, the wide application of genome editing to grapevine faces many challenges, above all, the previously mentioned bottlenecks of the length and the variety-specific efficiency of the regeneration process. In addition, a general constraint is represented by the need to improve several aspects for a precise and efficient editing. Ren et al. (2021) demonstrated that the use of the identified U3/U6 and UBQ2 promoters could significantly increase the editing efficiency in grapevine by improving the expression of sgRNA and Cas9, respectively. Moreover, this study represented the first example of multiplex genome editing in grapevine through the simultaneous editing of the sugar-related tonoplastic monosaccharide transporter (TMT) family genes TMT1 and TMT2. The occurrence of the off-targets, which are highly undesired, was recently investigated by Wang et al. (2021) in grapevine, showing that their frequency is likely insignificant compared with variations caused by tissue culturing and/or Agrobacterium infection. However, the use of Cas variants with higher specificity, accuracy and ability to recognize different PAM sequences, may further reduce the occurrence of these unfavorable events. The requirement of a specific PAM site (NGG) adjacent to the target site limits the number of potential targets. Up to now, five types of CRISPR/Cas9 target sites have been identified and characterized and a user-friendly database for editing grape genomes has been developed (Wang et al. 2016b). Additional general drawbacks of CRISPR/Cas9 technology are represented by the pleiotropic effects associated with the knockout of target genes, the challenging of gene knock-in approach compared to knock-out and the need of a biallelic editing in the case of recessive mutation. These aspects represent a severe limitation in grapevine, species in which functional analysis has been performed on a relatively small number of genes. An alternative strategy to limit pleiotropic effects associated with an abolished gene function is represented by the quantitative regulation of gene expression achieved with genome editing on cis-regulatory elements (RodríguezLeal et al. 2017). For selecting the best target sequences the grapevine reference genome can be used. However, after this step, a subsequent sequencing of those regions in the genotypes of interest is needed to avoid bumping into SNPs which can prevent an optimal recognition by the endonuclease and consequently the DNA cleavage.

4.13.3 Towards the Generation of Transgene-Free Resistant Grapevines The adoption of NBTs might represent a revolutionary cutting-edge in worldwide grapevine breeding and cultivation, but this requires government support in setting up an updated regulatory framework. Some non-European countries (e.g. USA and Australia) have established that if no foreign DNA is present in a genome edited variety it will not be subject to additional regulation and risk assessment, whereas European Union strongly reaffirmed the precautionary principle and genome edited

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organisms are currently included in the strict legal framework of genetically modified organisms. Yet, a recent document by the EU announced the revision of the legal status of NBT products (https://ec.europa.eu/food/sites/food/files/plant/docs/ gmo_mod-bio_ngt_exec-sum_en.pdf) which may facilitate their diffusion in the near future. In any case, the absence of foreign DNA is mandatory for complying with legal clues on organisms subjected to NBTs. The production of DNA-free edited plants is mainly based on two strategies (Zhou et al. 2020). The first one involves the stable integration in the genome of the CRISPR/Cas9 genetic components through A. tumefaciens T-DNA gene transfer and their subsequent removal. While for annual plants these components can be eliminated by self-fertilization and segregation in the first generation of offspring, in case of vegetatively propagated woody fruit crops this could be achieved by the use of site-specific recombination systems which leads to the excision of the foreign DNA. In grapevine, some preliminary studies successfully tested the mechanisms for the removal of foreign DNA. Dalla Costa et al. (2016) set up the experimental conditions for the application of a heat-shock treatment to activate the site-specific recombinase Flippase (Flp) which recognizes the target sequences. Heat-shock induction for the removal of the kanamycin resistance gene nptII was carried out on genetically modified ‘Brachetto’ in vitro lines. The same research group recently proposed an alternative approach based on heat-shock treatment (Dalla Costa et al. 2020). The procedure exploits the cleavage activity of Cas9 not only to edit the endogenous target site, but also to remove foreign DNA by placing two additional synthetic target sites next to the left and right borders. In this study the CRISPR/Cas9 system was used to knock-out the MLO7 gene involved in the susceptibility of PM and a very detailed analysis the bacterial T-DNA molecular features at the insertion site, crucial for the excision of T-DNA cassette, was performed. The second strategy to obtain DNA-free edited plants is based on the transient expression of the CRISPR/Cas9 components from non-integrating foreign DNA, not yet applied in grapevine, or on the direct delivery of the in vitro assembled ribonucleoprotein (RNP) composed by purified Cas9 protein and gRNAs. This approach was adopted by Malnoy et al. (2016) demonstrating that the direct delivery of CRISPR/Cas9 RNPs to ‘Chardonnay’ protoplasts enables targeted gene editing, despite whole plants from edited protoplasts could not be regenerated. Subsequently, Osakabe et al. (2018) provided a stepwise protocol for the design and transfer of CRISPR/Cas9 components to apple and grapevine protoplasts, and Ren et al. (2019) helped to optimize CRISPR/Cas9 performance in grape by showing that sgRNAs with high GC content improved editing efficiency in grapevine and that editing efficiency also depends on selecting the appropriate cultivar. However, several additional important technological steps still need further development. For instance, a selectable marker-free method is required for the recovery of edited plants at high frequencies. Furthermore, the delivery of RNP complexes via protoplasts transfection is limited only to some plant species and in grapevine the regeneration process from single cell is a major bottleneck. The isolation of protoplasts from embryogenic grapevine tissue and the regeneration of these protoplasts into plants were successfully reported in few early works for two V. vinifera cultivars ‘Seyval blanc’ (Reustle

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et al. 1994) and ‘Koshusanjaku’ (Zhu et al. 1997). Recently, a stepwise protocol for the regeneration of whole plants from embryogenic callus-derived protoplasts of two Italian varieties, ‘Garganega’ and ‘Sangiovese’ was developed (Bertini et al. 2019). These works paved the way to further specific development of regeneration protocols, broadening the spectrum of varieties prone to be edited by CRISPR/Cas9 technology.

4.13.4 Future Challenges Conventional breeding has been fundamental for grapevine domestication and improvement, resulting in a huge amount of different varieties adapted to the cultivation in a wide range of pedoclimatic conditions. However, due to the low accessibility of desirable variations or gene combinations, cross and mutation breeding of new cultivars requires the production and analysis of large numbers of offspring, and takes a long time. The gene editing technology developed in recent years allows precise engineering of desirable variants with unprecedentedly high efficiency and resolution, greatly expanding the range of variations available and reducing our reliance on naturally existing mutations. Efficient transformation and regeneration procedures have been established for a number of grape varieties and the strength of the artificially generated variations driven by CRISPR/Cas9 technology has been demonstrated. However, despite several biotechnological approaches covering all the necessary steps, they need to be combined in complete procedures for the generation of cisgenic or edited plants. Finally, the adoption of high-throughput techniques, still applied to a limited extent to the grapevine, could help characterize the phenotype of plants obtained by NBTs in the vineyard and in a controlled environment, increasing the objectivity, automation and precision of data collected. A new biotechnology-driven revolution in viticulture could be just around the corner.

4.14 International Hybrid Regulations: Status and Background 4.14.1 Hybrids in Viticulture The use of hybrids in viticulture is under continuous discussion, even if this sector has a big challenge to maintain sustainable production under climate change scenarios and foster its adaptation. The use of new cultivars could be a medium-long term adaptation technique and provide new solutions to reducing pesticides, controlling vine decay, water management and stress, etc. Hybrids were used in the past for trying to solve relevant problems, like the phylloxera plague in Europe during the second half of the nineteenth century. It should be remarked that one of the possible

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solutions discussed was hybridization because American species are often naturally phylloxera-resistant or tolerant (V. aestivalis, V. rupestris, V. riparia and V. labrusca). Even if this problem was generally solved by grafting American rootstock with European varieties, some areas had a great dispersion of these American direct producer vine varieties and hybrids were so successful (see Sect. 4.6.1). For instance, in 1958, 30% of French vineyards (400,000 ha) were covered by fungus-resistant grape varieties or in Pontevedra (Galicia, Spain) in 1983, covering 73% of total vineyard area (Martínez and Pérez 1995). Nevertheless, due to organoleptic (insufficient quality, foxy aroma and strawberry flavours in wine), compositional (high methanol or malvidin content) or ethical (genetic modifications) questions, not all countries accept this material for making commercial wines.

4.14.2 Hybrid Wine Profiles American and Asian species are repeatedly backcrossed to V. vinifera cultivars with the main objective of transferring their resistances (mainly powdery and downy mildew) into the vinifera genetic background, restoring or improving their traits and of course, maintaining their oenological aptitude (de la Fuente 2018). A typical characteristic of the red wines produced from these cultivars is the malvidin content in their wines. Malvidin is an anthocyanin (principal red colouring matter), present in the form of malvidin-3,5-diglycoside, and being a common natural compound in the red grapevine skins, together with the other coloring pigments. Due to this discussion, the OIV defined in this “compendium of international methods of wine and must analysis”, a clear methodology for analysing malvidin glucoside (OIVMA-AS315-03; 377/2009) content and fixed the maximum acceptable malvidin limit (15 mg/L) for a wine. Besides this, the true situation is that new cultivars or some hybrids mainly based on V. vinifera, but with one or more backcrossed genes from wild American species from breeding programs (e. g. ‘Regent’), even if they are classified as V. vinifera, they exceed the OIV threshold for malvidin diclucosides. Some cultivars are rejected for the production of quality wine at the European level (Art. 81 b CE 1308/2013). This discussion is never ending at the international level, but it should keep on being discussed because scientific limits are not well applied to this topic at present, and OIV standards usually help to harmonize these questions.

4.14.3 Evidence of Hybrid Utilization Worldwide Despite the above mentioned problems concerning hybrid wines, the use of hybrids is common in non-European countries. For instance, sparkling wines in Brazil are frequently based on V. labrusca and hybrids (Caliari et al. 2014), being in some regions more than 90% of the total vineyard area for wine production. It should be noted that Brazil has a total surface vineyard of 79.094 ha, in which close to half

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are planted with hybrids (data source OIV; 2015). China, which started in the 1950s a great breeding program facing the cold resistance for wine and fresh grapevine varieties, has arisen more than 70 new cultivars, today which means thousands of ha (Li 2014). Furthermore, the Korean hybrid grape cv. ‘Cheongsoo’ was selected in 2005 and spread for its good winemaking performance (Chang et al. 2014; Kim et al. 2015). In the United States, several breeding programs have released well-adapted wine and table grape cultivars with improved disease and virus resistance (Reisch and Reynolds 2015), and these have been widely adopted, especially in regions where it is more difficult to grow V. vinifera cultivars. Additionally, the University of California, Davis, has released five new winegrape cultivars derived from a PD resistant genotype of V. arizonica. There are no regulations restricting the planting of any of these new cultivars, other than the need to register the name with the U.S. Tax and Trade Bureau if the name is intended for use on a wine label (https://www.ttb.gov/wine/grape-var iety-designations-on-american-wine-labels). Even in Europe, there are some interspecific hybrids produced by crossing V. vinifera and other species, which can provide certain traits of Vitis spp. The complex hybrid ‘Aletta’ was qualified in 2009 by the Hungarian register, and in 2012 the surface area was 423 ha and now has risen to 1,300 ha (Hajdu 2015). France created the national observatory for the development of resistant vine varieties in 2016 (OsCar; https://observatoire-cepages-resistants.fr/en/), a participatory network under a minimum of 6 years program for studying and validating the potential of these new cultivars in different locations and their adaptation before establishing them as new commercial varieties, under a temporary or final registration. This observatory is a great example of public and private collaboration between research centres (INRAEIFV) and producers associations, linked to the French denomination of origin institution (INAO). The collaboration resulted in four INRA ResDurI cultivars (‘Voltis’, ‘Artaban’, ‘Vidoc’, and ‘Floreal’), which have a significant impact to the French wine sector. Germany also has more than 50 years of breeding programs with some cases of success (e.g. PIWI family). Cooperative (VCR) breeding efforts in Italy resulted in several new resistant cultivars currently being plant in Europe and North America, including ‘Fleurtai’, ‘Soreli’, ‘Merlot Kanthus’, and ‘Cabernet Volos’. Including the four new varieties ‘Termantis’, ‘Nermantis’, ‘Valnosia’, and ‘Charvir’ recently released by FEM, a total of 31 mildew resistant/tolerant cultivars are now registered at the Italian grapevine variety catalogue (http://catalogoviti.politicheagricole.it/cat alogo.php).

4.14.4 Regulation Framework This complexity of existing and used Vitis species (see Sect. 4.5.1) offers a great number of different inter- and intra specific crossings and adds difficulties to establish definitions and regulations on this topic. Under this composite framework, the OIV is working (since 2016) on defining relevant concepts concerning the classification of

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grapevine material used. The genetic resources and vine selection (GENET) group of experts from Commission has drafted the first version of this document (VITIGENET 19–610), including a provisional definition of cultivated variety, grapevine variety, clone, direct producer hybrid, etc. This will be a relevant work from the experts, and it could have a great impact on the world wine sector. Some discussions remain at the group and by now this project resolution is kept at step 3. Together with this resolution, Commission I is also working on another draft concerning management of plant material exchanges: VITI 14–565. OIV Guidelines for production and exchange of viticultural plant material: phytosanitary and genetic aspects. OIV has recently approved other resolutions, which have a real impact on the selection process: OIV process for the clonal selection of vines (OIV-VITI 564A-2017) and OIV process for the recovery and conservation of the intravarietal diversity and the polyclonal selection of the vine in grape varieties with wide genetic variability OIVVITI 564B-2019). The first one is the updated version of the previous resolution (OIV-VITI 1–1991) including one definition for the selected clone: “A clone is the vegetative progeny of a single vine plant. For selection purposes this single plant is chosen for its varietal identity, its phenotypic traits and its sanitary state”. Other definitions should be addressed in future resolutions as mentioned before. The second one defines the polyclonal selection protocol as a process for the recovery and conservation of intravarietal diversity and polyclonal selection of grapevines on vines with wide genetic variability. In annex I, this resolution has a glossary of concepts that could be used at an international level, but this glossary should only be applied within the scope of this resolution. At the European level, the use of hybrids for wine production under a protected designation of origin (PDO) label is currently banned, however, the interest in these varieties and wines produced, either under the protected geographical indication (PGI), without a quality seal or in third countries is increasing (Aranda and Armengol 2019). Since 2013, the regulation on PDOs and PGIs has been established by the Parliament and European Council Regulation (EU) 1308/2013, establishing the common market organization (CMO) for agricultural products, and specifically for wine products (in Articles 92 to 111). Wines labelled under a PDO must be produced by a V. vinifera variety (Article 93) and wines qualified under a PGI, must be produced by V. vinifera or hybridizations between V. vinifera and other species of Vitis genus. Even more, some specific hybrids are detailed in this legislation as forbidden varieties for wine production: ‘Noah’, ‘Othello’, ‘Isabella’, ‘Jacquez’, ‘Clinton’, and ‘Herbemont’ (Article 81), without any label consideration. In some Countries, new disease resistant cultivars are registered as V. vinifera.

4.14.5 New Regulations and Perspectives During recent years, a new common agricultural policy (CAP) and therefore a new CMO, are being drafted and discussed by European countries, and they are expected

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in 2023 (at the latest). Discussion is on the table, and some grapevine varieties for wine production could be allowed, with the main objective to “increase resistance to diseases and improve the grapevine adaptation to climate change”. In that case, some hybridizations or backcrossed varieties from V. labrusca or others could be planted and produced. In 2018, within the proposal on the CMO regulation, some relevant modifications were proposed to the Commission, including the possibility to accept the six forbidden hybrids. On the positive side, these varieties could be beneficial for both producers and consumers, by significantly limiting the amount of pesticides used and therefore, having a positive impact on the environment and profit margins of the farmers. On the other hand, it was underlined that opening of these wine grape varieties belonging to V. labrusca and of the six forbidden varieties would decrease the quality of the wine products and therefore, could affect the reputation of European wines. Discussions showed a clear difference of opinion between the main wineproducing countries (strong and motivated opposition) and the rest of the Member States (more flexible or keen to accept it). This point is still being discussed today. Disease resistant vines and future vineyards underline the role of further research and innovation in the sector and the need to (a) find new genetically resistant varieties to reduce the negative aspects linked to the use of pesticides or (b) explore current varieties for wine production with enough genetic variability, necessary to face adaptation needs. With current technological advances and specialized knowledge, there is a large potential for R&D in viticulture, boosting some sustainable varieties which would adapt to agronomic conditions and which could be properly selected with wine tasting quality criteria. It should be remarked that the OIV definition of wine is as follows: “Wine is the beverage resulting exclusively from the partial or complete alcoholic fermentation of fresh grapes, whether crushed or not, or of grape must” and the official OIV grapevine varieties and synonyms database does not differentiate between V. vinifera and other cultivars (de la Fuente 2018).

4.15 Future Perspectives Growers can now utilize grape varieties (from inter- and intraspecific hybridization) and rootstocks (normally hybrids of American Vitis spp.) with tolerance to biotic stresses. This resilience can be further improved by breeding programmes selecting new clones and producing new varieties and rootstocks. The history of grapevine breeding for disease resistance (mostly for wine grapes) began with the FrenchAmerican hybrids and demonstrated the technical, societal and regulatory hurdles that need to be overcome (Bavaresco 2019). Climate change will likely push forward the demand for wine and table grape varieties with better adaptation to warmer and likely drier climates, and for rootstocks with better adaptation to drought and salinity. For wine and table grapes this process may depend on gene editing techniques capable of altering gene expression to improve fruit and wine quality under new climates. At any rate, it seems likely that climate change will spur on the discussion of whether and

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where we will need better adapted fruit and rootstock varieties, and what breeding and improvement strategies we will use to achieve these goals. Considering fruiting varieties, about the technical aspects, a wider exploitation of intravarietal variation is needed, particularly of the ancient V. vinifera varieties; we cannot select resistant or tolerant clones, but less susceptible individuals are known and could be exploited in clonal selection programs. Moreover, a larger utilization of all the available V. vinifera germplasm should be encouraged, because unexpected findings do occur, such as the discovery of strong PM resistance genes in Central Asian vinifera. Traditional breeding methods have been improved and time-consuming procedures utilized for classical hybridization have been improved and accelerated by the application of MAB approaches, and may improve further with the application of transgenesis, cisgenesis, and genome editing. Marker-assisted breeding is a very useful if precise phenotyping analysis is performed. Phenomics is a promising approach with the capacity to greatly improve breeding progress. It will be crucial for exploiting and linking in a correct way the genomic information to the plant’s physiology and behaviour. On the other hand, only a thorough genetic characterization will allow for an understanding of which genes are involved in the resistance response of the plant. Marker-assisted selection currently supports both the choice of the parents to be hybridized and the selection of the proper individuals in the segregating populations (progeny). Regarding the selection of the new progeny, MAS reduces the number of seedlings to be grown, but field trials are still necessary to verify the behaviour of the new plants under different growing conditions. Since MAS allows a reduction in the number of seedlings to be grown, a larger number of seeds can be managed and this is positive because the higher the number of seeds, the greater the possibility of selecting the optimum individuals. Moreover, within the whole “economy” of a specific breeding program, MAS will allow many more pathogen and pest resistance evaluations to be conducted, and will allow greater progress beyond resistance to PM, DM and PD. It is crystal clear that for a thorough genetic improvement a comprehensive program is required, linking a variety of ad hoc programs. Multiple parallel programs shall consider both quality- and resistancerelated traits, focusing on a final shared goal. It will be challenging to obtain a new individual completely and durably resistant to all the pathogens and pests but, even though a few treatments are required, the overall impact of resistant varieties will be a healthier environment and populace, and a more sustainable wine industry. Another aspect to be emphasized is the need to develop local breeding programs in order to obtain new individuals well adapted to that specific environment. In fact, other pedoclimatic conditions (with different pathogen/pest races and pressures) might modify the vine response in terms of both grape quality (ratio sugars/acids, aromas, etc.) and of disease resistance. Thus far, the reaction of wine growers and makers to new disease resistant wine varieties has not been highly appreciative because of the relatively poor quality of the earliest hybrids when compared to traditional pure vinifera varieties. Marker-assisted breeding has the potential of maintaining high resistance by following marker expression over multiple generations, allowing the breeder to focus on fruit and wine quality in the later generations when the percentage of vinifera

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in the advanced selections is high. Future breeding programs for biotic stress resistance, in which breeders can focus on fruit and wine quality while selecting in the early generations, should carefully select against poor quality fruit characteristics and for high wine quality. The NBTs, especially genome editing, are very promising methods to help with the development of improved fruit and wine quality through the alteration of gene expression and biochemical pathways. We are at the dawn of a new (scientific) revolution, enabling scientists to alter plants for suitable and sustainable cultivation. The potential “plus” given by genome editing consists of the possibility to rearrange only the disease/pest resistant genes without manipulating the other traits of the plant, especially those related to the quality parameters for wine and table grapes. Gene editing may have a very large impact on the expression of biochemical by-products we consider responsible for high wine quality. However, a thorough understanding of the genome and phenome and very effective phenotyping and genotyping techniques will be needed. When societal issues are considered, few problems are likely to arise with the selection of new clones, while the acceptance of new disease resistant or geneedited varieties may be problematic for wine grapes, regardless of the technologies with which they were obtained. Table and raisin grapes, being a regular fruit, may encounter fewer issues, if obtained by the CBTs. In addition, new wine variety names might create mistrust among consumers, but only if the wine is sold with the variety name; by contrast, for table grapes a new name might be very attractive. Much more problematic will be dealing with the NBTs, for both wine and table grapes. Although genome/gene editing techniques do not transfer foreign genetic material and are based on the use of molecular scissors (biological mutation), they do recall a genetic manipulation and therefore a hostile reproach by the public is likely to occur, even in the countries where NBTs will be allowed. That is why education as well as open dialogue between scientists and the public on a rational basis is relevant. All of the participants in the wine chain, including retailers and the consumers, will need to be convinced of the science behind gene editing for this technology to become a real innovation. Moreover, there is the need to move the policy discussion from the national/international level to local communities, which will be the first to feel the context-dependent impacts of any release. In other words, we need collective oversight (Kofler et al. 2018). Concerning the regulatory aspects, new disease resistant wine grape varieties will have no restriction in countries outside the EU, while in EU they will be allowed to produce table and PGI wines and most likely also PDO wines. In the next review of the wine CMO, clearer provisions will be established on this topic. In France, for instance, INAO created a new category of wine grape varieties called “grapes for climate and environmental adaptation” (including the new disease resistant varieties) to be used in the production of PDO wines and approval is expected by the EU in the next CMO. In the case of new resistant varieties for table/raisin grapes, no international cultivation restrictions are present, and in the countries with a national grapevine register (NGR), their registration is only mandatory to allow propagation by nurseries. Derived from both classical breeding and MAB, a new grape variety can undergo the patent process. In the EU, the community plant variety office (CPVO), a

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self-financed EU agency, is responsible for the management of the community plant variety rights system, covering the 27 Member States. Located in Angers, France, the CPVO was created by the Council Regulation 2100/941 and has been operational since April 1995. The grape varieties (including the resistant ones) protected by plant variety rights are registered and can be found in the CPVO database (https://cpvoex tranet.cpvo.europa.eu/Denominations). On paper, it is impossible to distinguish the resistant varieties from others, because they are registered as V. vinifera. A new vine coming from the NBTs will be most likely considered as a clone, bearing precise distinguishable characteristics. Considering rootstocks, the perspectives are to improve the resistance/tolerance toward current/emerging pathogens and pests by both CBTs, ETGMs and NBTs. No societal problems are expected to occur with NBTs since the rootstocks are not the fruit bearing part of the plant. Concerning the regulatory aspects, the registration of new rootstocks is under the same requirements as for the fruiting varieties (Directive 2004/29/CE of 4 March 2004). The nurseries (in the EU) have some rules to follow, i.e. to propagate genotypes registered in the NGR while the grape growers can use the rootstock they wish, without any restriction.

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Chapter 5

Wild and Related Species as a Breeding Source for Biotic Stress Resistance of Peach Cultivars and Rootstocks Thomas M. Gradziel

5.1 Introduction Peach, Prunus persica (L.) Batsch, represents the most economically important stone fruit with global production surpassing 26 million tons with a production area of more than 1.45 million ha (FAOSTAT 2020). China is the main producer with over 14.2 million tons. Spain and Italy are the major European producers with significant production also from the United States and Iran. Peaches are consumed as a fresh or processed fruit, with most processing by canning with frozen products as well as juices and purées also being important. Globally, approximately half the total production is for processing-type peaches which are usually nonmelting-clingstone types because of their more desirable fruit firmness. Peaches for fresh market are often melting-freestone types, but nonmelting clingstones, even melting clingstone remain popular in certain regions. Nectarine, a type of peach where a genetic change has resulted in glabrous or fuzzless fruit, has become increasingly important as a fresh market peach owing to its improved eating quality, though this change also makes it more vulnerable to insect and disease damage. Peach, along with interspecific hybrids to closely related species, are important rootstocks for stone fruit, particularly cultivated peach and almond. Peach is also widely planted as an ornamental tree because of its showy bloom. Peach is primarily grown in temperate climates though production in subtropical climates is possible using low-chill cultivars.

T. M. Gradziel (B) University of California-Davis, Davis, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_5

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5.2 Biotic Stresses The major categories of biotic stresses for peach cultivars and rootstocks include diseases, pests and viruses. Economically important regional diseases caused by fungi include fruit brown rot (FBR) caused by various Monilinia species, powdery mildew (PM) primarily by Podosphaera pannosa (Wallr.:Fr.) de Bary and Podosphaera clandestina (Wallr.:Fr.)Lév. and peach leaf curl caused by Taphrina deformans (Berk.) Tul. Fungal gummosis as caused by Botryosphaeria dothidea (Moug.:Fr.) Ces., De Not. is also economically important in certain regions. Important bacterial diseases include bacterial canker caused by Pseudomonas syringe pv. syringae van Hall, cytospora canker caused by Cytospora leucostoma (Pers.) Sacc., bacterial spot caused by Xanthomonas arboricola pv. pruni (Smith). Important foliage diseases are anthracnose (Gloeosporium amygdalinum and Colletotrichum acutatum), shot hole caused by Stigmina carpophila), travelure (Fusicladium amygdali), and fusiccocum (Fusicocum amygdali). Blossom blight, as caused by the Monilinia species M. laxa, and M. cinerea and less often by Botrytis cinerea, can severely damage bloom and young developing fruit. As with many fruit and foliar diseases, they are most serious in years with frequent rains. Subsequent infection and disease development on the fruit results in fruit brown rot (FBR) which is arguably the most serious peach disease worldwide estimated to be responsible for up to 80% of all postharvest losses (Obi 2018). Peach trees are vulnerable to the same viruses affecting stone fruits: primarily being the NEPO (Tomato black ring, Tomato ring spot, Yellow bud mosaic) and ALAR groups (ringspot, prune dwarf, line pattern, calico, apple mosaic). Different mosaic patterns on leaves and flowers can result from different combinations of viruses. More recently, the Plum pox virus (PPV), has become an important disease damaging both trees and fruit (Martínez-Gómez et al. 2004). Owing to the severe threat to production of peach and other stone fruits, regional quarantines are often used to limit the virus spread, though these quarantines can also severely hamper transport and marketing of both fruit as well as nursery trees. Similar quarantine and market restrictions are also commonly employed to prevent the introduction of invasive pests. Important peach pests, include peach tree borer (Anarsia lineata) as well as navel orange worm (Paramyelois transitella) (Rice et al. 1996). Green aphids (Myzus persicae (Sulzer) can damage production as well as vector PPV. Mite species causing serious economic damage include two spotted spider mites (Tetranychus urticae Koch), brown almond mites (Bryobia rubriculus Scheuten), the European red mite (Pannonycus ulmi Koch) and the pacific spider mite (Tetranychus pacificus). Mite damage results from reduction in both production and fruit quality, and is particularly problematic under environments with high temperatures, moisture stress and dust. Important rootstock diseases include crown gall (CG) (Agrobacterium tumefaciens) which can be introduced by infections through the root and crown during nursery tree production with subsequent colonization of the infected tree followed by further spread within and among orchards. Oak root fungus (ORF) (Armillaria

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mellea) probably causes the most serious disease losses worldwide. Infection by Phytophthora species can result in ‘crown rot’ which can be particularly damaging where rootstocks are exposed to excess moisture over time. Finally, soil-borne nematodes represent a very serious rootstock problem (McKenry 1989). Root knot (RKN) (Meloidygyne incognita (Kofoid, White) Chitwood; Meloidygyne javanica), ring nematode (Criconemoides spp.), dagger nematode (Xiphinema spp.) and lesion nematode (Pratylenchus spp.) are the most destructive globally. Nematodes can also be important vectors for virus diseases including Tomato ringspot as well as Yellow bud mosaic virus. Similarly, a higher risk of developing bacterial canker is associated with the presence of ring nematodes. Under conducive environments, usually warm, rainy conditions, losses from biotic stress can be severe. Losses from FBR disease alone are estimated to be in excess of $170 million annually. Losses ranging from 50 to 90% can be common under favorable environments, especially when chemical control is absent or ineffective. Even with chemical control, losses from 10% to as high as 60% can be common (Obi 2018; Obi et al. 2020). Indirect losses also accrue from the expenses for fungicide applications as well as problems in marketing blemished fruit. Depending upon the extent of disease/pest establishment, entire orchards can be lost, as is the case with ORF in the southeast US (Beckman and Pusey 2001) while commercial production in entire regions may be destroyed by the presence of invasive diseases or pests such as PPV (Martínez-Gómez et al. 2004). Environments conducive to greater orchard tree stress and so heightened disease and pest damage are expected to increase with future global warming (IPCC 2021).

5.3 Genetic Resources of Resistance Genes Peach has a very limited germplasm base owing to a domestication bottleneck followed by further inbreeding during modern variety development (Peace 2017). However, related Prunus species offer a wealth of variability because of their diverse evolutionary pathways. Species of subgenus Amygdalus include peaches as well as almonds. In addition to the cultivated peach (Prunus persica) five wild peach species: Tibetan peach (P. mira Koehne), Kansu peach (P. kansuensis Rehd.), Chinese wild peach (P. davidiana var. potaninii Rehd), Fergana peach (P. ferganensis (Kost.et Riab.) and Tibetan almond (Prunus tangutica), are readily inter-crossable and have been used to a limited extent for genetic improvement, particularly for rootstocks. Cultivated almond (Prunus dulcis) as well as an estimated 40–50 wild almond species are also readily hybridized and introgressed to peach primarily for rootstock development. The closely related subgenus Prunus contains plums and apricots (Potter et al. 2007; Potter 2011). Hybridization and introgression between peach and species in the subgenus Prunus are possible though difficult, occasionally requiring tissue culture for embryo rescue (Liu et al. 2012).

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5.4 Diversity Commercial peaches originated from a very limited Chinese germplasm (Byrne et al. 2012; Li et al. 2013; Hesse 1975; Akagi et al. 2016). Consequently, both phenotypic variation as well as variability in disease and insect resistance is similarly limited. Greater genetic variability is sometimes found within regional land races near the centers of domestication such as China, Japan and Korea, as well as isolated areas of subsequent dissemination, such as central Asia, South Africa, South and Central America (Cao et al. 2014; 2016). As an example, the cultivar Bolinha was bred for a high tolerance to FBR disease utilizing resistance sources of local Brazilian land races (Feliciano et al. 1987; Fu et al. 2018). Genetic analysis of these resistance sources, however, indicates that tolerance is based on multiple small-effect resistance mechanisms, frustrating traditional breeding methods including MAS and MAB. Additional genetic variability is found in the ornamental peaches (Cao et al. 2014; Akagi et al. 2016) though fruit quality in these types is typically poor. Greater genetic diversity is present in the previously cited peach species that are generally found in central to western China. An extensive, largely untapped variability is also available in the closely related cultivated almond and the large number of its wild relatives (Gradziel 2011). While also associated with poor edible fruit quality, the diverse origins of these species have resulted in distinct developmental pathways which, when transferred to peach, can result in more profound phenotypic changes including disease, pest resistance not observed among crosses between peach species. The extensive range within almond species for both genetic as well as evolutionary diversity have been well documented by numerous regional researchers (see Rahemi et al. 2012).

5.5 Species Sources of Biotic Stress Resistance Peach and its close wild species relatives are classified as in the genus Prunus, subgenus Amygdalus, section Persica, representing a related and so easily introgressed germplasm, though one that has proven relatively limited in genetic diversity and so breeding opportunities. The limited genetic variability is also a consequence of the self-fruitful and so inbreeding nature of these species. The cultivated almond and its wild relatives are classified as in the genus Prunus, subgenus Amygdalus, section Amygdalus and represent an unusually diverse germplasm owing to both a diverse range of habitats spanning the length of Eurasia as well as an obligate outcrossing requirement within most species. This diversity has long been utilized for rootstock improvement (interspecies rootstocks) but only recently used for cultivar improvement. Interspecies breeding barriers, while present, are often relatively easily overcome. Much greater effort is required, however, for successful hybridization and gene integration from the similarly diverse yet more distantly related plums in the genus Prunus, subgenus Prunus, section Prunus.

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5.5.1 Prunus Subgenus Amygdalus Section Persica Prunus davidiana is the wild peach species most extensively utilized in crop improvement, primarily for rootstock breeding and also because it has been a good source of resistance to rootknot nematodes (RKN) (Reighard and Loreti 2008). Several regionally important RKN resistant rootstocks including Nemaguard, Nemared, Guardian and Barrier-1 have Prunus davidiana in the parentage (Brooks and Olmo 1961). Nemaguard also demonstrates good resistance to M. incognita, M. javanica, M. arenaria, but is susceptible to a newly discovered root-knot species, M. floridensis (Nyczepir and Beckman 2000; Handoo et al. 2004). ‘Nemaguard’ has been reported to be vulnerable to P. vulnus, verticillium and other fungal root rots, iron chlorosis and root asphyxiation but somewhat resistant to CG. ‘Nemaguard’ is particularly sensitive to feeding by ring nematode (M. xenoplax), which can lead to tree injury and death from bacterial canker (Pseudomonas syringae pv. syringae van Hall) and to orchard replant disease syndromes (ORDS) such as peach tree short life (Zehr et al. 1976; Nyczepiret et al. 1983; Pascal et al. 1998). The more recently developed ‘Guardian’ rootstock has a higher tolerance to ring nematode, bacterial canker, ORDS (Reighard et al. 1997; Nyczepir et al. 1999, 2006). ‘Guardian’ has also been reported to be less susceptible to P. penetrans and comparable to ‘Nemaguard’ in susceptibility to P. vulnus (Reighard and Loreti 2008). ‘Barrier-1’ combines good resistance to RKN with a deep rooting ability and associated improved anchorage and nutrient mining and is also less vulnerable to waterlogging (WL) (Roselli 1998; Loreti and Massai 2002). In the area of cultivar breeding, Foulongne et al. (2003) have identified P. davidiana as having resistance or tolerance to PM with QTRs located on linkage groups (LG) 1, 2, 4, 6 and 8. Subsequent research by Sauge et al. (2012) has also identified quantitative resistance to green peach aphid with multiple QTR’s identified on all LG groups except 7. Prunus mira, while also reportedly to tolerant to resistant to RKN (Cao et al. 2011a, b), has not been used extensively in either rootstock or cultivar improvement. Other resistances attributed to P. mira include PM (Layne and Bassi 2008), peach mosaic virus (PMV) (Pine 1976) and it appears to be a good source for transferring the pillar tree architecture to peach (Gradziel, unpublished data), effectively converting orchards from the traditional three-dimensional to a two-dimensional conformation, greatly simplifying orchard management for disease and pest control (Scorza et al. 1985; Devyatov 1996). The remaining wild species in this subgenus, including Prunus kansuensis and Prunus tangutica, have not been extensively utilized for either rootstock or cultivar improvement, though they are used as natural rootstocks for fruit production in their native regions (Rahemi 2002; Wang et al. 2002). Several reports have identified P. kansuensis as a source for major genes for resistance and/or tolerance to RKN with resistance located on LG2 (Cao et al. 2011a, b; Maquilan et al. 2018a, b). Both P. kansuensis and P. tangutica are also regionally important ruderal species or germplasm useful for reforestation efforts (Moreno et al. 1994). P. tangutica is sometimes cited as having CG resistance but this has not been confirmed.

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Regional accessions of Prunus persica have also been important sources for rootstock improvement, though all are vulnerable to ORF (Dennis 2003). In poorly drained soils they are susceptible to infection by Phytophthora spp. related crown rot (Elena and Tsipouridis 2000). The ‘Lovel’l peach is widely planted as a rootstock and has been a source of improved tolerance to ring nematode and bacterial canker (Bliss et al. 1999). The ‘Rubira’ peach has been reported to be more tolerant of PM (Loreti 1984) and resistant to green peach aphids (Massonie and Paison 1979) where a major resistance gene has been located to LG1 (Lambert and Pascal 2011; Lambert et al. 2016; Pascal et al. 2017). ‘Rubira’ peach has also been reported to be less susceptible to CG and P. vulnus than other peach seedlings but is susceptible to RKN as well as M. arenaria (Massonie and Paison 1979; Loreti 1984). Resistance to RKN was reported by Claverie et al. (2004) to be located on LG2. A single dominant gene conferring resistance to PM was reported by Pascal et al. (2017) on LG8. Quantitative tolerance to FBR was reported on LG 2, 3 and 4; while Yang et al. (2013) isolated QTLs for resistance to Xanthomonas on LG 1, 4, 5 and 6. Hybrids between peach and almond have become important rootstocks for peach and other stone fruits because of their improved vigor as well as disease and pest resistance, though whether these desirable traits are inherited from a species parent or are consequence of the unique interspecies hybrid interaction is often unknown. The peach-almond hybrid ‘GF 677’ is extensively planted in Europe as an effective rootstock for stone fruit owing to its tolerance to calcareous soils as well as to ring nematode and CG. However, it is susceptible to A. mellea, M. incognita, A. tumefaciens, Phytophthora cactorum, S. purpureum (Loreti and Massai 1995) and to a lesser degree Verticillium alboatrum (Loreti and Massai 2002). The almond by peach hybrid rootstock ‘Adafuel’ is similarly very susceptible to RKN. (Moreno et al. 1994) but is reportedly resistant to PM, plum rust (Tranzschelia prunispinosae), shot hole (Corineum beijerinckii). Reighard and Loreti (2008) provide a detailed review of the important contributions of almond by peach hybrids in their excellent review of commercial rootstocks for peach.

5.5.2 Prunus Subgenus Amygdalus Section Amygdalus Although almond, including cultivated almond and its wild relatives, are classified in a different section (Amygdalus) than peach (Persica), these species represent a valuable source of resistance to biotic stresses for both cultivar and rootstock improvement. This is a result of their genetic/genomic similarity which presents minimal barriers to hybridization and subsequent introgression as well as the extensive genetic/genomic diversity acquired as the different almond species evolved within distinct environments across Eurasia. A high genetic/genomic variability is further promoted by the obligate-outcrossing common to almond species. Prunus dulcis, the cultivated almond, represents the most extensively used germplasm source for both peach cultivar and rootstock improvement, despite its relatively limited

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genetic variability which is a consequence of both domestication and breeding bottlenecks (Gradziel 2011). Notwithstanding this relatively narrow germplasm, Prunus dulcis represented an enormous expansion of genetic options when compared to the highly inbred peach (Scorza et al. 1985) and is often hybridized with peach as a rootstock to combine desired biotic, abiotic resistance, often with improved growth vigor which provided additional tolerance to stressful growth conditions (Prudencio et al. 2020). The historical requirement of seed propagation for most early hybrid rootstocks further encouraged the utilization of readily available commercial peach and almond selections. Successive self and backcross progeny from these hybrids rapidly segregated to either peach or almond phenotypes, encouraging their use in cultivar improvement, particularly as they provided desired traits unavailable within the recurrent parent. An example is seen in the inheritance of tolerance to FBR disease derived from the P. dulcis cultivar ‘Nonpareil’ as well as the peach cultivar ‘Bolinha’, bred from South American peach land races (Martínez-García et al. 2013). Although ‘Bolinha’ represents a promising source of FBR tolerance, inheritance is hampered by the multiple resistance components controlled by multiple genes (Fu et al. 2018). In contrast, FBR tolerance is readily transferred from almond with major QTL’s identified on LG 1 and 4 (Martinez-Garcia et al. 2013; Pacheco et al. (2014). Major resistance genes reported for other important diseases including PM located on LG 2 (Donoso et al. 2016) and peach gummosis (Botryosphaeria dothidea) reported by (Mancero-Castillo et al. 2018) to be located on LG 6 or 8. Prunus dulcis has also been cited as a source of resistance for RKN with a major resistance gene located in LG 2 (Saucet et al. 2016) and LG 7 (Van Ghelder et al. 2010). Almond also shows a high level of tolerance to PPV and its tolerance has been successfully transferred to advanced peach breeding lines (Martínez-Gómez et al. 2004) though the tolerance observed under greenhouse conditions has been reported to breakdown under field conditions (Rubio et al. 2013). Besides the use of peach species rootstocks for peach cultivars, the majority of commercial rootstocks utilized for peach and other stone fruits are species hybrids, primarily between almond and peach. Because of its self-sterility, almond has historically been used at the seed parent for the early seed propagation of hybrid rootstock, though the recent widespread use of tissue culture makes this unnecessary (Reighard and Loreti 2011). As previously discussed for the ‘GF677’ and ‘Adafuel’ hybrid rootstocks, it is often difficult to accurately identify the specific species source of reported resistances. However, any identification of promising biotic resistance in these hybrids will facilitate a more comprehensive trait characterization and so the possibility for more efficient introgression for peach cultivar improvement. Only a few peach-almond hybrids have so far been exploited as sources of genes for peach cultivar improvement. An enormous untapped germplasm remains given the wide range, diverse origins of these hybrids which include such regionally important cultivars as ‘Adefuel’, the various ‘Brights Hybrids’, ‘Cornerstone’, ‘Felinem’, ‘Garnem’, the ‘Hansen’ hybrids, ‘Mirobac’, ‘Montegro’, ‘Nickels’, ‘Paramount’, ‘Sirio’ and ‘Titan’. In addition to conferring resistance to soil-born pests and diseases, there is increasing evidence that the rootstocks may also function in inducing tolerance/resistance in the scion cultivar (Cirilli et al. 2016), as has been shown for the

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apparent induction in peach of tolerance to PPV when grafted onto the GF 305 rootstock (Rubio et al. 2013; Dehkordi et al. 2018). An even more extensive breeding germplasm is present in wild almond species. In their centers of origin, these species are often used as rootstocks for stone fruit particularly on soils where peach rootstocks are inadequate to cope with the complex biotic and abiotic stresses (Prudencio et al. 2020). Specific species cited for their value to tolerate ORDS include P. arabica, P. bucharica, P. dehiscens, P. kotschyi (Grasselly, 1976a); P. orientalis (syn. P. argentea) P. turcomenica (Ak et al. 2001; Martinez-Gomez et al. 2007; Sorkheh et al. 2009; Gharaghani and Eshghi 2015 as well as P. scoparia, P. lycioides (Browicz and Zohary 1996; Dejampour et al. 2013). P.petunnikowii (Evreinov; 1952), (P. lycioides, P. eburnea, P., P. orientalis, P. kotschyi, P., P. fenzliana,(Jahanban and Jamei 2012 in). P. fenzliana, which may be the progenitor of cultivated almond (Gradziel 2011), has also been noted for its value as a disease tolerant rootstock that otherwise does not dramatically affect normal tree development and final size (Browicz and Zohary 1996). However, as modern orchards evolve towards more integrated pest and disease management, controlling tree size and architecture may become essential (Devyatov 1996). Almond species identified as conferring varying degrees of scion size control include P. nana, (Ozbek 1978), P.kuramica (Grasselly 1976a, b), P. orientalis, P. turcomenica (Ak et al. 2001); P webbii (Dimitrovski and Ristevski 1973) and other regional accessions of P. fenzliana, (Grasselly 1976a, b; Rahemi et al. 2012). Tolerance to to Capnodis sp. has been reported in P. orientalis and P. turcomanica (Ak et al. 2001). Evreinov (1952) has also cited P. petunnikowii as being exceptionally tolerant of drought stress as well as resistant to CG.

5.5.3 Prunus, Subgenus Prunus, Section Prunus Plum species, both wild, cultivated, have been an important source for biotic stress resistance for peach and other stone fruits despite the presence of more formidable breeding barriers including difficulty in the initial hybridization and the frequent occurrence of sterile progeny resulting from subsequent hybrid breakdown. Ploidy differences can further complicate breeding efforts, with Prunus domestica and the closely related Prunus insititia being hexaploid, while other species such as P. spinosa are tetraploid. Many plum species are of the same ploidy (diploid) as peach thus facilitating gene transfer, though requiring significantly greater effort than needed for the subgenus Amygdalus. One result of this greater difficulty is that plum germplasm has been primarily utilized for rootstock improvement, driven primarily by its improved disease resistance, general good graft-compatibility with peach and other stone fruits (Reighard and Loreti 2011). Because of graft-incompatibility with some stone fruits such as almond, plum species are often first crossed to either peach or almond to combine disease resistance with graft-compatibility. The plum species most extensively utilized in peach rootstock breeding is Prunus cerasifera, with interspecies hybrids to peach, almond, other diploid plums available commercially. Renaud

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et al. (1988) found that the commercial interspecies hybrid rootstocks ‘Myran®’ [(P. cerasifera x P. salicina) x P. persica] as well as ‘Ishtara®’ [(P. cerasifera x P. saliciana) x (P. persica x P. cerasifera)],were resistant or tolerant to ORF (A. mellea) presumably contributed by P cerasifera. Beckman and Pusey (2001), however, found these rootstocks were susceptible ORF caused by A. tabescens. The.Krymsk86. rootstock has shown some resistance to root-lesion nematode, but they have been susceptible to RKN (Pinochet et al. 2000; Reighard and Loreti 2011). Claverie et al. (2004a) has mapped a dominant gene for resistance to RKN to LG 7. Other rootstocks having P. cerasifera as a parent have been reported to show greater tolerance to Tomato ring spot virus (Hoy and Mircetich 1984; Halbrend et al. 1994, Moreno et al. 1995) and possibly to Phytophthora spp. (Reighard and Loreti 2011).The Prunus pumila rootstock ‘Pumiselect®’ is resistant to M. javanica, tolerant of sandy soils and drought but is susceptible to WL, asphyxia, A. tabescens and iron chlorosis (Reighard et al. 2007). Selections of P. pumila such as ‘Mando’ have been reported as more tolerant of ring nematodes (Westcott et al. 1994) while ring nematode tolerance in another Prunus pumila rootstock ‘Pumiselect ®’ was less than ‘Nemaguard’ but higher than ‘Lovell’ (Reighard et al. 2007, Reighard and Loreti 2011). Rootstocks containing the hexaploid species Prunus insititia as well as Prunus domestica have been reported to be resistant or immune to RKN as well as M. arenaria and M. javanica but only moderately resistant to P. vulnus (Rahemi and Yadollahi 2006; Sorkheh et al. 2009). A dominant gene in P. salicina conferring RKN resistance was reported by Claverie et al. (2004a) to be located on LG 7. The widely used commercial Prunus domestica derived rootstock ‘Tetra’ has shown useful RKN (Meloidogyne spp.) resistance as well as tolerance to P. cinnamomi and A. mellea but was highly susceptible to P. vulnus (Nicotra and Moser 1997). In contrast, the Prunus domestica derived rootstock Penta’ was found to be susceptible to M. xenoplax and similar to ‘Nemaguard’ in its tolerance to P. vulnus (Nicotra and Moser 1997; Reighard and Loreti 2011). This group tends to be generally more tolerant of WL (Reighard and Loreti 2011) but have been reported to be more susceptible to ORDS as well as chlorotic leaf spot virus (Grasselly 1987; Reighard and Loreti 2011) and P. syringae (Reighard 1994). Rootstock tolerance to abiotic stresses is similarly important since these stresses predispose the plant to diseases and pests (Prudencio et al. 2020). For example, susceptibility to Phytophthora root rots are often associated with the stressful environment with WL so that disease tolerance may also be dependent upon the use of rootstock resistant to WL and associated asphyxiation (Amador et al. 2012; Arismendi et al. 2015). Recent research has shown levels of rootstock resistance or tolerance to drought and other abiotic stresses (Jiménez et al. 2013; Bedis et al. (2017), Bielsa et al. 2016); salinity (Momenpour et al. 2018), iron deficits (Jiménez et al. 2011; Gonzalo et al. 2011, 2012) as well as high temperature and CO2 levels (Dridi 2012; Jiménez et al. 2020). Higher tolerance to chlorosis (Jiménez et al. 2008; Moreno et al. 2008) and drought stress (Cochard et al. 2008; Jiménez et al. 2013) have been reported for P. dulcis, P. cerasifera and their hybrids with peach

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and closely related species than are normally present in peach rootstocks. Plum rootstocks, including “Mariana 2624” (P. cerasifera × Prunus munsoniana), “Myrobalan 29C” (Prunus cerasifera), and “Replantac”(P. cerasifera × P. dulcis) also demonstrate greater capacity to survive WL and associated root hypoxia (Pinochet 2010; Amador et al. 2012). Bliss et al. (1999) had previously reported promising resistance to heavy soils and CG as well as to silver leaf fungus (Stereum purpureum) in hybrids containing Prunus insititia.

5.6 Molecular, Genomic and Genetic Prospects Efficient breeding progress in peach is significantly delayed by its long juvenile phase, associated seed-to-seed generation time and large plant size, thus reducing the per hectare progeny planting density and so breeding efficiency. A fuller implementation of molecular, genomic techniques is commonly recommended to achieve the faster, more efficient breeding required if resistance to current and anticipated biotic stress needs are to be met. Comprehensive reviews by Gogorcena et al. (2020) and Prudencio et al. (2020) details the past progress and future opportunities of such efforts for breeding peach and almond for abiotic stress resistance and this information is similarly applicable to breeding for biotic stress resistance. Emerging opportunities may allow the improved deployment of these techniques to more fully utilize wild species as sources of biotic stress resistance. In particular, recent genomewide association studies (GWAS) approaches offer particular promise for studying the biotic stress response mechanisms of related wild species which should result in improved genetic knowledge (Kole et al. 2015). Early attempts at mapping the peach genome were hindered by the lack of genetic variability within this largely inbred cultivated species (Arús et al. 2012). The solution was the utilization of interspecific almond by peach hybrids and F2 populations to produce the required polymorphism needed to obtain saturation maps (Joobeur et al. 1998; Dirlewanger et al. 2004). Results have formed the basis for the IPGI reference genome with dissemination of breeder information through the RosBreed and the Genome Databases for Rosaceae projects, thus becoming the standard reference not only for peach but other Prunus species as well (Arús et al. 2012; Verde et al. 2012). Early applications include marker-assisted-selection (MAS), marker assisted breeding (MAB) and, to a lesser extent, marker-assisted introgression (MAI) (Serra et al. 2016). Unfortunately, MAS has proven of limited value in peach as it is practical for only a few Mendelian trait loci, primarily those associated with fruit attributes such as, fruit firmness (Peace et al. 2005), fruit epidermis (Vendramin et al. 2014) color (Sandefur et al. 2017) shape (Picañol et al. 2013) and maturity (Eduardo et al. 2015; Meneses et al. 2016) and resistance to pests (Gillen and Bliss 2005). In addition, MAS success is limited to traits controlled by mayor genes (Laurens et al. 2018) and much less successful for traits associated with QTLs. A further limitation in interspecies introgression is that markers developed for one breeding line will often not work with other breeding lines or species because of genetic changes occurring during diversification,

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evolution and domestication (Vanderzande et al. 2018). Many of the limitations of MAS and MAI appear to be overcome by more recent strategies utilizing GWAS (Rafalski 2010). Interspecies populations are particularly valuable in this approach to provide the required marker density. Resulting information is useful not only for improving breeding selection but also improving our understanding of the domestication process, including opportunities to re-domesticate cultivated crops utilizing the wider germplasm available in its species relatives (Gradziel 2020). GWAS will also facilitate a fuller integration of the different ‘omic’ methods to make breeding more efficient and effective (Kole et al. 2015; Pereira 2016). GWAS appears effective not only for breeding complex, quantitative traits, but also those strongly affected by environmental interactions and epigenetic regulation (Biscarini et al. 2017; Gogorcena et al. 2020). Such interactions would be particularly important in breeding improved interspecies rootstocks, including the exploitation of variation in miRNA (Zhang and Wang 2015), methylation (Fresnedo-Ramírez et al. 2017), as well as more recently studied factors such as lncRNA (Deniz and Erman 2017; Wang et al. 2017) and associated epigenetic gene silencing (Swiezewski et al. 2009; Heo and Sung 2011). Opportunities as well as limitations of GWAS are demonstrated by Li et al. (2019) who studied a diverse range of cultivated and wild genotypes to better understand crop evolution and, at the same, time identify candidate genes for a range of fruit quality and developmental traits. However, as pointed out by Gogorcena et al. (2020), the requirement that the structural variant is not a SNP can be an important limit to this method (see also Vendramin et al. 2014). Ironically, the primary breeding constraint for peach and most other tree crops is not the ability to effectively evaluate the large populations of seedlings required to achieve the rare genetic recombination required for commercial success. Rather, it is the initial ability to consistently generate the required large progeny population sizes which could conservatively be estimated at about 10,000 new seedling progeny per year for a moderate sized breeding program. Biotic as well as abiotic stresses remain the main sources of failure. For example, the generation of 10,000 hybrid seed would typically require 30,000 to 40,000 controlled pollinations given a typical seed-set of approximately 35%. This needs to take place in the very narrow bloom period which is often only one to two weeks during the spring when abiotic (rains, freezes, inadequate winter chill, etc.) as well as biotic (bloom diseases, pests) stresses can be severe. Even with good seed-set from breeding crosses, 20% or more of resultant fruit are typically lost from abiotic (frost, hailstorms, winds, etc.) and biotic (diseases and pests) stresses prior to harvest and stratification. Finally, peach like other Prunus seed, is particularly vulnerable to various ‘“damping-off’ diseases during stratification and planting, further reducing final progeny population size by 20% or more. Improved resistance to biotic as well as abiotic stresses will thus improve both orchard production consistency/efficiency for peach and other stone fruit but can also dramatically increase realizable breeding population sizes to the levels required for the rapid and efficient progress needed to meet the diverse and unprecedented challenges associated with future climate, orchard management and market changes.

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Chapter 6

Genomic Designing of New Almond-Peach Rootstock-Variety Combinations Resistant to Plum Pox Virus (Sharka) Manuel Rubio, Federico Dicenta, and Pedro Martínez-Gómez

6.1 Introduction Stone fruit trees are affected by a large number of viral diseases that can cause important economic losses (Rubio et al. 2017). Among these diseases, sharka caused by Plum pox virus (PPV) is the most significant of these viruses, inducing extensive yield losses in Japanese plum (Prunus salicina L.), prune (P. doemestica L.), apricot (P. armeniaca L.), sweet cherry (P. avium L.), sour cherry (P. cerasus L.) and peach [P. persica (L.) Batsch] due to reduced fruit quality, premature fruit drop and rapid natural virus spread by aphid vectors. PPV has been classified as a quarantine pathogen in most countries, and as one of the Top 10 Viruses in crops (Scholthof et al. 2011; García et al. 2014; Rodamilans et al. 2020). Although there is no anti-virus treatment that can be applied to infected trees or orchards, PPV may be managed by multiple approaches, such as quarantine and management activities, certification programs, vector control and the use of resistant varieties. The best method for controlling PPV is preventing the spread of the virus to new fruit-growing areas (Sochor et al. 2012), although genetic resistance is the definitive control strategy for PPV in affected areas (Martínez-Gómez et al. 2000, 2004; Rubio et al. 2003). In the case of peach, no sources of resistance to PPV have been described (Rubio et al. 2012). Given this lack of sources of resistance, the induction of resistance to PPV in peach ‘GF305’ by grafting the almond [P. dulcis (Miller) Webb] cultivar ‘Garrigues’ (Rubio et al. 2013) can have many advantages and can be a natural M. Rubio (B) · F. Dicenta · P. Martínez-Gómez Departament of Plant Breeding, CEBAS-CSIC, Espinardo, Murcia, Spain e-mail: [email protected] F. Dicenta e-mail: [email protected] P. Martínez-Gómez e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_6

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alternative for controlling the disease. In addition, from an agronomical point of view, other parallel works are planned under greenhouse conditions in Spain to study the commercial application of the resistance induced by the use of ‘Garrigues’ as interstock (intermediate rootstock). The objective of this Chapter is an assessment of the regulation of the resistance to PPV transmitted by grafting to develop new almond-peach rootstock-variety combinations resistant to PPV.

6.2 PPV Infection in Peach and Related Prunus Peach is the most important Prunus species with an annual production of 25.7 million tons in 2019 around the world (http://faostat.fao.org). Main producers are China, Spain and Italy (Table 6.1). However, peach production is seriously threatened by different strains of Plum pox virus (PPV, sharka disease) mainly in Europe (Scholthof et al. 2011; García et al. 2014; Rodamilans et al. 2020). Sharka disease symptoms show a wide range of characteristics, being easily confused with other disorders. Symptoms may appear on flowers, leaves and fruits. On peach species, the symptoms may vary depending on the cultivar and PPV strain. Intensity and symptoms distribution may appear only in a few leaves or fruits isolated or expressed throughout the entire tree. In additions, symptoms expression is linked with weather conditions, only being easily detected in spring, and frequently disappearing in summer. Fruit symptoms include light deformations and decolorations. On the other hand, leaf PPV symptoms may appear from a very slight chlorosis to a very severe, reaching to complete deformations, chlorotic punctured (Fig. 6.1). In peach, however, no sources of resistance to PPV have been described (Rubio et al. 2012). Table 6.1 Global peach production (FAOSTAT, 2019; http://www.fao.org/faostat)

Country

Production (million t)

China

15.82

Spain

1.54

Italy

1.22

Greece

0.92

Turkey

0.83

USA

0.73

Iran

0.59

Others

4.29

Total

25.74

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Fig. 6.1 Plum pox virus (sharka) symptoms in peach leaves and fruit

6.3 Genetic Resources of PPV Resistance in Prunus Germplasm Different works have shown several described cases of PPV resistance in different Prunus species studied. Apricot is the most studied species in this genus. There are several resistant apricot cultivars available in the market, all obtained by traditional breeding using resistance genes from North American cultivars such as ‘Stark Early Orange’, ‘Harlayne’, and ‘Orange Red’ (Martínez-Gómez et al. 2000). However, several studies have been searching for origin of the resistance to PPV in apricot, identifying natural apricot populations resistant among the Central Asian mountain forests (Decroocq et al. 2016). In the case of peach, however as we mentioned before, no sources of resistance have been identified thus far, so alternative methods must be adopted to obtain resistance (Rubio et al. 2012). The lack of resistance among the huge number of peach varieties is being tried to be solved by incorporating resistant genes from other related species. P. ferganensis (Kostov and Rjabov) and P. davidiana (Carrière) Franch were the first species described as potential sources of resistance to PPV. Nevertheless, the introgression of resistance has been questioned, and the importance of the genetic background in the effective transmission of resistance has been highlighted (Rubio et al. 2010). Furthermore, the resistance to sharka observed in almond was reported many years ago by different authors (Rubio et al 2003), suggesting the potential use of almond species as good candidate for resistance donor via interspecific crosses (Martínez-Gómez et al. 2004) due to its close genetic phylogeny. Several teams around the world are working on it, and not only for PPV resistance, trying to map the genetic determinants for different characters and to implement the genomic selection for accelerating the introgression of resistance gene from almond in to peach (Serra et al. 2016; Eduardo et al. 2020).

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In plum species, the situation is similar to the peach for Japanese plums, with no natural sources of resistance found so far (Rubio et al. 2010). However, some European plums have shown a mechanism of resistance based on the hypersensitive response (Hartmann and Petruschke 2000; Neumuller et al. 2009). This response consists of the death of the affected area while the rest of the tree remains free of the virus and therefore healthy. In addition, Prunus domestica is suitable for genetic transformation, PPV susceptibility factors were targeted through gene silencing (Scorza et al. 2013). Regarding the molecular bases of the PPV/Prunus interaction, high-throughput transcriptome sequencing (RNA-Seq) approaches have been assayed to obtain the best possible knowledge of the molecular processes associated with the expression of the traits of susceptibility/resistance to Plum pox virus (PPV and sharka) in fruit trees of the Prunus genus. These assays have shown that the first early response to PPV infection in susceptible peach and apricot genotypes is associated with the first induction of genes related to resistance to pathogens related to jasmonic acid, resistance proteins, chitinases, cytokinins or Lys-M proteins. On the other hand, when the virus is established, an overexpression of Dicer protein DCL2a genes have been observed. This could enhance PPV silencing and could be the cause of the elimination of virus symptoms in resistant genotypes. In most cases, however, suppression of gene silencing by the PPV proteins HCPro and P1 is observed with the later multiplication of the virus (Rubio et al. 2015a, b). On the other hand, studies of the genetic and molecular bases of PPV resistance have mainly focused on apricot species. In this species, different hypotheses have been established with respect to the genetic control of resistance to PPV, including that this control is due to a single gene and that it is involved with or controlled by two or three genes (Rubio et al. 2007 and Llácer et al. 2008). At this moment, however, the monogenic hypothesis is the most extended with a main locus modified by another locus with a more reduced effect. In this sense, a main quantitative trait locus (QTL) has been located in the ligature group (LG) 1 of the apricot genome as responsible for PPV resistance (Lambert et al. 2007). A genomic region of 194 kb in LG1 (scaffold 1 of the peach reference genome, positions 8.050.805–8.244.925) has been described by the group of Dr. Marisa Badenes from IVIA of Valencia as responsible for resistance in apricot where the PPVres resistance gene is located (Zuriaga et al. 2013). These authors described a family of MATH domain homology genes involved in the control of resistance through downregulation of two of these MATHd genes, ParPMC1 and ParPMC2. This downregulation genes has been suggested to be caused by an RNA silencing mechanism triggered by the pseudogenization of the resistance allele of ParPMC2 (Zuriaga et al. 2018), being recently validated and applied in marker assisted selection (Polo-Oltra et al. 2020). This downregulation associated with PPV resistance in apricot has been also validated through the genetic transformation of Nicotiana benthamiana and plum by the group of Dr. Lorenzo Burgos from CEBAS-CSIC of Murcia. Overexpression of ParPMC1 and ParPMC2 using a constitutive promoter increased the susceptibility of transformed plants (Alburquerque et al. 2018).

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Finally, in the case of European plum, the hypersensitive resistance has been described as monogenic (Hartmann and Neumüller 2006). However, no molecular evidence has been described for this kind of hypersensitivity resistance. Monogenic resistance, in this case mediated by RNA silencing, has been also characterized and used in the case of transgenic prunes PPV resistant transformed with the coat protein coding sequence of the virus (Scorza et al. 2013). On the other hand, genetic engineering and the use of biotechnology can help to develop sharka resistant cultivars (Ilardi and Di Nicola-Negri 2011). There is already a transgenic European plum called ‘Honey Sweet’ that is resistant to PPV (Scorza et al. 2013). This was the first genetically engineered PPV-resistant plum commercialized, almost 25 years after it was attained; thus far, it is only available in the USA. This delay shows that even when it is affordable to obtain transgenic Prunus resistant to PPV, there are still many impediments to obtaining permission to grow and commercialize transgenic fruit (Rubio et al. 2017). The transfer of resistant genes by conventional breeding techniques is challenging and time-consuming, but at this moment, it is the most common and safest way to generate new resistant cultivars.

6.4 Induced Resistance to Plum Pox Virus (Sharka) in Peach by Almond Grafting Diverse experiments were developed a few years ago by the host group at CEBASCSIC of Murcia to identify sources of resistance to PPV, using an in house inoculation protocol (‘severe test’) (Fig. 6.2) (Rubio et al. 2003). The grafting experiment, using 10 almond varieties on peach ‘GF305’ rootstock infected with PPVD (Dideron Type), showed a lack of PPV symptoms. After this first experiment,

Fig. 6.2 PPV phenotyping process. Plant model: GF305 rootstock infected with PPV and grafted with the Prunus species or genotypes to be tested. Pictures show the greenhouse where the evaluation is carried out and the cold chamber, where the plants are submitted to artificial rest periods

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the host group established an original grafting model for sharka resistance. This model has demonstrated that grafting the almond cultivar ‘Garrigues’ onto ‘GF305’ peach (a very susceptible PPV indicator) seedlings heavily infected with PPV-D can progressively reduce disease symptoms and virus accumulation (Rubio et al. 2013). ‘Garrigues’ almond grafting could thus be used as a natural vaccine (Jones and Dangl 2006) against PPV in peach. This response appears to be specific between almond and peach. Furthermore, grafting ‘Garrigues’ onto ‘GF305’ before PPV inoculation completely prevented virus infection, showing that resistance is constitutive and not induced by the virus (Rubio et al. 2013). Grafting ‘Garrigues’ onto peach varieties grafted onto a commercial rootstock should prevent the infection of the PPV. At the commercial level, the use of ‘Garrigues’ as intertstock (intermediate rootstock, bridge rootstock, intermediate wood, inter-stem, etc.) could be an alternative way to protect peach cultivars against PPV.

6.5 Transmission of Resistance Induction to ‘Garrigues’ Offspring In order to study the possible transmission of resistance induction, different cross between ‘Garrigues’ and three peach cultivars (1 nectarine, 1 yellow peach and 1 traditional Spanish peach) has been assayed. The PPV phenotyped, using the same protocol described previously, has confirmed the transmission of the resistance from ‘Garrigues’ to the three offsprings (Rubio et al. 2021). After corroborating the resistance, 30 descendants (10 by offspring) has been selected and buds from these resistant descendants (almond × peach) were grafted onto the ‘GF305’ rootstocks showing strong sharka symptoms. The first results suggest that Garrigues ‘effect’ is weak, being difficult so far confirmed a similar behavior, in the 30 descendants studied. However new studies are in process.

6.6 Use of Garrigues as an Interstock (Intermediate Rootstock) in the Propagation of New Varieties of Peach at a Commercial Level The use of ‘Garrigues’ as interstock in the propagation of new peach varieties grafted onto commercial rootstock can generate resistant plants. We assume that ‘Garrigues’ interstock should transmit the effector molecule of this induced resistance, producing a variety of commercially valuable resistant plants. The identification of the molecular mechanisms involved in the induced resistance should improve the efficiency of the use of Garrigues as an interstock (intermediate rootstock) in the propagation of new varieties of peach at a commercial level.

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Currently, an experiment is being carried out to probe the potential use of ‘Garrigues’ as “protector” against PPV (Figs. 6.3 and 6.4). The trial consists in a

Fig. 6.3 Experimental design of the evaluation of the field applicability of induced resistance to PPV (sharka) in peach by almond grafting as interstock

Fig. 6.4 Real plant model, including a commercial rootstock (G × N in the picture), the interstock ‘Garrigues’ almond and finally a commercial peach cultivar grafted onto Garrigues

Peach Cultivar Interstock Garrigues

Rootstock

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group of commercial peach varieties grafted onto ‘Garrigues’ interstocks (intermediate rootstock) that previously were grafted on the commercial rootstocks GF677, GxN 15 and GF305. Due to the huge peach catalogue, the assay is a very small representation of peaches, but trying to include most of the phenotypic variability displayed by peach. This phenotypic types include white and yellow flesh, cling and free stone, nectarines and platycarpa. The results are being hopeful, none of the susceptible peaches has shown sharka symptoms when they were grafted onto Garrigues in the first screening assay. This assay is currently on-going in order to obtain reproducible and consistent results.

6.7 Molecular Basis of the Induced Resistance to Plum Pox Virus (Sharka) in Peach by Almond Grafting Mobility of various macromolecules including DNA and RNA genetic components and proteins between the scion and stock has been documented suggesting that the graft could be a means for the horizontal transfer of genes (Stegemann and Bock 2009; Harada 2010). These results unequivocally proved that not only phenotypic traits but also the core molecular building blocks could be altered in the grafted individuals (Haroldsen et al. 2012; Chen et al. 2020). It has been shown in Arabidopsis that a significant proportion of the endogenous small RNAs of all size classes (21–24 nt) can move across the graft union. This movement can give rise to specific physiological reprogramming and epigenetic changes in the recipient tissues (Lewsey et al. 2016; Pagliarani and Gambino 2019). Regarding graft-transmissible PPV resistance from almond to peach, in a recent study comparing the hormonal balance of healthy ‘GF305’ peach versus ‘GF305’ peach inoculated with a PPV-D isolate, the ‘G305’ peach seedlings that were grafted with the almond cultivar ‘Garrigues’ showed significant differences with the seedlings that were not grafted. PPV inoculation produced a significant increase in Gibberellic Acid 3 (GA3) and abcisic acid (ABA) and a decrease in the other phytohormones analyzed, including cytokinin trans-zeatin (tZ), Gibberellic Acid 4 (GA4), 1-aminocyclopropane-1-carboxylic acid (ACC), Salicylic Acid (SA) and Jasmonic Acid (JA). These imbalances were related to the virus infection and the presence of chlorosis symptoms, particularly in the case of ABA concentration. Additionally, grafting ‘Garrigues’ onto ‘GF305’ produced an increase in GA3, GA4, SA and ABA and a decrease in the rest of the phytohormones analyzed, tZ, ACC and JA. Grafting ‘Garrigues’ almond onto the PPV-inoculated peach ‘GF305’ produced the opposite effect in some phytohormones, resulting in an increase in tZ, and JA and a concurrent increase in SA. These results showed the significant involvement of SA in the induced resistance response in peach after almond grafting. This SA-induced resistance, consisting of a decrease in symptoms and an absence of other reactions producing necrosis, seems to be different to from SAR and ISR. SA signaling should

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also activate a cytokinin response to induce PPV resistance, linking plant growth and defense against PPV (Nikbakht-Dehkordi et al. 2018). Studies of differential expression by RNA-Seq revealed a series of genes overexpressed in ‘GF305’ after the grafting of ‘Garrigues’ that could be involved in the induction of resistance. These included genes of resistance to pathogens like PATHOGENESIS-RELATED THAUMATIN-LIKE PROTEIN, CHORISMATE MUTASE 2, SNAKIN-2 and ETHYLENE-RESPONSIVE TRANSCRIPTION FACTOR 4. In addition, the overexpression of genes involved in metabolic pathways of the hormones studied was observed, corroborating the hormonal data (NikbakhtDehkordi et al. 2018) at the mRNA level. These results obtained by RNA-Seq were validated by qPCR (Rubio et al. 2021). Additionally, several candidate genes (including Glucan endo-1,3-Beta DGlucosidase, Leucine rich repeat N-terminal domain, or Speckle-type POZ protein) upregulated after almond granting should be considered “susceptible” genes necessary to PPV infection. This down-regulation of the candidate susceptible genes should be due to a gene methylation process mediated by a sRNA molecule. On the other hand, transcriptomic results showed several defense genes included RTM genes, NAM proteins, TFIIB, TLPs (Thaumatin like protein), or dehydration-responsive protein overexpressed after ‘Garrigues’ grafting and are candidate “resistance” genes to be responsible of this induced response. We propose that grafting provides a path for horizontal gene transfer. Based on these results, we can deduce the following resistant hypothesis of grafting ‘Garrigues’ to peach. First, grafting induced a series of signal transduction genes in high expression and there is an interesting correlation among constitutive thaumatin like protein, PR proteins, ABA compound, and disease susceptibility to PPV; secondly, protein kinase interacts with transcription factors or other factors and upregulate the expression relevant susceptible genes (Rubio et al. 2021). On the other hand, at the sRNA level, recent results showed that ‘Garrigues’ induced very different profiles in peach that could also be related to the expression of resistance (Rubio et al. 2021). Finally, epigenetics describes phenomena associated with changes in gene expression that occur without modification in the genomic nucleotide sequence. DNA cytosine methylation is one of the main epigenetic mechanisms in all eukaryotes, and it is produced and maintained over time by several molecular pathways and is likely involved in plant-pathogen interactions including plant-virus interactions (Gambino and Pantaleo 2017; Ramirez-Prado et al. 2018). Virus resistance and tolerance through DNA-methylation has been recently described in different plant species, including Nicotiana, tomato and grapevines among others, by different authors (Sahu et al. 2014; Dal Bosco et al. 2018; Wang et al. 2018). Currently an integrated methylation, mRNA-Seq and miRNA-Seq analysis is performed at CEBAS-CSIC of Murcia (Spain). Small RNAs (sRNAs) associated with the epigenetic silencing of genes coding for the host factors required for viral infection could be protecting ‘Garrigues’ almond against PPV. These sRNAs might move via grafting, inducing gene methylation and thus silencing the susceptibility genes in peach according to the effect of mobile sRNAs on DNA methylation previously

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described (Lewsey et al. 2016). This hypothesis is based on the mechanism of downregulation of two of the ParPMC1 and ParPMC2 MATH genes validated through qPCR (Zuriaga et al. 2018) and genetic transformation of Nicotiana benthamiana and plum (Alburquerque et al. 2018) that has been described as producing PPV resistance in this specie. This downregulation should be due to a gene methylation process according to our starting hypothesis. This hypothesis also agrees with the known effect of DNA methylation as an epigenetic mechanism involved in plantpathogen interactions, including plant-virus tolerance or resistance (Ramirez-Prado et al. 2018). In this new perspective, it is not resistant genes but rather downregulated or suppressed (methylation or silencing) susceptibility genes that are responsible for this resistance to PPV.

6.8 Future Perspectives Resistance to PPV in ‘Garrigues’ can be transmitted through the graft union through phloem and protect the highly susceptible ‘GF305’ peach. After a transcriptome analysis of seven samples (5 peaches and 2 almonds) by RNAseq (mRNA), several candidate genes have been identified together with some sRNAs. In addition, an epigenetic mechanism should control this response. DNA methylation linked to the induced resistance in peach should be regulated by mobile small RNAs, as indicated in recent results of different groups (Lewsey et al. 2016). This epigenetic regulation of the induced resistance through small RNAs should be an interesting possibility. On the other hand, it is necessary the corroboration of the “Garrigues effect” at commercial level (nurseries and orchards), to develop a continuous threaten of PPV for peach production. The use of ‘Garrigues’ as interstock in the propagation of new peach varieties grafted onto commercial rootstock can generate resistant plants should also be an environmental friendly way to control PPV in peach. Acknowledgements This study has been supported by the projects “Epigenetic regulation of the resistance to Plum pox virus (sharka) induced in peach by almond grafting and its application as interstock” of the Spanish Ministry of Science, Education and Universities (RTI2018-095556-BI00) and“Breeding stone fruit species assisted by molecular tools” from the Seneca Foundation of the Region of Murcia (19879/GERM/15).

References Alburquerque N, Zuriaga E, Badenes ML, Dardick C, Burgos L (2018) Primeras pruebas funcionales de los genes ParPMC de resistencia a Sharka: transformación en Nicotiana y P. domestica. IX Congreso de Mejora Genética de Plantas, Murcia, September de 2018, p 73 Chen WW, Takahashi N, Hirata Y, Ronald J, Porco S, Davis SJ, Nusinow DA, Kay SA, Mas P (2020) A mobile ELF4 delivers circadian temperature information from shoots to roots. Nat Plants 6:416–426

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Dal Bosco D, Sinski I, Ritschel P (2018) Expression of disease resistance in genetically modified grapevines correlates with the contents of viral sequences in the T-DNA and global genome methylation. Transgen Res 27:379–396 Decroocq S, Cornille A, Tricon D, Babayeva S, Chague A, Eyquard JP, Karychev R, Dolgikh S, Kostritsyna T, Liu S, Liu W, Geng W, Liao K, Asma BM, Akparov Z, Giraud T, Decroocq V (2016) New insights into the history of domesticated and wild apricots and its contribution to Plum pox virus resistance. Mol Ecol 25:4712–4729 Eduardo I, Alegre S, Alexiou KG, Arus P (2020) Resynthesis: marker-based partial reconstruction of elite genotypes in clonally-reproducing plant species. Front Plant Sci 11:1205 García JA, Glasa M, Cambra M, Candresse T (2014) Plum pox virus and sharka: A model potyvirus and a major disease. Mol Plant Pathol 15:226–241 Gambino G, Pantaleo V (2017) Epigenetics in plant–pathogen interactions. In: Rajews N, Jurga S, Barciszewski J (eds) Plant epigenetics. Springer, Berlin (Germany), pp 385–404 Harada T (2010) Grafting and RNA transport via phloem tissue in horticultural plants. Scientia Horticulturae 125:545–550 Hartmann W, Neumüller M (2006) Breeding for resistance: breeding for Plum pox virus resistant plums (Prunus domestica L.) in Germany. EPPO Bull 36:332–336 Haroldsen VM, Szczerba MW, Aktas H, Lopez-Baltazar J, Odias MJ (2012) Mobility of transgenic nucleic acids and proteins within grafted rootstocks for agricultural improvement. Front Plant Sci 3:39 Hartmann W, Petruschke M (2000) Sharka resistant plums and prunes by utilization of hypersensitivity. Acta Hort 538:391–395 Ilardi V, Di Nicola-Negri E (2011) Genetically enginered resistance to Plum pos virus infection in herbaceous and stone fruit hosts. GM Crops 2:24–33 Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329 Lambert P, Dicenta F, Rubio M, Audergon JM (2007) QTL analysis of resistance to sharka disease in the apricot (Prunus armeniaca L.) ‘Polonais’ x ‘Stark Early Orange’ F1 progeny. Tree Genet Genomes 3:299–309 Llácer G, Badenes ML, Romero C (2008) Problems in the determination of inheritance of Plum pox virus resistance in apricot. Acta Hort 781:263–267 Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A, Urisch MA, Baulcombe DC, Ecker JR (2016) Mobile small RNAs regulate genome-wide DNA methylation. Proc Nat Acad Sci 113:E801–E810 Martínez-Gómez P, Dicenta F, Audergon JM (2000) Behaviour of apricot (Prunus armeniaca L.) cultivars in presence of sharka (Plum pox potyvirus): a review. Agronomie 20:407–422 Martínez-Gómez P, Rubio M, Dicenta F, Gradziel TM (2004) Resistance to Plum Pox Virus (RB3.30 isolate) in a group of California almonds and transfer of resistance to peach. J Amer Soc Hort Sci 129:544–548 Neumuller M, Lanzl S, Hartmann W (2009) Towards an understanding of the inheritance of hypersensitivity resistance against the sharka virus in European Plum (Prunus domestica L.): generation of interspecific hybrids with lower ploidy levels. Acta Hort 814:721–726 Nikbakht-Dehkordi A, Rubio M, Babaeian N, Albacete A, Martínez-Gómez P (2018) Phytohormone signaling of the resistance to Plum pox virus (PPV, Sharka Disease) Induced by Almond (Prunus dulcis (Miller) Webb) Grafting to Peach (P. persica L. Batsch). Viruses 10:238 Pagliarani C, Gambino G (2019) Small RNA mobility: Spread of RNA silencing effectors and its effect on developmental processes and stress adaptation in plants. Intl J Mol Sci 20:4306 Polo-Oltra A, Romero C, López I, Badenes ML, Zuriaga E (2020) Cost-effective and time-efficient molecular assisted selection for Ppv resistance in apricot based on ParPMC2 Allele-Specific PCR. Agronomy 10:1292 Ramirez-Prado JS, Abulfaraj AA, Rayapuram N, Hirt H (2018) Plant immunity: from signaling to epigenetic control of defense. Trends Plant Sci 23:833–844 Rodamilans B, Valli A, García JA (2020) Molecular plant-plum pox virus interactions. Mol PlantMicrobe Interact 33:6–17

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Rubio M, Martínez-Gómez P, Dicenta F (2003) Resistance of almond cultivars to Plum pox virus (sharka). Plant Breed 122:462–464 Rubio M, Martínez-Gómez P, Audergon JM, Dicenta F (2007) Testing genetic control hypotheses for Plum pox virus resistance in apricot. Sci Hort 112:361–365 Rubio M, Pascal T, Bachellez A, Lambert P (2010) Quantitative trait loci analysis of PPV resistance in Prunus davidiana P1908. Tree Genet Genomes 6:291–304 Rubio M, Martínez-Gómez P, García-Bruntom J, Pascal T, García-Ibarra A, Dicenta F (2012) Sensitivity of peach cultivars against a Dideron isolate of Plum pox virus. Sci Hort 144:81–86 Rubio M, Martínez-Gómez P, García JA, Dicenta F (2013) Interspecific transfer of resistance to Plum pox virus by grafting. Ann Appl Biol 163:466–474 Rubio M, Rodríguez-Moreno L, Ballester AR, Castro M, Bonghi C, Candresse T, Martínez-Gómez P (2015) Analysis of gene expression changes in peach leaves in response to Plum pox virus infection using RNA-Seq. Mol Plant Pathol 16:164–176 Rubio M, Ballester AR, Olivares PM, Castro de Moura M, DicentaF, Martínez-Gómez P (2015b) Gene expression analysis of Plum pox virus (Sharka) Susceptibility/Resistance in apricot (Prunus armeniaca L.). PLoS One 10:e0144670 Rubio M, Martínez-Gómez P, Sánchez-Navarro JA, Pallás V, Candresse T (2017) Recent advances and prospects in Prunus virology. Ann Appl Biol 171:125–138 Rubio M, Martínez-García PJ, Nikbakht-Dehkordi A, Prudencio AS, Gomez, EM, Rodamilans B, Dicenta F, García JA, Martínez-Gómez P (2021) Gene expression analysis of the resistance to Plum pox virus (sharka) induced in peach by almond grafting. Sci Rep (submitted) Sahu PP, Sharma N, Puranik S (2014) Post-transcriptional and epigenetic arms of RNA silencing: a defense machinery of naturally tolerant tomato plant against Tomato Leaf Curl New Delhi Virus. Plant Mol Biol Rep 32:1015–1020 Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Foster G (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954 Scorza R, Callahan A, Dardick C, Ravelonandro M, Polak J, Malinowski T, Zagari I, Cambra M, Kamenova I (2013) Genetic engineering of plum pox virus resistance: ‘HoneySweet’ plum. Plant Cell Tiss Org Cult 115:1–12 Serra O, Donoso M, Picanol R, Batlle I, Howad W, Eduardo I, Arús P (2016) Marker-assisted introgression (MAI) of almond genes into the peach background: a fast method to mine and integrate novel variation from exotic sources in long intergeneration species. Tree Genet Genomes 12:96 Sochor J, Babula P, Adam V, Krska B, Kizek R (2012) Sharka: the past, the present and the future. Viruses 4:2853–2901 Stegemann S, Bock R (2009) Exchange of genetic material between cells in plant tissue grafts. Science 314:649–651 Wang C, Wang C, Xu W (2018) Epigenetic Changes in the Regulation of Nicotiana tabacum response to Cucumber Mosaic Virus Infection and symptom recovery through single-base resolution methylomes. Viruses 10:402 Zuriaga E, Soriano JM, Zhebentyayeva T, Romero C, Dardick C, Cañizares J, Badenes ML (2013) Genomic analysis reveals MATH gene(s) as candidate(s) for plum pox virus (PPV) resistance in apricot (Prunus armeniaca L.). Mol Plant Pathol 14:663–677 Zuriaga E, Romero C, Blanca JM, Badenes ML (2018) Resistance to Plum pox virus (PPV) in apricot (Prunus armeniaca L.) is associated with down-regulation of two MATHd genes. BMC Plant Biol 18:25

Chapter 7

Genomic Designing of New Plum Pox Virus Resistant Plumcot [Prunus Salicina Lindl. x Prunus Armeniaca L.] Varieties Through Interspecific Hybridization María Nicolás-Almansa, D. Ruiz, A. Guevara, J. Cos, Pedro Martínez-Gómez, and Manuel Rubio

7.1 Introduction We can consider fruit tree breeding as an applied science (different to the basic sciences) which requires empirical support based on observation and experimentation. At the same time, fruit tree breeding is a design science, as it comes up with models to meet aims that expand human possibilities. In fact, the design of new varieties involves applied knowledge, because the models proposed have a practical dimension: they seek to solve specific problems (in the short, medium or long term) (Fig. 7.1). This activity has a link with technology since it can lead to innovation, an achievement produced by the creative transformation of reality. This can lead, for example, to the creation of a new plant variety, which is a desired transformation. To develop suitable new cultivars, we need to know the relevant variables that influence

M. Nicolás-Almansa · D. Ruiz · P. Martínez-Gómez (B) · M. Rubio Departament of Plant Breeding, CEBAS-CSIC, Espinardo, Murcia, Spain e-mail: [email protected] M. Nicolás-Almansa e-mail: [email protected] D. Ruiz e-mail: [email protected] M. Rubio e-mail: [email protected] A. Guevara · J. Cos Department of Hortofruticulture, IMIDA, Murcia, Spain e-mail: [email protected] J. Cos e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_7

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Fig. 7.1 Classification of fruit tree brreding as an applied science of design

our knowledge of the possible future in the success of new cultivars (Martínez-Gómez 2020). It is thus necessary to examine the internal and external variables influencing the phenomenon in question. Both types of variable must be subjected to scientific evaluation. The first internal variables to consider in any fruit tree breeding program are derived from plant traits that are considered as objectives. The knowledge of these internal variables of genetic type will indicate their suitability with respect to the proposed design objectives. Secondly, internal variables also include the current methodologies available for use in the selection of individuals. These methodologies are closely related to the level of knowledge available at the molecular levels especially in relation to the development and application of new markers for the selection of individuals and will give us an idea of the efficacy and feasibility of new designs or cultivars. Finally, we can include various economic factors within the production framework, i.e., the goals, processes and outcomes (Martínez-Gómez 2017). In this applied biological context, interspecific hybridization is a common practice used in breeding programs with the aim of transfering interesting genes from one species to another. Interspecific hybrids are more difficult to obtain, since the genetic barriers to hybridization are increased because of the great genetic distance between parents (Martínez-Gómez et al. 2003). On the other hand, self-compatibility as well as sharka resistance are two of the principal aims of the Japanese plum (Prunus salicina Lindl.) breeding program coordinated by CEBAS-CSIC and IMIDA. Because of that, a considerable number of interspecific crosses between Japanese plum and self-compatible, sharka-resistant apricot (Prunus armeniaca L.) cultivars have been performed during the last years

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in order to obtain resistant and self-compatible plumcots (interspecific hybrids) (Nicolás-Almansa et al. 2020). The objective of this Chapter is an assessment of the development of new Plum pox virus resistant plumcot varieties from a double molecular and phenotype perspective.

7.2 PPV Infection in Apricot, Plum and Related Prunus Species Plum is one of the most important Prunus species after peach with an annual production of 12.6 million tons in 2019 followed by apricot (annual production of 4.1 million tons in 2019) (http://faostat.fao.org). Main producers are Turkey, Iran, Uzbekistan and Algeria in the case of apricot and China, Serbia, Romania, Chile and Iran in the case of plum (Table 7.1). Sharka disease, caused by Plum pox virus (PPV), is the most significant of these viruses, causing extensive yield losses in Japanese plum, apricot, prune (P. domestica L.), sweet cherry (P. avium L.), sour cherry (P. cerasus L.) and peach [P. persica (L.) Batsch] due to reduced fruit quality, premature fruit drop and rapid natural virus spread by aphid vectors. This agent has been classified as a quarantine pathogen and as one of the Top 10 Viruses in crops (Scholthof et al. 2011; García et al. 2014; Rodamilans et al. 2020). In this species symptom uysually include decoloration of fruits and leaf chlorosis (Fig. 7.2). Although there is no anti-virus treatment that can be applied to infected trees or orchards, PPV may be managed by multiple approaches, such as quarantine and management activities, certification programs, vector control and the use of resistant varieties. The best method for controlling PPV is preventing the spread of the virus to new fruit-growing areas (Sochor et al. 2012), although genetic resistance is the definitive control strategy for PPV in affected areas (Martínez-Gómez et al. 2000, Table 7.1 Global apricot and plum production (Fao Stat 2019) Apricot

Plum

Country

Production (million t)

Country

Production (million t)

Turkey

0.85

China

7.01

Uzbekistan

0.53

Romania

0.69

Iran

0.32

Serbia

0.55

Italy

0.27

Chile

0.46

Algeria

0.21

Iran

0.35

Spain

0.14

USA

0.34

Pakistan

0.11

Turkey

0.31

Others

1.67

Others

2.83

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Fig. 7.2 Plum pox virus (sharka) symptoms in apricot and plum leaves and fruits

2004; Rubio et al. 2003). However, in the case of Japanese plum, no sources of resistance to PPV have been described (Rubio et al. 2011). At molecular level, regarding susceptibility to PPV in Prunus, high-throughput transcriptome sequencing (RNA-Seq) approaches have been employed to obtain the best possible knowledge of the molecular processes associated with the expression of the traits of susceptibility/resistance to Plum pox virus (PPV and sharka) in fruit trees of the Prunus genus. These assays have shown that the first early response to PPV infection in susceptible peach and apricot genotypes is associated with the first induction of genes related to resistance to pathogens related to jasmonic acid (JA), resistance proteins, chitinases, cytokinins or Lys-M proteins. On the other hand, when the virus is established, an overexpression of Dicer protein CL2a genes has been observed. This could enhance PPV silencing and could be the cause of the elimination of virus symptoms in resistant genotypes. In most cases, however,

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suppression of gene silencing by the PPV proteins HCPro and P1 is observed with the later multiplication of the virus (Rubio et al. 2015a, b).

7.3 Genetic Resources of PPV Resistance Prunus Germplasm Several works have shown different described cases of PPV resistance in the different Prunus species studied. Apricot is the most studied species in this genus. There are several resistant apricot cultivars available in the market, all obtained by traditional breeding using resistance genes from North American cultivars such as ‘Stark Early Orange’, ‘Harlayne’, ‘Goldrich’ and ‘Orange Red’ (Martínez-Gómez et al. 2000). In the case of Japanese plum or peach, however, no sources of resistance have been identified thus far, so alternative methods must be adopted to obtain resistance (Fig. 7.3). Regarding PPV resistance mechanisms in Prunus species, there are different cases depending on the Prunus species. In the prune and European plum, resistance is based on the hypersensitive response to PPV shown by a few genotypes (Hartmann and Petruschke 2000; Neumuller et al. 2009). This response consists of the death of the affected area while the rest of the tree remains free of the virus and therefore healthy. Finally, in sweet and sour cherry, only three types of PPV isolates (type C) (Scholthof et al. 2011; García et al. 2014; Rodamilans et al. 2020). On the other hand, studies of the genetic and molecular bases of PPV resistance have mainly focused on apricot species. In this species, different hypotheses have been established with respect to the genetic control of resistance to PPV, including that this control is due to a single gene and that it is involved with or controlled by two or three genes (Rubio et al 2007; Llácer et al. 2008). At this moment, however, the monogenic hypothesis is the most extended with a main locus modified by another locus with a more reduced effect. In this sense, a main quantitative trait locus (QTL) has been located in the ligature group (LG) 1 of the apricot genome as responsible for PPV resistance (Rubio et al. 2014). A genomic region of 194 kb in LG1 (scaffold 1 of the peach reference genome, positions 8.050.805–8.244.925) has been described by the group of Dr. Marisa Badenes from IVIA of Valencia as responsible for resistance in apricot where the PPVres resistance gene is located (Zuriaga et al. 2013). These authors described a family of MATH domain homology genes involved in the control of resistance through downregulation of two of these MATHd genes, ParPMC1 and ParPMC2 (Zuriaga et al. 2018). Finally, in the case of European plum, the hypersensitive resistance has been described as monogenic (Hartmann and Petruschke 2000). However, no molecular evidence has been described for this kind of hypersensitivity resistance. Monogenic resistance, in this case mediated by RNA silencing, has also been characterized and used in the case of transgenic prunes resistant to PPV transformed with the coat protein coding sequence of the virus (Scorza et al. 2013). PPV C types can affect European and Japanese plum species (Sihelská et al. 2017) (Fig. 7.3).

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Fig. 7.3 Plum pox virus infection in the most important commercial species of the Prunus genus including susceptibility [the most important isolate types affecting each species are indicated between parenthesis: D (Dideron), M (Marcus), EA (El Amar) and C (Cherry)] and resistance sources

On the other hand, genetic engineering and the use of biotechnology can help to develop sharka-resistant cultivars (Ilardi and Di Nicola-Negri 2011). There is already a transgenic European plum called ‘Honey Sweet’ that is resistant to PPV (Scorza et al. 2013). This was the first genetically engineered PPV-resistant plum commercialized, almost 25 years after it was attained; thus far, it is only available in the USA. This delay shows that even when it is affordable to obtain transgenic Prunus resistant to PPV, there are still many impediments to obtaining permission to grow and commercialize transgenic fruit (Rubio et al. 2017). The transfer of resistant genes by conventional breeding techniques is challenging and time-consuming, but

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at this moment, it is the most common and safest way to generate new resistant cultivars.

7.4 Development of New PPV Resistant Plumcots The development of new plumcot varieties strated in the USDA plum breeding program at Byron in USA in 1984. The objective was the development on plumcot material adapted to the humid southeastern United States. In this program a plumcot breeding line, BY69-1637P, has also been released. This selection produces lightmedium crops of tart, orange-fleshed fruit. The black skin has a very short fuzz. It was released for use in further breeding (Okie et al. 1992). Later, a new plumcot variety named ‘Spring Satin’ was developed (Okie 2005). In 1987 started anoither plumcot breeding program at the Fruit-Growing Institute at Plovdiv in Bulgaria. Cultivars and selected wild species of Prunus were included in the breeding program. The new cultivar ‘Standesto’ was obtained by conventional interspecific hybridization carried out in 1990, from the parent combination P. domestica ‘Stanley’ x P. armeniaca ‘Modesto’. The tree of ‘Standesto’ is moderate in growth, showing an intermediate plumapricot habitus. The long annual shoots are typically mixed, curved by the leaf nodes as in apricot. The leaves have an intermediate shape, but closer to the plum type. Fruits ripen in the first decade of August. They are oval-elongated in shape, asymmetrical, weighing a little over 41 g. Fruit skin is dark violet-blue, finely fuzzy, thin. Fruit flesh is golden yellow, moderately juicy, sweet, with slight acidity and a good mixed apricot-plum taste and mixed aroma. The stone resembles the plum type, free from flesh, representing more than 4% of the total fruit weight. ‘Standesto’ is a fully fertile cultivar and it bears fruits regularly and abundantly. It is tolerant to Plum pox virus. Fruits are well accepted by the consumer for fresh consumption, dried or processed into marmalades, jams, etc. ‘Standesto’ and all the other plumcots obtained by interspecific combination of P. domestica x P. armeniaca could reasonably be assigned to a new separate botanical species under the taxonomy name Prunusx domestiaca Zhiv (Avagyan 2012). More recently, new plumcot breeding programs started in 1999 at the National Institute of Horticultural & Herbal Science (NIHHS) of the Rural Development Administration (RDA) in Korea. The frist registered cultivar has been ‘Harmony’, a plumcot originating from a cross between ‘Soldam’ plum and ‘Harcot’ apricot. It was first selected as PA7-1657 in 2004 for its high fruit quality with attractive appearance. After further evaluation of its characteristics, it was named as ‘Harmony’ in 2007. It blooms almost same time as ‘Harcot’. Since its anthers have no pollen, apricots blooming at the same time should be co-planted to facilitate insect pollination. ‘Harmony’ ripens in early July at Suwon (127.01° E, 37.17° N) Korea, 5 days later than ‘Harcot’ and 27 days earlier than ‘Soldam’. Fruit is round and skin color is reddish orange. Fruit flesh is light orange, marketably firm, sweet and adherent to the pit. Average fruit weight is 71.3 g and total soluble solids concentration is 13.4° Brix (Jun et al. 2011). Inside this breeding program, in 2016 a new plumcot variety

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called ‘Tiffany’ was registered showing fruits of great size and quality (Nam et al. 2016). A new plumcot variety named “Symphony”, was also bred by an interspecific cross between “Soldam” plum (P. salicina) and “Harcot” apricot (P. armeniaca) in Rural Development Administration, Korea. In a recent study, we evaluated postharvest characteristics of “Harmony”, “Tiffany”, and “Symphony” plumcot cultivars bred in Korea. “Harmony” and “Symphony” changed exocarp color from yellow to red during storage at 25 °C, however “Tiffany” maintained exocarp color in red. Examination of exocarp color change for “Harmony” and “Tiffany” was performed only for 4 days at 25 °C due to occurrence of decay, however “Symphony” remained for 7 days under the same condition. During storage for 4 days at 25 °C, “Tiffany” exhibited a dramatic decrease of fruit firmness but “Symphony” showed the slowest softening among the cultivars. Considering the rate of exocarp color change and fruit softening, shelf-life of “Symphony” was longer than the others. In addition, respiration and ethylene production rate in “Symphony” were significantly lower than the other cultivars at harvest and during storage at 25 °C. Overall data indicated that three plumcot cultivars exhibited different postharvest characteristics as well as fruit morphology including fruit size and exocarp and mesocarp color despite sharing the same parents. Therefore, postharvest technology in each plumcot cultivar should be developed based on the cultivar-specific postharvest characteristics in further study (Kwon et al. 2020). In China, the first registered plumcot vaiety was ‘Weihou’. In a complete study, eleven indicators of the plumcot were simplified into four items: soluble solid content, hardness, pH and polyphenoloxidase to reflect the maturity of the fruit. Among the eleven testing indicators, these four indicators could simply reflect the quality. Results showed that the four indicators: soluble solid content, maturity of the fruit hardness, pH and polyphenoloxidase reflect the quality and maturity (Niu et al. 2015). In this context, the solution to the lack of PPV resistance in plum should be the interspecific cross between plum and apricot in the called plumcot. The plumcot is an interspecific hybrid between Japanese plum species (Prunus salicina Lindl) and apricot species (Prunus armeniaca L.), which provides a new fruit typology of high agronomic and market potential by combining the characteristics of these two stone fruit species (Jun and Chung 2007) (Fig. 7.4). Interspecific cross pollinations of plum x apricot showed much higher fruit set than those of apricot x plum. Low percentage of fruit set in the combination of plumcot x plum and plumcot x plumcot was observed. However, the interspecific crosses of plumcot with apricot were compatible. For the stable fruit set of plumcot cultivars, co-planting with apricot as a pollinizer was necessary. Of plumcot cultivars, ‘Beniasama’ and ‘Red pricot’ are pollen-sterile, while ‘New Castle Gold’ and ‘Plum apricot’ are fertile although their pollen grains showed low germination rate. In the case of interspecific crosses between plum and apricot, the percentages of fruit set were higher in female parents with shorter pistils than ones with longer pistils (Jun and Chung 2007). Within the framework of apricot and Japanese plum breeding programs developed at CEBAS-CSIC in Murcia (Spain), the release of commercial plumcots is one of the proposed objectives (Nicolás-Almansa et al. 2020).

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Fig. 7.4 Leaves, flowers and fruts of a plumcot genotype

New genetic material was created at the USDA/Agricultural Research Service in Fresno, California to evaluate PPV resistace after artificial inoculations by grafting and in conditions of natural virus transmission in Greek by the aphid vectors present in the field. Four trees from each of seven apricot cultivars, seven plumcots, one Pluot and one Aprium were planted at the NAGREF-Pomology Institute experimental orchard, where Sharka disease is endemic, in February 1994. However, all plumcot cultivars were found heavily PPV infected by the third year after planting, with very severe disease symptoms. The Aprium and Pluot also demonstrated a severe susceptibility to the disease. Among the apricots examined, only K106-2 (Robada) and ‘Havecot’ have escaped disease in the field (Karayiannis and Ledbetter 2009). On the other hand, first results of evalution of plumcot aginst PPV showed the clear resistance of some interspecific plumcot hybrids and the suitability of the iuse of these new design in the implementation of PPV resistance in plum through new plumcot varieties (Nicolás-Almansa et al. 2020, 2021). The PPV resistance behavior of the plumcot is not wide extended, perhaps, but in some case this resistance has been identified cooroborating the hypothesis of the transmission of PPV resistance from apricot to plumcot. However, this resistance of new plumcot varieties must be evaluated. Unfortunetelly, recent studies showed the susceptibility of these interspecific hybrdis to Xanthomonas arbicola (Dumin et al. 2020). These results showed that approximately 60% of the plumcot leaves in the affected orchard were infected by this disease, which caused 40% total production loss. At the early stage of infection, disease symptoms appear as small, angular and water-soaked spots and develop into circular brown spots at the later stages of infection. As the disease progresses, the leaf tissues around the spots became yellow and the lesions enlarged. When the adjacent lesions merged and the necrotic tissues fall off, shot-hole symptoms appear on the leaves.

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7.5 Agronomic Behavior of Plumcots Transmission of agronomic traits in plumcot from apricot and plum to plumcot has been largely studied. Ledbetter et al. (1994) evaluated five plumcot progenies from the hybridization of plum and apricot for full bloom, vegetative bud break and fruit harvest dates, pollen viability, fruit weight and both fruit skin and flesh color. Ripening dates and fruit weight of plumcots were influenced by the parental apricot. In addition, pollen sterility was observed in only one of the 40 scored plumcots. While both parental plums and apricots were similar in both skin and flesh colors, plumcots varied continuously from red–purple through yellow-green. No clear differences were observed between progenies with regard to fruit skin and flesh colors. Breeding strategies for enhanced fruit productivity are discussed. The flowering time of the interspecific hybrids was evaluated every 3–4 days and recorded in the field in stage 65 according to BBCH scale (Meier et al. 1994) when 50% of flowers were opened. Blooming density was also registered with a score of 0 = null and 3 = maximum. The pistils pubescence and chalice and corolla color were evaluated by observation (Nicolás-Almansa et al. 2020). In addition, regarding flower biology, due to the small number of self-compatible varieties in the Japanese plum species, interspecific crosses between Japanese plums and self-compatible apricot cultivars have been performed during the last years in order to obtain the mentioned resistance to PPV and and self-compatible plumcots (interspecific hybrids). In this study, pollen viability was checked placing on a germination medium formed by 15% sucrose and 1.2% agar. After cultured for 6–8 h at 22 °C, the germinated pollen was counted and the germination percentage was calculated. It is considered that pollen grains are viable providing the length of the growing pollen tube was higher than the pollen grain diameter Nicolás-Almansa et al. (2020, 2021). On the other hand, according to the survey results for 5 years of planting, tree growth was similar in the two most common training systems Y shape with no trellis (YNT) and Y-palmette with trellis (YPT). However, canopy occupation and fruit yield of YPT were significantly higher than those of YNT. The fruit weight and sugar content were not significantly different between two systems. The fruit drop rate tended to be lower in YPT than in YNT. From the above results, it is expected that the YPT type will contribute to the increase of canopy occupation and fruit yield and reducing the fruit drop rate compared to the YNT (Kim et al. 2017). In a recent study, ripening date in plumcot hybrids was determinated when the fruits were at physiological maturity stage. Productivity was also registered with a score of 0 = null and 5 = maximum. Additionally, some fruit quality traits were analysed, distinguishing between physical traits (fruit weight, stone weight, fruit color and firmness) and biochemical traits (soluble solids and acidity). Fruit and stone weight were measured using a digital balance with an accuracy of 0.01 g. Color measurement was made in the skin and flesh of the fruit, using Minolta Chroma Meter, and the assessment of the color was made using the Hue angle parameter. Firmness was determinated by a compression test in Newtons (N) using a Lloyd press. Soluble solids content (SSC) was measured in ºBrix using a digital Optic Ivymen System.

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Finally, acidity and pH was evaluated using 2 g of a homogenized sample diluted in 20 ml of destilled water, and the values wer e obtained as a grams of malic acid/100 ml, since this is the dominant organic acid in apricots and plums. All of the evaluated quality traits were analyzed in 12 fruits per genotype. Regarding acidity and soluble solids content, we evaluated them with three replicates from the pool of 12 fruits (Nicolás-Almansa et al. 2020, 2021). Regarding pomological traits, all plumcot hybrids have pubescent skin, characteristic of apricot, and also a skin color (reddish and purplish) similar among them. The genotype with the most striking flesh color is P2 × A1-1, which has an intense red color. The maximum fruit firmness is in genotype P1 × A1-4 with 39,65 N, and P1 × A1-1 has the highest soluble solids content with 17,53 ºBrix. In addition, all interspecific genotypes have a low intensity of flowering and productivity. The genotype with the highest blooming density and yield is P1 × A1-1 with a value of 2. On the other hand, the hybrid P2 × A1-3 has the earliest flowering, however it has the lowest flowering intensity and has not borne fruit yet. Finally, genotypes P1 × A1-2 and P3 × A1-2 has not been able to flourish until now. The blossomed hybrids present flowers with pistil pubescence and pink corolla, characteristics that come from the apricot parent. All interspecific genotypes have a low intensity of flowering and productivity. The genotype with the highest blooming density and yield is P1 × A1-1 with a value of 2. On the other hand, the hybrid P2 × A1-3 has the earliest flowering, however it has the lowest flowering intensity and has not borne fruit yet. Finally, genotypes P1 × A1-2 and P3 × A1-2 has not been able to flourish until now. The blossomed hybrids present flowers with pistil pubescence and pink corolla, characteristics that come from the apricot parent (Nicolás-Almansa et al. 2020, 2021). On the other hand, regarding biochemical flavor constituents, evaluation of volatiles was performed in Tenax traps, eluted with ether, and examined by gas chromatography-mass spectrometry. Forty-one compounds from seven chemical classes were identified in the plumcot fruit samples. Seven of the identified volatiles were unique to plumcot, and not present in either the plum or apricot parent. These aromatic profiles from plumcot accessions more closely resemble apricot profiles rather than plum (Gómez and Ledbetter 1993). In addition, the aromatic profiles of the parents (apricot and plum) and the progenies (plum x apricot) demonstrated that the plumcot progeny retained the ability to produce volatile compounds typical of the parents and that components important to the aromas and flavors of the parents were produced at high levels (Gómez et al. 1993). In plumcot, total volatiles obtained from fruit sample extractions were very similar in each developmental stage; however, the aromatic profile of constituents changed as fruit maturity progressed to a tree ripe stage. Important differences were found in the volatile constituent profiles for both fruits; at the tree ripe stage, the concentration of lactones and terpenic alcohols, characteristic compounds of apricot aroma, were much higher in apricot than plumcot, the latter more resembling a plum aromatic profile (Gómez and Ledbetter 1997). On the other hand, regarding sugar composition, sucrose, fructose, and glucose content increased with fruit development, unlike content of sorbitol in plumcot varieties. Plumcot contained the highest fructose, in comparision with peach that showed

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the maximum content of sucrose at full maturation stages. Fructose and glucose were highly correlated in plumcot, plum, and peach. Total soluble solids averaged 17.5, 14.8, 11.9, and 10.6° Brix in apricot, plumcot, plum, and peach, respectively, whereas total acidity was 0.9, 1.4, 0.5, and 0.3% in four Prunus cultivars at ripened stages. In relation to organic acid, shikimic acid was significantly correlated with oxalic acid in apricot, plumcot, and plum, but not in peach (Bae et al. 2014). Finnaly in relation to the postharvest physiology and quality of plumcot a recent study evaluating ‘Harmony’ fruits stored at 0, 5, 10, and 20 °C, respectively, with three different ripeness stages grouped by skin color development was performed. Furthermore, authors treated 1 mu L-L-1 1-MCP was treated at 10 °C for 17 h and stored at 10 °C for 12 days to evaluate the effectiveness for better shelf-life. The results indicated that lower storage temperature than room temperature effectively reduced the respiration rate with delaying quality changes in plumcot fruits. While, the fruits showed worse fruit taste than the fruits stored at 10 and 20 °C. Reversely, the fruits stored at 20 °C showed more respiration rate and ethylene production. 1-MCP treatment effectively reduced the skin red color development, ethylene production, CO2 and softening of plumcot ‘Harmony’ fruits. Overall results indicated that the optimum harvest time and storage temperature could be 30–50% red color and near 10 °C. Postharvest 1-MCP application at the level of 1.0 µ L.L-1 could maintain fruit quality well in plumcot fruits (Lim et al. 2013).

7.6 Molecular Characterization of Plumcots The application of these molecular tools will increase the viability and efficiency in the development of the new planned design. In this context, high-throughput sequencing technologies resulted in a great advance in the development and application of marker assisted selection (MAS) strategies. This situation does mean that MAS will replace conventional breeding; other ways is a necessary complement. The application of strategies at genomic, epigenetic, transcriptomic and proteomic level should be all integrated for a better understanding of the molecular mechanisms involved in the most important plant breeding aspects, which will facilitate the development and optimization of molecular markers to apply in the field exploitation of the fruit tree new varieties, offering and integrating complete technological offers. In the case of plumcot interspecific hybrids this molecular characterization is very interesting to avoiud scape or accidentral pollinations considering as plumcot genotypes that are plums or apricots. First molecular chacracterization of plumcots was performed by using isoenzyme markers. Starch gels of three buffer systems and acrylamide gels were used for electrophoretic separation of twenty enzyme systems. Results showed the low polymorphism of these kind of markers (Byrne and Littleton, 1989). Later, a new study to find isoenzyme markers for plum x apricot (plumcot) hybrids to uniquely identify hybrid seedlings from plum x apricot crosses.

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Ten Japanese plum cultivars, 17 apricot cultivars, seven plum x apricot (plumcot) hybrids, which were derived from the breeding program of Agricultural Research Service in Fresno and two complex hybrids (Pluot and Aprium) were examined electrophoretically. The most informative enzymes for identifying plumcots were peroxidase (PRX-2, PRX-Cathodal), acid phosphatase (ACP-2) and shikimate dehydrogenase (SKD-1, SKD-2). In addition, superoxide dismutase bands SOD-lc and SOD-ld and phosphoglucomutase PGM-2b showed activity only in plums and in plumcots. The existing polymorphism allowed to distinguish individually all seven examined plumcots (Manganaris et al. 1999). More recently, the molecular characterization of these interspecific hybrids have been performed by using simple sequence repeat (SSR) primers to confirm the interspecific status. These markers were selected due to the previous observed polymorphism of the parents of the different crosses. Ahmad et al. (2004) investigated the genetic diversity among 14 plums, 6 pluots and one plumcot representing commercial cultivars in California, with 28 microsatellite markers. Of the 28 SSR markers, 25 were from sweet cherry (Prunus avium L.) and three from peach (Prunus persica L.). Approximately 80% of the cherry primers generated amplification products in plum and pluots, showing transportability between these Prunus species. One to eight putative alleles per locus were displayed by the tested SSRs in plums and pluots. In plum and pluot samples a total of 100 alleles were identified with an average of 4.3 alleles per primer combination. The SSR markers were successfully used for the discrimination of all tested cultivars. In pluots, 76 alleles were found in which 63 (83%) were specifically coming from plum, 9 (12%) were common in plum, pluots and apricot while no allele in the pluots was observed that was contributed from apricot. In plumcot, 49 alleles were observed in which 25 (51%) were from plum, 18 (36%) were specifically from apricot and 6 (12%) were common in plum, plumcot and apricot. Relationships among the 28 plum, pluot and apricot cultivars were represented by a dendrogram, constructed on the basis of 168 SSR markers. The dendrogram showed the. plums and pluots form. a cluster distinct from the apricots, with pluot cultivars interspersed among plum cultivars and more closely related to plum than to apricot. Plumcot made a separate branch and was placed between the plum and apricot cluster. The obtained results by Ahmad et al. (2004) clearly suggested that the SSR markers are valuable tools for identification of cultivars and diversity analyses in plum with a polymorphism level much higher than the case of the use iof isoienzymes. A new study also showed the genotyping by SSR markers of the nearly 700 genotypes generated by crossings. The application of these SSRs markers clearly identified a total of 13 interspecific genotypes (Nicolás-Almansa et al., 2021). This result shows the difficulty to obtain interspecific hybrids, since a success rate of 2% was obtained. All the real interspecific hybrids come from crosses where plum was used as the male parent and apricot as the female parent (Fig. 7.5). On the other hand, regarding the molecular chacaracterization of flower incompatibility and identification of S-alleles, Duan et al. (2009) identified four S-RNase genes in different plumcot genotypes. All of them displayed typical structural features of Prunus S-RNases, i.e. one signal peptide, five conserved regions, one

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Fig. 7.5 Allelic segregation of the SSR marker CPSCT005 in a plumcot interspecific family. The arrows point the parental alleles, and those are identificated by letters (A, B and C). P1 and P3 are the female parent, while A1 and A3 are the male parent of the crossings

Rosaceae-specific HV region and two introns. At the amino acid level, plumcot SelfIncompatuibiulity (SI) shared an extremely high similarity (99.5%) with P. salicina Sh-RNase, indicating that they likely represented the same S-RNase. In comparison with other Prunus S-RNases, plumcot S(1) showed a 65.6% to 80.4% similarity. Likewise, P. simonii S(2) and P. simonii S(4) were likely identical to P. armeniaca S(2)-RNase and P. salicina Sb-RNase, respectively, and showed 66.5% to 78.7% similarity to other Prunus S-RNases. In the case of P. simonii S(3), it shared 66.5% to 89.6% similarity to other Prunus S-RNases. Similarity analysis well mirrors that plumcot originated from the cross of plum and apricot. Phylogenetic analysis indicated that the S-RNase divergence predated speciation in Prunus. Sequence information provided in the four plumcot S-RNases will be useful for function analysis in self-incompatible response. Recent studies also showed that the identification of S-alleles was made successfully using two different pair of consensus primers of S-RNase, Pa-ConsIF-PaConsIR2 and PruC2-PCER (Nicolás-Almansa et al. 2020). The plumconts who have not segregated the Sc allele are: P1 × A3-1 since its male parent has Sc allele in heterozygosis with the S9 allele, and the hybrid P3 × A1-1 inherits Sy allele from the female parent and presents a Sz allele that does not match either parent, so it will have to be studied further. The rest of plumcots segregate the allele Sc, which

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Fig. 7.6 Evaluation of floral compatibility using S-allele PCR in different plumcot genotypes

confers the self-compatibility in apricot, so a priori they should be self-compatible. However, the studies of pollen viability determined androsterility of all genotypes. These results suggest that interspecific hybridization causes androsterility in the offspring (Fig. 7.6).

7.7 Future Perspectives Plumcot is an interspecific hybrid between plum (P. salicina) and apricot (P. armeniaca) that plays an important role in non-timber forestry industry and making medicine in chine. In addition, the design of new interspecific hybrdis should be of great interst mainly in plum bredding. These new designs showed the valuable use of apricot as a source of self-compatibility and Plum pox virus resistance in plum through the generation of interspecific hybrids Prunus salicina Lindl. x P. armeniaca L. (plumcots) with hybrids of good agronomical characteristics.

References Ahmad R, Potter D, Southwick SM (2004) Identification and characterization of plum and pluot cultivars by microsatellite markers. J Hort Sci 79:164–169 Avagyan A (2012) “Standesto”, the First Bulgarian Plumcot Cultivar. Acta Hort 966:219–222

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Martínez-Gómez P, Dicenta F, Audergon JM (2000) Behaviour of apricot (Prunus armeniaca L.) cultivars in presence of sharka (Plum pox potyvirus): a review. Agronomie 20:407–422 Martínez-Gómez P, Rubio M, Dicenta F, Gradziel TM (2004) Resistance to Plum Pox Virus (RB3.30 isolate) in a group of California almonds and transfer of resistance to peach. J Amer Soci Hort Sci 129:544–548 Meier U, Graf H, Hack H, Hess M, Kennel W, Klose R, Mappes D, Seipp D, Stauss R, Streif J, Boom TVD (1994) Phanologische Entwicklungsstadien des Kernobstes (Malus domestica Borkh. und Pyrus communis L.), des Steinobstes (Prunus-Arten), der Johannisbeere Ribes-Arten und der Erdbeere Fragaria x ananassa. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 46(7):141–153 Nam EY, Jun JH, Chung KH, Kwon JH, Yun SK, Yun IK, Cho KH (2016) Tiffany red-fleshed plumcot. Hort Sci 51:1304–1307 Neumuller M, Lanzl S, Hartmann W (2009) Towards an understanding of the inheritance of hypersensitivity resistance against the sharka virus in european Plum (Prunus domesticaL.): generation of interspecific hybrids with lower ploidy levels. Acta Hort 814:721–726 Nicolás-Almansa M, Guevara A, Rubio M, Cos J, Carrillo A, García-Montiel F, Salazar JA, Martínez-Gómez P, Ruiz D (2020) The apricot as a source of self-compatibility and Plum pox virus resistance in the generation of interspecific hybrids Prunus salicina Lindl. x Prunus. armeniaca L. (plumcots). Acta Hort 1290:115–118 Nicolás-Almansa M, Guevara A, Salazar JA, Rubio M, Martínez-Gómez P, Ruiz D (2021) Molecular and phenotypic characterization of interspecific Prunus salicina x Prunus armeniaca (plumcot) hybrids. Acta Hort 1307:267–274 Niu JL, Liu MX, Peng QM (2015) Analysis of main index components and cluster of plumcot “Weihou” during different harvest periods. Xingjiang Agric Sci 52:33–36 Okie WR, Thompson JM, Reilly CC, Meredith FI, Robertson JA, Lyon BG (1992) Segundo, Byrongold and Rubysweet plums and BY69-1637P plumcot–fruits for the Southeastern United-States. Fruit Var J 2:102–107 Okie WR (2005) “Spring Satin” Plumcot. J Amer Pomol Soc 59:119–124 Rodamilans B, Valli A, García JA (2020) Molecular Plant-Plum pox virus interactions. Mol PlantMicrobe Interact 33:6–17 Rubio M, Martínez-Gómez P, Dicenta F (2003) Resistance of almond cultivars to Plum pox virus (sharka). Plant Breed 122:462–464 Rubio M, Martínez-Gómez P, Audergon JM, Dicenta F (2007) Testing genetic control hypotheses for Plum pox virus resistance in apricot. Sci Hort 112:361–365 Rubio M, García-Ibarra A, Dicenta F, Martínez-Gómez P (2011) Plum pox virus (Sharka) sensitivity in Prunus salicina and Prunus cerasifera cultivars against a Dideron-type isolate. Plant Breed 130:283–286 Rubio M, Ruiz D, Egea J, Martínez-Gómez P, Dicenta F (2014) Opportunities of marker assisted selection for Plum pox virus resistance in apricot breeding. Tree Genet Genomes 10:513–525 Rubio M, Rodríguez-Moreno L, Ballester AR, Castro M, Bonghi C, Candresse T, Martínez-Gómez P (2015) Analysis of gene expression changes in peach leaves in response to Plum pox virus infection using RNA-Seq. Mol Plant Pathol 16:164–176 Rubio M, Ballester AR, Olivares PM, Castro de Moura M, DicentaF, Martínez-Gómez P (2015b) Gene expression analysis of Plum pox virus (Sharka) Susceptibility/Resistance in apricot (Prunus armeniaca L.). PLoS One 10:e0144670 Rubio M, Martínez-Gómez P, Sánchez-Navarro JA, Pallás V, Candresse T (2017) Recent advances and prospects in Prunus virology. Ann Appl Biol 171:125–138 Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Foster G (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954 Scorza R, Callahan A, Dardick C, Ravelonandro M, Polak J, Malinowski T, Zagari I, Cambra M, Kamenova I (2013) Genetic engineering of Plum pox virus resistance: ‘HoneySweet’ plum. Plant Cell Tiss Org Cult 115:1–12

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Chapter 8

Integrated Genomic Designing and Insights for Disease Resistance and Crop Protection Against Pathogens in Cherry Antonios Zambounis, Dimitrios Valasiadis, and Anastasia Boutsika

8.1 Introduction Cherry belongs to the Prunus genus and is among the most important fruit tree crops worldwide and mainly in temperate areas (Fernandez i Marti et al. 2012). Particularly, the cultivated sweet cherry (Prunus avium L.) is an outbreeding deciduous tree of the Rosaceae family, sharing a diploid genome (2n = 16) (Arumuganathan and Earle 1991). On the contrary, the tetraploid sour cherry, P. cerasus, is believed to have originated from a hybridization event between P. avium and another tetraploid species, P. fruticosa (Potter 2012). Sweet cherries are gaining importance due to their nutritional benefits for human health, as their consumption has potential preventative properties against diseases such as Alzheimer’s, cancer, and inflammation-related diseases (McCune et al. 2010). Furthermore, cherries contain unique phytochemical compounds with important attributes to human health (Kelley et al. 2018). Global production was around 3.6 million tons in 2017, while cherry is a vital crop to consider for further researchto sustain its global competitiveness. Climate change is projected to lead to a global temperature rise until 2050, whereas disease outbreaks that threaten the production and yield of fruit trees, including cherry, are also expected to intensify (Sarkar et al. 2017). For this reason, appropriate measures and actions must be undertaken (Ray et al. 2012), as the likelihood of extreme weather conditions may dramatically increase the emergence of new or more aggressive strains of pathogens that may result in further yield losses (Watson

A. Zambounis (B) · A. Boutsika Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization ‘Demeter’ (ELGO-Demeter), 57001 Thessaloniki-Thermi, Greece e-mail: [email protected] D. Valasiadis Laboratory of Pomology, Department of Agriculture, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_8

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et al. 2018). Interestingly, cultivars of sweet cherries exhibit a wide range of phenotypic diversity indefense reactions against pathogens. In recent years, particularly fungal diseases have been more pronounced and caused extensive damages. Among the most common fungal pathogens of sweet cherry fruits, Monilinia spp. is the causal agent of brown rot disease (Borve et al. 2017). During storage, sweet cherry fruits are susceptible to serious postharvest decays by Monilinia spp., Botrytis cinerea, and occasionally by Alternaria alternata, Penicillium spp. and Cladosporium spp. (Romanazzi et al. 2001). Vascular wilt and root rot are usually caused by soilborne pathogens including fungi, such as Fusarium species (Urbez-Torres et al. 2016) and oomycetes of the genus Phytophthora (Türkölmez and Dervis 2017). Implementation of innovative cultivation practices and integrated disease management with fewer inflows of commercial chemical fungicides are important for the efficient and environmentally friendly control of cherry pathogens. In cherry, genomics research andnew plant protection strategies have gained more insights lately. The exploitation of early and reliable diagnostics has been considered for the integrated management of disease outbreaks (Zambounis et al. 2020a). Besides, the accurate intraspecific genotyping of pathogen populations is also crucial for assigning efficiently and more accurately the signatures of genetic variation acting among them. Genomics approaches can assist cherry breeding programs for disease resistance inmultiple aspects, such as the evaluation and selection of resistant cultivars by employing molecular markers, and the precise determination of pathogens epidemiology across cultivars. Furthermore, metagenomics and microbiome analyses can uncover the structural shaping of fungal or bacterial communities that are associated with infections caused by themain pathogens of the crop. Genomics approaches may also facilitatethe assessment of the susceptibility of pathogenic strains to fungicides and the investigation of tolerance mechanisms through the employment of molecular and -omics technologies. The proper implementation of these approaches would undoubtedly facilitate the quality improvement of cherry end-product and cultivars, while at the same time will protect the environment with fewer and more friendly fungicide applications. Towards these frames, the implementation of a dissemination plan among stakeholders and the scientific community is a prerequisite. In the past, breeding approaches have undoubtedly improved cherry resistance to biotic stresses, but an important future challenge will be to maintain this contribution even under the projected adverse environmental scenarios of climate change. The integration of innovative breeding techniques such as marker-assisted selection (MAS) and omics approaches is essential for the enhanced adaptation of cherries to pathogen attacks (Zambounis et al. 2020a and reference therein). In addition, the indigenous cherrycultivars and wild cherry species offer an invaluable pool for sourcing desirable defense-related genes. This natural genetic diversity may provide information about the availability of target donor defense genes and genetically divergent genotypes, which can serve as potential parents in crosses to reach the optimum genetic polymorphism required for mapping and breeding for disease resistance.

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Nowadays, the massive amounts of genomic data generated from a hitherto of state of the art sequencing technologies, along with the availability of public data repositories, could accelerate the development of cherry tolerant cultivars against pathogens. Besides, a major tool for enhancing the breeding efforts in a directed way is the development of functional molecular markers related to loci conferring resistance to pathogens. Advances in MAS approaches will expand our knowledge and eventually lead to genomics-assisted breeding (GAB) towards disease resistance and adaptation (Zambounis et al. 2020a and references therein). Several sequencing projects related to the completion of genomes and transcriptome profiles under pathogen challenge, are currently ongoing for major deciduous fruit trees and will enhance the effectiveness of breeding methods for disease resistance. Nowadays, genomic selection (GS) has been considered as one of the most promising breeding strategies, while its advantages over traditional practices have been demonstrated (Crossa et al. 2017). These GS approaches may be integrated with high-throughput phenotyping for the identification of functional markers for well-characterized major defense genes. Furthermore, characterization of genetic diversity in cherry cultivarscan be achieved through whole-genome re-sequencing (WGRS), along withthe discovery of genes associated with disease resistance responses through the application of genotyping-by-sequencing (GBS) approaches (Zambounis et al. 2020a).

8.2 Biotic Stresses on Cherry Crop The phytopathogens are major limiting factors in cherry production, particularly due to their rapid evolution and the ever-changing environmental conditions that are projected to be adversely affected by climate change (Zambounis et al. 2020a). The economic losses from fungal, bacterial and viral diseases in cherry pose a serious threat to yield and quality of fruits in severe cases of infection.

8.2.1 Description of Fungal Diseases Cherry is intensively plagued by a plethora of phytopathogenic fungal species (Zambounis et al. 2020a), while the long-distance aerial dispersal is an important pathogen survival strategy, especially for pathogens with a biotrophic life stage. In general, there are no available cherry cultivars with durable resistance to all fungal diseases, while cherry trees are particularly susceptible to infections during blooming and harvest periods (Borve et al. 2017). Among the fungal diseases on fruits, grey mold that is caused by the necrotrophic fungus Botrytis cinerea is considered one of the most important pre- and postharvest diseases. The pathogen infects all parts of cherry flowers (Borve et al. 2017 and references therein) and depending on the weather conditions, floral infection leads to blossom blight or invisible latent infections (Tarbath et al. 2014). B. cinerea sporulates predominately on necrotic and

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decayed tissues, forming numerous conidia that are the most significant dispersal propagules of the pathogen, which subsequently initiate invisible (latent) or visible (quiescent) fruit infections (Tarbath et al. 2014). Moreover, brown rot caused by Monilinia spp. is one of the most destructive diseases of stone-fruits, including cherry (Ortega et al. 2019), while Monilinia laxa, M. fructicola, and M. fructigena are among the three most widespread species (Côté et al. 2004; Wang et al. 2018). These pathogens differentially occur around geographical regions and their prevalence depends also on the distribution of their hosts (Berrie and Holb 2014). M. laxa and M. fructicola are the most prevalent species in Europe, whereas M. laxa is considered an endemic species worldwide (Villarino et al. 2013). M. fructicola is also important in North America and Australia, whereas M. fructigena is prevalent across Europe and Asia (Martini and Mari 2014). In orchards and upon storage conditions the economic losses are ranging up to 25% and 8%, respectively across Europe (Berrie and Holb 2014). Infection may cause serious losses on cherry fruits, especially in seasonal periods with wet weather conditions during flowering or immediately before harvest. However, yield losses are associated mainly with blossom blight and brown rots on mature fruits (Fig. 8.1). The phenological stage has a significant effect on cherry fruit susceptibility, whereas for example, fruits

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Fig. 8.1 Symptoms of infection of sweet cherry by Monilinia spp. a in flower and b in fruit

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are initially tolerant to M. laxa before getting their red coloring (Xu et al. 2007). Thereafter, as fruits are getting mummified, there is a gradual aggregation into pseudosclerotia, which serves as the primary source of inoculum in the next growing season. Other fungal pathogens affecting cherry fruits include the C. acutatum, where similar races and isolates are grouped to the C. acutatum complex (Damm et al. 2012). Particularly, affected sour cherry fruits may dry out early in the season, while fruits of sour and sweet cherry typically show signs of decay near harvest or postharvest stage. Notably, the teleomorph Glomerella acutata has never been observed in cherries, whereas the C. acutatum conidia are released by water splash from acervuli, which are black structures on cherry fruits (Borve et al. 2017). Additionally, fruit rot may be caused by different species within the genus Mucor and primarily by Mucor piriformis. Furthermore, Sclerotinia sclerotiorum occasionally causes severe fruit rots, while the necrosis spreads from an infected flower to the surrounding blossoms sticking together and then moves to adjacent young fruits. Among other types of decay at the post-harvest stage, Alternaria rot is quite frequent on ripe sweet cherries and may result in more than 15% of losses during storage (Ippolito et al. 2005). Isolates of Alternaria spp. complex efficiently survive in cherry orchards and the spores are disseminated through the air. Furthermore, Penicillium expansum has a worldwide distribution causing postharvest rot that isknown as blue mold, which is more prevalent in long-storage or on fruits during their prolonged ripening developmental stage (Borve et al. 2017). The pathogen produces the patulin mycotoxin that is mainly associated with pome fruits, but it is also predominantly observed on sweet cherries (Sanzani et al. 2013). Both Cladosporium herbarum and Aspergillus niger may also infect fruits during storage conditions and occasionally lead to severe postharvest losses (Barkai-Golan 2001). In temperate zones, cherry leaf spot caused by Blumeriella jaapii along with brown rot are the most important fungal diseases of cherries (Borve et al. 2017). The pathogen seriously affects the foliage, whereas almost all cherry cultivars are susceptible (Wharton et al. 2003), which is also evident for the causal agent of powdery mildew (Podosphaera clandestina) (Olmstead et al. 2000). Moreover, the causal agent of the shot-hole disease, Wilsonomyces carpophilus, is a minor problem on sour cherry compared to sweet cherry (Adaskaveg and Ogawa 1990). Finally, Taphrina wiesneri is associated with leaf curl and possibly disturbs the hormonal balance of the host (Masuya et al. 2015). Crown and root rots are caused by various species of Phytophthora spp., such as P. parasitica, P. citrophthora, P. cambivora, P. cinnamoni, P. citricola, P. megasperma, P. drechsleri, P. cryptogea, P. cactorum and other unidentified species in cherry (Borve et al. 2017 and references therein). Particularly, P. parasitica that has a broad host range (Kamoun et al. 2015; Panabieres et al. 2016), rarely occurs in well-managed orchards, whereas weakened trees are more prone to root rot. The first symptoms in the canopy are generally characterized by poor growth, discoloration, yellowing and falling of leaves, dieback and wilt. However, the more pronounced symptoms are reported at the collar and crown base of the affected plants, where trunk cankers can be observed such as brown and necrotic decays.

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Moreover, Verticillium dahliae produces a hyaline mycelium and may cause a rapid decline in cherry-growing regions, whereas the commonly used cherry rootstocks are considered susceptible. The initial symptoms of the disease include a sudden wilting of leaves which usually turn yellow, show upward rolling and may eventurn dull with a pale brown color in individual branches in the early summer (Borve et al. 2017). The conidia can be easily transported from infections sitesto twigs through the transpiration stream. Phomopsis spp. species are generally considered secondary or opportunistic pathogens. For example, the symptoms of P. amygdali, the main causal agent of such rots in cherries, may sometimes be confused with those of blossom blight caused by Monilinia spp. Finally, Armillaria root rot caused by A. mellea is considered one of the most significant soil-borne diseases of sweet cherry worldwide. The pathogen commonly occurs in orchards with weakened trees or at replanted infected sites (Borve et al. 2017).

8.2.2 Description of Bacterial Diseases Bacterial diseases are frequently a major limiting factor in the production of cherries that may cause significant yield losses reaching up to 50% under favorable environmental conditions. Two of the most important bacterial diseases are bacterial canker and crown gall (Pulawska et al. 2017). The occurrence of other bacterial diseases on cherries is less common, but their severity may suggest that they could turn into serious issues in the near future. The causal agents of bacterial canker belong to the Pseudomonas syringae species complex, which comprises numerous polyphagous species that infect more than 180 plant species and fruit trees (Pulawska et al. 2017 and references therein). The bacterial isolates causing bacterial canker on cherry trees are classified at three genomospecies (gs): P. syringae pv. syringae (Pss), P. syringae pv. morsprunorum race 1 (Pmp1) and P. syringae pv. morsprunorum race 2 (Pmp2) and P. syringae pv. avii (Psa) (Ménard et al. 2003). Recently, a new species (Pseudomonas cerasi sp. nov) was also described on cherries and mainly in sour cherry (Kału˙zna et al. 2016), whereas P. syringae pv. cerasicola has been associated with bacterial gall disease on ornamental cherry trees in Japan (Kamiunten et al. 2000). Since the canopy is usually affected, the first symptoms may remain unnoticed. However, roundish or irregular-shaped galls are usually formed at the trunk basis near the soil surface, at the graft or bud ssections, or even on roots (Pulawska et al. 2017). Furthermore, bacterial leaf spot iscaused by Xanthomonas arboricola pv. pruni (Pulawska et al. 2017). The phylogenetic relationships among pathovars have been determined using the housekeeping gene rpoD (Hajri et al. 2012). The complete genome determination of a genotype-representative strain from Europe (Pothier et al. 2011) confirmed the presence of a large type III effector repertoire (Hajri et al. 2012).

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The availability of other draft genomes of X. arboricola isolates (Pereira et al. 2015) will assist the elucidation of pathogenesis processes associated with bacterial leaf spot disease.

8.2.3 Description of Viral Diseases Viruses may also infect cherries, while their transmission mode adds further challenges to the management control of the related diseases. For instance, Prune dwarf virus (PDV) and Prunus necrotic ringspot virus (PNRSV) are responsible for significant crop losses worldwide (Cembali et al. 2003). Furthermore, the Cherry leaf roll virus (CLRV) belonging to Secoviridae family (Sanfacon et al. 2012) has a bipartite genome of two single-stranded positive-sense RNAs and may result in serious sour cherry losses (Buttner et al. 2011). Although CLRV distribution may appear irregular, the pathogen can be detected in all parts of an infected cherry tree (James et al. 2017).

8.3 Methods for Control of Cherry Pathogens The majority of cherry commercial cultivars and rootstocks are more or less susceptible to common crop diseases. The susceptibility is highly dependent and influenced by the pathogen and rootstock/scion combination (Kappel et al. 2012). The adoption and implementation of phytosanitary practices, such as removal of rotten fruit or mummies, careful pruning of infected twigs during the dormant season, destruction of cankered twigs and efficient irrigation management are essential and may reduce the inoculum levels (Borve et al. 2017). Besides, new cultivation practices and innovative protocols for the integrated management of cherry diseases are highly important in order to minimize the environmental footprint and the inflows of chemical control agents. Unfortunately, traditional control of cherry fungal pathogens such as Monilinia spp. relies on the application of synthetic fungicides that are applied up to five times per growing season. Thus, among the most effective fungicides available for control of brown rot are those that belong to chemical classes of the demethylation-inhibiting (DMI) triazole, anilinopyrimidine and phenylpyrrole classes. However, alterations in the shaping of Monilinia spp. populations due to climate change are expected to reduce the efficiency of fungicides and raise the costs of current control measures (Hrusti´c et al. 2015). Additionally, strobilurins are among the most effective fungicides for powdery mildew. Moreover, the prevention of postharvest rots in sweet and sour cherries fruits is crucial due to their high commercial value, but effective control methods against the main fungal diseases are not existent (Feliziani et al. 2013). Pyrimethanil and thiabendazole have traditionally been used for blue mold control, but their intense applications over the years have led to the appearance of

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resistant Penicillium populations. In general, the precise timing of fungicide applications is crucial, asin cases of blossom blight control where flowers must be protected before the occurrence of the prolonged wetness and mild temperatures which significantly favor the infection. Moreover, some organic fungicides are not highly effective in orchards for the control of fungal pathogens. The rotation of fungicides with different modes of action is highly recommended to avoid the selection pressure that may lead to the emergence of fungicide-resistant pathogens races. Besides, in order to restrict fungicide applications, appropriate risk analysis should be implemented taking into account temperature, moisture conditions, inoculum potential, pathogen epidemiology, latent infections and fruit phenological ripening stages (Xu et al. 2007). Furthermore, extensive knowledge of the respective pathosystems towards the prevention of fruit infections is also essential. The uncovering of pathogen diversity through genotyping along with the decoding of fungal populations tructures are also crucial for the improvement of control strategies. Notably, the rapid evolution of novel or hybrid races (such as in Phytophthora spp.) is known to affect the genetic structure of pathogen populations contributing to their rapid adaptation to adverse conditions. This may eventually lead to an overcoming of cherry resistance responses, or even at pathogens resistance to fungicides. As previously mentioned, resistance to bacterial diseases hasnot been identified in cherry cultivars so far. The most effective strategies for primary control of bacterial diseases, such as crown gall and bacterial canker include the implementation of strict quarantine and sanitation measures, soil solarization, early detection systems, eradication processes, and healthy propagated plant material from nurseries (Pulawska et al. 2017). Reliable disease forecasting models could also help towards efficient control, along with strict phytosanitary measures during the importation and exportation of cherry materials.

8.3.1 Biocontrol Methods with Natural Products and Biotic Agents Fungicide applicationis the most common practice for the control of cherry diseases, however, a lot of times is ineffective, quite costlywith negative sideeffects on the environment. Thus, innovative and environmentally friendly approaches with a small environmental footprint are in urgent need to avoid the development of pathogenresistance to specific chemical substances. The optimization of integrated disease management practices will further increase the income of farmers, leading to the production of superior cherry end-products. Previously, biological control against brown rot in cherry trees has been achieved with epiphytic fungi, such as Aureobasidium pullulans and Epicoccum purpurascens (Wittig et al. 1997). Furthermore, the bio-priming methodology is a valuable perspective for sustainable and integrated plant protection (Ramírez-Carrasco et al. 2017). This methodology is based on the activation of plant molecular mechanisms after the intervention with defense

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inducers, which enable defense mechanisms to be activated timely during future pathogen attacks. Besides, novel bioactive compounds such as photosensitizers that may impair the virulence of phytopathogenic species may also be explored for further usage in integrated disease management (Zambounis et al. 2020b). It is also known that biologically active plant extracts may exhibit prominent antifungal properties (Yanar et al. 2011; Díaz et al. 2018).

8.3.2 Profiling Microbial Communities for Pathogens Control The accurate determination of the eukaryotic and prokaryotic microbiome with the application of metagenomic approaches may substantially contribute to the efficient control of many cherry phytopathogens, as the early elucidation of the shaping and the deciphering of complex communities interactions might contribute to the sustainable management of severe diseases (Price et al. 2009). Nowadays, these highthroughput screening (HTS) approaches are adequately applied in plant pathology and microbe ecology, providing an efficient approach for the analysis of microbial diversity and the related endophytic and epiphytical communities (Müller and Ruppel 2014; Taylor et al. 2014; Abdelfattah et al. 2015, 2016; Zambounis et al. 2019). Furthermore, metagenomic approaches may also provide valuable insights intothe effect of different disease management practices against important postharvest pathogens, which can significantly deteriorate fruit yield and quality (Zambounis et al. 2020c).

8.4 Diagnostics and Genotyping of Cherry Pathogens Attempts to effectively manage diseases in the cherry crop will undoubtedly benefit from the timely application of accurate molecular detection techniques that capture the population dynamics of pathogens. Early molecular identification of pathogens and quiescent infections is an important factor towards the establishment of an integrated system for disease management, eliminating reckless fungicide applications. For instance, molecular methods (multiplex PCR) for the identification of Monilinia spp. were developed, whereas a similar method based on the presence and differences in the size of cytochrome b gene intron was also reported (Hily et al. 2011). Species identification based on molecular methods was also reported in the case of powdery mildew infections (Santiago-Santiago et al. 2014), as well within the C. acutatum complex (Damm et al. 2012). It is quite meaningful to monitor the geographical proliferation and dispersal of cherry pathogens. The uncovering of pathogenetic profilesis necessary for a more comprehensive understanding of the epidemiology of diseases. The systematic study

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Fig. 8.2 Application of an HRM analysis for the efficient differentiation and genotyping of Phytophthora spp. (Zambounis et al. 2016b)

of pathogen population diversity, along with valid, early and accurate detection measures would assist efforts for the integrated management of diseases (MoralesRodríguez et al. 2019). Furthermore, the meticulous investigation of the genetic variability of pathogen populations, the correlation of infections with cultivation practices and environmental conditions, require the adoption ofvalid and reliable techniques for the detection of cherry pathogens. Nowadays, high-resolution melting (HRM) analysis is a molecular analytical method that has been extensively employed for DNA genotyping applications due to its high simplicity, sensitivity and specificity (Ganopoulos et al. 2012). According to this technique, amplicon-specific melting curve profiles are generated and differences can be assigned to genetic variations of pathogens (Zambounis et al. 2016a) (Fig. 8.2). The HRM has already been employed in the genotyping of various pathogenic fungal and oomycete species (Ganopoulos et al. 2012; Zambounis et al. 2015a, 2016a, b, 2021). Additionally, this method has become increasingly applied in plant-fungal diagnostics (Zambounis et al. 2015b). The diagnostic methods of bacterial canker are commonly based on bacterial isolation on nutrient media followed by morphological and biochemical characterization coupled with pathogenicity tests (Pulawska et al. 2017). Repetitive PCR (rep-PCR) is one of the first DNA-based molecular tools that was developed for P. syringae taxonomic purposes. Another fingerprinting technique for P. syringae strains is the PCR-based melting profile analysis (Kału˙zna et al. 2010). Besides, primers for specific detection of individual phylogroups of the P. syringae species complex were also published (Borschinger et al. 2016). So far, rep-PCRs have been successfully applied to distinguish Pss, Pmp1 and Pmp2 from wild cherry trees (Vicente and Roberts 2007), as well as on P. syringae strains isolated from different stone fruits including sweet and sour cherry (Kału˙zna et al. 2010). Furthermore, a rapid and highly specific PCR assay was developed for the identification, detection and discrimination of the cherry bacterial canker causal agents Pmp1 and Pmp2

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(Kału˙zna et al. 2016). Lately, a set of 12 strains that are responsible for cherry bacterial canker were selected for de novo whole-genome sequencing through PacBio next generation sequencing (NGS) technology (Ruinelli et al. 2015). Interestingly, the genomic analysis of several P. syringae populations demonstrates that this pathogen can utilize wild species as a reservoir of effector genes (Monteil et al. 2016). Recently, a genome-wide analysis assessed the evolution of the effector genes amongst diverse strains of P. syringae (Hulin et al. 2018). In the case of X. arboricolapv. pruni detection, several high-sensitivity molecular methods have been developed (Pulawska et al. 2017 and references therein). Additionally, approaches based on the loopmediated isothermal amplification (LAMP) technique enhance the on-site detection and prevent further pathogen spread. In the case of viruses that affect cherry crops, CLRV can be detected by biological assays, serological methods and molecular techniques (Buttner et al. 2011. Previously, a restriction fragment length polymorphism (RFLP) assay was developed to differentiate CLRV isolates (Buchhop et al. 2009). More recently, a real-time polymerase chain reaction (RT-PCR) based protocol for the multiplex detection of four viruses infecting sweet cherry has been described (Zong et al. 2014).

8.5 The Astonishing Role of Cherry Cultivars Towards the Efficient Control of Pathogens For the efficient control of the main cherry diseases, the use of cherry cultivars with durable resistance and adaptation to specific regional climatic conditions is the most holistic and environmentally friendly approach. Itpromotes the economic viability of agricultural systems and utilizes the encrypted genetic diversity present in cherry germplasms. Besides, phenotypic and genotypic characterization of sweet cherry genetic resources have been reported (Ganopoulos et al. 2011, 2016). This diversity can be exploited in breeding programs for disease resistance and is crucial for the incorporation of desirable pathogen resistance traits in cultivars. Particularly, wild cherry species can be an outstanding, useful and polymorphic source of resistance traits that could contribute to the effectiveness of breeding programs. Historically, wild species have been of considerable importance in plant breeding, but much less so in sweet and sour cherries (Iezzoni 2008). The pedigree information of these cultivars maybe unknown, while it seems that they may have evolved independently at different introgression events many decades ago during their evolutionary history (Potter 2011). Nowadays, the application of molecular and genomic techniques may accelerate the identification of genetic materials with increased resistance to the main cherry diseases. GAB approaches have also been applied to facilitate the selection process in terms of resistance to major fungal diseases. Moreover, the whole genome analysis of cherry cultivars will also advance the efficiency of the selection in breeding programs. Currently, the complete sequencing of cherry cultivars and the mapping of genetic loci related to disease resistanceare creating a significant level of

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knowledge and tools. The simultaneous application of MAS and GAB approaches, along with the phenotypic evaluation in field conditions will accelerate the breeding process for disease resistance in cherries.

8.6 Exploring Defense Mechanisms and Genes During Pathogens Interaction Upon challenge with pathogens, plants rely on a sophisticated repertoire of innate immune surveillance systems that are recruited for the recognition of pathogenassociated molecular patterns (PAMPs) or damage-associated molecular patterns (DAMPs) (Zambounis et al. 2020d). This initial level of defense reactionsis often mediated by a hitherto of rapid-evolving and cell-surface pattern-recognition receptors (PRRs) that usually contain ligand-binding domains, such as leucine-rich repeats (LRRs). This primary immune response is referred to as PAMP-triggered immunity (PTI) and is mainly effective against necrotrophic pathogens (Zambounis et al. 2020d). PTI involves the activation of disease resistance (R) genes that are mainly comprised of a domain of nucleotide-binding sites (NBS) and a C-terminal tandem array of LRRs (Couto and Zipfel 2016). Specifically, this superfamily of genes encodes for NOD-like receptors (NLR) which are the largest number of R genes in plants and confer resistance against a plethora of pathogens (Cesari et al. 2014). For example, the genome of Arabidopsis contains more than 150 NLR genes and the majority of these NBS-LRR genes occurin just 38 clusters (Guo et al. 2011). Effector-triggered immunity (ETI) is thesecond arm of immune response and often functions in the host cell cytoplasm. It is directly activated by detecting pathogen effectors or indirectly by regulating the plant proteins that have been altered by effectors. Furthermore, hormonal signaling through ethylene (ET), jasmonate (JA) and salicylic acid (SA)-mediated pathways are involved in the downstream regulation of ETI and PTI defense responses (Kong et al. 2015). One of the most abundant groups of R genes encode for the pathogenesis-related (PR) proteins which are involved in the downstream defense reactions, leading tothe establishment of systemic acquired resistance (SAR) and induced systemic resistance (ISR) (El-kereamy et al. 2011). The majority of PR genes in the sweet cherry genome belong to PR-1 and PR-4 families. PR-1 is SA-dependent, while the Non expressor of Pathogenesis-Related Genes 1 (NPR1) plays a significant role in response to pathogens (Durrant and Dong 2004). As plant defense mechanisms are under constant pressure to respond timely against rapidly evolving pathogens (Whitham et al. 2016; Zambounis et al. 2020a), climate change may dramatically affect the susceptibility of the cherry cultivars and new virulent pathogens races may overcome R and PR genes. So far, the effect of climate change on sweet cherry resistance against pathogens hasreceived little attention to date. The genes involved in defense reactions against pathogens are employed in numerous breeding programs for disease resistance through MAS approaches

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(Zambounis et al. 2020a). According to Shirasawa et al. (2017), defense-related genes (RPM1, RPP13, RGA2 homologues) were predicted and functionally annotated as disease resistance genes in the sweet cherry genome. These genes are usually clustered in close physical mapping and underlying quantitative trait loci (QTLs) were described as being involved in defense reactions against numerous plant pathogens (Larkan et al. 2016). RPM1 homologues belong to NBS-LRR class, along with other known R genes and recognize specifically the AvrRpm1 type III effector avirulence protein from P. syringae (Mackey et al. 2002). Besides, the NBSLRR disease resistance protein RPP13 contains an NB-ARC domain and confers resistance to the biotrophic oomycete Peronospora parasitica that causes downy mildew in Arabidopsis (Cheng et al. 2018).

8.7 Molecular Breeding Approaches for Disease Resistance in Cherry Classical breeding approachesfor cherry disease resistance are mainly limited by the long period that is necessary for seedling selection and cultivar generation (Rikkerink et al. 2007; Iwata et al. 2016; Zambounis et al. 2020a). Previous studies have assessed the resistance levels of sweet cherry cultivars against some economically important pathogens, including the causal agents of powdery mildew and bacterial canker (Mgbechi-Ezeri et al. 2017). In recent years, the exploitation of state-of-the-art technologies inmolecular genetics and genomics has substantially contributed to the availability of germplasm resources for key stone fruit species (Ru et al. 2015. In cherry, these resources will enable the identification of genetic loci that may be linked with disease resistance genes (Zambounis et al. 2016c, 2020a). Nowadays, molecular markers associated with resistance genes are valuable tools for the acceleration of the selection process of superior genotypes and are characterized byhigh reproducibility and accuracy (Parita et al. 2018). Thus, the application of MAS can been efficient and accurate tool for integrated disease management (Bowen et al. 2011). This approach can be exploited for germplasm characterization, introgression and pyramiding of several resistance genes (Kumar et al. 2014; Karapetsi et al. 2020).

8.8 QTL Mapping Effective defense response to important pathogens is controlled by a small number of major genes and large QTLs (Iwata et al. 2016). QTL association mapping and linkage genetic mapping or bulked segregant analysis are also important techniques to move forward with the application of MAS in cherry. Several sweet cherry genetic maps that are based on QTLs studies exist for different and essential agronomic traits (Clarke et al. 2009; Klagges et al. 2013; Quero-Garcia et al. 2014). Previously, genetic loci and

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QTLs associated with disease resistance have been reported in deciduous trees, such as those related to scab in apple (Bus et al. 2010), plum pox virus in apricot (Soriano et al. 2008), brown rot in peach (Pacheco et al. 2014), downy and powdery mildew in grapevine (Riaz et al. 2011; van Heerden et al. 2014). However, there is a limited amount of relevant insights for cherry diseases (Zambounis et al. 2020a), despite that linkage maps and QTL mappings hould be considered for disease resistance breeding (Miladinovi´c et al. 2015; Guajardo et al. 2015). Furthermore, the comprehensive investigation of the complex structure of the sweet cherry genome and defense genes is a pivotal task. The estimated sweet cherry genome size through NGS analysis has been recently published (Shirasawa et al. 2017), whereas the chloroplast and mitochondrial genome sequences have been also released (Chen et al. 2018; Yan et al. 2019).

8.9 Disease Resistance Genes and Genomics-Assisted Breeding in Cherry The integration of MAS with innovative genomics-assisted approaches and highthroughput sequencing platforms allows precise and high-density genotyping at the genomic level for disease resistance. Therefore, excess amounts of possible single nucleotide polymorphism (SNP) markers, either through SNP genotyping or by implementing GBS approaches (Sonah et al. 2013), may be generated in a costeffective manner (Davey et al. 2011), raising the possibilities and the efficiency of plant breeding programs (Varshney et al. 2014). In turn, genome-wide predictions and GS might increase the accuracy of genome-estimated breeding values (GEBVs) (Spindel and McCouch 2016), as well as the efficiency of targeted selection for genome-wide association studies (GWAS) (Heffner et al. 2010) for improved stress-tolerant varieties and the creation of superior pre-breeding material (Spindel and McCouch 2016). Resistance gene analogs (RGAs) are an extensive group of possible R genes that arecharacterized by highly conserved domains and structures. RGAs constitute pivotal candidates for enhanced disease resistance, while they are commonly employed as useful functional markers that are linked to R genes (Zambounis et al. 2020a). Recently, a considerable diversifying selection acting on 173 RGAs homologues of sweet and wild cherry was found, while robust evidence of positive selection acting in the clustered paralogous gene groups (PGGs) across their phylogenies was observed (Zambounis et al. 2016c) (Fig. 8.3). Furthermore, analyses revealed that the majority of positively selected residues sites are localized widely across the RGAs sequences. The clustered distribution of such genes might also be pronounced of high birth and death rates with diversifying episodes acting on their NB-ARC domains, putatively affecting the ligand-binding specificities (Zambounis et al. 2016c; Zambounis et al. 2017).

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Fig. 8.3 Nucleotide alignment of 173 RGAs sequences in cherry (Zambounis et al. 2016c)

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Particularly, sweet cherry breeding for powdery mildew resistance seems to be quite promising. A single major gene named PMR is responsible for the inheritance of the resistance, which is dominantly occurring among progenies from biparental crosses and their reciprocals of commercial segregation lines (Olmstead and Lang 2002). Thus, accurate molecular markers can identify co-segregation and flanking of PMR gene (Renick et al. 2008). Besides, as the management of bacterial canker caused by P. syringae is often challenging on cherry crops due to a lack of effective chemical control (Kennelly et al. 2007), the identification of particular allele genes that provide resistance is a major goal (Mgbechi-Ezeri et al. 2017). The expression analysis of genes also provides valuable insights about cherry resistance response (Alkio et al. 2014). Large-scale gene expression profiling through RNA sequencing would assist the elucidation of complex resistance mechanisms. Besides, analysis of the overall transcriptome upon infection with RNA sequencing (RNA-seq) technologies would allow the profiling of the induced transcriptional mechanisms (Zambounis et al. 2020d).

8.9.1 Re-sequencing of Cherry Cultivars for Disease Resistance Nowadays, cherry varieties with remarkable high adaptation to diseases may be candidates for targeted genome re-sequencing. This approach would offer significant resources for deciphering their encrypted disease resistance background, allowing the acceleration of breeding towards protection against pathogens (McClure et al. 2014). In annual crops, genomic resources and several SNPs associated with agronomic traits is well documented and allows the exploration of phenotypic diversity through the detection of numerous SNPs on the underlying loci (Xu et al. 2012). On the contrary, there are no available details to such extent for fruit trees (Xanthopoulou et al. 2020). As the sequencing costs of high-throughput sequencing technologies for genome-wide analysis have rapidly decreased, genomic approaches such as WGRS can offer crucial and cost-effective advantages towards the discovery of a wider range of allelic variants that control defense reactions against pathogens. WGRS approaches have been previously employed in fruit trees, such as citrus (Rawat et al. 2017), plum (Marti et al. 2018), peach (Cao et al. 2014), as well as in sweet cherry genotypes and cultivars (Shirasawa et al. 2017; Ono et al. 2018). The recent completion of one assembly (352.9 Mb) of the sweet cherry genome has enabled more novel discoveries (Shirasawa et al. 2017). The exploration of genomic variations, such as deletions, substitutions and duplications of defense genes could help explainthe divergence and evolution of these variations among the sweet cherry cultivars and facilitate the identification of functional variations that contribute to disease resistance. This approach is essential for the evaluation of natural resistance resources and it would also assist the incorporation of durable disease resistance in a crop that is consistently plagued by many phytopathogens. Nowadays, innovative

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and environmentally-friendly production systems withminimal use of chemical pesticides are strongly recommended for sustainable agriculture. Therefore, as climate change alters dramatically the susceptibility of sweet cherry cultivars to rapidly evolved andemergent pathogens with high adaptability, it is more than crucial to thoroughly investigate the repertoire of highly impact structural variations in genes involved in defense reactions among cherry cultivars, in order to facilitate the selection of superior cultivars. Furthermore, these genes during their evolutionary expansion depict usually new ligand-binding specificities commonly under diversifying selection through a number of different modes, ranging from SNPs mutations to tandem genes duplications.

8.9.2 Variation in Genes Involved in Defense Reactions and Evolutionary Concepts Towards Disease Resistance in Sweet Cherry As previously mentioned, it is highly important to decipher the structural genetic variations across the defense-relatedgenes in cherry cultivars. A recent study reported the allelic variants and the whole-genome variation between sweet cherry genotypes and cultivars fromthe Greek germplasm (Xanthopoulou et al. 2020). A high degree of potentially functional variations was observed, while several high-impact allelic variants that may be associated with disease resistance genes were discovered. Furthermore, a high number of heterozygous SNPs and missense variants along with insertion-deletion mutations (InDels) were mapped on 107 R genes across the sweet cherry genotypes. Among the sweet cherry genome accessions, particular cultivars were found to be the most affected in terms of both SNPs and InDels variations. All the highly impact mutations, both SNPs and InDels, were clustered according to their total numbers in the relevant mapped NLR genes (Xanthopoulou et al. 2020). Among the genes that mostly contributed to the variants with high impact, the first two genes contain NB-ARC domains, whereas the third one contains two copies of LRRs of type LRR-4 and were homologues of RPM, which is regarded as a quite dynamic and polymorphic locus in A. thaliana. The missense mutations in RPM1 locus were highly enriched in the NBS domain, suggesting that this region plays a key role in the early defense responses (Tornero et al. 2002). These findings allow further assigning of these NSB-LRR proteins as the foremost surveillance mechanism against rapidly evolving pathogens, while they also provide effective genomics tools to breeders for speeding up the development of sweet cherry cultivars with more durable resistance. In the same study, a few variations were also observed among the PR genes across the different sweet cherry accessions, while the majority of SNPs were intron variants and were mapped in two genes (Xanthopoulou et al. 2020). The finding of fewer variations across the PR genes was rather expected, as these genes comprise the basal defenseand are more conservative in their nucleotide structure and less abundant across plant genomes. Therefore, these results highlight that NLR genes

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are promising resources for breeding broad-spectrum resistance (Wang et al. 2016; Li et al. 2019; Xanthopoulou et al. 2020). The integration of genomics and genetics would assist the characterization of NLRomes in segregating populations and accelerate the cloning and mapping efforts of novel disease resistance loci (Piquerezt et al. 2014). Nowadays, genome-wide association and QTL mapping have become more available with the application of NGS sequencing approaches, whichcan speed up the identification of genes responsible for disease resistance. The above methods can facilitate the application of GAB approaches and the selection of resistant germplasms through MAS and QTL mapping by mainly targeting the highly expanded family of NBS/LRR genes (Dangl et al. 2013; Zambounis et al. 2020a). Furthermore, the RGAs can also be considered as valuable targets for the development of functional markers and have been widely utilized in disease resistance breeding programs (Perazzolli et al. 2014). As evolutionary events, such as repeats numbers variations, site mutations, duplications and tandem gene conversions affect the binding specificities of LRR domains of RGAs, (Sekhwal et al. 2015), it is vital to accurately identify the positive selective signs at the amino acid residues in the solvent-exposed regions of the LRR domains, which may lead to the acquisition of novel recognition patterns against pathogens (Zambounis et al. 2016c, d, e).

8.9.3 Future Prospects and Conclusions Genomics approaches are effective and highly promising to be adopted for crop protection against pathogens in cherry. Besides, the development and exploitation of resistant cultivars is the most sustainable and long-term solution against rapidly evolving pathogens, minimizing the need for extensive application of chemical fungicides. Particularly, MAS and GAB can be integrated into the evaluation and selection of superior cherries varieties with elevated disease resistance and adaptation to infections. The reducing cost of sequencing technologies further allowsvarious genomic analyses in sweet cherry. These include de-novo sequencing, GBS, and WGRS analyses which facilitate SNPs identification and various persistent mutations related to disease resistance across cherry populations. Additionally, RNA-seq technology can decipher the differential expression patterns and the transcriptional immune responses between resistant and sensitive genotypes and/or across different time points, following the inoculation with particular pathogens. Although a vast range of such valuable information can be generated from genomic approaches, commercial usage of these methods in cherry phytopathology is currently limited. In the future, the integration of different genomic data would undoubtedly enable a comprehensive approach for crop protection in the cherry crop.

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Chapter 9

Development of Biotic Stress Tolerant Berries Birut˙e Frercks, Dalia Gelvonauskien˙e, Ana D. Juškyt˙e, Sidona Sikorskait˙e-Gudžiunien˙ ¯ e, Ingrida Mažeikien˙e, Vidmantas Bendokas, and Julie Graham

9.1 The Benefits of Berry Genera: Fragaria, Rubus, Ribes, Vaccinium The main berries having the highest economic value in the world according to FAOSTAT data (2018) are strawberry (Fragaria × ananassa Duchesne), raspberry (Rubus idaeus L.), blackcurrant (Ribes nigrum L.) and blueberry (Vaccinium corymbosum L., V. angustifolium (Aiton) Rydb). Globally, the main producers are China for strawberry, the Russian federation for raspberry and currants, and the USA for blueberry. The main production areas of berries and currants in the European Union are Spain, Poland, and Germany (Table 9.1). B. Frercks (B) · D. Gelvonauskien˙e · A. D. Juškyt˙e · S. Sikorskait˙e-Gudži¯unien˙e · I. Mažeikien˙e · V. Bendokas Lithuanian Research Centre for Agriculture and Forestry, Institute of Horticulture, 58344 Akademija, LTKedainiai distr., Lithuania e-mail: [email protected] D. Gelvonauskien˙e e-mail: [email protected] A. D. Juškyt˙e e-mail: [email protected] S. Sikorskait˙e-Gudži¯unien˙e e-mail: [email protected] I. Mažeikien˙e e-mail: [email protected] V. Bendokas e-mail: [email protected] J. Graham James Hutton Institute, Errol Road, Dundee Scotland D2 5DA, UK e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 C. Kole (ed.), Genomic Designing for Biotic Stress Resistant Fruit Crops, https://doi.org/10.1007/978-3-030-91802-6_9

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Table 9.1 Growing area and production quantity of strawberries, raspberries, currants, and blueberries (according to data FAOSTAT 2018) Culture

Total in world

Total in Europe

Leading countries

Area harvested, ha

Production quantity, tones

Area harvested, ha

Production quantity, tones

Strawberry

372,361

8,337,099

163,543

1,680,164

China, USA, Mexico, Turkey, Spain

Raspberry

124,971

870,209

100,455

593,746

Russian Federation, Mexico, Serbia, Poland

Currant

122,273

662,586

120,306

648,114

Russian Federation, Poland, Germany

Blueberry

109,270

682,790

20,407

119,570

USA, Canada, Peru, Spain, Poland

Strawberry (Fragaria × ananassa), blueberry (Vaccinium corymbosum, V. angustifolium), raspberry (Rubus idaeus), blackberry (Rubus fruticosus), and blackcurrant (Ribes nigrum) are valuable sources of health-promoting bioactive compounds (Table 9.2). Berries are edible fresh, frozen, or processed into jams, juice, nectar, jellies, wines, ingredients in yogurt, candy, ice cream, liqueurs, cake toppings with some additional use in cosmetics (Nicoletti et al. 2015; Bender et al. 2017; Bermúdez-Oria et al. 2020), as food colorants, additives, and as pharmaceutical ingredients (Khoo et al. 2017; Ispiryan and Viškelis 2019). Berries are rich in bioactive pharmaceutical compounds—anthocyanins and polyphenols (Manganaris et al. 2013; Ferlemi and Lamari 2016; Forbes-Hernandez et al. 2016; Morta¸s and Sanlıer ¸ 2017; Kasim et al. 2017; Olas 2018; Ispiryan and Viškelis 2019; Stanys et al. 2019; Bendokas et al. 2020; Zorzi et al. 2020). These compounds may help to reduce the risk of various chronic disease conditions such as cancer, cardiovascular diseases, neurodegenerative diseases, arthritis, lung diseases, stroke, diabetes, and cataracts, as well as delay aging, antimicrobial effects (Morta¸s and Sanlıer ¸ 2017; Khoo et al. 2017; Bendokas et al. 2018; Diaconeasa et al. 2020; Kalt et al. 2020; Kranz et al. 2020). Particularly high concentrations of natural antioxidants in small berry fruits result in beneficial health effects. One of the main functions of antioxidants is to neutralize free radicals and thus protect from the oxidative damage of proteins, lipids, and nucleic acids. Berries are often referred to as natural functional products due to the high content and ample diversity of health-promoting substances (Kasim et al. 2017; Dhalaria et al. 2020; Zorzi et al. 2020) and epidemiological studies show a link between berry consumption and health. Foods supplemented with berry extracts are healthier and command a higher commercial value. The demand for berries and their products is the basis for developing and expanding industrial berry farming.

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Table 9.2 Bioactive pharmaceutical compounds in berries and their products and biological and pharmaceutical activities Strawberry (Fragaria × ananassa Duchesne.) Polyphenols/Anthocyanins

225 mg/100 g fruits/60–80 g per 100 g FW, Olas (2018)

Biological and pharmaceutical activities Antioxidant, anti-inflammatory, antihyperlipidemic, antihypertensive, antiproliferative, antimicrobial, anticarcinogenic Human disease prevention

Cancer, cardiovascular disease, diabetes, neurodegenerative diseases, obesity, vision diseases, digestive diseases

References Hannum (2004), Giampieri et al. (2012), Basu et al. (2014), Giampieri et al. (2015), Skrovankova et al. (2015), Forbes-Hernandez et al. (2016), Kasim et al. (2017), Muthukumaran et al. (2017), Kranz et al. (2020), Fierascu et al. (2020) Raspberry (Rubus idaeus L.) Polyphenols

126 mg/100 g fruits Olas (2018)

Biological and pharmaceutical activities Antibacterial activity, anti-inflammatory, antioxidant, anticarcinogenic, antitumoral, chemo preventive Human disease prevention

Aging and cognitive function, cancer, cardiovascular diseases, certain types of cancer, coronary heart disease, diabetes, inflammatory diseases, obesity, weight management

References Beekwilder et al. (2005), Szajdek and Borowska (2008), Skrovankova et al. (2015), Frum et al. (2017), Kasim et al. (2017), Morta¸s and Sanlıer ¸ (2017), Ispiryan and Viškelis (2019) Blackcurrant (Ribes nigrum L.) Polyphenols/Anthocyanins

560 mg/100 fruits/1741.6 mg/100 g DW, Olas (2018)

Biological and pharmaceutical activities Anticarcinogenic, anti-inflammatory, anti-obesity, antioxidant, antimicrobial, antitumoral, regulation of blood glucose, neuroprotection Human disease prevention

Asthma, brains diseases, cancer, cardiovascular diseases, degenerative disease, liver disease, neuroprotective effects, ophthalmological diseases, osteoporosis, pancreas, and kidney diseases

References Moyer et al. (2002), Szajdek and Borowska (2008), Lyall et al. (2009), Castro-Acosta et al. (2016), Ferlemi and Lamari (2016), Frum et al. (2017), Bender et al. (2017), Kasim et al. (2017), Bendokas et al. (2018), Cortez and de Mejia (2019), Stanys et al. (2019), Bendokas et al. (2020) Blueberry (Vaccinium corymbosum L., V. angustifolium (Aiton) Rydb) Polyphenols/Anthocyanins

525 mg/100 g fruits/1562.2 mg/100 g DW, Olas (2018) (continued)

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Table 9.2 (continued) Biological and pharmaceutical activities Antibacterial activity, anti-inflammatory, anti-mutagenic activity, anti-obesity, antioxidant, antitumoral, chemo-preventive, glucoregulatory function, neuroprotection, prebiotic activity Human disease prevention

Brains and cognition diseases, cardiovascular diseases, degenerative diseases, diabetes, neurodegeneration, obesity, reduction of oxidative stress, vision diseases

References Basu et al. (2010), Krikorian et al. (2010), Stevenson and Scalzo (2012), Skrovankova et al. (2015), Kasim et al. (2017), Kelly et al. (2018), Silva et al. (2018), Kalt et al. (2020), Stef˘anescu et al. (2020)

9.2 Impact of Biotic Stress on Cultivation and Qualities of Berries Global losses in agriculture have been estimated at around 35% of annual production due to abiotic and biotic factors. Depending on the location where pathogens parasitize the plants, they are divided into ecto- and endoparasites. Ectoparasites colonize outside of the plant (insects). Endoparasites are divided into two forms, intercellular and intracellular parasites. They include fungi, bacteria, viruses, viroid’s, nematodes, and parasitic plants (Sharma et al. 2020). The commercial value of berry plantations, plant health, longevity, yield, quality, and quantity are determined by climatic conditions, technology, quality of planting material, cultivar resistance to pests and diseases, pest and pathogen aggressiveness and ability to adapt to climatic conditions. Berry plants are affected by various pathogens, including fungi (including oomycetes), bacteria, several viruses, and pest problems, including aphids, mites, weevils and beetles and their larvae and nematodes. Among the biotic factors, the pathogenic fungi are major infectious agents, with more than 70% of serious economically damaging diseases of crops are caused by fungi (Larrañaga et al. 2012; Nadziakiewicz et al. 2018). These can affect all parts of the plant and cause damage or even death of plant. Fungal diseases such as Botrytis spp., Colletotrichum spp., Phytophthora spp., Verticillium spp. and the pests including Tetranychus urticae, Myzus spp. Xiphinemas spp., Pratylenchus spp., Longidorus spp., and nepoviruses are widespread and adapted to infect a broad range of plant species. Recently, pests and diseases have begun to spread to regions where they haven’t traditionally been found, possibly due to increased movement of planting material and climate change. Highbush blueberry is a prime example of this. Highbush blueberry (V. corymbosum), native to North America, was introduced into Europe around 1930 and production has increased dramatically (Martin et al. 2012). Subsequently, several of the associated diseases and pests have been introduced into Europe: Blueberry scorch virus, Peach mosaic rosette virus, Tobacco ringspot virus, Blueberry shoestring virus, Blueberry

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red ringspot virus, the aphid Ericaphis fimbriata, insect Dasineura oxycoccana, and fungi Monilinia vaccinii-corymbosi and Phomopsis vaccinii. Blueberry scorch virus (BlScV ) is common in Northern part of the USA and Canada, and in 2004 it was established in Italy and in the Netherlands and Poland in 2008. Changes in climate will likely result in altered ranges of many viruses’ biological vectors: aphids, thrips, whiteflies, mealybugs, mites etc. leading to changes in virus distribution (Martin et al. 2012). The occurrence of Monilinia vaccinii-corymbosi was reported for the first time in Austria (Gosch 2003) and Phomopsis vaccinii, reported for the first time in Lithuania (Gabler et al. 2004; Kaˇcergius and Jovaišien˙e 2010).

9.2.1 Problems Due to Weeds The negative influence of weeds on fruit crops is complex. Weed species composition and abundance depend on climate and soil properties, small fruit plants, cultivation techniques, and fertilization. Weeds are typical for exact geographical regions, however, some species such as Convolvulus arvensis L., Chenopodium album L. are cosmopolitan plants. Small fruit plants are very vulnerable to damage by weeds (Lisek 2014). Weeds such as black nightshade (Solanum nigrum) during mechanical harvesting of berries can present a contamination risk in blackcurrant plantations, as both berries look very similar. Bindweed (Convolvulus arvensis) can restrict plant growth and affect future yields (Cook et al. 2019). All agricultural weeds compete with crops for water, nutrients, and light. Parasitic weeds are particularly noxious since they also directly extract valuable water and a part or all nutrients from the host plants (Kebede and Ayana 2018; Fernández-Aparicio et al. 2020). Parasitic weeds have evolved a specialized feeding structure, the haustorium—a physiological bridge through which water and nutrients are transported from host to parasite (Runyon et al. 2010; Aly and Dubey 2014). Economically important parasitic weeds that have spread worldwide are Cuscuta spp., Striga spp. and Orobanche spp. and causing important losses in many crops (Rispail et al. 2007). Several species of Cuscuta are very host-specific, while others have a broad range of hosts. Economically important plants affected by Cuscuta spp. include Vaccinium ashei, Vaccinium macrocarpon, while Cuscuta europaea L. is parasitic for raspberries. The highest yield losses (80–100%) have been reported in cranberry fields in Massachusetts and Wisconsin due to Cuscuta spp. weeds. Crops with weeds are excellent for the distribution and spread of pests and diseases. Weeds can easily cause higher economic loss than diseases and insects in complex (Bushway et al. 2008). The longevity of the crop differs between crop type and cropping strategy and, therefore the impact weeds can have. High blueberry bushes are exploited for 15–50 years, raspberry, currant, and gooseberry for 8–15 years, and strawberry up to 4 years (Lisek 2014). Weeds in plantations influence the longevity of berry plants, yield quantity and quality. The main weeds in berry plantations include: Epilobium adenocaulon Hausskn., Artemisia vulgaris L., Capsella bursa-pastoris (L.) Medik., Cardamine hirsute L., Chamaenerion angustifolium (L.) Scop., Cirsium arvense

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(L.) Scop., Cirsium vulgare (Savi) Ten., Convolvulus arvensis L., Echinochloa crusgalli (L.) P. Beauv., Elymus repens (L.) Gould., Epilobium ciliatum Raf., Equisetum arvense L., Galium aparine L., Galinsoga parviflora Cav., Geranium pusillum L., Poa annua L., Rorippa sylvestris (L) Besser, Rumex obtusifolius L., Senecio vulgaris L., Solanum nigrum L., Sonchus oleraceus L., Stellaria media (L.) Vill., Taraxacum officinale F. H. Wigg., Viola arvensis Murray (Lisek 2012; Lisek 2014; Kahu 2003; Kopytowski and Banaszkiewicz 2008; Cook et al. 2019).

9.2.2 Pathogens, Viruses and Pests Decreasing Yield and Causing Plant Death 9.2.2.1

Fungal Diseases

Fragaria, Vaccinium, Rubus and Ribes plants are damaged by a multitude of diseases and pests. Strawberry (F. ananassa) is one of the most commercially important fruit crops worldwide and is grown in many countries. Strawberry plantations in many regions are constrained by economically damaging diseases that affect the basal part of the petioles, crown, fruits and root system. Due to the disease damage cause considerable decrease of yield (Table 9.3). The berries could be affected by more than 50 different genera of fungi (Garrido et al. 2011). The genera Botrytis, Colletotrichum, Verticillium, Phytophthora, Podosphaera, Rhizoctonia are included among the most significant (Garrido et al. 2011; Petrasch et al. 2019; Samtani et al. 2019; Jiménez 2020; Leroch et al. 2013). Gray mold (Botrytis cinarea) is one of the most common and serious diseases wherever strawberries are grown. It may destroy up to 80–90% of flowers and fruit during humid seasons on unsprayed plants (Xu et al. 2012) similarly for Colletotrichum Anthracnose fruit rot. Root rots caused by Pythium, Rhizoctonia, and Cylindrocarpon spp. reduces strawberry yield by 25– 85% (Martin and Bull 2002). Fusarium wilt (Fusarium oxysporum) and rhizoctonia (Rhizoctonia solani and R. fragariae) root rot are two crown and root diseases that favour high temperatures; when they appear, severe damage with losses as high as 50% can result (Garrido et al. 2011). The strawberry root rot complex or black root rot are frequently detected and an increasing problem in perennial strawberry plantings worldwide (Moroˇcko 2006). The most common root pathogens are Fusarium spp., Cylindrocarpon spp., Rhizoctonia spp., Phoma spp. (Parikka and Kukkonen 2002; Paynter et al. 2014) and Pythium spp., Gnomonia fragariae (Moroˇcko 2006) species. Raspberry diseases are shown in Table 9.4. In raspberry, root rot, cane diseases are the main problems worldwide. One of the biggest problems in North America are root rot diseases. Phytophthora root emerged as a major threat in raspberry production in Europe around the 1980s. Australia had unusually humid conditions in 1994– 1996 and here Phytophthora fragariae var. rubi was known as a major disease in raspberries worldwide. Verticillium wilt (Verticillium albo-atrum Reinke & Berthier) and Phytophthora root rot (Phytophthora spp., P. fragariae var. rubi, P. megasperma,

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Table 9.3 Strawberry diseases Pathogen

Disease

References

Fungal Alternaria alternata (Fr.) Keissl

Black leaf spot

Anwar et al. (2018)

Botrytis cinerea Pers. ex Fr

Botrytis fruit rot, graymold

Leroch et al. (2013)

Colletotrichum acutatum J.H. Simmonds; C. gloeosporioides (Penz.) Penz. &Sacc; C. fragariae A.N. Brooks

Anthracnose leaf spot, anthracnose fruit rot, crown rot and black spot

Garrido et al. (2011), Lewers et al. (2007)

Diplocarpon earliana (Ell. &Ev.) Wolf

Leaf scorch

Miliˇcevi´c et al. (2002)

Fusarium oxysporum f. sp. fragariae

Root and crown disorders

Phillips and Golzar (2008), Fang et al. (2012)

Macrophomina phaseolina (Tassi) Goid.; Phomaexigua Sacc

Root and crown disorders

Phillips and Golzar (2008), Fang et al. (2012)

Mycosphaerella fragariae Tull. Lindau

Purple leaf spot, black seed disease

Carisse and McNealis (2019)

Gnomonia fragariae Kleb

Root rot and petiole blight

Moroˇcko (2006), Fang et al. (2012)

Phomopsis obscurans (Ell. &Ev.) Sutton

Leaf blight

Abd-El-Kareem et al. (2019, 2020)

Phytophthora cactorum (Lebert & Cohn); Phytophthora fragariae Hickman

Phytophthora crown and root Pérez-Jiménez et al. (2012), rot Fang et al. (2012), Anandhakumar and Zeller (2008), Meszka and Michalecka (2016)

Rhizoctonia fragariae S.S. Husain & W.E. McKeen

Black root rot

Phillips and Golzar (2008); Fang et al. (2012)

Sphaerotheca macularis (Wall.) Lind

Powdery mildew

Karajeh et al. (2012)

Verticilliumalbo-atrum Reinke et Berth; V. dahlia Kleb

Verticillium wilt

Pérez-Jiménez et al. (2012)

Angular leaf spot

Pérez-Jiménez et al. (2012), Gétaz et al. (2020a)

Bacteria Xanthomonas fragariae Kennedy and King

P. cactorum) infected fruiting raspberry canes wilt and die before harvest. New canes may become infected, wilt and finally die during their first year of growth. Cane blight (Diapleella coniothyrium (Fuckel) Barr) is another destructive disease in all cultivated raspberries, it causes yield loss up to 30% (Bushway et al. 2008). The occurrence of Spur blight (Didymella applanata (Niessl) Sacc) leads to economically notable losses that can reach till 60% in humid years. The pathogen reduces yields by blighting the fruit-bearing spurs, inducing early leaf drop and destroying buds on canes that later develop into fruit-bearing side branches (Stevi´c et al. 2017).

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Table 9.4 Raspberry diseases Pathogen

Disease

References

Arthuriomyces peckianus (E. Howe) Cummins and Y. Hiratsuka; Gymnoconia nitens (Schwein.) F. Kern & H.W. Thurston

Orange rust

Martin et al. (2017)

Pucciniastrum americanum (Farl.) Arth.; P. arcticum Transzschel

Late leaf rust

Martin et al. (2017)

Sphaerulina rubi Demaree & M.S. Wilcox

Leaf spot

Martin et al. (2017)

Podosphaera macularis (Wallr.) U. Braun & S. Takam (formerly Lind); P. aphanis (Wallroth) Braun & Takamatsu

Powdery mildew

Harvey and Xu (2010)

Phragmidium rubi-idaei (DC.) P. Karst

Yellow rust

Anthony et al. (1985)

Seimatosporium lichenicola (formerly Sporocadus lichenicola)

Ascospora dieback

Martin et al. (2017), Dolan et al. (2018)

Elsino eveneta (Burkholder) Jenkins

Anthracnose

Martin et al. (2017)

Diapleella coniothyrium (Fuckel) Barr; Didymella applanata (Niessl) Sacc

Cane and spur blight

Martin et al. (2017), Dolan et al. (2018)

Leptosphaeria coniothyriumSacc

Cane blight

Martin et al. (2017), Dolan et al. (2018)

Botrytis cinerea Pers. F

Botrytis fruit rot and blossom blight

Kozhar and Peever (2018), Carisse et al. (2018)

Alternaria alternata Keissi; Cladosporium cladosporiodes Bensch

Fruit rot disease

Kozhar and Peever (2018), Carisse et al. (2018)

Phytophthora fragariae var. rubi, P. megasperma; P. cactorum; Fusarium spp.; Pythium spp.; Rhizoctoniaspp.

Root rot

Gigot et al. (2013), Stewart et al. (2014)

Verticillium albo-atrum Reinke & Berthier; Verticillium dahlia Kleb

Verticillium wilt

Martin et al. (2017)

Armillaria mellea (Vahl: Fr.) P. Kumm

Armillaria root rot

Baumgartner and Rizzo (2001), Dolan et al. 2018

Crown gall and cane gall

Martin et al. (2017)

Fungal

Bacteria Agrobacterium tumefaciens Smith & Townsend; A. rubi Hildebrand

(continued)

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Table 9.4 (continued) Pathogen

Disease

References

Pseudomonas syringae Van Hal

Bacterial blight

Obradovi´c et al. (2008)

Raspberries are highly susceptible to Botrytis cinerea Pers. F., which causes wilt and grey mould fruit rot—the most common and severe diseases of the fruit of the Rubus species in the world (Oduse and Cullen 2012). Most commercial black currant production is in Central, Eastern and Northern Europe (Woznicki 2016). Important foliar diseases in R. nigrum plantations include mildew (Sphaerotheca mors-uvae), leafspot (Drepanopeziza ribis), gray mold (Botrytis cinerea), white pine blister rust (Cronartium ribicola) and septoria leafspot (Septoria ribis) (Table 9.5). Leaf spot occurs wherever blackcurrants are grown in North America, Central America, New Zealand, Europe, Japan, and Australia. There are up to 50% of yield losses in blackcurrant crops in the United Kingdom because of B. cinerea-induced flower abscission (Boyd-Wilson et al. 2013). Infection with blackcurrant leaf spot may result in yield losses up to 75% or more, because of pre harvest defoliation and fruit infection (Vagiri et al. 2017; Masny et al. 2018). The highbush blueberry (Vaccinium corymbosum L.) is considered one of the most commercially important berry crops. Fungal pathogens cause important blueberry diseases: mummy berry (causative agent Monilinia vaccinii-corymbosi), Phomopsis twig blight and canker (causative agent Phomopsis vaccinii), Fusicoccum canker Table 9.5 Black currant diseases Pathogen

Disease

References

Botrytis cinerea Pers

Botrytis dieback and flower blight

Walter et al. (2007)

Botryosphaeria ribis Grossenb. & Duggar

Botryosphaeria dieback

Singer and Cox (2010)

Drepanopeziza ribis (Kleb.) Höhn

Black currant leaf spot (anthracnose)

Vagiri et al. (2017), Masny et al. (2018)

Cronartium ribicola Fisch White pine blister rust

Vagiri et al. (2017), Masny et al. (2018)

Mycospheaerella ribis (Fuckel) Kleb.); M. grossulariae Wallr

Septoria leafspot

Šikšnianas et al. (2008), Vagiri (2012), Masny et al. (2018)

Sphaerotheca mors-uvae (Schw.) Berk.; S. macularisWallr.)

European powdery mildew, North American powdery mildew

Šikšnianas et al. (2005), Šikšnianas et al. (2008), Vagiri et al. (2017), Masny et al. (2018), Kikas et al. (2021)

Nectria cinnabarina (Tode) Fr

Coral spot

Hummer and Dale (2010)

Puccinia caricina DC

Puccinia rust

Hummer and Dale (2010)

Fungal

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(causative agent Fusicoccum putrefaciens), anthracnose fruit rot (causative agent Colletotrichum acutatum), and Alternaria fruit rot (causative agent Alternaria spp.) (Table 9.6). Mummy berry is a threat in wet sites. Due to mummy berry disease, growers loose over 36% of yield (Florence and Pscheidt 2017), while without chemical control, losses due to this disease are estimated in the range of 10–50% (Jenkins et al. 2008). Phomopsis twig blight and canker are present to fluctuating extent in most blueberry plantations in Michigan. Phomopsis vaccinii colonize young fruiting twigs and can lead to fruit losses of two or three pints per bush on susceptible blueberry cultivars. Yield loss due to anthracnose ranges from 10 to 20%, but during storage, losses may reach 100% (Jenkins et al. 2008).

9.2.2.2

Viruses

Viruses from more than sixteen families (Table 9.7) parasitize cells and cause a multitude of diseases in Fragaria, Vaccinium, Rubus and Ribes plants. There are usually Secoviridae, Closteroviridae and Bromoviridae positive-strand RNA viruses, which cause diseases with various symptoms. The wide range of symptoms (yellowing, spotting, various distortions on different organs) can be induced by viruses and lead to reduced plants or fruits quality and yield. The extent of these losses has been shown. Strawberry crinkle virus (SCV), Strawberry pseudo mild yellow edge (SMYEV), Strawberry mottle virus (SMoV) and Strawberry vein banding virus (SVBV) are considered the four most economically important viruses of strawberry in most production areas (Martin and Tzanetakis 2006; Sharma et al. 2018). Economic losses also occur when the virus infection is symptomless. For an example, asymptotic infection by SMYEV can reduce the total strawberry fruit weight by 63% compared with healthy plants (Torrico et al. 2017). Conflicting reports on the economic impact of SMYEV probably result from variations in virus strains, evaluated cultivars and the likelihood that mixed infections occur in the field resulting in synergy with SMYEV and environmental conditions in the numerous studies. It was reported that SMYEV may reduce plant vigor and yield up to 30%. Strawberry necrotic shock virus (SNSV) can significantly impact strawberry production, reducing yield loss up to 15% and runner production up to 75%. Incidences of plant infections with Strawberry pallidosis associated virus (SPaV) and Beet pseudoyellows virus (BPYV) infection reached as high as 90% in southern California strawberry plantations and over 70% in the Watsonville area, this coinfections with several viruses caused a serious decline (Martin and Tzanetakis 2006). Raspberry bushy dwarf virus (RBDV) is a pollen-borne virus and causes infection on red raspberry, black raspberries, and blackberries plants worldwide, and this infection can reduce the raspberry yield up to 40% (Martin 2002). In North America RBDV has reached epidemic proportions. Study results revealed that this virus has spread in 70% of surveyed raspberry fields. The incidence of RBDV in tested plants was 35% and contrast greatly among the cultivars in Latvia (P¯upola et al. 2009). Blackcurrant reversion virus (BRV) is one of the most damaging and economically important viruses of R. nigrum plants worldwide.

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Table 9.6 Blueberries diseases Pathogen

Disease

References

Botrytis cinerea Pers. ex Fr.

Blossom blight, fruit rot

Rivera et al. (2013)

Alternaria tenuissima Kunze: Fr.

Alternaria fruit rot

Mehra et al. (2013), Miles et al. (2013)

Alternaria alternata (Fr.) Keissl

Alternaria leaf spot, fruit rot

Zhu and Xiao (2015), Nadziakiewicz et al. (2018), Wang et al. (2020)

Fungal

Colletotrichum Anthracnose fruit rot on gloeosporoides Penz & Sacc., leaves, fruits, and stems C. acutatum Simmonds, C. fioriniae

Cannon et al. (2012), Kim et al. (2009)

Phomopsis spp., P. vaccinii (Shear)

Phomopsis twig blight, red wart

Dil et al. (2013), Prodorutti et al. (2007), Jeger et al. (2017)

Phytophthora cinnamomic Rands

Phytophthora root rot

Bryla and Linderman (2007), Prodorutti et al. (2007)

Monilinia Vaccinii-Corymbosi Monilinia blight (mummy Reade berries)

Florence and Pscheidt (2017)

Thekopsora minima (Arthur) Sydow & P. Sydow

Leaf rust

Babiker et al. (2018)

Chondrostereum purpureum (Pers.) Pouzar

Silver leaf

Rojo et al. (2017)

Sporocadus lichenicola Corda Twig canker

Serdani et al. (2010)

Verticillium dahliae Kleb

Verticillium wilt

Serdani et al. (2018)

Botryosphaeria corticis Demaree & Wilcox, Godroniacassandrae Peck f . sp. vaccinii

Stem canker

Polashock and Kramer (2006), Prodorutti et al. (2007), Fulcher et al. (2015)

Neofusicoccum parvum Pennycook & Samuels, N. australe Slippers, Crous & M.J. Wingf., N. macroclavatum Burgess, Barber & Hardy

Stem blight

Fulcher et al. (2015)

Septoria spp.

Septoria leaf spot and stem canker

Prodorutti et al. (2007)

Microsphaera vaccinii Cooke & Peck

Powdery mildew

Prodorutti et al. (2007)

Valdensinia heterodoxa Peyr

Valdensinia leaf blight

Kukuła et al. (2017)

Exobasidium spp.

Exobasidium leaf and fruit spot

Ingram et al. (2019) (continued)

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Table 9.6 (continued) Pathogen

Disease

References

Pseudomonas syringae Van Hall

Bacterial canker

Prodorutti et al. (2007)

Agrobacterium tumefaciens Conn

Crown gall

Prodorutti et al. (2007)

Xylella fastidiosa Wells et al.

Bacterial leaf scorch

Ferguson et al. (2017)

Bacteria

BRV has been reported in 17 countries, mainly in Northern and Central Europe, Russia, and New Zealand. BRV is transmitted by the gall mite Cecidophyopsis ribis, which acts as a natural vector significantly contributing to the spread of the virus in orchards. Individual forms of some virus can cause different lesions. Symptoms caused by the European form of BRV in infected black currant are less harmful to plants than symptoms caused by the Russian form of BRV. Malformation of the flowers and proliferation of the sepals finally causes sterility of blackcurrants with a consequent complete loss of the crop (Dolan et al. 2011). The general occurrence of BRV was 27%, although it varied significantly among the analyzed Ribes habitats, exceeding 40% in home gardens and germplasm collections (Zulg‘ e et al. 2018). Scorch disease caused by Blueberry scorch virus (BlSV) reduced yield in cultivar ‘Pemberton’ of blueberries, with the loss related to the number of years bushes showed typical symptoms. The yield was reduced by more than 85% in the third year of symptom expression (Bristow et al. 2000). Plant host ranges of individual viruses differ from narrow to very broad. Some viruses exhibit low specificity for their hosts and can attack a range of plant genus’s. Some members of the genus Nepovirus can infect most herbaceous and woody plant species. Plants of Rubus, Ribes and Fragaria genus are important hosts of Tobacco ringspot virus (TRSV), Tomato ringspot virus (ToRSV), Arabis mosaic virus (ArMV), Raspberry ringspot virus (RpRSV), Tomato black ring virus (TBRV) (Murant and Lister 1987). There are viruses highly host specific in berry plants also (Table 9.7). All of them are major or minor significant for plants development and growth. Highly widespread viruses such as Blueberry necrotic ring blotch virus (BNRBV), Strawberry latent ringspot virus (SLRSV), SMYEV or BRV are major and can infect the whole plant and cause a systemic infection—diseases (Susi 2004; Conci et al. 2009; Mazyadr et al. 2014; Robinson et al. 2016). Several virus complexes at the same time may occur in plant and their damaging effect and economical losses are often enhanced (Pˇribylová et al. 2002; Martin et al. 2013). New technologies, including large scale sequencing combined with bioinformatics, helps in identifying new viruses in berry plants—Raspberry latent virus (Quito-Avila et al. 2011), Ampelovirus are associated with blackberry yellow vein disease complex (Thekke-Veetil et al. 2012), BNRBV (Quito-Avila et al. 2013) or Strawberry polerovirus-1 (SPV-1) (Xiang et al. 2015). Biological vectors (pollen or pest) for the physical transmission of the virus from one host to another are required to spread infection in berry plantations. The transmission of viruses by pests is a particular process. Each plant virus can be transmitted by only

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Table 9.7 Specific virus for berries plants (according to data Converse (1987), Martin and Tzanetakis (2006), Sharma et al. (2018)) Virus name

Genus

Family

Fragaria chiloensis cryptic virus (FClCV)

Alphacryptovirus

Partitiviridae

Fragaria chiloensis latent virus (FClLV)

Ilarvirus

Bromoviridae

Strawberry chlorotic fleck-associated virus (SCFaV)

Closterovirus

Closteroviridae

Strawberry crinivirus 3 (?)

Crinivirus

Closteroviridae

Strawberry crinkle virus (SCV)

Cytorhabdovirus

Rhabdoviridae

Fragaria spp.

Strawberry latent C virus (STLCV)

Rhabdovirus

Rhabdoviridae

Strawberry latent ringspot virus (SLRSV)

Nepovirus

Secoviridae

Strawberry mild yellow edge virus (SMYEV)

Potexvirus

Alphaflexiviridae

Strawberry mottle virus (SMoV)

Stramovirus

Secoviridae

Strawberry necrotic shock virus (SNSV)

Ilarvirus

Bromoviridae

Strawberry pallidosis-associated virus (SPaV)

Crinivirus

Closteroviridae

Strawberry vein banding virus (SVBV)

Caulimovirus

Closteroviridae

Strawberry polerovirus-1 (SPV-1)

Polerovirus

Luteoviridae

Black raspberry cryptic virus BRCV)

Alphacryptovirus

Partitiviridae

Black raspberry necrosis virus (BRNV)

Sadwavirus

Secoviridae

Raspberry bushy dwarf virus (RBDV)

Idaeovirus

Unassigned

Rubus spp.

Raspberry latent virus (RpLV)

Reovirus

Reoviridae

Raspberry leaf blotch virus (RLBV)

Emaravirus

Fimoviridae

Raspberry leaf mottle virus (RLMoV)

Closterovirus

Closteroviridae

Raspberry ringspot virus (RpRSV)

Nepovirus

Secoviridae

Raspberry vein chlorosis virus (RVCV)

Unassigned

Rhabdoviridae

Rubus canadensis virus 1 (RuCV-1)

Foveavirus

Betaflexiviridae

Rubus yellow net virus (RYNV)

Badnavirus

Caulimoviridae

Blackberry chlorotic ringspot virus (BCRV)

Ilarvirus

Bromoviridae

Blackberry virus E (BVE)

Allexivirus

Alphaflexiviridae

Blackberry virus S (BVS)

Marafivirus

Tymoviridae

Blackberry virus X (BVX)

Unassigned

Alphaflexiviridae

Blackberry virus Y (BVY)

Brambyvirus

Potyviridae

Blackberry virus Z (BVZ)

Unassigned

Dicistroviridae

Blackberry yellow vein-associated virus (BYVaV)

Crinivirus

Closteroviridae

Ribes spp. Blackcurrant reversion virus (BRV)

Nepovirus

Secoviridae

Gooseberry vein banding associated virus (GVBAV)

Badnavirus

Caulimoviridae (continued)

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Table 9.7 (continued) Virus name

Genus

Family

Blueberry latent spherical virus (BLSV)

Nepovirus

Secoviridae

Blueberry latent virus (BBLV)

Unassigned

Partitiviridae

Blueberry leaf mottle virus (BLMoV)

Nepovirus

Secoviridae

Blueberry necrotic ring blotch virus (BNRBV)

Blunervirus

Kitaviridae

Blueberry red ringspot virus (BRRV)

Soymovirus

Caulimoviridae

Blueberry scorch virus (BlScV)

Carlavirus

Betaflexiviridae

Blueberry shock virus (BlShV)

Ilarvirus

Bromoviridae

Blueberry virus A (?)

Unassigned

Closteroviridae

Blueberry red ringspot virus (BRRSV)

Soymovirus

Caulimoviridae

Vaccinium spp.

one biological vector type. Chemical control agents against virus vectors are useful in this case. However, there are no effective chemical protective measures against viral diseases and virus-free planting material is the main option of healthy in berry plantation (Brennan 1990; Martin et al. 2012; Martin et al. 2013; Tzanetakis and Martin 2017).

9.2.2.3

Bacterial Diseases

Xanthomonas fragariae was long time considered the only bacterial pathogen on strawberry. A newly detected disease called ‘bacterial leaf blight’ was observed on strawberry plants in northern Italy in 1993, caused by a new pathogen Xanthomonas arboricola pv. Fragariae (Xaf) (Scortichini 1996). The pathogen causes dry, brown necrotic leaf spots and large brown V-shaped lesions along the leaf margin, midvein and major veins. The pathovar status of X. arboricola from strawberry was recently discussed, based upon infection symptoms, biochemical tests, polymorphism analysis and comparative genomics (Gétaz et al. 2020b). Severe crop losses on strawberries because of Xanthomonas arboricola pv. fragariae infections have never been reported. Another bacterial disease of strawberry is caused by Ralstonia solanacearum (formerly, Pseudomonas solanacearum) (bacterial wilt), generally occurs in nursery seedlings but rarely in strawberry plants grown in the fields. No data of association with strawberry fruit have been found. Fire blight, caused by the bacteria Erwinia amylovora, is the most devastating disease of economically important rosaceous crops. Strains of E. amylovora are separated into 2 groups based on host range: Spiraeoideae and Rubus strains. Spiraeoideae strains infect wide host ranges in many rosaceous genera, mainly Malus, Pyrus, Prunus, Fragaria, and Crataegus (Asselin et al. 2011). Erwinia pyrifoliae is a causative agent of Asian pear blight and is related to Erwinia amylovora. In 2013, Erwinia pyrifoliae was found on strawberry plants

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(cv. Elsanta) under greenhouse cultivation conditions in the Netherlands. Symptoms included an intense blackening of the immature fruits, fruit calyx, the attached stems, malformed fruits, and bacterium slime on the young fruits’ surface (Wenneker and Bergsma-Vlami 2015). For many years blueberry (Vaccinium corymbosum) plants have been considered resistant or tolerant to diseases. However, diseases and pests are becoming a growing concern of the cultivation of this plant species. Blueberry is rarely infected by bacterial pathogens, which could seriously affect the yield. Agrobacterium spp., R. rhizogenes, and A. rubi causing crown or cane gall is not considered a common disease of blueberry, but when an outbreak occurs, the results are devastating. A. tumefaciens enters plants through wounds on the stems during pruning of the fields, by frost, insect injury, machine harvesting. Infected plants generally produce smaller and fewer berries while plants with severe galling do not produce any berries (Kuzmanovi´c et al. 2019). Bacterial blight caused by Pseudomonas syringae can be a veer blueberry disease during rainy springs, especially in frost-damaged tissues (Stockwell et al. 2015). It multiplies in buds and on expanding aerial plant tissues through natural openings or wounds. Only previous season-produced canes are affected. Tissue changes color from reddish-brown to black when infected. Buds in the infected place fail to open and die along with stem necrosis. In Poland, the only bacterial pathogen described was a tumorigenic Agrobacterium spp. However, in 2013 Kału˙zna et al. reported a new leaf spot disease belonging to Pseudomonas LOPAT group Ia—P. syringae and Ib—P. syringae subsp. savastanoi and P. delphini. Pseudomonas syringae pathovar ribicola is known to cause severe defoliation of Ribes aureum (Charnock 1998), while pathovar syringae is associated with shoot wilt and fire blight in raspberry plants in the Pacific Northwest region of the United States, coastal California, the British Columbia region of Canada and Serbia (Koike et al. 2014; Ivanovi´c et al. 2012). The bacterial leaf scorch caused by Xylella fastidiosa is native to US and has spread to such countries: Italy, France, the Netherlands. It is also present in Taiwan, Iran, Caribbean, Turkey, Lebanon, Kosovo, Georgia, and India. First symptoms appear on the edges of leaves and progress to a burnt appearance along the leaf margin (Holland et al. 2014). Infected leaves drop from the bush and the plant eventually die. Xylella fastidiosa bacteria resides in the xylem of host plants and can be spread by insect vectors or grafting and pruning.

9.2.2.4

Pest

Aphids, mites, spotted wing Drosophila, whitewings, and nematodes cause serious plants’ problems and are also virus vectors. Aphids are the most important pests in Temperate climate zone agriculture. They directly influence the health of plants and carry the numerous viruses destructive for plants (Andrianova et al. 2018). The most damaging species of aphids are Aphis schneideri, Cryptomyzus galeopsidis, Cryptomyzus ribis and Hyperomyzus lactucae (Woznicki 2016). Other major pests of Ribes

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are leaf-curling midge (Dasineura tetensii Rübs.), sawfly (Nematus ribesii) and, especially in New Zealand currant clearwing (Synanthedon tipuliformis) (Woznicki 2016). White Peach Scale Pseudaulacaspis pentagona TargioniTozzetti (Homoptera: Diaspididae), is a cosmopolitan pest that originated in Eastern Asia, and it has become one of the main threats to blackcurrant cultivation in France (Kuzmin et al. 2020). Aphids also transmit virus diseases with a range of species significant in raspberry worldwide transmitting viral plant pathogens that cause huge yield losses (Jones 1976; Dossett and Kempler 2012; Gordon et al. 1997). Highbush blueberry pests (the brown marmorated stink bug Halyomorpha halys and the spotted-wing drosophila Drosophila suzukii) originated in Asia and spread into both North America and Europe. Drosophila suzukii has a tremendous economic impact on blueberry growers. Yield losses have been reported from North America— up to 40% and Japan—up to 77%. (Pest Risk Analysis Blueberry scorch virus—EPPO PRA). The three primary insect pests of blueberries in the North Central Region are blueberry maggot, Japanese beetle, and cranberry fruit worm. Each of them can be transferred with fruits during mechanical harvest and there is a zero tolerance for all these insects in fruit (Jenkins et al. 2008). Plant-parasitic nematodes play a significant role in decreasing crop yield (Gigot et al. 2013). Several parasitic nematodes were related to red raspberry disease worldwide (Poiras et al. 2014; Mohamedova and Samaliev 2018; Mokrini et al. 2019). Dagger nematodes (Xiphinema Americanum, X. bakeri and X. diversicaudatum) and needle nematodes (Longidorus attenuates, L. elegantus and L. macrosoma) belongs to ectoparasitic nematodes that are associated with this crop since they transmit some devastating viruses (Mokrini et al. 2019).

9.3 The Genetic Response of Berry Plants to Biotic Stresses The genetic diversity of plants in resistance and susceptibility to pests and diseases is the basis for crop breeding. One of the main aims of breeding is to find resistance or tolerance traits to prevent pest infestation or disease infection or at least to limit the damage (Mitchell et al. 2016). An integrated pest management (IPM) approach using resistant or tolerant cultivars can be successful just if the traits and genetic mechanisms underlying resistance are known (Mitchell et al. 2016). The infection process of plants depends on three factors: the pathogen’s properties, the host, and the environment. A renowned disease triangle is the interaction between a susceptible host, a virulent pathogen, and an environment favorable for disease development. (Agrios 2008). The infection can disrupt photosynthesis, respiration, and transpiration, be influential on plant growth and development or lead to plant death. The first level of protection in plants is the cuticula and cell wall, which make an impenetrable barrier against pathogens entering the plant (Micali et al. 2011). If this barrier is damaged plants have developed defense mechanisms to fend off pathogen attacks. Other structural features such as cane and leaf hairs, root vigor and bush density can impact pathogen ability to infectious can developmental timings

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(Mitchell et al. 2018). Other plants protection mechanisms are defense through intricate hormonal regulation and on the molecular level: pathogen-associated molecular patterns (PAMP) pathogen-triggered immunity (PTI), effector-triggered immunity (ETI), and RNA interference (RNAi) (Velásquez et al. 2018).

9.3.1 The Genetic Response to Parasitic Weeds Economically important parasitic weeds spread worldwide are obligate root hemiparasites Striga and Orobanche and obligate stem holoparasite Cuscuta spp. causing important losses in many crops (Rispail et al. 2007). The Cuscuta species cause serious problems for berries. Cranberry, blueberry, and raspberry are a potential host for Cuscuta spp. (Albert et al. 2008; Mishra 2009) and moreover it was established that Cuscuta can transmit viral diseases in different currant species (Špak et al. 2009). Therefore, here the genetic response from host plants to Cuscuta spp. will be described. Several reviews are recommended for further reading on Striga and Orobanche (Rispail et al. 2007; Clarke et al. 2019; Fernández-Aparicio et al. 2020). Cuscuta species C. pentagona and C. campestris are most important parasitic weeds in agriculture. They are distributed worldwide and have a wide host spectrum (Kebede and Ayana 2018). The genomes of Cuscuta spp. are already sequenced (Kim et al. 2014; Yang et al. 2016; Vogel et al. 2018). The genes needed for photosynthetic activity are lost in Cuscuta spp. therefore that parasites have low rates of photosynthesis. Moreover, several dozen high confidences horizontally transferred genes from the parasite’s hosts were identified (Vogel et al. 2018). In autotrophic plants horizontal gene transfer is a rare event in contrast to parasitic plants. Transfer of DNA or RNA between unrelated species is possible through directly contacts (haustoria) between parasites and their host, Yang et al. (2016). The movement of RNAs is bidirectional and with different rates of dependency on the host. This indicates that mechanisms regulating haustoria selectivity may be host-specific (Kim et al. 2014). Transgenes in host plants trigger effective RNA interference in Cuscuta spp. inhibiting the parasite growth and could be used as potential strategy for crop improvement (Clarke et al. 2019). It was established also that the parasite Cuscuta micro RNAs inhibits the host mRNAs with the target on auxin receptors, plasma-membrane-localized kinase, phloem protein and transcriptional repressor (Shahid et al. 2018). Depending on whether the resistance of crops occurs before or after the haustorium attaches to the host surface, there are two types of resistance: pre-attachment or post-attachment resistance (Fernández-Aparicio et al. 2020). During pre-attachment resistance, the host plant prevents parasite attachment by reducing the production of germination stimulants, production of germination inhibitors, inhibition of haustorium formation and development of mechanical or structural barriers (Clarke et al. 2019). Post-attachment resistance is initiated when the parasite haustorium attaches to the host surface and penetrates in the host tissues to connect with the vascular system (Fernández-Aparicio et al. 2020).

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To our knowledge, there are not any studies so far on how berry plants respond (or not) to Cuscuta spp. at the molecular level, but the hypothetical model for interaction mechanisms is suggested: by attacking susceptible plants Cuscuta parasite release susceptibility triggers including common phytohormones and yet unknown signals, which are perceived by the host plant receptors and consequently manipulate hosts to line on susceptibility-related responses and gene expression. At an equivalent time, wound-related and defense-related responses that occur within the context of host penetration might get blocked by yet unknown suppressors. Resistant plants might prevent a parasitic attack passively, e.g., by reinforced cell walls as mechanical barriers or by non-responsiveness to susceptibility triggers. Incompatibility could also result from a deficient blocking of the host wound or defense response. Defense reactions could be actively triggered by host immunoreceptors (PRRs) that detect specific parasite-associated molecular patterns (PAMPs) or secondary generated (e.g., by parasitic hydrolytic enzymes) damage-associated molecular patterns (DAMPs) (Kaiser et al. 2015). It is believed that many DAMPs are released during haustorium formation when large-scale remodeling of host cells occurs and may be critical determinants of the compatibility of parasite interactions (Clarke et al. 2019).

9.3.2 The Genetic Response to Fungal Diseases Fungal pathogens are common for many Rosaceous plants during pre- and postharvest depending on location (Rugienius et al. 2020) thought the frequency of occurrence differs in the different crops. Strawberry fruits are a defenseless target for microbial pathogens (Barbey et al. 2019) due to their softness, weak mechanical barrier, and carbohydrate content through this varies with genotype Amil-Ruiz et al. 2011). The are some natural sources of strawberry resistance to diseases among wild species and in some varieties of cultivated F. × ananassa. The main problem is that the resistance is mostly polygenic and quantitatively inherited, making it challenging to associate molecular markers with disease resistance genes (Amil-Ruiz et al. 2011). In terms of the fruit rots, Botrytis cinerea is a highly harmful pathogen of strawberries as it infects strawberries before and after harvest leading to significant economic losses to worldwide (Petrasch et al. 2019). The negative effect of FaWRKY25 transcription factor on the jasmone acid (JA)—mediated strawberry resistance pathway against B. cinerea has been investigated. Due to FaWRKY25 overexpression JA content was significantly lowered. Therefore, the fruits’ resistance against B. cinerea, indicates the crucial role of FaWRKY25 in B. cinerea resistance (Jia et al. 2021). On the transcriptomic level the comparative analysis of between the immature-green (IG) and mature-red (MR) stages of strawberry cultivars demonstrated that the defense response significantly differed between mature stages rather than between the cultivars (Lee et al. 2021). Botrytis cinerea and Phytophthora cactorum induce remarkably similar transcriptomic responses in Fragaria vesca. The RNA-seq data showed upregulation of several

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defense-related genes upon B. cinerea infection, including genes involved in salicylic acid, jasmone acid, ethylene signaling and synthesis of secondary metabolites (Badmi et al. 2019). Another serious fruit rot is caused by Colletotrichum acutatum which also affects roots and other plant tissues. In strawberry, an endo-ß-1,3-glucanase gene (Faßgln1) from F. × ananassa cv. Chandler has been isolated, expression of which is suppressed after infection with C. acutatum (Casado-Díaz et al. 2006). Resistance gene analogs (RGAs) in strawberries were reported by Martínez Zamora et al. (2004). Resistance (R) proteins expression has been shown to increase in response to C. acutatum (Casado-Díaz et al. 2006). The R gene collection in the genomes of commercial octoploid strawberry and two diploid ancestral relatives were identified at genomic and transcriptomic levels (Barbey et al. 2019). More recently, RGA genes differentially expressed in the resistant strawberry genotype Bukammen relative to susceptible FDP821 during the early infection stage infection with P. cactorum, another fruit, and root pathogen, have been detected (Chen et al. 2016). The pathogenic fungi Verticillium dahliae and Phytophthora fragariae injure the strawberry roots, which in most cases result in plant death (Vaughan et al. 2006). The gene expression of several PR-10 genes increases after Verticillium infection. The highest levels of expression were detected first in roots and in a later time point in leaves (Besbes et al. 2019). In blueberry, screening for resistant germplasm has been carried out for some fungal pathogens. The difference in gene expression in resistant and susceptible cultivars to Anthracnose fruit rot, caused by the fungus Colletotrichum acutatum was established, showing that the resistant cultivar recognizes the pathogen at an earlier point infection than the susceptible cultivar. The identified E2 ligase gene (EST04) was found in both cultivars but expressed only in resistant blueberry cultivar Elliott indicates the role of E2 ligase in the resistance response in cultivar Elliott against Anthracnose fruit rot (Miles et al. 2011). In total, 600,000 transcriptome sequences (Rowland et al. 2012) and approximately 25,000 protein-encoding genes (Die and Rowland 2013) in the draft genome assembly of blueberry are estimated and publicly available. Recently, the biggest class of R genes, NBS-LRR genes, containing a nucleotide-binding site (NBS) and leucine-rich repeats (LRRs), was investigated for blueberry (Die et al. 2018). In total, 106 NBS-encoding genes (including 97 NBS-LRR) were found in the blueberry genome were found. They were grouped into 11 classes based on their domain architecture. The authors conclude that the search for blueberry R-like genes provides is a source for potential resistance genes and candidate molecular markers, which could be useful for development of markerassisted disease resistance selection (Die et al. 2018). Genetic resistance in a range of cultivars to Mummy Berry Fruit Rot and Shoot Blight caused by Monilinia VacciniiCorymbosi has been evaluated (Ehlenfeldt et al. 2010) and it was suggested that both morphological and biochemical factors were important, some of which may be useful in resistance breeding. Susceptible genotypes for Phytophthora root rot caused by Phytophthora cinnamomic were indicated (Yeo et al. 2016). Since the beginning of this century this pathogen has become widespread in Europe (Gosch 2006). One of the main

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objectives of modern blackcurrant breeding programs is the development of resistance/tolerance cultivars to fungal disease like mildew (Podosphaeramors-uvae), septoria leaf spot (Mycosphaerella ribis), anthracnose (Drepanopeziza ribis), rust (Cronartium ribicola), (Masny et al. 2018) and currant cane dieback (Botryosphaeria ribis syn. Neofusicoccum ribis), (Singer and Cox 2010). Most investigations to date have focused on screening for resistant germplasm to fungal disease. Resistant genotypes for the fungal disease have been evaluated in Estonia (Kikas and Libek 2020; Kikas et al. 2021), Ukraine (Mezhenskyj et al. 2020), and Lithuania (Šikšnianas et al. 2005, 2008). By evaluation of Polish, Lithuanian, British and Estonian cultivars, the cultivars ‘Vyˇciai’ (Lithuania) and ‘Elmar’ (Estonia) have been indicated as relatively weak damaged by anthracnose and they have no damage by gall mite (Kikas and Libek 2020). Also, some hybrids were found to be resistant to gall mite and gooseberry mildew: No. 3-08-1 (‘Ben Alder’ × ‘Titania’), 7-08-1, 7-08-2 (‘Intercontinental’ × ‘PamyatVavilova’) and 15-09-1 (‘Asker’ free pollination), and the green-fruited genotype No. 8-09-3 (‘Öjebyn’ × ‘Mairi’) (Kikas et al. 2021). In Ukraina different currants were evaluated (10 black, 5 red and 1 white) and resistant genotypes to diverse disease have been found: to all fungal disease (‘Kyianochka’, ‘Aspirantska’, ‘YuvileinaSherenhovoho’, ‘Lebidka’), to powdery mildew (‘Didorivska’, ‘Poltava 584’ ‘Vasylko’), to powdery mildew and white pine blister rust (‘DochkaVorskly’, ‘Hovtva’ ‘Universytetska’), to powdery mildew, anthracnose, and/or septoriosis (‘Pam‘yati Leonida Mykhalevskoho’, ‘Petrivska’, ‘Poliana Holosiivska’, ‘Malva’, ‘Olha’ and ‘Tikych’). In Lithuania, the interspecific hybrids resistance to fungal desisease has been evaluated. Parental R. Americanum plants were undamaged by powdery mildew and slightly damaged by Septoria leafspot and anthracnose. In hybrids (F1–F3) of crossings R. nigrum cv. ‘Vakariai’ and R. nigrum cv. ‘Belorusskayasladkaya’ with R. Americanum and reciprocal crossings the lower level of disease-damage was observed in hybrid families having a cytoplasm from R. Americanum (Šikšnianas et al. 2005). The wild genotype Ribes sanguineum Pursh. Was indicated as a donor of leaf fungal disease resistance in blackcurrant breeding as among interspecific hybrids R. nigrum (cv. ‘Ben Tirran’, ‘Ben Lomond’ or ‘Laimiai’) × R. sanguineum, the number of plants resistant to powdery mildew, Septoria leaf spot and anthracnose increase significantly (Šikšnianas et al. 2008).

9.3.3 The Genetic Response to Bacterial Diseases and Virus Infection The most widespread and destructive bacterial diseases in plants are the Gramnegative bacteria of the genus Erwinia, Xanthomonas and Pseudomonas. In 1962, Kennedy and King published the first report of an angular leaf spot (ALS) on strawberry caused by bacteria Xanthomonas fragariae and has increasingly spread across all strawberry production. Roach et al. (2016) identified a quantitative trait

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locus (QTL), termed Fragaria × ananassa Resistance to Xanthomonas fragariae 1 (FaRXf1). FaRXf1 provides resistance to all four clades of X. fragariae. More recently, an RNA-seq study was conducted on material after artificial inoculation with X. Fragariae at two different infection stages, early, with visible symptoms appearing and late-phase disease (Gétaz et al. 2020a). A total of 361 genes out of 28,588 known genes in strawberries were significantly differentially expressed. Genes involved in suppression of photosynthetic functions and chloroplast metabolism were downregulated at a later infection stage in infected plants, whereas genes involved in pathogen recognition and specific plant defense regulation, as pathogen-associated molecular pattern receptors and pathogenesis-related thaumatin encoding genes, were more expressed. Quantitative trait loci (QTLs) for fire blight resistance (Erwinia amylovora) were identified for Malus, however, no genomic regions linked to fire blight resistance were reported for other Rosaceae species. Rubus strains cause infection only on raspberry and blackberry. Erwinia amylovora was reported to cause infection of Fragaria ananassa and Fragaria moshata in Bulgaria (Atanasova et al. 2012), and the strains isolated from Maloideae and Rosoideae plants were geneticaly different. Active and passive defense against virus infection occurs in plants. Plants have developed several mechanisms for intracellular parasitic viruses: innate immunity, RNA silencing, translation repression, ubiquitination-mediated and autophagymediated protein degradation, and other dominant resistance gene-mediated defenses (Wu et al. 2019). Specific resistance genes in plants are activated to find and destroy virus-infected cells. Usually, these genes are specific to a particular virus. Dominant resistance gene-mediated defenses are identified and well-studied in Rubus and Ribes plants. Ce gene response to BRV resistance in gooseberries (Brennan and Graham 2009) and Bu gene response to RBDV resistance in R. idaeus “GlenClova” (Stephens et al. 2016). Conventional breeding of virus-resistant berry plants may be possible when resistance genes are presented in genetically compatible wild relatives. Bu gene for Raspberry bushy dwarf virus RBDV resistance occurred in Rubus germplasm. Nevertheless, only a few new cultivars have been invented with the Bu gene as it’s assumed it’s linked with horticulturally negative traits and thus lost in the process of cultivation (Martin 2002; Martin et al. 2013). In another case—passive protection, when the plant does not allow the virus to multiply and spread because the host plant does not synthesize the components necessary for the virus viability. Ribosome-inactivating proteins are ubiquitously distributed in plants and some of them can reduce the propagation of many plant viruses (Truniger and Aranda 2009). Latent infections with these virus species in berry plants suggest that this system exists but has not yet been studied. Plants also have a common defense system similar to immunity for detecting and degradation of viral RNA, called RNA silencing (Wassenegger and Pélissier 1998). RNA silencing is assumed as one of the primary antiviral defense mechanisms (Wu et al. 2019). Symptoms of BRV infection in blackcurrant plants may disappear during vegetative growth due to post-transcriptional gene silencing (Ratcliff et al. 1997). R. cereum, R. dikushka, R. pauciflorum, R. nigrum ssp. sibirucum are resistant to BRV also and are

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used as donor of resistance in blackcurrant breeding programs (Shikshnianas et al. 2005; Brennan and Graham 2009; Sasnauskas et al. 2017; Nellist 2018). However, the defence mechanism of these species is unclear, and an investigation is underway (Barney and Hummer 2005; Brennan et al. 2008; Mazeikiene et al. 2019). There is no knowledge also whether this resrstance is directly targeted against BRV in these species. The satellite RNA of BRV has been related to the severe form of blackcurrant reversion disease, but its effect on symptoms is unknown (Latvala-Kilby et al. 2000; Susi 2004).

9.4 Possibilities and Tools of Genome Designing in the Development of Biotic Stress-Resistant Plants 9.4.1 Background Hybridization is the classical approach for introducing valuable traits into new berry cultivars, however the gene pool in particular species can be limited, and sometimes there is a lack of classical resistance genes in that species. To overcome this problem interspecific crossbreeding is a classic method to introduce genes for resistance to biotic stress factors into commercial berries species from related donor plants. In order to improve berry quality and maintain resistance to pests, pathogens and diseases, interspecific hybrids are often backcrossed with commercial varieties. Therefore, the selection of parental species is one of the most important steps in interspecific hybridization, so this material must be studied in advance and chosen according to the desired trait for introduction. Table 9.8 show Fragaria, Rubus Ribes and Vaccinium species which may be used as donors for interspecific hybridization. As well as classical resistance genes there is also potential to utilise physical or structural traits in biotic resistance breeding (Graham et al. 2014; Karley et al. 2016; Mitchell et al. 2016). Plant traits conferring resistance and that act as a physical barrier are trichomes, spinescence, waxy cuticles, sclerophylly, cane pubescence, and others. Slippery films or crystals due to the action of epicuticular waxes prevent pathogens or pests from adhering to the plant surface (White and Eigenbrode 2000) or egg-laying (Voigt and Gorb 2010). Glandular trichomes deter pests through repellence or toxicity (Figueiredo et al. 2013) while non-glandular trichomes prevent insect attachment, limit pest movement or oviposition (Tian et al. 2012). Oviposition of Tetranychus urticae is reduced on raspberry leaves in which the trichomes are of high-density. (Karley et al. 2016). Long term resistance to diseases and pests is determined by the genotype of the cultivar, the peculiarities of pathogen microevolution, as well as the dynamics of abiotic and anthropogenic environmental factors (Bestfleisch et al. 2015). Marker-assisted selection (MAS) can be utilised alongside traditional breeding. MAS is a genotype-based selection in which specific regions of DNA are closely linked to agronomic research goals for improving resistance against pest, pathogens and diseases (Choudhary et al. 2008) are utilised for selection, rather

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Table 9.8 Fragaria, Rubus, Ribes and Vaccinium species with genetic resistance to disease and pathogens Disease or pathogen

Donors of resistance

Fragaria spp. Grey mould

Fragaria virginiana, F. vesca subsp. bracteata

Bacterial angular leaf spot

F. virginiana, F. Moschata, F. vesca

Verticillium wilt

F. chiloensis (some cultivars), F. iinumae, F. vesca

Crown and leather rot

F. vesca

Powdery mildew

F. moschata, F. chiloensis

Fusarium wilt disease

Fragaria chiloensis

References Korbin (2011), Jamieson et al. (2013), Bestfleisch et al. (2015), Vining et al. (2015) Rubus spp. Cane botrytis

R. coreanus, R. parvifolius, R. phoenicolasius, R. pileatus, R. thibetanus

Spur blight

R. phoenicolasius, R. thibetanus

Cane spot

R. coreanus, R. parvifolius, R. phoenicolasius, R. pileatus, R. thibetanus

Phytophthora

R. idaeusstrigosus, R. pileatus, R. sumatranus, R. thibetanus

Beetle resistance

R. crateagifolius, R. coreanus, R. occidentalis, R. phoenicolasius

Aphid resistance

R. occidentalis

Fruit rot

R. occidentalis, R. pileatus

References Knight (2004), Foster et al. (2019) Ribes spp. American powdery mildew

R. alpinum, R. americanum, R. aureum, R. cereum, R. cynobasti, R. dikuscha, R. divaricatum, R. glutinosum, R. hirtellum, R. hudsonianum, R. irriguum, R. janczewskii, R. leptanthum, R. longeracemosum, R. multiflorum, R. nigrum sibiricum, R. niveum, R. oxyacanthoides, R. pauciflorum, R. petiolare, R. petraeum, R. sanguineum, R. warscewiczii, R. watsonianum

White pine blister rust

R. aciculare, R. alpinum, R. americanum, R. cereum, R. cynobasi, R. dicanthum, R. dikuscha, R. glaciale, R. gluinosum, R. hallii, R. innominatum, R. leptanthum, R. lurudum, R. nigrum sibiricum, R. orientale, R. pauciflorum, R. petraeum, R. pinetorum, R. procumbens, R. rubrum, R. ussuriense, R viburnifolium

Anthracnose leafspot

R. americanum, R. aureum, R. burejense, R. ciliatum, R. cynobasti, R. cereum, R. cynobasi, R. dikuscha, R. divaricate, R. gluinosum, R. gracile, R. irriguum, R. moupinense, R. multiflorum, R. nigrum sibiricum, R. niveum, R. non-scriptum, R. oxyacanthoides, R. pauciflorum, R. petraeum, R. pubescens, R. rotundifolium, R. rubrum, R. sanguineum, R. warscewiczii, R. watsonianum

Septoria leafspot

R. americanum, R. dikuscha, R. divaricatum, R. nigrumsibiricum, R. pauciflorum (continued)

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Table 9.8 (continued) Disease or pathogen

Donors of resistance

Botrytis dieback

R. americanum

Blackcurrant reversion virus R. aureum, R. cereum, R. dikuscha, R. fuscescens, R. gordonianum, R. longeracemosum, R nigrum var. sibiricum, R. niveum Vein banding virus

R. divaricatum, R. sanguineum

Leaf-curling midge

R. alpinum, R. americanum, R. aureum, R. cereum, R. dikuscha, R. gluinosum, R. glassularia, R. orientale, R. sanguineum

Blackcurrant gall mite

R. cereum, R. glutinosum, R. uva-crispa, R. janczewskii, R. nigrum sibiricum, R. pauciflorum, R. ussuriense

References Brennan (2008), Barney and Hummer (2005) Vaccinium spp. Blueberry leaf rust

V. arboreum, V. darrowii

Reference Babiker et al. (2018)

than the trait itself. MAS can accelerate the process of hybridization-mediated plant breeding by allowing early selection of agronomic traits and biotic and abiotic stress tolerance. Hereby, MAS is the amazing tool for breeders in the process of developing varieties with transferred for subsequent generations of molecular markers associated with the genes of resistance or tolerance and the identification of valuable phenotypes at the juvenile stage of plant development (Nadeem et al. 2017; McCallum et al. 2018). In this chapter, we present what is known to date about the basis of resistance to the most important berry pathogens and where QTL have been identified and MAS utilised in Fragaria, Rubus, Ribes and Vaccinium genus.

9.4.2 Fragaria Spp. Plant breeding has impacted significant on strawberry leading to the highly productive plants that crop over a large season that are utilised today across the world. For reviews of strawberry development and genome assisted breeding see Simpson (2018) and Verma et al. (2018). As mentioned above some of the most serious strawberry pathogens include Botrytis, Colletotrichum, Verticillium, Phytophthora, Podosphaera, Rhizoctonia, Spotted Wing Drosophila, aphids, mites, whitewings and nematodes and viruses (Tables 9.3 and 9.7). Some progress in strawberry breeding to address these challenges has been made understanding the nature of genetic resistance and in using traditional and genomic breeding techniques.

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Fungal and Oomycete Pathogen Resistance Breeding

For a review of diseases of strawberry see Saville et al. (2014). Some progress has been made in understanding the nature of and in identifying potential sources of resistance to key fungal and oomycete pathogens.

Phytophthora Spp. Phytophthora spp. is a strawberry-damaging hemibiotrophic oomycete. Plants are damaged by P. cactorum and P. fragariae species causing strawberry crown rot and red stele root rot. These fungal diseases are causing significant economic losses in strawberry plantations worldwide (Nellist 2018). A single major gene locus Rpc-1 which determines resistance to crown rot disease was recently described in Fragaria vesca. Evaluation of an F2 population from a cross between resistant donor’Bukammen’ and susceptible cultivar’Haugastøl 3’ exposed a QTL located at the proximal end of LG 6 (Davik et al. 2015). Further studies proved that resistance to P. cactorum appears to be under polygenic control, with a second major locus FaRPc2 on LG 7D at Fragaria x ananassa genetic linkage map. In FaRPc2 region, four predominant SNP haplotypes were identified. Two of them are strongly linked with two different levels of resistance, suggesting the presence of multiple resistance alleles (Mangandi et al. 2017). Three other major effect QTLs (FaRPc6C, FaRPc6D and FaRPc7D) from a biparental cross of octoploid cultivated strawberry segregating for resistance to P. cactorum have been identified (Nellist et al. 2019). The GWAS (genome-wide association study) of 114 seedlings revealed an additional locus associated with resistance to P. cactorum. Two molecular markers Affx-88859864 on LG 5D and Affx-88900641 on LG 7D were found. The SNP marker Affx-88900641 was located within the QTL constructed by Mangandi et al. 2017 in region of FaRPc2 marker. Noh et al. (2018) suggested eleven DNA markers to crown rot resistance at the FaRPc2 locus. This identified abundance of molecular markers allows the selection of genotypes according with presence pyramidal resistance to crown rot in Fragaria spp. Resistance to red stele root rot caused by P. fragariae in strawberry described as a gene-for-gene mode (Van de Weg 1989). Several highly specific RAPD and AFLP molecular markers for several dominant Rpf genes were identified through QTL mapping of octoploid strawberry populations (Haymes et al. 1997; Haymes et al. 1998). According to sequences data of RAPD marker OPO-16C related to Rpf1 gene more appropriate for genotyping SCAR markers were suggested (Haymes et al. 2000; Rugienius et al. 2006).

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Colletotrichum Acutatum Strawberry anthracnose, caused by fungus Colletotrichum acutatum, is a major disease of Fragaria × ananassa also. Disease lesions occuron all morphological structures of the plant. Different types of inheritance for anthracnose resistance are based on C. acutatum pathogenicity groups (Denoyes and Baudry 1995). The dominant Rca2 gene controls resistance to group 2 pathogenicity, and minor genes may also contribute to the resistance of Strawberry anthracnose in some cultivars (Denoyes-Rothan et al. 2005). Bulked segregant analysis (BSA) combined with AFLPs was used to identify four molecular makers related with resistance conferred by gene Rca2. Two of them STS-Rca2_417 and STS-Rca2_240 were converted into SCAR markers Both SCAR markers are characteristic to resistant genotypes of strawberry (Lerceteau-Köhler et al. 2005). Although these markers not suitable for diagnostic of resistance to isolates of pathogenicity group 1—C. gloeosporioides, C. fragariae or C. acutatum (Miller-Butler et al. 2019). A QTL analysis was performed using SNP and new major locus FaRCa1, associated with resistance to C. acutatum in strawberry was detected on linkage group 6B and such molecular marker performs to confer resistance to isolates of pathogenicity group 1 (Salinas et al. 2019).

Verticillium Dahliae Verticillium dahliae is a soilborne pathogen which damages strawberry plants grown in outdoor conditions, and this ascomycete may outspread on the more than 200 different dicotyledonous plant species (Maas 1998). Single dominant gene related to resistance to V. dahliae has been identified in the popular model plants (Kawchuk et al. 2001; Hayes et al. 2011; Zhang et al. 2011). Varying levels of resistance have been identified in octoploid plant of Fragaria (Shaw et al. 1996; Vining et al. 2015; Pincot et al. 2020) looked at the potential for genetic gains in breeding resistant cultivars, identifying a few highly resistant accessions. The mapping of population ‘Redgauntlet’ × ‘Hapil’ using SSR markers revealed that resistance to Verticillium wilt is under complex control in strawberry (Antanaviciute et al. 2015). Cockerton et al. (2019) identified 4 SNP markers which are located on the same linkage groups as reported by Antanaviciute et al. (2015) and 6 new QTLs related to Verticillium wilt resistance. The molecular markers FaRVd2B and FaRVd6D assigned to cultivars ‘Redgauntlet’ and ‘Chandler’ respectively, were associated with resistance germplasm across the wider strawberry.

Podosphaera Aphanis Powdery mildew caused by Podosphaera aphanis (Fragaria × ananassa) affecting leaves, petioles and flowers and fruit of strawberry. Disease causing major yield losses through unmarketable production of berries (Maas 1998). Genetic resistance to powdery mildew inherited through polygenic heredity (Nelson et al. 1995; Nelson

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et al. 1996). Higher resistance is possible on the leaves and fruits of aging plants (Asalf et al. 2014). Wild genotypes of F. chiloensis and F. virginiana are known as donors of resistance to powdery mildew (Hancock et al. 2002; Luby et al. 2008; Nellist 2018). MLO homologues have been identified in diploid species (Pessina et al. 2014) and work is required to determine whether knockdown of MLO genes could reduce susceptibility to powdery milder in strawberry. Nineteen molecular markers related to powdery mildew resistance in strawberry were described in a US patent application characterising a major QTL for resistance in the cross combination among ‘Miyazaki Natsu Haruka’ and line ‘08 To-f’ (Koishihara et al. 2015). Recently, using two bi-parental strawberry populations ‘Emily’ × ‘Fenella’ and ‘Redgauntlet’ × ‘Hapil’ for QTLs mapping was reported both stable and transient QTLs for powdery mildew resistance. Six loci exhibiting stable resistance between locations and years were identified, along with many other QTLs that were detected only one time (Cockerton et al. 2018). In ‘Sonata’ × ‘Babette’ population study, 3 significant QTLs for resistance to powdery mildew were established (Sargent et al. 2019). A single QTL on linkage group LG7A from a glasshouse-based experiment and two other QTLs on linkage groups LG5b and LG7X2 from a field-based disease trial. The marker 8082 is established to be most closely associated with the resistance QTL in the glasshouse experiment. In the physical proximity of the QTL, a cluster of 5 TIR-NBS-LRR resistance genes were found, the closest distance from marker 8082-45 bp. The likely orthologs of the QTL identified by Sargent et al. (2019) with a major QTL identified from an unrelated Japanese study (Koishihara et al. 2015) supports the potential utility of the loci identified. For MAS application, further research would be required to validate at this time presented QTLs and to develop SCAR markers for early diagnostic of cultivar with genetic resistance to powdery mildew (Sargent et al. 2019).

Botrytis Cinerea Grey Mould Disease grey mould caused by Botrytis cinerea is one of the most destructive for strawberry plant (Maas 1998). Weather conditions where a lot of condensate accumulates on the leaves of plants are preferable for disease development. Bestfleisch et al. (2015) identified several partially resistant genotypes. The partly resistant wildtype genotype of F. vesca subsp. bracteate might provide a potential donor, but the diploid nature of it, make breeding process complicate for crossing with the octoploid F. ananassa. As classic breeding of plants for result to B. cinerea tolerance or resistance are complicated, alternative approaches for resistant plant selection should be considered (Petrasch et al. 2019). A chitinase gene from common bean expressed in strawberry correlated with resistance to Botrytis rot (Vellicce et al. 2006). Chitosan has been shown to induce resistance to grey mould through JA signalling (Peian et al. 2021). The functional role of WRKY transcription factor FaWRKY11 has examined in the regulation of the defence responses to B. cinerea in strawberry (Wang et al. 2021). Transient transformation was conducted to altering FaWRKY11 gene expression. The disease incidence of the fruits overexpressing FaWRKY11 was significantly

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alleviated compared to control fruit, conversely the degree of damage suffered by the silenced fruit tissue was higher than that of the control.

Fusarium Wilt One of the greatest threats to strawberry growers is fusarium wilt caused by Fusarium oxysporum f. sp. fragariae. Variation in susceptibility has been observed and Fragaria chiloensis has been identified as a donor of resistance (Dávalos-González et al. 2006). Proteomics studies comparing resistant and susceptible plant response to the pathogen have identified molecular components (Fang et al. 2012). Pincot et al. (2018) analysed 565 F.·ananassa genotypes and identified the Fw1 allele of R gene which was present in 97% of the germplasm resistant to fusarium wilt. Cultivars with this allele should be broadly useful in breeding of fusarium wilt resistant cultivars.

9.4.2.2

Bacterial and Viral Diseases

Angular Leaf Spot Angular leaf spot caused by Xanthomonas fragariae is the most destructive bacterial disease of strawberry plants (Kennedy and King 1962). No commercial cultivars currently have resistance however resistance has been investigated in wild polyploid of Fragaria spp. (Maas et al. 2000, 2002). Genes conferring resistance to angular leafspot disease have been introgressed into F. × ananassa (Jamieson et al. 2013). A dominant allele at a single locus controls resistance to X. fragariae (Jamieson et al. 2014; Roach et al. 2016). Roach et al. (2016) identified a highly heritable molecular marker FaRXf1 close related with resistance QTL to all four pathogen clades of X. fragariae.

Viral Diseases Viral diseases result in loss of vigour and stunting as well producing symptoms. Distinctions in tolerance level to viral diseases occur in strawberry however more research is needing in terms of the mechanisms leading to tolerance or to plant resistance.

9.4.2.3

Pest Resistance Breeding

Aphids Aphids are a problem in themselves and transmit virus diseases of strawberry. The feeding behaviour of Chaetosiphon fragaefolii was evaluated on strawberry cultivars

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‘Albion’, ‘Aromas’, ‘Camarosa’ and ‘San Andreas’ using the electrical penetration graph technique. The results suggest that trichomes act as a physical barrier creating difficulties for the aphid to feed, thereby altering its feeding behaviour in the four cultivars studied (Benatto et al. 2018).

Spotted Wing Drosophila Drosophila suzukii has become a global pest that lays its eggs in fleshy tissue. Over the last decade SWD has been detected in many countries worldwide including North America (2008), Italy (2009), England (2012) and Scotland (2014). The fly infests both cultivated and wild hosts, and when found in significant numbers, it can cause considerable economic damage. The pest prefers a moderate climate with temperatures around 20 °C, but it can survive in colder conditions and overwinter as an adult in temperatures below zero. Several strawberry accessions have been investigated for resistance and significant variation has been observed in fly emergence though the mechanism of resistance is unclear (Gong et al. 2016) though provides valuable breeding material. In another study, strawberry accessions were identified that significantly reduce adult fly emergence from infested fruit due to enrichment of methyl anthranilate within the fruit. It was found that this compound triggers embryo lethality in a concentration-dependent manner. Interestingly, adult females are attracted to methyl anthranilate at certain concentrations, and they lay eggs despite the lethal effect on their development (Bräcker et al. 2020). The potential for allele mining and also using as a biological control needs to be investigated.

Two Spotted Spider Mite Tetranychus urticae Koch is prevalent pest in greenhouses and outdoors where strawberries are grown. Differences have been identified in the susceptibility of cultivars to TSSM (González-Domínguez et al. 2015; Karlec et al. 2017; Dana et al. 2018; Gong et al. 2018; Fahim et al. 2020). The role of leaf trichomes was investigated and level of resistance was correlated with the density of trichomes on the leaf surface revealing important parents for breeding resistance (Figueiredo et al. 2013; de Resende et al. 2020).

9.4.3 Rubus Spp. Raspberry belongs to Rubus genus in the Rosoideae subfamily of Rosaceae, genus includes over 740 species which characterized by high genetic diversity (Foster et al. 2019) some of them may provide a source of resistance to pests and diseases. Some sources of pest and disease resistance in diverse Rubus spp. have been identified and exploited in classical plant breeding (Keep et al. 1977; Jones 1987; Jennings 1988;

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Knight 1991; Williamson and Jennings 1992; Birch et al. 2002; Jones et al. 2002). For recent reviews on breeding efforts see Jennings (2018); Graham and Jennings (2020) and with developments in linkage mapping and genomics these sources should be more readily utilised.

9.4.3.1

Fungal Pathogen Resistance Breeding

For a review of fungal diseases in Rubus see Jennings and Dolan (2014).

Phytophthora Fragaria Var. Rubi Root rot, caused by Phytophthora fragariae var. rubi, is one of the most damaging disease of Rubus spp. plants in North Europe (Harrison et al. 1998) and significantly limits plantation life span. Root rot affects all aspects of plant growth: plant height, cane number and root sucker characteristics (McCallum et al. 2018). Several breeding programmes have resistance to root rot as a major target. Pattison et al. (2007) presented a two gene hypothesis for resistance, and Graham et al. (2011) subsequently identified two QTLs for resistance which include both resistance and tolerance in terms of root growth. Some cultivars of raspberries ‘Latham’, ‘Winkler’s Sämling’ and wild species R. strigosus, R. occidentalis, R. vulgatus and R. ursinus have identified as potential donors of resistance (Barritt et al. 1979; Bristow et al. 1988), however the original nature of resistance is still unknown. Pattison et al. (2007) combined generation means with molecular markers and QTL analysis to map resistance to Phytophthora root rot in red raspberry population NY00-34 (‘Titan’ × ‘Latham’) × ‘Titan’. Genetic linkage maps of parental genotypes were constructed using AFLP, RAPD, RGAP (resistance gene analog polymorphism) and analysed for QTL map associated with different resistance parameters assayed in a hydroponic system (Pattison et al. 2004). The resistance to Phytophthora root rot explained by two major genes system possibly corresponding to the two regions in parental linkage maps. Weber et al. (2008) generated molecular markers SCAR618 and CAP464 from loci associated with PRR resistance. Markers were partially validated and success rate of 76% for resistance cultivars identification was established. More recently molecular markers linked to a resistance have been developed in using a segregating population derived from a cross between resistant cultivar ‘Latham’ and susceptible to root rot cultivar ‘Glen Moy’ with excellent yield characteristics. QTL for root vigour on linkage group 3 and 6, co-locate with disease resistance identified (Graham et al. 2011). Using a marker developed in this study a new cultivar ‘Glen Mor’ has recently been released with resistance to root rot and excellent fruit quality (James Hutton Limited 2021).

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Phragmidium Rubi-Idaei Yellow rust (Phragmidium rubi-idaei) the increase in cases is related with the more common and widespread cultivation under tunnels of susceptible cultivars (e.g., ‘Glen Ample’ and ‘Tulameen’). A dominant gene Yr responsible for resistance in cultivar ‘Latham’ was identified by Anthony et al. (1986). The inheritance of complete and incomplete resistance to rust in a half diallel cross studied. Was found that found that cultivar ‘Boyne’ is heterozygous for one resistance gene Yr, and it inherited from ‘Latham’. According to research Graham et al. (2006) this gene was located on LG 3 in QTL linkage map of the population ‘Latham’ × ‘Glen Moy’. Investigated population also segregates for resistance to yellow rust, and Graham et al. (2006) concluded that ‘Latham’ is heterozygous for Yr gene also.

Cane Diseases Cane botrytis (Botrytis cinerea) and spur blight (Didymella applanata) dominate in the same ecological niche (Williamson and Jennings 1986). For breeding resistance to cane botrytis and spur blight, Williamson and Jennings (1986) suggested a common resistance mechanism. In attempts to control cane diseases, it had been known that the distinctive morphological traits, most notable being cane pubescence in red raspberry is related with resistance to cane botrytis and spur blight (Knight and Keep 1958; Jennings and Brydon 1989). Subsequently, Graham et al. (2006) identified two major loci associated with resistance suggesting multiple gene control. One of these gene regions co-locates with gene H (Graham et al. 2004), which controls cane pubescence and gene H is now used in breeding as a visual marker for resistance to these two diseases. Cane spot or anthracnose (Elsinoe veneta) causes deep wounds that disrupt the circulation of water and nutrients in the plants of raspberry and leading to plant destruction and economic loss. Resistance to this pathogen is associated with spinescence of European red raspberry genotypes, but North American varieties are susceptible. Genetic control of the trait has not been firmly established on QTL mapping (Graham et al. 2006).

9.4.3.2

Pests Resistance

For a review of arthropod pests in Europe see Jennings (1988), Gordon et al. (1997).

Aphid Resistance To date, four aphid species in Rubus spp. crops are reported: Amphorophora agathonica, A. idaei, Aphis idaei and A. rubicola. They cause huge economic harm through their role as virus biological vectors severely reducing productivity and yield quality

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(McCallum et al. 2018) studied. The genetic control of A. idaei resistance obtained from various sources was studies and attributed to several single dominant genes (A1 – A10 , AL518 , AK4a ) (Knight et al. 1960; Keep and Knight 1967). As resistance-breaking biotypes against gene A1 have appeared, a further gene A10, related to resistance to A. idaei was identified in the black raspberry cultivar ‘Cumberland’ (Keep and Knight 1967) and has become commonly used in raspberry breeding programs (Birch et al. 2011). Nowadays, breeders are attempting to combine gene A10 with other genes related with resistance to aphids and developments in MAS technology will simplify this gene pyramiding strategy to offer cultivars with genetic resistance to aphids in a shorter period. Resistance is strongly dependent from the A. idaei biotype, with some genes providing resistance to certain biotypes (Sargent et al. 2007). The A1 locus conferring A. idaei resistance was mapped by Sargent et al. (2007) in a red raspberry (R. idaeus) population of ‘Malling Jewel’ × ‘Malling Orion’ and a closely linked SSR marker Rub103a could be useful in selecting genes with resistance to aphid from different sources and facilitate gene pyramiding. Interestingly, the region around this marker coincides with the location of QTL for resistance to some of Rubus spp. pathogens: spur blight, cane botrytis and rust (Graham et al. 2006). A. agathonica is the main biological vector of Raspberry mosaic virus complex in North America. Currently, three sources of resistance to aphids have been detected in wild germplasm and used to develop mapping populations to identify the inheritance of these valuable traits (Dossett and Finn 2010). A mechanism for resistance to this insect has been suggested by Lightle et al. (2012). In black raspberry, a locus for aphid resistance, Ag4 , has been mapped on linkage group 6. For prediction of resistance to A. agathonica depending on the source, four DNA tests (an HRM, a gel-based and two SSR) were established (Bushakra et al. 2018).

Vine Weevil Vine weevil (Otiorhynchus sulcatus) larvae cause significant damage feeding below ground on roots for an extended period between summer and spring. At present, there are no known genetic targets for breeding resistance to this pest in Rubus, although Rubus genotypes with improved root vigor might better tolerate root infestations (Price 1991; Mitchell et al. 2016). QTL approaches have been used for detection of genetic markers for vigor in raspberry (e.g., root vigor (Graham et al. 2011)) that could be targeted for Rubus breeding.

Spotted Wing Drosophila (Drosophila Suzukii) (SWD) SWD, as discussed in strawberry in 9.4.2.3.2 is also a serious problem in raspberry by direct oviposition damaging the skin of the fruit. There is currently a lack of information on what may be relevant in breeding for resistance as a relatively new pest. Wöhner et al. (2021) screened germplasm to determine if there were preferences

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for particular genotypes based on citric acid content, Brix and firmness. Oviposition correlated with firmness, and this may provide a trait and genetic resource for breeding, and the development of markers to assist in this process is underway (Simpson et al. 2017).

Two-Spotted Spider Mite Tetranychus Uticae Differences have been observed in oviposition and mite distribution of TSSM between raspberry cultivars (Sonneveld et al. 1996; Hanson et al. 2005). In common with findings on strawberries discussed in Sect. 4.2.3.3, oviposition was considerably reduced on Ribes spp. genotypes with high leaf trichome densities (Karley et al. 2016). The identification of genetic markers to this trait is useful in breeding (Graham et al. 2014).

Cane Midge Resseliella Theobaldi (Barnes) Cane midge in raspberry leads to cane blight a disease complex due to midge infestation followed by infection by several pathogens. Cane splitting is one of the most significant factors for this disease complex (Jennings 1988). Raspberry genotypes differ in the degree of cane splitting, and regions of the genome associated with this trait have been identified by Woodhead et al. (2013). A correlation between cane splitting and cane height has been detected, shorter genotypes demonstrating less cane splitting than longer ones. Loci accounting for 49% of height variation have been identified (Graham et al. 2009; Woodhead et al. 2013), allowing to breed genotypes directly or indirectly with reduced tendency to splitting.

9.4.3.3

Virus Disease Resistance

Virus problems often do not receive the same level of attention as other pest and disease problems. For a review of viruses identified in Rubus species, see Martin et al. (2013) 86who listed 30 viruses that have been reported to contaminate black raspberry (Rubus occidentalis), red raspberry and blackberry. Some viruses are currently detected only in Europe (Raspberry leaf blotch virus) or in the United States (Blackberry virus Y ). These differences could be twofold: caused by propagation of different plant stocks in the United States and Europe or caused by biases in the testing regimes employed in these continents (Dolan et al. 2018). Viruses tend to be managed through vector control when possible. Raspberry bushy dwarf virus is the most important pollen-transmitted virus in raspberry. It affects the development of the fruit and leads to reduced drupelet numbers and increased size of these drupelets, resulting in unmarketable fruit (Dolan et al. 2018). Some studies have been conducted to identify strategies for resistance to some raspberry viruses. The segregation of Raspberry leaf spot (RLSV) and raspberry

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vein chlorosis (RVCV) was quantified in two different environments. Significant linkages to mapped markers and resistance loci were set up on linkage groups 2 and 7 (Rusu et al. 2006; McCallum et al. 2018). Oher studies have examined the change in the transcriptome of raspberry in response to Tomato ringspot virus (ToRSV) infection. Here over 2000 genes were differentially expressed between infected and non-infected plants. Analysis of the genes showed functional enrichment in cell wall biogenesis, the oxidation–reduction process, lyase activity and terpene synthase activity. These genes may be involved in the Rubus spp. plants immune response through the interaction of several metabolic pathways; however, this needs further study (González et al. 2020).

9.4.4 Ribes Spp. Blackcurrants and other currants are native to colder climates and form the basis of processing industries’ rich sources of phytochemicals. Traditionally these crops were unknown in parts of the world due to transmitting pine blister rust (Munck et al. 2015) that affects the lumber industry. Some problems from strawberry and raspberry also cause problems in this species such as Phytophthora, SWD and TSSM and some of the control measures may be appropriate in this species particularly the architectural and morphological traits. Reviews can be found of pest problems and control strategies in Mitchell et al. (2011) and Brennan and Jarret (2014).

9.4.4.1

Resistance Breeding

Gall Mite (Cecidophyopsis Ribis) Gall mite (C. ribis) is the most serious pest of blackcurrant (Ribes nigrum L.), transmitting Blackcurrant reversion virus (BRV) which cause blackcurrant reversion disease. Introduction of resistance to gall mite (Cecidophyopsis ribis) may serve as a good example of interspecific hybridization in Ribes spp. Currently, two gall mite resistance genes are known, dominant gene P found in R. nigrum spp. sibiricum (Anderson 1971) and Ce gene in gooseberry (Knight et al. 1974). Resistance based on Ce has been used in breeding programs for blackcurrant in United Kingdom. Breeding programs for introgression of P gene from R. nigrum ssp. sibiricum cultivars are ongoing (Miseviciute 1981; Shikshnianas et al. 2005; Brennan 2008; Mazeikiene et al. 2019), and new blackcurrant cultivars ‘Aldoniai’ and ‘Didikai’ with dominant P gene (inherited from R. nigrum spp. sibiricum) were created (Mažeikien˙e et al. 2017). Nuclear-based SSR, AFLP and SNP are some of the commonly used markers for genome and QTL mapping in order to recognize sequences controlling resistance traits in Ribes spp. (Mazeikiene et al. 2012). Several linkage group maps of molecular markers associated to resistance to gall mite and/or BRV with QTLs were created (Russell et al. 2011; Brennan et al. 2008), and a marker was developed

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(Brennan et al. 2009). A linkage map of the resistance locus controlled by gene P using AFLP and SSR markers was also developed (Mazeikiene et al. 2012). The molecular marker of P gene was validated in R. nigrum spp. sibiricum, R. americanum and R. aureum (Mazeikiene et al. 2017). A complex study of these markers reliably identifies Ribes species, cultivars and hybrids resistant to gall mite and Blackcurrant reversion virus and could be useful for MAS without phenotypic evaluation in Ribes spp. (Mazeikiene et al. 2019; Mazeikiene 2020).

Currant Borer Synanthedon Tipuliformis Clerck The larvae of the currant borer and a clearwing moth are pests of cultivated black, red and white currants plantations throughout the world. Genetic resistance has not been reported or employed as a pest control strategy. Hummer and Sabitov (2004) tested 150 diverse black (Ribes section: Botrycarpum), red and white currants (Ribes section: Ribes) for natural infestation by the currant borer and differences were found with some accessions having low or no counts. Other studies have also identified differences (Jermyn 2002). This information will provide breeding strategies against this pest.

White Pine Blister Rust (Cronartium Ribicola Fisch.) White pine blister rust (Cronartium ribicola Fisch.) is virulent on several hosts of Grossulariaceae including Ribes spp. (Kaitera et al. 2012; Munck et al. 2015). Blackcurrant cultivars resistant to white pine blister rust were created after including R. ussuriense Jancz. into breeding programs. Germplasm of several species of Ribes (Table 9.5) have resistance to white pine blister rust and can be used as resistance donors in breeding programs.

Powdery Mildew Sphaerotheca Mors-Uvae (Schwein) Powdery mildew is a foliar disease caused by fungi Sphaerotheca mors-uvae (Schwein) (Braun and Takamatsu 2000). Nine oligogenes responsible to powdery mildew resistance are known, while R. glutinosum and R. sanguineum are primary resistance donors to American gooseberry mildew. Other breeding strategies considered as control options have examined the phenolic compounds in leaves and the variability of these across accessions as a tool for resistance breeding (Vagiri et al. 2017).

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9.4.5 Vaccinium Spp. Blueberries are susceptible to some of the pathogen problems faced in the other berry crops discussed here. However, little information is available to date on genetic resistance to the main pest and pathogens in blueberry or for marker-assisted resistance breeding in blueberry. Genetic resources are being developed in terms of linkage maps and genome studies (Rowland et al. 2014; McCallum et al. 2016; Schlautman et al. 2018) and in terms of pest and disease resistance, genetic information is available on the regulation of fruit firmness in blueberry which may offer a tool for fungal pathogens or pests like SWD as in the example in Sect. 4.4.1.3 (Cappai et al. 2018). Marker-assisted breeding for root traits has been initiated in blueberry, which may also provide a breeding tool for biotic stresses (Nunez et al. 2015).

9.4.5.1

Disease Resistance

A review of blueberry diseases can be found in McCallum and Graham (2014). Babiker et al. (2018) tested resistance to leaf rust in Vaccinium species and stated that accessions of V. arboretum displayed immunity against Thekopsora minima. According to the symptoms on the infected V. darrowii leaves, the resistance of these plants to leaf rust is presumed. The level of anthracnose susceptibility of commercially available southern highbush cultivars against Colletotrichum gloeosporioides was followed by measurement of incidence and severity of disease over time (Phillips et al. 2018). Depending on the resistance, the different cultivars blueberry varied in the lesions number and areas on leaves, but the observed lessons remained similar as in V. corymbosum. Differences in susceptibility can be utilized in breeding.

Fruit Rots The complex of pathogenic fungi has been associated with cranberry fruit rot, including Phyllosticta vaccinii, Physalospora vaccinii, Phomopsis vaccinii, Colletotrichum gloeosporioides, Coleophoma empetri etc. (Oudemans et al. 1998). This disease brings one of the biggest losses to cranberry growers. The first genetic map and QTL analysis of cranberry (Vaccinium macrocarpon) were developed using SSR and SCAR markers (Georgi et al. 2013). Seven QTL were found for resistance to fruit rot (FRR) (Georgi et al. 2013; Schlautman et al. 2015). The number of results of this genetic study is insufficiently, due to the limited segregation of the FRR in the study population and the insufficient number of molecular markers in the gene map. An important update providing a new set of V. macrocarpon genetic maps identified new QTL associated with FFR and supported those QTL proposed in the previous work was carried out (Daverdin et al. 2017).

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Pest Resistance

Elephant weevil larvae, Orthorhinus cylindrirostris (F.) (Coleoptera: Curculionidae), reduce blueberry yield and reduces the longevity of plantations. (Murdoch et al. 2017). Varieties developed in recent years have higher pathogen resistance. The absence of susceptible varieties in plantations limits the reproduction and spread of the O. cylindrirostris. Targeted selection of plants for this pest allows the crossbreeding of resistant genotypes for new cultivars. Five cranberry cultivars were evaluated due to the population densities of the three economically important pest insects (cranberry fruit worm (Acrobasis vaccinii Riley), sparganosis fruit worm (Sparganothis sulfureana Clemens), and black headed fireworm (Rhopobota naevana Hubner). The obtained data showed that cranberry cultivars are characterized by different levels of resistance, which should be considered during crossbreeding and plant selection (McMahan et al. 2017).

9.5 Future Prospects for Biotic Control Sales of berries continue to rise while there is a desire by consumers for sustainable and local production. Coupled with a reduction in the use of actives for pathogen control and the changing climate, the need for biotic stress resistance has never been greater. The requirement for pathogen resistance also has considered against background of move to protected cropping, with much of the world’s soft and stone fruits now grown in tunnels. These tunnels modify the environment and have enabled growers to evolve production systems that extend production capability beyond the traditional cropping season (see Both et al. 2019). These tunnel systems offer protection from the weather, tend to produce better quality fruit and higher yield, extend plantation life, and offer some protection against certain pests and diseases. Therefore, plant breeding leading to appropriate varieties is crucial for introducing resistance genes into commercial cultivars that will be grown environments and under particular growing conditions. Plant breeding is however a long and expensive process. Modern plant breeding methods, such as marker-assisted selection or genome editing, have emerged for use alongside traditional methods such as hybridization and mutagenesis. In this chapter, we have reviewed the most damaging agents in different berry plantations and methods to reduce that damage through resistance breeding assisted using molecular markers. This will lead to a reduction in the use of chemical plant protection agents particularly when used alongside other IPM approaches (Graham et al. 2019; Karley et al. 2016). The ability to detect pathogen infection early and understand the impact the abiotic environment has on biotic trait expression and understand the abiotic environment’s impact on biotic trait expression also require developments in phenotyping technology to support those genetic/genomic developments. This will provide tools to

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understand both the pathogen pressures and the genetic response to them under particular environments. When coupled with the expansion of genomics technologies, the opportunities for the development of specific genotypes for prevailing climatic and market conditions are considerable. For review see Williams et al. (2018). Target breeding of resistance plants needs to be seen as a powerful tool as part of an agroecological approach to crop-growing, this requires investigation of genetics, biology, interaction and regulatory measures of host–pathogen-disease systems (Birch et al. 2011; Kremen et al. 2012). Birch et al. (2011) developed a framework for an agroecological approach that provides pathogen and pest management measures with biological control, i.e., using biological protection measures, altering ecological habitats, modelling ecosystems in the environment, and altering the microflora outside and inside the plant.

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