Plant Growth and Stress Physiology (Plant in Challenging Environments, 3) 3030784193, 9783030784195

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Plant in Challenging Environments 3

Dharmendra K. Gupta José Manuel Palma Editors

Plant Growth and Stress Physiology

Plant in Challenging Environments Volume 3

Series Editors Dharmendra K. Gupta, Ministry of Environment, Forests and Climate, New Delhi, India José Manuel Palma, Estación Experimental del Zaidín, Granada, Granada, Spain Francisco J. Corpas, Estación Experimental del Zaidín, Granada, Spain

This book series provides recent advancements in wide areas related to higher plants and how they adapt / evolve under environmental changes in a scenario of climate change. It investigates plants under the complementary point of views, including agronomy aspects (vegetables and fruits), nutrition and health (food security), “omics,” epigenetics, contamination by heavy metals, environmental stresses (salinity, drought, high and low temperatures), interaction with beneficial or pathogenic microorganisms, and application of exogenous molecules (nitric oxide, melatonin, chitosan, silicon, etc.) to palliate negative effects. It also includes changes due to climatic condition (high/low rainfall) taking into account that the climate change is often the reason why plants evolve in a challenging environment. This book series also covers molecular-/cellular-level responses of plants under different climatic reasons. Families of molecules derived from hydrogen peroxide (H2O2), nitric oxide (NO) and hydrogen sulfide (H2S) designated as reactive oxygen, nitrogen and sulfur species (ROS, RNS and RSS, respectively) are included since, depending on the production level, they function both as signal molecules and as a mechanism of response against adverse/changing environmental conditions that can produce multiple cellular damages, alter the redox state or even trigger cell death. During these ensued metabolic processes, some anti-oxidative/oxidative enzymes are also disturbed or triggered abruptly, but there are adequate mechanisms of regulation/homeostasis in the different subcellular compartments to keep these enzymes under control. In the last decades, the progression in this field has been enormous, but still there is so much in this field to understand the plethora of phenomena behind.

More information about this series at http://www.springer.com/series/16619

Dharmendra K. Gupta  •  José Manuel Palma Editors

Plant Growth and Stress Physiology

Editors Dharmendra K. Gupta Ministry of Environment, Forests and Climate Change New Delhi, India

José Manuel Palma CSIC Estación Experimental del Zaidín Granada, Spain

ISSN 2730-6194     ISSN 2730-6208 (electronic) Plant in Challenging Environments ISBN 978-3-030-78419-5    ISBN 978-3-030-78420-1 (eBook) https://doi.org/10.1007/978-3-030-78420-1 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are solely and exclusively license 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

Preface

Plants are sessile organisms that have adapted continuously their physiology to a changing environment to ensure their survivor. It implicates a versatile metabolism which allow plants to face-threatening situations such as salinity, drought, flooding, high and low temperatures, radiation, contamination by heavy metals and metalloids (Cd, Hg, Pg, As, and others) and xenobiotics from diverse nature, pests and other pathogens. All these perspectives make necessary a good knowledge of how plants function under normal conditions and which mechanisms and strategies are used by them to cope with the above unfavorable conditions. Of course, this implies a global view of each species in its surrounding medium where climatologic conditions may drive the final response of the plant. This gains relevance in a scenario of climate change already installed on our planet. Such knowledge will be decisive to improve our crops and to face the dramatic situations of millions of people who still suffer hunger. More and better Agriculture is indispensable to provide the necessary amount and quality of food for those people who find in the scientific community an ally to solve their nutritional needs. Especially, when contamination, increasing temperatures of the planet, and elevated costs of design agriculture may impose some asymmetric distribution of wealth. This book compiles much science on “Plant Growth and Stress Physiology”, and provides substantial knowledge on how plants reorganize their metabolism to adapt to unwanted conditions. It means acclimation, but the term resilience is used increasingly to describe how plants not only adapt but also finally get benefit from hostile conditions. A team of good experts from all over the world have contributed to update many issues regarding plant growth and stress physiology in this volume. Thus, general aspects of the growth and development of plants and their adaptation to unfavorable conditions will be addressed. Several situations which impose to plants stressful situations such as water deficit and contamination by heavy metals, and how plants deal with them (accumulation and phytoremediation strategies), will be also depicted in this book. The molecular sensing mechanisms and those which involve cross-talk and signaling events (nitric oxide and hydrogen peroxide) within the plant tissues and with their surroundings, especially with the bacterial v

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community in the rhizosphere are also subject of the present work. Finally, practices to improve yield and quality of plant products through either management of plant-­ associated microorganisms, organic fertilization or revegetation will be visited as well. The target of this book is not only experts in plant biology and the overall scientific community but also teachers and students from any discipline since it has been written by authors with expertise in their scientific field and in disseminating science. The editors are deeply acknowledged to all of them and want to also highlight their enthusiasm and disinterested availability with this work at any time. New Delhi, India Granada, Spain

Dharmendra K. Gupta José M. Palma

Contents

1 Plant Stress, Acclimation, and Adaptation: A Review��������������������������    1 Anindita Mitra, Sampriti Kataki, Aditya N. Singh, Apoorva Gaur, B. H. N. Razafindrabe, Piyush Kumar, Soumya Chatterjee, and Dharmendra K. Gupta 2 Insights into Role of Invisible Partners in Plant Growth and Development��������������������������������������������������������������������������������������   23 Revuru Bharadwaj, Sarma Rajeev Kumar, and Ramalingam Sathishkumar 3 High Temperature Sensing Mechanisms and Their Downstream Pathways in Plants������������������������������������������   49 Nobuhiro Suzuki 4 From Beneficial Bacteria to Microbial Derived Elicitors: Biotecnological Applications to Improve Fruit Quality������������������������   73 Beatriz Ramos-Solano, Ana Garcia-Villaraco Velasco, Enrique Gutiérrez-­Albanchez, Jose Antonio Lucas, and Javier Gutierrez-Mañero 5 Come Hell or High Water: Breeding the Profile of Eucalyptus Tolerance to Abiotic Stress Focusing Water Deficit����������������������������������������������������������������������������   91 Edgard Augusto de Toledo Picoli, Marcos Deon Vilela de Resende, and Shinitiro Oda 6 Organic Fertilization of Fruit Trees as an Alternative to Mineral Fertilizers: Effect on Plant Growth, Yield and Fruit Quality ������������������������������������������������������������������������������������  129 Elena Baldi and Moreno Toselli

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7 Evaluation of Turbulence Stress on Submerged Macrophytes Growing in Lowland Streams Using H2O2 as an Indicator ��������������������������������������������������������������������  151 Takashi Asaeda, M. Harun Rashid, L. Vamisi Krishna, and M. Rahman 8 Opportunities of Revegetation and Bioenergy Production in Marginal Areas������������������������������������������������������������������������������������  167 Agustina Branzini and Marta S. Zubillaga 9 Biochar Behaviour and the Influence of Soil Microbial Community�����������������������������������������������������������������  181 Ihuoma N. Anyanwu, Chinedum U. Nwajiuba, Emmanuel B. Chamba, Victor Omoni, and Kirk T. Semple 10 New Insights into the Functional Role of Nitric Oxide and Reactive Oxygen Species in Plant Response to Biotic and Abiotic Stress Conditions ����������������������������������������������������������������  215 Mounira Chaki, Juan C. Begara-Morales, Raquel Valderrama, Lorena Aranda-Caño, and Juan B. Barroso 11 Selenium Transport, Accumulation and Toxicity in Plants������������������  237 Ryoung Shin and Ju Yeon Moon 12 Selenium in Algae: Bioaccumulation and Toxicity��������������������������������  261 Dubravka Špoljarić Maronić, Tanja Žuna Pfeiffer, Filip Stević, and Nikolina Bek

Chapter 1

Plant Stress, Acclimation, and Adaptation: A Review Anindita Mitra, Sampriti Kataki, Aditya N. Singh, Apoorva Gaur, B. H. N. Razafindrabe, Piyush Kumar, Soumya Chatterjee, and Dharmendra K. Gupta

Abstract  Plant stress impacts a detrimental effect on growth. Stress component may be promoted by either abiotic (physical, chemical or environmental) or biotic (biological agents or pathogen) factors. Stresses are the important reason for persistent losses in the agrarian produces which badly affects the biomass production and survivability in most crops. Heavy metals activate a wide range of physiological and metabolic variations affecting the enzymatic processes. To counteract the stress, plants develop strategies like accumulating organic compounds, solutes, osmolytes, stress proteins and detoxifying enzymes. Diverse signalling pathways/genes regulating the response of plants against abiotic and biotic stress are contributing to stress responses. This review represents plant stress tolerance in general based on the up-to-date research data. Keywords  Heavy metal · Metallothiothein · Stress proteins · Abiotic · Pathogen

A. Mitra Bankura Christian College, Bankura, West Bengal, India S. Kataki · S. Chatterjee Defence Research Laboratory, DRDO, Tezpur, Assam, India A. N. Singh · A. Gaur · D. K. Gupta (*) Ministry of Environment, Forest and Climate Change, Indira Paryavaran Bhavan, Aliganj, New Delhi, India e-mail: [email protected] B. H. N. Razafindrabe Faculty of Agriculture University of the Ryukyus, Okinawa, Japan P. Kumar Paryavaran Complex, New Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_1

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1.1  Introduction Plant stresses may be defined as any detrimental impact on plant growth and development, triggered by either an environmental or biological factor, or by both. Plants undergo a range of biotic and abiotic stresses due to ever-changing climatic conditions such as global warming, sporadic but heavy rainfall and exhaustion of productive land and water resources (Ahmad et al. 2019). Abiotic stresses enforced upon plants may be sourced either from physical or chemical environmental factors and biotic stresses are imposed by any biological agents and pathogen (Verma et  al. 2013). Injuries caused by mild stress for a short duration can be overcome by plants while severe stresses for a longer duration lead to several hazardous effects such as delayed or hindered flowering and fruit setting, seed formation and enhanced senescence (Verma et al. 2013). Abiotic stresses are also reported to promote outbreaks of pests, pathogens, insects and weeds (Ziska et al. 2010; Peters et al. 2014; Ahmad et al. 2019). However, in natural field condition, plants generally confront collateral abiotic stresses such as drought and salinity or drought and heat that are more pernicious to global crop production. Ample evidences are available on the cross-­ tolerance of plants to a diversity of abiotic stresses (Hossain et  al. 2018; Harshavardhan et al. 2018; Shiri et al. 2015). Plant responses to different abiotic stresses follow common signalling pathways and hence plants tolerant to one type of abiotic stress become acclimatized to other different types of abiotic stresses, known as cross-tolerance (Zhu 2016). Apart from encountering a range of abiotic stresses, plants also experience several biotic stresses, commonly through pathogens (fungi, virus, bacteria, nematodes), pest (insects, mites) or herbivore attack concomitantly or consecutively (Ahmad et al. 2019). The causative agents for biotic stresses endorse various types of diseases, infections and damage to plants and thus impose a great pressure on plant productivity (Gull et al. 2019). Plants may encounter a single (only one stress), multiple individuals (two or more stresses occurring without any overlap), concurrent (two or more stresses occurring simultaneously with a little overlap), and repetitive stresses (single stress or multiple stresses followed by recovery periods, last for shorter or longer duration) depending on the number of interacting factors (Ahmad et al. 2019). However, the tolerance capacity of the plants towards multiple stress factors may either improve or predispose the plant toward a wide range of stresses (Ahmad et al. 2019). For example, concurrent drought and cold stress in North China results in a severe reduction in the productivity of Vitis vinifera (Su et al. 2015). Similarly, plants confronted with concurrent biotic stresses (such as combinations of fungal and bacterial attack) are more acutely mutilated than by individual pathogen infection (Lamichhane and Venturi 2015). The effects of abiotic stresses in plants may impart positive or negative impacts in developing susceptibility or resistance to biotic stresses such as powdery mildew, rust, and wilt depending on the timing and severity of drought and/or salinity stress. Niakoo et al. (2019) reported that a diverse set of gene expression is upregulated in response to concurrent stresses to produce secondary metabolites (e.g. phenolics) to mitigate the effects of a broad range of

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stresses. Plants also express distinctive responses in addition to general responses and also can modify their responses to concurrent stress factors. This chapter aims to summarize the different stresses in plants and the general response of plants to these stresses to cope up.

1.2  Stresses in Plants Different types of environmental factors like drought, salinity, high concentration of heavy metals in soil, and extreme heat are the major abiotic stresses that prevail in modern agriculture. Reduction in crop yield of about 50–70% has been attributed to abiotic stresses depending upon the intensity and duration of stresses, type of plant and the phase of growth (Jaleel et al. 2008). Abiotic stresses are the leading cause for persistent losses in the agricultural production throughout the world as it adversely affects the survivability, biomass production, and grain yield in the majority of crops (Athar and Ashraf 2009). Plant responses to different abiotic stresses include altered gene expression, anatomical and morphological changes, attenuated photosynthetic efficiency, reduced nitrogen-fixing capability and modulation in the enzymatic activities related to a metabolic reaction. Drought or water stress is one of the acute abiotic stresses and is responsible for declined agricultural production worldwide. Drought has a negative impact on plant growth and development and induces loss of membrane integrity, stomatal closure, altered pigment content, osmotic alterations and reduced water retention capacity. It adversely affects photosynthetic activity by limiting CO2 influx, reduces the accumulation of abscisic acid (ABA), osmolytes proline, mannitol, sorbitol and thus hindering the formation of free radical scavenging compounds (ascorbate, glutathione, α-tocopherol, etc.), suppressing the synthesis of new proteins and mRNAs (Osakabe et al. 2014), reducing carboxylation and efficiency of electron transport chain of the chloroplasts inside the mesophyll cells (Feller and Vaseva 2014). Salinity is another destructive stress following drought which reduces crop productivity. Soil salinity may be increased due to anthropogenic activities sourced from deforestation, over grassing, water-borne and air-borne salts deposition in soils and chemical contamination. Due to increased salinity, the basic structure of the soil is disrupted with higher sodium content as well as other salts that ensues reduced soil porosity and soil aeration and poor water conductance. Plants exposed to high salt concentration in soil face interference in the process of seed germination, seedling growth and vitality, vegetative growth, flowering and fruit set, leading to lower yield and quality production (Pandey et al. 2020). Salinity induces osmotic stress and ionic toxicity (Munns and Tester 2008; Porcel et al. 2012) as elevated salt in the soil promotes higher osmotic pressure in soil solution than the plant cells, thus, restraining the plant uptake of water and essential minerals (like K, Ca, and Mn) due to creation of water potential deficit zone in the soil (Pandey et al. 2020). Persistent accumulation of salts leads to a further adverse situation called ‘physiological drought’ when plants are unable to uptake water present in the soil (Porcel

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et al. 2016). Depending on the genotype, adaptability and other physiological features, plants respond differently to the salinity that may be reflected in the plant growth and development. For example, Salt sensitive plants such as Zea mays, Oryza sativa, Phaseolus vulgaris, and Glycine max (glycophytes) cannot endure the higher levels of salt concentration, while halophytes, for instance, Medicago sativa, Atriplex amnicola, and Lepidium species can well-flourish in high salinity levels. Osmotically stressed plants express some secondary effects at the physiological, biochemical, and molecular level such as reduced cell expansion, receded membrane function, impaired cytosolic metabolism and increased reactive oxygen species (ROS) production (Mushtaq et al. 2020). Like other stress responses, modulation of enzymatic activities is found under salt stress conditions as proved by the enhanced activities of the antioxidative enzymes like superoxide dismutase, peroxidase, and catalase, as well as of phenylalanine ammonia-lyase and tryptophan decarboxylase (Gao et al. 2008; Mishra et al. 2013). It is assumed that global warming due to anthropogenic emission of CO2 would worsen the problem of salt stress and desertification (Lavania et al. 2015). In the presence of excess CO2, the inflated electrons generated can react with O2, resulting in the formation of detrimental ROS, that causes photoinhibition. The overproduction of ROS ultimately promotes the loss of cellular integrity by imposing pernicious effects on cell membranes and other cell organelles (mitochondria, chloroplasts, and peroxisomes) and major biomolecules like proteins and lipids (Mittler 2002; Ahmad et al. 2008). Over the last few decades excessive increase of atmospheric CO2 and CH4, chlorofluorocarbons and nitrous oxides concentration has triggered negative consequences to global warming. As a result, heat stress has become the primary limiting factor) for crop production and food security worldwide (Friedlingstein et al. 2010; Lobell et al. 2011; Abdelrahman et al. 2017; Hassan et al. 2020). It has been presumed that heat stress has reduced wheat (Triticum aestivum L.) global productivity by more than 6% per degree Celsius rise in temperature (Asseng et  al. 2015). Although heat stress has some positive impacts on productivity in colder climatic regions (Challinor et al. 2014), it can severely affect different aspects of plant physiology including seed germination, growth, development, photosynthesis and reproduction which ultimately affect total productivity (Hasanuzzaman et al. 2012). Heat stress induces poor seed germination by perturbing the activity of starch digesting enzymes and abscisic acid (ABA) synthesizing enzymes (Essamine et al. 2010) as well as by impairing protein synthesis in seed embryo (Riley 1981). As reported by Akman (2009), the growth of coleoptile was found to stop completely at temperatures above 37 °C. Stunted growth, reduced tiller and dry biomass production were observed in wheat and sugarcane due to heat stress (Mitra and Bhatia 2008; Srivastava et  al. 2012). Additionally, heat stress results in various morphological abnormalities such as leaf scorching, sun burning of stems, branches, leaves and twigs, leaf rolling, damage of leaf tips, discoloration of fruits, leaf senescence and abscission (Rodríguez et al. 2005; Omae et al. 2012). Plant growth is hindered due to a reduction in nutrient and water uptake at high temperature (Huang et al. 2012) and restriction of nutrient transport from root to shoot (Huang et al. 2008). The most eminent process in plant physiology, the photosynthesis, is greatly impeded by high

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temperature. Heat stress promotes abated water content in leaf, compromised stomatal conductance as well as inter-cellular CO2 concentration (Greer and Weedon 2012). Crucial enzymatic activities related to the photosynthetic process (such as phosphate synthase, ADP-glucose pyrophosphorylase, and invertase) are also curtailed by high temperature leading to reduction of starch production (Djanaguiraman et al. 2009). Heavy metal (HM) stress is another important abiotic stress in plants that mostly stemmed from anthropogenic processes due to immoderate use of fertilizers, pesticides combined with sewage irrigation, and solid waste from mines, industries, urban activities and agricultural practices (Sharma et al. 2014). Some HMs such as cadmium, lead, chromium, arsenic, mercury, etc. are non-essential elements and do not have any biological role (Chetia et al. 2011). Coupled with essential materials (water, nutrients, minerals) needed for their growth, plants take up non-essential HMs from soil and groundwater through their roots and survive by mitigating the toxic effects through diverse detoxification mechanisms within their system (Singer 2006; Chatterjee et al. 2013). Metal toxicity in organisms is imparted through oxidative stress by the production of excessive free radicals or ROS and intruding the function of essential cellular enzymes (especially in the case of metalloenzymes) (Prasad and Freitas 2003). Plant root rhizosphere plays a significant role in developing metal tolerance, where, soil microflora in the rhizospheric region have the ability to get rid of several contaminants along with HMs from the surroundings by a range of enzymatic processes (Mitra et al. 2017b). Phytotoxicity elicited by different metals triggers a wide range of physiological and metabolic modulations (Villiers et al. 2011). The visible toxic responses of plants induced by different HMs include reduced plant growth, leaf chlorosis, necrosis, turgor loss, poor rate of seed germination, and deformed photosynthetic apparatus, often correlated with progressing senescence processes or with the plant death (Dalcorso et al. 2010). Combined biotic stresses are very common in plants. For example, brown apical necrosis of Juglans regia caused by combined biotic stress from simultaneous attacks by bacterial (Xanthomonas arboricola) and fungal (Fusarium spp., Alternaria spp., Cladosporium spp., Colletotrichum spp., or Phomopsis spp.) pathogens (Belisario et al. 2002). Primarily fungi, bacteria, nematodes and viruses are disease-causing pathogens. Two types of fungal parasites are known viz. nectrotrophs that kill host cells by releasing toxins, and biotrophs that along with bacteria cause vascular wilts, leaf spots and cankers among other symptoms, and can spread the infection to different parts of the plant body (Gimenez et al. 2018). Nematodes consume the plant cells content and plant-parasitic nematodes are responsible for soil-borne diseases and attack plants’ root system. Nematode infection results in nutrient deficiency, wilting or stunting in plants. Viruses cause local lesions and systemic damage that ultimately lead to stunting, chlorosis and malformations affecting different parts of the plant. On the other hand, insects and mites damage plants through feeding or egg-laying or as vectors for transmitting pathogens (Schumann and D’Arcy 2006). Plants exposed to different abiotic and biotic stresses are schematically represented in Fig. 1.1.

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ABIOTIC Reduced chlorophyll content Enhanced transpiration Reduced photosynthesis

BIOTIC

Drought

Virus

Salinity

Bacteria

Heat

Fungus

Cold

ROS generation Leaf senescence

STRESS IN PLANTS

Heavy metals

Nematodes

Plant growth reduction Reduced photosynthesis ROS generation

Insects Herbivores

Decreased CO2 fixation Seed germination reduction

Reduced plant biomass Disease susceptibility

Fig. 1.1  Impact of different abiotic (drought, salinity, heat, cold, heavy metals) and biotic (pathogen, insect pest, herbivores) stresses in plant physiology

1.3  P  lant Responses Against Multiple Stressors to Develop Tolerance The intricate interplay between abiotic and biotic stresses induces complex counter-­ responses to different stressors in plants for protecting them from multiple aggressors (Pastori and Foyer 2002; Rasmussen et  al. 2013). These responses may be through synthesizing secondary metabolites (e.g., alkaloids, terpenoids etc), phytohormones, changes in ion influx, inducing an antioxidative system for combating the stresses by triggering metabolic reprogramming towards defense (Yasuda et al. 2008; Bartoli et al. 2013). The common regulatory pathway under biotic stress and abiotic stress responses of plants are represented in Fig. 1.2.

1.4  A  cclimation and Adaptation Against Multiple Stressors Through Different Signalling Pathways 1.4.1  Redox Signalling A rapid outburst of reactive oxygen species is generally found following different stress exposure in plants triggering oxidative stress (Wojtaszek 1997; Foyer and Noctor 2013). Although ROS are fatal for organisms, the ROS generation is delicately balanced in plants to escape tissue damage for regulating the plant’s stress responses (Mori and Schroeder 2004; Choudhury et al. 2013). In plants, low levels of ROS have an important role in cell signalling (acting as second messengers)

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STRESS IN PLANTS

ABIOTIC

BIOTIC

Membrane receptor(s)

Plasma membrane

Signal transduction

NADPH oxidase/Rboh

Ca2+

ROS

Ca regulated proteins

MAPK

Antioxidant systems

Hormones

Stress response Gene expression

Physiological response

Stress tolerance Fig. 1.2  The common signalling pathway under biotic stress and abiotic stress in plants to develop tolerance. Stress-induced ROS generation triggers the activation of the MAPK signalling pathway, phytohormone release and activation of the antioxidant system which in turn alters the gene expression and physiological responses for developing tolerance in plants. (Modified from Wang et al. 2016)

regulating plant stress responses, while high levels are deleterious to the plants (Garg and Manchanda 2009). Abiotic stresses promote ROS production through disbalancing the electron transfer reactions in plants (Gill and Tuteja 2010; Mitra et  al. 2017a) while under biotic stress, membrane-bound NADPH oxidases (and NADPH oxidase-like also called respiratory burst oxidase homologs, RBOHs) or peroxidases intentionally induce ROS generation to kill or restrict the pathogen propagation through hypersensitive response (HR) (Zurbriggen et al. 2010). ROS play a significant role in cell signalling under biotic stress. For example, ROS help to increase the drought tolerance in Arabidopsis thaliana by inducing de novo xylem formation to enhance water flow when infected with the vascular pathogen Verticillium spp. (Xia et al. 2009). A crucial role is played by ROS to develop cross-­ tolerance in plants to combat abiotic and biotic stresses, especially through ABA signalling pathway. In Arabidopsis, NADPH oxidase in guard cell, induces AtrbohD and AtrbohF genes mediating ROS generation leading to ABA-mediated stomatal

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closure, cytosolic upsurge of Ca2+ ion, and HR to pathogen attack (Ichimura et al. 2000; Chinchilla et al. 2007). Another redox signalling mechanism embraces oxidation of glutathione (GSH) pool in association with the rise in total GSH under abiotic stresses, which is considered as one of the key players in H2O2-induced heavy metal tolerance (Chandrakar et al. 2016b). In plants, an upsurge of GSH following heavy metal exposure thereby reduces the negative impacts of oxidative damage.

1.4.2  MAP Kinase Pathway Mitogen-activated protein kinases (MAPKs), which is highly conserved in the eukaryotic system and mediate signal transduction in several cellular processes, are known to be involved in different biotic/abiotic or combined stress responses (Samajova et al. 2013; Rejeb et al. 2014; Ramegowda et al. 2020). In response to heavy metal stress, released ROS play a vital role in activating the MAPK signalling pathway (Chandrakar et  al. 2020). Two leading MAPK cascades (MEKK1-­ MKK4/5-MPK3/6 and MEKK1-MKK2-MPK4/6) involved in both abiotic and biotic stress signaling have been noticed to control the levels of ROS in A. thaliana (Pitzschke et  al. 2009; Jalmi and Sinha 2015). In Arabidopsis, GbRLK gene (receptor-­like kinase from Gossypium barbadense) was shown to downregulate the stress-responsive genes to combat against salinity and drought by reducing water loss and thus enhancing tolerance (Zhao et al. 2013). Salicylic acid (SA) mediated activation of MAPK pathways following pathogen attack in plants and consequent expression of PR genes for defense reactions has been reported (Xiong et al. 2003). Likewise, protein kinases activated by salicylic acid during salt stress confers osmotic tolerance in Arabidopsis (Feng et  al. 2015). Studies by Chinchilla et  al. (2007) reported that pathogen-associated molecular patterns (PAMPs) like flagellin stir up MAPK cascades to initiate pathogen response signalling. MAPK signalling synergistically interacts with ROS mediated and ABA signalling pathways to boost up plant defense and to produce cross-acclimation to both abiotic and biotic stress (Lu et al. 2002; Miura and Tada 2014; Zhou et al. 2014). In rice, MAPKs (known as OsMPK5) are overexpressed to develop the ABA-mediated resistance against the necrotrophic brown spot pathogen Cochliobolus miyabeanus and abiotic stress tolerance (De Vleesschauwer et  al. 2010). In plants, heavy metal (Cd, Cu, and As) induced activation of MAPKs has been reported by several scientists (Jaspers and Kangasjarvi 2010; Karuppanapandian et  al. 2011; Kreslavski et  al. 2012; Baxter et  al. 2014). In O. sativa an increased number of transcripts of OsMSRMK2 (OsMPK3 homolog), OsMSRMK3 (OsMPK7 homolog), and OsWJUMK1 (OsMPK20–4 homolog) under Cu and Cd exposures has been observed (Yeh et al. 2007; Rao et al. 2011).

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1.4.3  R  ole of Phytohormones and Growth Regulators in Stress Signalling Pathway Plant hormones are known to play important roles in developing tolerance to a range of biotic and abiotic stress in addition to regulating all phases of plant growth and development (Davies 2010; Ramegowda et al. 2020). The specific phytohormones such as (ABA, SA, jasmonic acid (JA), and ethylene (ET) form the baseline pathway that triggers signalling cascade after perceiving the abiotic and biotic stresses (Verma et al. 2016). ABA is the multifunctional phytohormone involved in different stages of the life cycle in plants and also in the perception of abiotic stress and adverse environmental situation (Bücker-Neto et al. 2017; Sytar et al. 2018). ABA interacts synergistically and antagonistically at different levels regulating both biotic and abiotic stress responses (Fujita et al. 2006). ABA signalling pathway is mediated by ABA receptors namely PYR/PYL/RCAR (pyrabactin resistance 1/PYR1-like regulatory component), phosphatase 2Cs (PP2Cs), and Snf1-related kinases 2 (Klingler et  al. 2010). Under Cu and Zn stress, three genes namely PYL, PP2C, and SnRK2 are responsible for ABA signal transduction during seed germination in C. sativus (Wang et al. 2014). In O. sativa Cd and Cu exposure boosted MAPK signalling and ABA level providing increased Cd and Cu tolerance (Yeh et  al. 2003, 2004). Similarly, an increased amount of ABA was detected in Empetrum nigrum and Cicer arietinum, following exposure to Cu and Pb (Monni et al. 2001; Atici et al. 2005). As a secondary effect, increased synthesis of ABA under abiotic stresses triggers the stomatal closure, that prevents the invasion of pathogens through these passive ports (Melotto et  al. 2006). Hence, in such circumstances plant develops cross-tolerance against both biotic and abiotic stresses (Lim et  al. 2015; Berens et al. 2017). Some plants can regulate the pathogen entry by stomatal movement after detecting microbe-associated molecular patterns (MAMPs) such as flagellin and chitin (Zeng and Hey 2010). For example, In Arabidopsis, tomato and moss (Physcomitrella patens), MAMP-triggered stomatal closure was found to be regulated by ABA (Melotto et al. 2017). SA promotes the development of the systemic acquired resistance (SAR) and regulation of plant defense responses against biotrophic and hemibiotrophic pathogens, while JA and ET mainly control the defense responses against necrotrophic pathogens and insect pest and herbivores attack (Dong 1998). In plants, synthesis of SA is induced in response to pathogen attack and SA signalling is initiated involving its receptors and regulators NPR1 (non-expressor of PR-genes 1), and NPR3 and NPR4 to protect the undamaged part of the plants distant from the site of pathogen attack (broad-spectrum plant defense called SAR) (Dong 1998). Additionally, SA is known to protect the plants against a variety of abiotic stresses like heavy metals, extreme temperature, salinity, osmotic stress, drought, ozone, and

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UV-irradiation (Zhang et al. 2015; Nazar et al. 2015; Naser et al. 2014; Khan et al. 2013). For example, in O. sativa and G. max, following exposure to arsenic (As), the metalloid-exerted oxidative injury is effectively reduced via strengthening the antioxidant defense mechanism (Singh et al. 2015; Chandrakar et al. 2016a). During heavy metal stress, SA reduces the contents of ROS, osmolytes/ionsleakage, and lipid peroxidation reaction, while it augments the total chlorophyll content, total lipids, and linolenic acid (Chandrakar et al. 2020). The JA signalling is mediated by its receptor (COI1, a F-box protein) and co-­ ordination of a number of transcription factors [such as Jasmonate Insensitive 1 (JIN1)/MYC2] and ethylene response factor ERF1, ERF2, ERF5, and ERF6 (members of AP2/ERF family)] regulating the JA responsive marker gene plant defensin 1.2 (Deshaies 1999; Moffat et  al. 2012). Like other phytohormones, JA is also responsible for plant defense against abiotic stress such as salinity, drought, high or low temperature, heavy metals, ozone, and UV-irradiation (Yan et al. 2015; Hu et al. 2017; Per et al. 2018). Ethylene, a gaseous hormone that plays vital role in fruit ripening and senescence, is also involved in biotic stress response against necrotrophic, biotrophic, and hemibiotrophic pathogens (Ramegowda et al. 2020). The role of ET in developing resistance in plants against abiotic stress such as cold and freezing, salinity, drought, heavy metal exposure, heat, and flooding has been studied in detail (Kazan 2015). ET signalling is mediated through different ethylene receptors such as ETR1, ETR2, Ethylene Response Sensor 1 (ERS1) and ERS2. These receptors activate a membrane protein Ethylene Insensitive 2 (EIN2). Downstream to the EIN2 are transcription factor EIN3 and Ethylene Insensitive 3-Like 1 (EIL1) in the nucleus triggering the activation of ET responsive genes (Yang et  al. 2015). ET acts synergistically with SA, JA, and ABA in the plant’s defense against pathogens (Ramegowda et al. 2020). Several authors reported the upsurge in the number of transcripts of ethylene biosynthesis-related genes (ACS1, ACS2, ACO4, and ACO5) in the roots of O. sativa exposed to Cr, suggesting their involvement in developing Cr resistance (Steffens 2014; Trinh et al. 2014). Likewise, Cd stress in A. thaliana was found to induce the ethylene biosynthesis through upregulation of ACS2 and ACS6 genes (Schellingen et al. 2014). Auxin (indole-3-acetic acid, IAA) is an essential phytohormone having manifold activities in regulating the growth and development of plants exposed to various abiotic stresses (Sytar et al. 2018). Srivastava et al. (2013) observed the unaffected growth of B. juncea under As stress if IAA applied exogenously. A similar report of the exogenous application of an IAA precursor, L-tryptophan in the O. sativa radicles shows improved growth and yield under Cd stress in comparison to seedlings raised without IAA precursor in Cd-contaminated soil (Farooq et al. 2015a, b).

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1.5  Tolerance to Heavy Metals 1.5.1  Synthesis of Metal Chelators One of the sophisticated strategies against metal stress employed by plants is through chelation and sequestration of metals by high-affinity metal binding ligands such as phytochelatins (PCs) and metallothioneins (MTs). PC synthesis is stimulated by a wide range of metal cations (such as Cd, Cu, Zn, Ag, Au, Pb, Hg) and anions (As) due to transpeptidation of (γ-glutamyl-cysteinyl)-glycine from GSH by the action of PC synthase (PCS) (Gasic and Korban 2007). A number of studies have suggested that PC–metal complexes are sequestered into vacuoles (Shukla et al. 2016). Metallothioneins are low molecular weight Cys-rich peptides present in both animals and plants. They are capable of high-affinity binding with heavy metal ions via Cys residues and play a significant role in essential heavy-metal homeostasis in plants (Sharma et al. 2014). MTs play a vital role in carrying out a series of activities such as sequestration of toxic metals, transportation of Zn and Cu, precluding interaction of toxic metals with other biomolecules, thereby reducing phytotoxicity (Shukla et al. 2016).

1.5.2  Secretion of Organic Acids in Root Exudates Plants grown in heavy metal contaminated soil secrete organic acids (such as oxalic acid, citric acid, malic acid, tartaric acid and succinic acid) in root exudates for chelating metals to reduce the bioavailability of such toxic metals (Yu et al. 2019). Carboxyl groups present in the organic acids chelate with heavy metals to convert them into non-toxic immobilized form. For example, organic acids in the root exudates of Phyllostachys pubescenswas was found to precipitate lead and reduce Pb availability to plant (Chen et  al. 2016). A significant increase in the secretion of organic acids (about 1.76–2.43 times) in the roots of cadmium-accumulator rice was observed in comparison to Cd-sensitive varieties (Fu et al. 2017).

1.6  Tolerance to Heat Stress Heat tolerance in plants varies among species and different short term and long-­ term strategies are adopted by plants to survive under heat stress. The major pathways include ion transport, abundance of late embryogenesis proteins, presence of osmo-protectants, and antioxidant defense system (Rodríguez et  al. 2005). Short term mechanisms of heat tolerance in plants are avoidance and acclimation as well as some morphological adaptation such as leaf rolling, small size leaves or

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alteration in leaf position and lipid composition in the membrane, and cooling through transpiration (Fitter and Hay 2002; Sarieva et al. 2010). Long term morphological changes in response to heat stress include increased density of leaf stomata and hair, and larger vessels (Srivastava et al. 2012). Plants are highly susceptible to a higher temperature during the active growth stages. When exposed to high temperature, plants are capable of reducing the rate of light absorption through small hairs on the leaf blade that act as protective surface cover. Some types of low molecular weight compounds called osmolytes are found to accumulate in plant tissue to develop heat tolerance and increase survival by conserving the cell structure (Hare et al. 1998; Sakamoto and Murata 2002). Different osmolytes such as sugars, proline, ammonium, sulphonium and glycine-betaine compounds are synthesized under heat stress (Sairam and Tyagi 2004). However, osmolyte concentration varies among species and genotypes (Ashraf and Foolad 2007). Similarly, plants also accumulate several secondary metabolites to combat heat stress (different phenolic compounds, such as flavonoids and phenylpropanoids).

1.7  Tolerance to Salt Stress Regulation of ion homeostasis within the cell is important for the maintenance of membrane potential and proper functioning of the enzymes involved in the metabolic reaction under abiotic stresses (Hasegawa 2013). Plants can efflux the redundant salt ions from cytosol through transporters (H+-ATPase, vacuolar H+-ATPase, H+-Pyrophosphate, and Ca2+-ATPase) to retain low concentration of Na+ ions within cytosol as high concentrations are deleterious for cell (Farooq et al. 2015a, b). The signalling pathway coordinating the activities of several transporters under salt stress is the ‘salt overly sensitive’ (SOS) stress signalling pathway that involves three proteins, SOS1, SOS2, and SOS3 (a Ca2+ ion binding protein and sensor for calcium signal) (Zhu 2003).

1.8  Plant Immune Response Against Biotic Stress To deal with biotic stresses plants have evolved a well responsive immune system (Gimenez et al. 2018). Passive immunity is the first line of defense in plants which is endorsed by waxy leaf or stem surface, thick cuticles and specialized trichomes to prevent insects or pathogens. Plants also release chemical compounds (secondary metabolites such as phenolics, alkaloids, flavonoids, terpenoids) to safeguard themselves against herbivory and pathogen infection (Taiz and Zeiger 2006). Further, plants possess two levels of pathogen recognition system to trigger immune responses: the first level of recognition involves Pattern Recognition Receptors (PRRs) that recognize pathogen-associated molecular patterns (PAMPs) as described in the previous section, activating PAMP-triggered immunity (PTI)

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(Monaghan and Zipfel 2012). In the second level of plant immune response known as effector-triggered immunity (ETI), the key player is a plant resistance protein (PRP), that recognizes specific effectors from pathogens or pests (Avr proteins) and invigorates plant defense mechanisms in a much more specific way (Kaloshian 2004; Spoel and Dong 2012). ETI actually triggers the hypersensitive responses (HR) that consequences to programmed cell death of the infected cells and the surrounding areas (Mur et al. 2007).

1.9  Antioxidant Defense System Under different abiotic stresses, excess ROS are produced in plants causing oxidative stress. Plants recruit antioxidant system to protect cellular and subcellular compartments from this fatal impact using antioxidant enzymes as well as non-enzymatic compounds.

1.9.1  Enzymatic Antioxidative System The role of different enzymes acting as ROS scavengers such as superoxide dismutase (SOD), glutathione peroxidase (GPX), glutathione reductase (GR), ascorbate peroxidase (APX), and catalase (CAT) to protect cells from the toxic effects of ROS under both abiotic and biotic stresses have been well studied (Samajova et al. 2013). SODs are members of the metalloenzyme family that safeguards the cells from oxidative stress by catalyzing the dismutation of superoxide radicals (O2•−) to H2O2 with the aid of diverse metals as cofactors (Li et al. 2017). Hydrogen peroxide is another highly reactive oxidizing agent later detoxified by CAT and the ascorbate– glutathione cycle, both of which regulate H2O2 level (Shigeoka et  al. 2002). The tetrameric, heme-containing enzyme CAT is a H2O2 scavenger, located exclusively in peroxisomes (Mitra et  al. 2018), which rapidly degrades H2O2 into water and molecular oxygen without consuming cellular reducing equivalents (Sharma 2012). The presence of a heme prosthetic group has been reported with CAT.  APX, an active scavenger of the H2O2, are members of class I heme-peroxidases found as different subcellular isoforms catalysing the reduction of H2O2 into water and two molecules of monodehydroascorbate (Anjum et al. 2016). GR, which functions in coordination with APX and is broadly located in diverse cell organelles, mediates the reduction of glutathione disulphide (GSSG) to glutathione (GSH) (using NADPH as an electron donor) and sustains a highly reduced state of GSH/GSSG and ascorbate/monodehydroascorbate and thus preserves the redox intracellular level as well during oxidative stress (Anjum et al. 2012). GPX, another member of a large peroxidase family having a broad substrate spectrum, catalyses the reduction of H2O2, organic and lipid hydroperoxides using the GSH pool directly as a

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reducing agent, thereby protecting the cells against oxidative damage (Anjum et al. 2010).

1.9.2  Non-enzymatic Antioxidative System Plants have a well-developed antioxidative system for combating the adverse environmental stresses by producing low molecular weight thiols, such as GSH, that plays a role in biosynthetic pathways, ROS detoxification of xenobiotics and antioxidant chemistry (Mitra et al. 2018). GSH is a nonprotein thiol synthesized from glutamate (Glu), cysteine (Cys) and glycine (Gly) by two adenosine triphosphate (ATP)-dependent reactions catalysed by gamma-glutamylcysteine synthetase (γ– ECS) and glutathione synthetase (GS). The accumulation of glutathione was observed in different plants exposed to various stresses such as salinity, drought, extreme temperatures (cold and heat), heavy metal toxicity, herbicides and air pollutants (Waśkiewicz et al. 2014). Ascorbate (AsA), synthesized in mitochondria but commonly found in the stroma of chloroplast, apoplast, cytosol, mitochondria and peroxisomes of the plant cell, is the most copious antioxidant in plants, which reacts with a range of ROS such as H2O2, O2•− and singlet oxygen (1O2). Ascorbate is the most substantial reducing substrate for the discharge of H2O2 via the ascorbate-glutathione cycle (Singh et  al. 2006) and restoration of membrane-bound carotenoids and α-tocopherol in plant cells (Sharma 2012). Exogenous application of AsA was found to be effective in alleviating the adverse effects of different abiotic stresses such as salinity, drought by enhancing chlorophyll, carotenoids, proline accumulation, and leaf area, improving water status and soluble protein while decreasing H2O2 levels in plant tissue (Akram et al. 2017).

1.10  Conclusion and Future Prospects Plants are exposed to a variety of stresses including abiotic and biotic stresses throughout their lifetime and accumulate low-molecular-weight organic compounds, compatible solutes or osmolytes, stress-specific proteins, heat-shock proteins, phytochelatins, metallothioneins, and activate many detoxification enzymes to acclimatize under a stressful situation. The thresholds of stress tolerance vary from species to species, and a few of them can successfully thrive under severe stresses completing their life cycles. However, most of the cultivated crop species are highly vulnerable and either dies or becomes less productive after being exposed to long periods of stress. Thus, knowledge about the enhancement of stress tolerance in plants not only presents a challenging basic research problem but could also have a significant impact on the benefit of agricultural productivity. Recent researches are gaining insight into the different signalling pathways/genes that

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regulate the plants response to abiotic and biotic stress and are directly or indirectly associated with multiple stress responses. These association may be synergistic or antagonistic in action leading to developing cross-tolerance. Furthermore, the integration of multiple omics (such as transcriptomics, proteomics or metabolomics) technologies will be very helpful to find a broad and precise view about the regulatory hubs in developing stress tolerance in plants in the near future.

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Chapter 2

Insights into Role of Invisible Partners in Plant Growth and Development Revuru Bharadwaj, Sarma Rajeev Kumar, and Ramalingam Sathishkumar

Abstract  Soil hosts a diverse array of microorganisms like bacteria, fungi, and protozoa, among others. These microbes frequently associate with plants and interaction occurs with the environment in a unique way as a holobiome (the host genome and associated microbiome). Plant associated symbiotic microbes often augment the host with an extra layer of complex complementary functions that increase host cell plasticity and plant fitness not only under normal conditions but even during the adverse and challenging environment. Advancement in functional genomics, proteomics and metabolomics helped to understand the molecular and biochemical events during plant-microbe interaction to a larger extent. The scope of this review encompasses the recent developments in the field of plant-microbe interaction with a focus on the positive role of beneficial microbes in improving plant growth and development. In addition, the role of endophytes and their ability to modulate the biosynthesis of secondary metabolites in plants are discussed. We conclude the chapter by proposing future application with special reference to basic and applied research related to the use of beneficial microbes in sustainable crop production and its utility for varied applications. Keywords  Abiotic stress · Bioactive metabolites · Endophytes · Holobiome · Pathogen resistance · Plant endophyte interactions · Plant metabolism

R. Bharadwaj · S. R. Kumar · R. Sathishkumar (*) Department of Biotechnology, Plant Genetic Engineering Laboratory, Bharathiar University, Coimbatore, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_2

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2.1  Introduction Possibly, all plant species have associations with microbial communities. Surprisingly, the number of microbial cells living on and within plant tissues outnumbers host cells. These communities of microbes are termed as 2nd genome of the plant, (Berendsen et al. 2012), one such group of microbes residing inside the tissues of the host plant are called endophytes. The term endophyte was first introduced by de Bary (1866) and it is attributed to any organism that grows within plant tissues. However, lately, it is more precisely redefined in terms of their types (fungal or bacterial) and relationships (obligate or facultative) with the host plant. Generally, endophytes can be found colonizing aerial parts or roots, mostly remain asymptomatic and does not show any noticeable damage to the host. Recent studies show that host plants’ survival and fitness are very much dependent upon endophytes (Hardoim et  al. 2015; Potshangbam et  al. 2017). The association between plant and endophytes has evolved more than 60 million years ago (Sprent 2008). Since the beginning, host-endophyte interaction has played an inevitable role in land ecosystems providing benefits for both partners associated. It is believed that endophytes have originated from the microbes present in the rhizosphere or seed-borne microbial communities. However, the functional genomic and transcriptomic analysis revealed that endophytes are highly versatile and harbor several genes with novel traits that are beneficial to the host plant. There are several examples describing the importance of plant- endophyte interactions. For example, in the rhizobia-legume symbiosis, one of the best-­characterized endophytic relationships, the bacterial partner governs host requirement for nitrogen and thus helps in fixing atmospheric nitrogen (Santoyo et al. 2016). Another classical example is the production of hormones by plants and their associated endophytic community. Abscisic acid (ABA) biosynthesis and ABA-mediated signaling pathways are activated by the presence of endophytes and activation of phytohormone signaling subsequently contribute to the plant growth enhancement under unfavorable conditions (Ilangumaran and Smith 2017). Endophytic phyto-­ augmentation is another example of exploiting endophytic microbial communities for cleaning up heavy and toxic metals. This technology relies on augmenting the phytoremediation capacity of plants with exogenous microbial strains to trigger associated plant-microbe interactions, thereby facilitating and improving remediation efficiency (Redfern and Gunsch 2016). There are several reports of the endophytic microbial community in improving plant metabolites and defense response (Khare et al. 2018). Interestingly, plant-microbe symbiotic interactions have huge potential to reduce the use of chemical fertilizers in agriculture and designer endophytes have emerged as a central pillar of sustainable agriculture worldwide in the recent decade. In this chapter, novel insights into plant-endophyte interaction are discussed. The influence of endophyte on improving plant primary/secondary metabolites and stress tolerance will be also discussed. Finally, the importance of these associations in sustainable agriculture will be explored.

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2.2  Novel Insights in Plant-Microbiome Research In the past few decades, researchers were successful worldwide in elucidating the plant growth promoting properties of endophytes. Furthermore, it is well established that endophytes help plants in many physiological/metabolic functions. However, few gaps and unsolved questions still persist about molecular-level interaction of the plant with its endophyte partner. In order to answer these questions, researchers attempted to use the latest molecular approaches for elucidating underlying genetic cascades of the plant-endophyte partnership (Wang et  al. 2018). Yi et al. (2018) used CRISPR-Cas9 based genome editing to identify petropectin and bacillibactin mutants of the rhizospheric bacteria Bacillus mycoides which are incapable of colonizing the Brassica rapa roots and failed to increase plant biomass and chlorophyll content. This could be attributed to the fact that petropectin and bacillibactin are essential for B. mycoides to colonize the host tissues (Yi et al. 2018). Similarly, disruption of mitogen activated protein kinase (MAPKK) gene in Phomopsis liquidambaris (PmkkA) resulted in a severe reduction in growth and upregulation of defense responses in rice. PmkkA is essential to trigger a downstream signaling cascade in endophyte and host tissues for establishing mutual interaction (Huang et  al. 2020). On other hand, CRISPR based technology was implemented to study key virulence genes of plant pathogens responsible for causing diseases. For instance, knock out of cysteine protease inhibitor gene (PpalEPIC8) from Phytophthora palmivora increased susceptibility towards papain, a cysteine protease secreted by papaya plants (Gumtow et al. 2018). Similarly, promoter editing of pathogen avirulence (Avr) effector gene, PsAvr3b in soybean root pathogen Phytophthora sojae increased the colonization in host roots. Lower expression level in mutant of PsAvr3b successfully colonized soya bean roots suggesting that Avr gene is responsible for eliciting defense responses in the host (Ochala et al. 2019). RNA interference (RNAi) technology is being used widely to understand the gene function by exploiting innate regulatory mechanism and this technique is also implemented in studying plant-microbe interactions. Disruption of endo-β-1,4-­ glucanase gene of cellulose biosynthesis in Populus increased mycorrhiza colonization which in turn improved plant growth and metabolism (Kalluri et  al. 2016). Rech et al. (2013) elucidated the function of kunitz protease inhibitor and serine carboxypeptidase of Medicago truncatula during arbuscular mycorrhiza symbiosis. These two proteins are induced and differentially expressed during mycorrhiza colonization and RNAi mediated functional disruption of these genes resulted in the abnormal arbuscular formation in host tissues (Rech et al. 2013). In another report, to elucidate the activity of mycorrhiza induced small secreted proteins (MiSSPs) in effective colonization of host, MiSSP8 gene function was disrupted using RNAi in Laccaria bicolor. The disruption of MiSSP8 activity impaired the colonization of the host by L. bicolor and the resulting phenotype lacked the formation of the fungal mantle and Hartig network formation (Pellegrin et al. 2019). Disruption of MtMSBP1, an early transcriptional regulator of mycorrhiza symbiosis activity in M. truncatula, leads to aberrant hyphae network formation and

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resulted in thick and septate appressoria of Glomus intraradices (Kuhn et al. 2010). Erysiphe pisi is an obligate pathogen causing powdery mildew disease in pea plants and through RNAi based method, it was established that haustoria of E. pisi secreted effector proteins responsible for causing disease symptoms in pea leaves. Further, foliar application of double- stranded (ds) RNA developed through RNAi reduced disease incidence in plants (Sharma et al. 2019). Recently, Meng et al. (2018) identified sorbitol responsive NUCLEOTIDE BINDING/LEUCINE-RICH REPEAT (MdNLR16) in apple which is responsible for increasing resistance against Alternaria alternata infections. RNAi suppression of MdNLR16 increased susceptibility towards A. alternata and interestingly, exogenous application of sorbitol decreased disease symptoms (Meng et al. 2018). Micro RNAs (miRNAs) and small interfering RNAs (siRNAs) are also known to play a significant role in establishing plant-microbe interactions. For instance, miR171 was differentially expressed in the epidermal and cortical cells of Lotus japonicas and assisted Mesorhizobium to successfully colonize roots for forming nodules (Holt et al. 2015). In accordance, ectopic expression of miR172 in soybean roots improved nodule formation, further increasing leghamoglobin content and nitrogenase activity in nodules (Yan et al. 2013). Inoculation of Rhizophagus and L. bicolor mycorrhiza fungi in Populus sp revealed differential expression of several miRNAs possessing gene targets involved in primary and secondary metabolism (Mewalal et  al. 2019). In another report, arbuscular mycorrhiza inoculation in M. truncatula and Nicotiana tabacum improved the expression of miR399 involved in phosphate induced stress response, and the interaction resulted in improved accumulation of phosphate in the roots (Branscheid et al. 2010). Gu et al. (2010) analyzed the expression levels of miRNAs during plant-mycorrhiza interactions upon phosphate stress. Few miRNAs were differentially regulated in roots (miR158, miR862-3p) and leaves (miR395, miR779.1, miR840, miR867). However, their specific function in the plant system is not yet known (Gu et al. 2010). Inoculation of Azorhizobium caulinodans in wheat resulted in the temporal expression of few miRNAs in the plant system. It was observed that miR167 (involved in lateral root growth) and miR393 (upregulated during pathogen attack and positive role in root development) were expressed in roots, whereas miR171 (downregulated during nitrogen deficiency) expression was higher in shoots. In addition, these miRNAs could be involved in plant growth and primary metabolism (Qui et al. 2017). Infection of maize with Herbaspirillum and Azospirillum induced the expression of miR397, miR398, miR408, and miR428. These miRNAs have a role in maintaining copper homeostasis and resulted in impaired defense responses which facilitated the colonization of diazotrophic bacteria (Thiebaut et al. 2014). Piriformospora indica facilitated rice growth during salinity stress by differential regulation of several miRNAs and their targets were sodium, potassium ion transporters, auxin-responsive genes and plant growth regulators (Kord et al. 2019). The use of synthetic bacterial communities (syncom) is emerging as a novel approach to understand the missing links in plant-microbe interactions (Vorholt et  al. 2017). Syncoms are produced by mixing the selected strains in respective volume and applying them to the plant. This novel approach aided in understanding the

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interaction of consortia with the host and their influence on plant system in a microenvironment (Vorholt et al. 2017). Later, engineering the specific bacterial communities can be used to study the interactions between species and community dynamics in various environments like terrestrial and aquatic, to name a few. (Sheth et al. 2016). Herrera Pardes et al. (2018) stated that the application of specific bacterial communities can modify the phosphate accumulation during phosphate stress in plants. Moreover introduction of selected communities can alter the host phenotype in complex systems (Herrera Pardes et al. 2018). Similarly, NRT1.1b (a rice nitrate transporter) is responsible for the selected recruitment of root bacterial communities in rice. Furthermore, re-inoculation of root bacteria as syncoms improved plant growth when organic nitrogen was supplied as nitrogen source (Zhang et al. 2019). So far, the plant-endophyte partnership is well studied to understand endophyte impact on plant growth; however, to completely understand initial communication between partners and underlying molecular cues, more research is required. High-­ end molecular biology tools and engineered microbes will be highly useful to decode the unanswered questions in upcoming years.

2.3  I nfluence of Endophytes on Plant Primary Growth and Secondary Metabolism Endophytes are typical plant dwelling microorganisms residing in host tissues without causing visible symptoms. Due to their continuous interaction with the host, endophytes can positively influence the host’s metabolism. In turn, plants get benefited from the endophytes in several ways like improved photosynthetic activity, nutrient assimilation, suppressing pathogen infections and upregulating secondary metabolism (Deng et al. 2020; Paul et al. 2020; Wang et al. 2020). For instance, non-symbiotic endophyte bacteria like Bacillus sp., and Streptomyces sp., isolated from Sphaerophysa salsula (commonly known as alkali swainsonpea) improved shoot fresh weight, chlorophyll content and nodule formation when inoculated along with rhizobia Mesorhizobium sp, grown under N-free culture conditions (Deng et  al. 2020). Similarly, Bacillus sp. isolated from Saccharum officinarum (sugarcane) displayed properties of producing indole acetic acid, phosphate solubilization, siderophore production, and antagonizing fungal pathogens. Furthermore, inoculation of endophytes improved root length and shoot biomass of sugarcane (Wang et al. 2020). Endophytes from sugarcane not only exhibited plant growthpromoting (PGP) activities, but also antagonistic properties against fungal pathogens like Bipolaris sacchari and Ceratocystis paradoxa (da Silveira et al. 2019). In the tuberous plant, Helianthus tuberosus endophytes produced 1-­aminocyclopropa ne-­1-carboxylate (ACC) deaminase during drought conditions and protected the plant from damage. Also, endophyte presence improved the inulin content even during drought conditions in H. tuberosus (Namwongsa et al. 2019). In Lupinus species, endophytic bacteria like Paenibacillus glycanilyticus and Pseudomonas

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brenneri improved nitrogen content in shoot and grain yield significantly (Ferchichi et  al. 2020). In another report, endophytic fungus Phomopsis liquidambaris enhanced the nodule formation, nitrogen fixation and yield in peanut (Arachis hypogaea). Interestingly, endophyte colonized roots released more amounts of flavonoids which attracted more nodule forming bacteria leading to more rhizobia symbiosis (Xie et al. 2019a, b). Similarly, P. liquidambaris inoculation improved rhizospheric environment, micronutrient availability and uptake in peanut (Xie et al. 2019a, b). Endophytic consortia isolated from the Salicaceae exhibited drought tolerance when inoculated in conifers and improved plant growth during edaphic conditions (Aghai et al. 2019). In some cases, endophytes promote plant health and tolerance during high-temperature conditions. For instance, Aspergillus japonicus isolated from Euphorbia indica protected agriculture crops like soybean and sunflower when grown at high temperatures (40 °C), and this tolerance is attributed to positive modulation of host metabolism by the endophytic fungus (Ismail et al. 2018). Transcriptomic analysis of Gilmaniella sp. inoculated Atractylodes lancea plants revealed the upregulation of genes related to primary metabolism like carbon fixation and carbohydrate metabolism, in addition to genes of terpene backbone synthesis such as farnesene and caryophyllene synthase genes which resulted in hyperaccumulation of sesquiterpenes (Yuan et al. 2019). Further, Trichoderma sp. improved the expression of genes and pigments responsible for photosynthesis thus improving the photosynthetic rate of plants (Harman et  al. 2020). Similarly, in Phyllostachys edulis (commonly known as the moso bamboo) endophytic bacteria improved photosynthetic rate, carbon assimilation, stomatal conductance and increased plant biomass. Christian et al. (2019) demonstrated that foliar endophytes improved uptake of nitrogen from the soil into leaves and improved plant biomass. Further, Piriformospora indica, a potential endophytic fungus is capable of performing various plant-beneficiary activities like imparting stress tolerance through modulating the expression of defense-related gene cascades, favoring plant growth through the production of phytohormones and displaying anti-fungal activities to protect the plant from diseases (Khalid et  al. 2019). Genome characterization of endophytic Sphingomonas sp. revealed its capability of producing gibberellins and interestingly upon inoculation in soybean, endophyte influenced plants to synthesize more gibberellins resulting in improved plant growth (Asaf et al. 2018). Endophytic Alternaria sp., native to Salvia militorrhiza, increased plant biomass as well as phenylpropanoid content in the leaves (Zhou et al. 2018a, b). In another report inoculation of native endophytic bacteria in S. militorrhiza upregulated terpene biosynthesis genes and increased in planta tanshinone levels (Yan et al. 2014). Inoculations of Bacillus amyloliquefacians and Pseudomonas fluorescens in Withania somnifera resulted in upregulation of genes related to withanolides biosynthesis and improved accumulation of withanolides content in leaves (Mishra et al. 2018). In recent a report, extracts of endophtytic fungus Aspergillus terreus improved withanolide A content in suspension cultures of W. somnifera (Kushwaha et  al. 2019). Treatment of Ginkgo biloba suspension cultures with extracts of Sphaeropsis sp. improved flavonoid production. This upregulation of flavonoid content was correlated with the overproduction of abscisic acid in endophyte treated

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suspension cultures (Hao et al., 2010). Furthermore, the addition of aqueous polysaccharide extract of Fusarium oxysporum to cell suspension culture of Dioscorea zingiberensis proliferated the cell growth and improved diosgenin content after 24th day (Li et  al. 2011). In the medicinal plant Atractylodes lancea the endophytic Pseudomonas sp. improved the sesquiterpenoid accumulation by inducing the plant to produce more carbohydrates and plants utilized these carbohydrates to synthesize secondary metabolites (Zhou et al. 2018a, b). In another report endophytic fungi Gilmaniella sp. enhanced production of sesquiterpenoids in A. lancea through inducing jasmonic acid pathway (Ren et al. 2012). Echinacea purpurea bacterial consortia inoculation improved the accumulation of alkamides possessing immune-­ modulatory and anti-inflammatory properties (Maggini et al. 2017). P. indica inoculations in Coleus forskohlii and Stevia rebaudiana increased the accumulation of signature metabolites. In Stevia, steviol glycosides production was increased due to the upregulation of steviol biosynthetic genes (Kilam et al. 2017). In Coleus, root biomass was significantly reduced and lateral roots were developed, however an increase in aerial biomass was observed including augmentation in photosynthetic rate, chlorophyll content and inflorescence development (Das et  al. 2012). In the contrary, native endophytes of Coleus forskohlii enhanced root biomass and improved forskolin content (Mastan et  al. 2019). Further, infection of endophytes positively influenced secondary metabolism in medicinal plants like Papaver somniferum, Catharanthus roseus and hyperaccumulation of signature metabolites was observed (Pandey et al. 2016; Pandey et al. 2017). With the available reports, it is highly conclusive that endophytes play an important role in enhancing plant primary and secondary metabolism. However, underlying genetic and molecular cascades of these interactions are still unknown. It will be interesting to know in-depth information on the plant-endophyte interactions at the molecular level.

2.4  E  ffect of Endophytes in Imparting Stress Tolerance to Host Plants Endophytes have co-evolved with their plant partner and are known to play a critical role in both plant development and ecosystem functioning (Turner et  al. 2013). Plant-associated microbes (not only endophytes but also other microorganisms) are increasingly being recognized for their ability to enhance plant fitness by altering biochemical, physiological and development responses (Philippot et al. 2013). To ascertain the importance of association of host plant and its endophyte during different stages of plant growth, the idea of what constitutes an individual host plant was redefined and plants are now called as “holobiont” (Bordenstein and Theis 2015; Vandenkoornhuyse et  al. 2015; Rosenberg and Zilber-Rosenberg 2016) or, also taken into consideration about the interactions with the environment and other organisms, as a “phytobiome” (Baltrus et al. 2017; Leach et al. 2017).

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The fact that plants are often exposed to a wide range of adverse environmental stress conditions (including both biotic and abiotic factors), which is unavoidable. Exposure of host plant to abiotic stress results in a series of sequential cellular, molecular, biochemical, physiological and morphological changes that negatively affect plant growth and productivity. Abiotic stress factors contribute to 60–70% of the yield losses in agriculture (Yakhin et  al. 2017; Ferrante and Mariani 2018). Endophytes employ mechanisms by which host plants overcome abiotic stress and it is mediated through the accumulation of stress-responsive molecules like osmolytes, secondary metabolites, and production of different classes of antioxidant enzymes. There are several reports demonstrating the interaction of endophytes with their host partner as a symbiotic association and such successful association helps host to tolerate adverse stress conditions (reviewed in Kasotia and Choudhary 2014). The mutual beneficial association between the host plant and the endophytic partner has known to significantly improve tolerance to stress factors including cold, chilling, drought, salinity, extreme soil pH, insect pests, and nematodes. It has been also reported that some plants are not resistant to habitat-imposed stress factors in the absence of microbial endophytes. Salinity stress occurs when water-soluble salts accumulate in the soil to a level that negatively impacts plants growth and subsequently agricultural productivity. Salinity stress impacts seed germination, seedling growth, vegetative growth, inflorescence development, panicle formation in monocots, ovule abortion, stamen development, senescence of fertilized embryos, etc. It is reported that ~20% of agricultural soil faces increase in salinity, and by the year 2050, approximately 50% of the agriculturally important area will be affected by severe salinity stress (FAO: High-Level Expert Forum, 2009). In the current scenario, the usage of beneficiary endophytes can help plants to mitigate stress conditions. Endophytic Bacillus pumilus AM11 and Exiguobacterium sp. AM25 significantly improved the tolerance of tomato plants under salt stress. Endophyte treated tomato exhibited higher biomass, enhanced photosynthetic rate and improved pigment levels compared to controls (Ali et al. 2017). Murphy et al. (2018) demonstrated the role of fungal endophytes in aiding barley to tolerate salt stress. A significant increase in plant growth, biomass, grain dry weight, number of tillers and number of grains were observed when barley plants were grown under 75 mM NaCl in presence of an endophyte. However, the authors also reported that no grain formation was observed in endophyte treated plants in 250 mM NaCl. It was concluded that fungal endophytes could help only in moderately salt-stressed conditions. Recently, it was reported in rice that, the endophytic microbiome of Indica rice seeds are shaped not only by the host plant genotype but also by their physiological adaptation during salinity stress. During salt stress in rice, endophytic communities of the salt-sensitive and -tolerant cultivars shift their dominance to bacterial groups belonging to Flavobacterium, Pantoea, Enterobacter, Microbacterium, Kosakonia and Curtobacterium (Walitang et  al. 2018). Afridi et al. (2019) established the role of Kocuria rhizophila and Cronobacter sakazakii in ameliorating salinity stress in wheat. Inoculation of endophytes in wheat enhanced morphological traits and antioxidant activities. Endophyte treated plants exhibited improved fresh and dry weight, root and shoot length, proline and

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chlorophyll contents. Authors implicate ACC deaminase activity of endophytic bacteria for imparting stress tolerance in wheat. In another study, nine endophytic fungi was isolated from maize and among them, Yarrowia lipolytica was capable of producing phytohormones like indole-3-acetic acid (IAA), indole-3-acetamide (IAM) and metabolites like phenolics and flavonoids. Inoculation of Y. lipolytica positively affected plant growth through enhanced levels of chlorophyll, carotenes, reduced electrolyte leakage, increase in peroxidase, catalase, IAA and proline contents were observed in plants exposed to salinity stress (Gul Jan et  al. 2019). Bharti et  al. (2016) reported modulation of an ABA-signaling cascade by the endophyte Dietzia natronolimnaea, responsible for salt tolerance in wheat by the upregulation of TaABARE (an ABA-responsive gene). Another study established the critical requirement of ABA in establishing symbiosis between beneficial fungus Piriformospora indica and A. thaliana roots (Peskan-Berghofer et al., 2015). The desert plant endophyte Enterobacter sp. SA187 colonized both the surface and inner tissues of roots and shoots of Arabidopsis and imparted salinity stress tolerance by producing a novel metabolite, bacterial 2-keto-4-methylthiobutyric acid (KMBA), which modulated the ethylene signaling pathway (de Zélicourt et al. 2018). The results from de Zélicourt et al. (2018) revealed a novel signaling phenomena during the beneficial microbe-induced plant stress tolerance. Overall, the beneficial effects of endophytes are attributed to producing reactive oxygen species (ROS)-scavenging enzymes like peroxidase, catalase and superoxide dismutase. ACC deaminase is another important endophytic enzyme which has an important role in the modulation of ethylene level in plants. Furthermore, extracellular secretions of endophytic metabolites act as compatible solutes (like proline and glycine betaine) that can balance the osmotic stress during severe salinity stress. Drought and temperature (heat, chilling or cold) can reduce crop productivity and yields leading to lower income for the farming community. Drought stress is a condition that happens when soil and atmospheric humidity are relatively low and the ambient air temperature is high. This results in an imbalance between the evapotranspiration and intake of water from the soil (Lipiec et al. 2013). Contrary to this, heat stress occurs when such that permanent harm to plant growth and development rises in soil and air temperature beyond a threshold level for a minimum amount of time. High-temperature stress leads to significant damage to cellular proteins that result in denaturation and aggregation, leading to cell death. At the whole plant level, all the above stress factors induce a cascade of physiological and molecular events resulting in reduced crop yield. Reduction in yield close to 21% and 40% were observed respectively in wheat and maize during drought stress (Daryanto et al. 2016). It has been reported that between 35% and 68% reduction in yield was reported in cowpea upon drought stress (Farooq et al. 2017). Aspergillus japonicus associated with plants like soybean and sunflower showed improved plant biomass under high-temperature stress (40 °C) compared to endophyte-free plants. Indeed, endophytic association mitigated heat stress by altering activities of plant hormones, an antioxidant enzyme like catalase, and ascorbic acid oxidase in both host plants.

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In addition, it was also observed that levels of phenolic, flavonoids, soluble sugars and other analyzed metabolites in endophyte associated seedlings also improved under heat stress compared to endophyte-free plants (Ismail et al. 2018). The ability of endophytes to increase wheat tolerance to drought and heat while improving germination efficiency was studied by Hubbard et al. (2014). A specific endophytic fungus increased thermotolerance in wheat and improved parameters like grain weight, as well as germination of second-generation seeds. Under drought conditions, two bacterial endophytes stimulated a longer root system and enhanced photosynthetic activity in pepper. Further, upon drought, bacterial colonization enhanced the expression and activity of vacuolar proton pumps (H+ -PPase/V-PPase) (Vigani et al. 2018). The induction of genes encoding stress- responsive proteins like aquaporin, dehydrin, etc. has been reported in mitigating drought stresses in rice by inoculation of endophytic Trichoderma harzianum (Pandey et al. 2016). It has been demonstrated that endophytic bacterial community assist plant to tolerate drought stress by producing abscisic acid, indole-3-acetic acid, and various volatile compounds. In addition, endophytic bacteria also aid in improving osmotic balance by maintaining relative water content, and enhancing the antioxidant activity of host plants by modulating signaling or regulatory genes of the respective pathway. Taken together, these bacterial-mediated drought tolerance metabolites help the plant to thrive during severe drought stress thus leading to improved plant growth and productivity. Low temperature causes impaired metabolism due to inhibition of enzyme functions, interactions among macromolecules, alteration in protein structure, and membrane properties (Andreas et  al. 2012). Similar to heat and drought stress, low temperatures damage many temperate crops when exposed to chilling or freezing temperatures and lead to reduced yield or complete infertility in plants. Burkholderia phytofirmans was able to reduce chilling-induced damage in grapevine by modulating sugar metabolism (Fernandez et al. 2012). Zhang et al. (2013) identified different fungal endophytes from three Antarctic bryophytes and suggest that these fungal endophytes are adapted to growth under cold stress conditions. Subramanian et al. (2015) demonstrated the role of Pseudomonas sp. in imparting chilling tolerance in tomato. Chilling resistance in endophyte treated plants was confirmed from reduced membrane damage and ROS levels, enhanced antioxidant activity in leaf tissues, and enhanced expression of cold-responsive genes LeCBF1 and LeCBF3. Further, the confocal microscopic analysis confirmed colonization and intercellular localization of cold-adapted Pseudomonas sp. All the above examples clearly demonstrate the plant growth-promoting ability of endophytes is due to their capability to secrete elevated amounts of various growth-promoting metabolites and thereby assisting their host plants to survive during stress condition. The above studies open the way to further decipher the role of specific endophytes in order to develop a strapping Bio agent for field application and use it as a thriving bio inoculum for application in crop plants.

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2.5  E  ndophytes-Mediated Biotic Stress Response in Host Plants Endophytic microorganisms increase plant tolerance to pathogens through induced defense mechanisms known as “induced systematic resistance” (ISR) (Zamioudis and Pieterse 2012). Various factors including antibiotics, salicylic acid, N-acylhomoserine lactones, siderophores, jasmonic acid, lipopolysaccharides, and volatiles (e.g., acetoin) are responsible for the induction of ISR in the host system. Though several endophytes have increased ISR mediated through fsalicylic acid induction, ethylene (ET) and jasmonic acid (JA) are inevitable molecules required for regulatory roles in signaling pathways implicated in ISR induction (Pieterse et al. 2012). In addition to endophytes present in roots, endophytes present in the above-ground tissues are also reported to regulate the host genetic expression for improving plant physiological responses and defense pathways (Estrada et al. 2013; Salam et al. 2017). Plant hormones like salicylic acid and jasmonic acid are known to play important roles during plant stress responses against phytopathogens by activating different pathogen responsive genes (PR) and their master regulator non-­ expressor of pathogenesis-related genes (NPR) (Khare et  al. 2016; Backer et al. 2019). Waqas et al. (2015) reported the role of Penicillium citrinum and Aspergillus terreus in imparting disease resistance and their ability to modulate hormonal signaling networks in plant defense against the stem rot caused by Sclerotium rolfsii on sunflower (Helianthus annuus L.). The negative impacts of S. rolfsii in endophyte-­ treated diseased plants were significantly less compared to control plants. Authors suggested that fungal association resulted in improved plant growth during disease incidence that was mediated by altering host plant defense mechanism. An interesting study by Meija et al. (2014) demonstrated pervasive genetic and morphological effects of the asymptomatic endophytes on their hosts. Authors reported that inoculation of endophyte-free Theobroma cacao leaves with Colletotrichum tropicale induced significant changes in the expression of defense responsive genes. Endophytes treated plants exhibited increased levels of lignin and cellulose. Interestingly, a cacao gene annotated as Tc00g04254 was highly induced by C. tropicale and transient overexpression of this gene in T. cacao leaves conferred resistance to Phytophthora capsici. Meija et  al. (2008) identified potential of fungal endophytes as biological control agents against pathogens in T. cacao. The production of volatile organic compounds (VOC) is an important defense mechanism to evade pathogens by plants. Together with plants, some of the endophytic bacteria are also known to produce VOCs that deter the growth of invading phytopathogens. Pseudomonas putida associated black pepper produced several VOCs and inhibited various classes of phytopathogens including bacteria, fungi and nematodes (Sheoran et al. 2015). Induced or constitutive production of specific secondary metabolites is another plant defense strategy against herbivores. Several grass species associated endophytes are reported to produce alkaloids.

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This is mentioned in detail below along with endophytes mediated metabolites production. Taken together it can be summarized that the presence of endophytes in host tissues can thus improve the defense response in the host by inducing the expression of defense responsive genes that either directly affects the predator growth or by producing antagonistic metabolites. Nonetheless, gene pools of both host and endophytes need to synchronize to protect the plants from parasites.

2.6  Role of Endophytes in Improving Phytoremediation Toxicity by heavy metals is one of the most important abiotic stresses that cause huge damage to various cultivated crops. In addition, heavy metal toxicity has become a major threat that minimizes crop productivity in acidic soils and interferes with several physiological processes including nutrient uptake, transport, metabolism, photosynthesis, and respiration. Several studies suggest the role of endophytes in reducing metal phytotoxicity through different mechanisms like extracellular precipitation, uptake and intracellular accumulation, sequestration to organelles like vacuole or tissues like leaf, or biotransformation of toxic metal form to less or non-­ toxic forms, among others (Mishra et al. 2017). It has been reported that endophytes like Pantoea stewartii, Microbacterium arborescens and Enterobacter isolated from Prosopis juliflora, growing in tannery effluent-contaminated soil having extremely high levels of metals like Cr, Cd, Cu, Pb, and Zn, improved growth of ryegrass and enhanced the uptake and accumulation of Cr in plant tissues (Khan et al. 2015). The endophytic bacterium Neotyphodium sp. enhanced Zn tolerance and uptake in Festuca rundinacea and Lolium perenne (Zamani et al. 2015). Syranidou et al. (2016) demonstrated the synergistic relationships between endophytes and the host plant Juncus acutus to deal with a mixed pollution consisting of emerging organic contaminants and metals. The beneficial effect of endophytes varied depending on the levels of contaminants; however, the composition of the root endophytic microbial community was altered in response to increased levels of metals and organic contaminants. Interestingly, the inoculated bacteria did not modify the microbial community structure. Mukherjee et al. (2018) reported remediation of arsenic (As) using As-tolerant endophytic microbes isolated from Lantana camara and Solanum nigrum as a secondary host. Endophytes significantly improved plant growth, bioaccumulation and below- ground to above-­ ground transport when applied as a consortium to host plants. Elevated glutathione levels and superior antioxidant defense mechanisms in the shoot and root of As-treated plants are some of the features that were observed in endophytes treated plants. A strong induction of a multidrug resistance-associated protein (MRP) transporter was observed in the root by the As +  endophytes that improved As-phytoremediation (Mukherjee et  al. 2018). Four different endophytic bacteria isolated from Betula celtiberica were tested for field-scale As bioaugmentation experiments by Mesa and co-workers (2017). In field experiments, iron-binding protein-like siderophore and IAA producers of the endophytic bacterial consortium

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enhanced As accumulation in both above- and below-ground parts of B. celtiberica. Experiments in conditions like field trials showed factors including soil As levels and pH influenced As uptake (Mesa et al. 2017). To understand the effect of endophytic bacteria in assisting phytoremediation in hydrocarbon contaminated soils, four different endophytes Stenotrophomonas sp., Flavobacterium sp., Pantoea sp., and Pseudomonas sp. were inoculated in white sweet clover growing on soils amended with diesel up to 20,000 mg·kg−1. During the course of a study, it was observed that growth inhibition in sweet clover by diesel toxicity was overcome in endophyte associated plants that exhibited significantly higher biomass. Among the four tested organisms, Pseudomonas sp. with hydrocarbon-degrading enzymes was an effective candidate in remediating hydrocarbons. The authors suggested using this strain to improve plant tolerance and hydrocarbon degradation in contaminated soils (Mitter et al. 2019). To reduce the negative impact of toxic compounds microorganisms produces a specific class of metabolites called biosurfactants. Marchut-Mikolajczyk et al. (2018) isolated different bacterial endophytes from the synanthropic plant Chelidonium majus. Among the different isolates, one of the endophytes, Bacillus pumilus exhibited higher emulsifying activity and showed very high degradation potential, for diesel oil and waste engine oil hydrocarbons. Further, the positive impact of the biosurfactant produced by B. pumilus on the growth of Sinapis alba in hydrocarbons contaminated soil was successfully demonstrated (Marchut-Mikolajczyk et  al. 2018). The potential interaction between microbial communities, host plant and ecosystem should be effectively explored with an eye on improving phytoremediation of heavy metals and organic pollutants.

2.7  B  io-Active Secondary Metabolites Produced by Endophytes Endophytic microbes possess various properties apart from participating in plant growth and development and one of the other beneficiary activities is to produce novel metabolites having significant importance in pharmaceutical and agricultural sectors (Table 2.1). For instance, Gaeumannomyces sp. isolated from the halophyte Phragmites communis produces anthraquinone derivatives having nitric oxide reduction activity in lipopolysaccharide-stimulated microglia BV-2 cells (Lee et al. 2017). Aspergillus sp isolated from the ethnomedicinal plant Mitrephora wangii produced β-thujaplicin (host flower signature metabolite) possessing a wide range of anti-microbial activities against human pathogens (Monggoot et al. 2018). Crude extracts of two endophytic fungi, P. citrinum and Geotrichum candidum, isolated from palm trees were able to inhibit bacterial pathogens like Bacillus thuringiensis, Enterococcus faecalis, and Salmonella enterica. Further, the extracts were also capable of combatting growth of the fungal pathogen Fusarium sporotrichioides (Ben Mefteh et  al. 2018). Bacillus atrophaeus and Bacillus mojavensis isolated

Aspergillus sp.

β-thujaplicin

Methyl esters of decanoic acids Vochysiamides A, B

Linoleic acid

Dankasterone

Phompsis sp. 14β,22E)-9,14-­ dihydroxyergosta-­ 4,7,22-triene-3,6-­dione, (5α,6β,15β,22E)-6-­ ethoxy-­5,15-­ dihydroxyergosta-­7,22dien-3-one

2.

3.

4.

5.

6.

7.

Mitrephora wangii

Host Phragmites communis

Phompsis sp.

Alternaria sp.

Aconitum carmichaeli

Aconitum carmichaeli

South African medicinal plants

Diaporthe vochysiae Vochysia divergens

Bacillus atrophaeus Glycyrrhiza uralensis

Endophytes Gaeumannomyces sp

Metabolite Anthraquinone derivatives

S. No. 1.

Table 2.1  Bioactive secondary metabolites produced by endophytes Activity Supresses the lipopolysaccharidestimulated inflammation in microglia BV-2 cells Inhibitory activity against human pathogens Inhibits wide range of plant fungal pathogens Active against Klebsiella pneumonia at MIC values 80 μg mL-1 Inhibits human pathogens like B. cereus, Escherchia coli, Enterococcus faecium, and E. gallinarum Active against Influenza H5N1 virus at IC50 values of 3.56 μM. Inhibits human and plant fungal pathogens Wu et al. (2013)

Ma et al. (2014)

Manganyi et al. (2019)

Noriler et al. (2019)

Mohamad et al. (2018)

Monggoot et al. (2018)

References Lee et al. (2017)

36 R. Bharadwaj et al.

Chaetomugulin D

Triterpenoid saponins

Fonsecinone D, Aurasperone B Pseurotin A

Steffimycin B

(S)-2-hydroxy-N-((S)1-((S)-8-­hydroxy-­1-­ oxoisochroman-3-­­yl)-3methylbutyl)-2-((S)-5oxo-2,5-­dihydrofuran-­ 2-yl)acetamide Dihydrobenzofurans, xanthenes

9.

10.

11.

12.

13.

14.

15.

Metabolite α-tetralone derivative

S. No. 8.

Oryza sativa

Amphipterygium adstringens

Erythrophloeum fordii

Limonia acidissima

Panax notoginseng

Ginkgo biloba

Host Arisaema erubescens

Fungal endophytes Pinus strobus from Massarinaceae

Bacillus amyloliquefaciens

Aspergillus fumigatus Streptomyces scabrisporus

Chaetomium globosum Fusarium sp and Aspergillus sp Aspergillus sp.

Endophytes Phoma sp.

Shi et al. (2015)

Siriwardane et al. (2015)

Jin et al. (2017)

Qin et al. (2009)

References Wang et al. (2012)

Inhibits growth of Saccharomyces cerevisiae, Microbotryum violaceum and Bacillus subtilis

(continued)

Richardson et al. (2015)

Inhibits Mycobacterium Trenado-­Uribe et al. (2018) tuberculosis at MIC values of 8 μg mL-1 Inhibits activity of enzymes Shahzad et al. (2018) like α-glucosidase and urease

Activity Inhibits Rhizoctonia solani and Fusarium solani notable fungal pathogens Inhibits brine shrimp Artemia salina Inhibits wide range of bacterial pathogens Toxicity towards brine shrimps Anti-inflammatory activity

2  Insights into Role of Invisible Partners in Plant Growth and Development 37

Fischerin

Orcinol and 4-hydroxymellein Cyclo-(L-Pro-L-­Val)

18.

19.

20.

Daldinia eschscholtzii

Fusarium solani

Penicillium sp.

Penicillium sp.

Orchids native of Thailand

Cassia alata

Alibertia macrophylla

Alibertia macrophylla

Bipolaris Rhazya stricta sorokiniana Neosartorya fischeri Glehnia littoralis

Endophytes Host Cladosporium Helianthus annuus cladosporides Alternaria brassicae Ginkgo biloba

Activity Inhibits the germination of lettuce seeds Possess antioxidant activities and anti-tyrosinase activity Inhibits acetylcholine esterase activity Possess antioxidant activity and inhibits ROS production and MAPK activity Inhibits plant pathogenic Cladosporium cladosporides Inhibits acetylcholine esterase activity Inhibits wide range of human pathogens and also controls tumor proliferation Anti-proliferative activity towards cancer cell lines

MAPK mitogen-activated protein kinase, MIC minimal inhibitory concentration, ROS reactive oxygen species

23.

22.

Novel aza-­ anthroquinone derivatives Daldionin

Olefins, β-ionine, Nonanol Sorokiniol

17.

21.

Metabolite Benzoic acid

S. No. 16.

Table 2.1 (continued)

Barnes et al. (2016)

Khan et al. (2018)

Oliveira et al. (2009)

Oliveira et al. (2009)

Bang et al. (2019)

Ali et al. (2016)

Pan et al. (2019)

References Waqas et al. (2013)

38 R. Bharadwaj et al.

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39

from the Chinese medicinal plant Glycyrrhiza uralensis were capable of inhibiting a wide range of fungal pathogens like Fusarium oxysporum, F. graminearum, Fulvia fulva, Alternaria solani, Ceratocystis fimbriata, Colletotrichum gloeosporioides, Pestalotiopsis microspora and Verticillium dahlia (Mohamad et al. 2018). Further, they also inhibited bacterial pathogens like Staphylococcus aureus, Bacillus cereus, Salmonella enteritidis and Escherichia coli. GC-MS analysis of extracts revealed that B. atrophaeus produced methyl esters of decanoic acids probably possessing antagonistic activities against pathogens (Mohamad et al. 2018). Diaporthe vochysiae, an endophytic fungus produced two novel carboxamides called vochysiamides A, B with vochysiamide B being active against the human pathogen Klebsiella pneumonia at very low concentrations (Noriler et  al. 2019). Endophytic Alternaria sp. produced linoleic acid which is capable of inhibiting human pathogens like B. cereus, E. coli, Enterococcus faecium, and E. gallinarum (Mangayani et  al. 2019). Interestingly, dankasterone produced by endophytic Phompsis sp. exhibited strong inhibitory activity against Influenza A (H5N1) pseudovirus at an IC50 value of 3.56 μM (Ma et al. 2014). Similarly, two new steroids were identified in culture extracts of Phomopsis sp. isolated from Aconitum carmichaeli and these compounds were active against fungal pathogens like Candida albicans, Aspergillus niger, Pyricularia oryzae, Hormodendrum compactum and Trichophyton gypseum (Wu et al. 2013). Ethyl acetate extracts of Phoma sp. isolated from Arisaema erubescens produced a novel α-tetralone derivative which exhibited inhibitory activities against Rhizoctonia solani and F. oxysporum at minimal concentrations (Wang et al. 2012) (Table 2.1). Qin et al., 2009 isolated a novel azaphielone derivative named as chaetomugulin D which is inhibitory against the brine shrimp Artemia salina and the fungus Mucor miehei (Qin et  al. 2009). Endophytic fungi from Panax notoginseng, Fusarium sp. and Aspergillus sp. produced triterpenoid saponins possessing a wide range of antimicrobial activities (Jin et al. 2017). Aspergillus sp. isolated from the seeds of Limonia acidissima produced two novel compounds, fonsecinone D and aurasperone B, and these compounds were moderately toxic against brine shrimps (Siriwardane et al. 2015). In another report, Aspergillus fumigatus isolated from Erythrophloeum fordii produced a novel compound named as spirotrypostatin K along with pseurotin A and a few other compounds. Further, pseurotin A was identified as anti-inflammatory compound which suppressed inflammation caused by lipopolysaccharide in BV2 microglia cells (Shi et al. 2015). Streptomyces scabrisporus isolated from the Amphipterygium adstringens secreted a novel compound, steffimycin B, and this compound showed inhibitory activity towards Mycobacterium tuberculosis at minimal concentrations (Trenado-Uribe et al. 2018). Polysaccharide extracts of F. oxysporum isolated from Otoba gracilipes displayed antioxidant activity (Caicedo et al. 2019). Crude extracts of Alternaria alternata isolated from neem plant showed inhibitory activities against various Gram-positive and Gram-negative pathogens. Scanning electron microscopic observation of pathogenic bacteria revealed disruption of bacterial cells after treating with crude extracts of endophyte (Chatterjee et  al. 2019). Bacillus amyloliquefaciens isolated from Oryza sativa produced a novel compound

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(S)-2-hydroxy-N-((S)-1-((S)-8-hydroxy-1-oxoisochroman-3-yl)-3-methylbutyl)-2((S)-5-oxo-2,5-­dihydrofuran-­2-yl) acetamide having inhibitory properties against bioactive enzymes like α-glucosidase and urease (Shahzad et al. 2018) (Table 2.1). Similarly, Paecilomyces formosus isolated from the roots of cucumber plant produced a novel compound called sester-terpenoid possessing antagonistic activities against α-glucosidase and urease enzymes at IC50 values ranging from 62 to 75 μg  g−1 (Bilal et  al. 2018). Two unknown fungal endophytes from family Massarinaceae produced dihydrobenzofurans and xanthenes which exhibited inhibitory activities against Saccharomyces cerevisiae, Microbotryum violaceum and Bacillus subtilis (Richardson et al. 2015). Culture filtrate extracts of endophytic Cladosporium cladosporides possessed benzoic acid capable of inhibiting lettuce seed germination (Waqas et al. 2013). Fungal endophyte extracts isolated from the plants belonging to arid regions showed significant inhibition towards plant pathogens as well as human liver cancer cell line HepG2 (González-Menéndez et  al. 2018). Alternaria brassicae isolated from Ginkgo biloba leaves produced host signature essential oil metabolites like olefins, β-ionine, nonanol; further, these compounds were shown to possess antioxidant properties as well as tyrosinase inhibition activity (Pan et al. 2019). Bipolaris sorokiniana isolated from Rhazya stricta produced a novel compound called sorokiniol and this compound was an inhibitor of acetylcholinesterase activity (Ali et al. 2016). Endophytic Neosartorya fischeri from Glehnia littoralis roots produced fischerin which inhibited glutamate-mediated cytotoxicity by uncoupling calcium ion influx (Bang et al. 2019). Penicillium sp. isolated from Alibertia macrophylla produced different compounds like orcinol, cyclo-(L-Pro-L-Val), 4-­hydroxymellein. While orcinol and 4-hydroxymellein were active against the plant pathogen Cladosporium sp., cyclo-(L-Pro-L-Val) was active in inhibiting acetylcholinesterase activity (Oliveira et al. 2009) (Table 2.1). Further, endophytic Fusarium solani produced novel aza-anthroquinone derivatives which were not only active against human pathogens but also active towards inhibiting tumor proliferation (Khan et al. 2018). Daldinia eschscholtzii from orchid plants produced a binaphthyl derivative daldionin and this compound exhibited anti-proliferative activity against cancer cell lines and reported to have moderate anti-microbial activity (Barnes et al. 2016).

2.8  Concluding Remarks and Future Research Directions One of the exciting scientific developments in the last few decades has been the understanding that the diverse and immensely active microbial communities play an inevitable role in plant growth and impart resistance to environmental stress factors. One such class of microbial community is endophytes that reside in plant tissues without causing any symptoms to host plants. Interaction between both partners results in improved plant health and reflects a significant application in low-input sustainable agriculture with high productivity even under adverse field conditions. Although several reports demonstrate the positive role of endophytes in improving

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plant performance, several key questions are also put forward by the scientific community. One of the important questions is to which extent the endophytic community supports plant growth and defense. Another important question to be answered is if the successful use of endophytic bacteria/fungi in open field conditions and most of the studies are performed under controlled conditions. There is still no clear idea of how these small organisms behave and improve plant performance when exposed to multiple stress factors. The development of designer endophytes and microbiome engineering to manipulate the plant’s endosphere microbiome is still way far from reality. Nevertheless, answering some of these questions could lead to greener ways of improving farming and targeted applications on crops may push forward a new paradigm shift in agriculture.

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Chapter 3

High Temperature Sensing Mechanisms and Their Downstream Pathways in Plants Nobuhiro Suzuki

Abstract  Plants, as sessile organisms, possess excellent strategies to acclimate to fluctuating temperature changes. Numerous studies have uncovered many pathways, not limited to the network of HEAT SHOCK TRANSCRIPTION FACTORS (HSFs) and HEAT SHOCK PROTEINS (HSPs), that are involved in the adaptation of growth to warm temperature or protection of cells against heat stress. It is relatively easy to imagine that response of plants to high temperatures might be initiated by the mechanisms which may sense temperature changes. Indeed, several candidates of warm temperature or heat stress sensors have been identified in the last decade. Although these sensors are localized in different organelles, their functions might be integrated via multiple signaling molecules such as Ca2+, reactive oxygen species (ROS), nitric oxide (NO) and plant hormones. In addition, mode of coordination between different signals could be modulated depending on temperature, timing, types of organs and growth stages. In this chapter, the roles of multiple warm temperatures and heat stress sensors will be addressed. Furthermore, the coordination between various signals that might function downstream of these sensors will be also discussed. Keywords Ca2 +  · Heat stress · High temperature sensing · Reactive oxygen species (ROS) · Signalling warm temperature

N. Suzuki (*) Department of Materials and Life Sciences, Faculty of Science and Technology, Sophia University, Chiyoda, Tokyo, Japan e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_3

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3.1  Introduction High temperature dramatically impacts all aspects of plant growth and development. Thus, high temperature can have detrimental effects on yield production worldwide and cause devastating economical and sociological impacts. It was recently reported that heat stress caused 5.5% and 3.8% reductions in global yields of wheat and maize, respectively, over the past decades (1980–2008) (Lobell et al. 2011). In addition, it is expected that the increase in the global mean temperature might exceed 2 °C by the end of the twenty-first century (Intergovernmental Panel on Climate Change 2014, http://www.ipcc.ch/). Therefore, to fulfill future food demand for the increasing population worldwide, it is urgent to establish strategies to enhance the adaptability of plants and crops to temperature increase. As sessile organisms, plants cannot escape from high temperature and are forced to alter their cellular metabolisms to prevent damages. To survive under natural environments with fluctuating temperature, plants evolved various strategies to adapt to irregular increases in temperature. Previous studies have identified many players that are involved in the regulation of responses to high-temperature (Katano et  al. 2018b; Li et  al. 2018; Mittler et  al. 2012; Sun and Guo 2016; Wang et  al. 2018). Among these players, five components were proposed as high temperature sensors in plants (Che et al. 2010; Finka et al. 2012; Jung et al. 2016; Kumar and Wigge 2010; Sakamoto and Kimura 2018; Sugio et  al. 2009). Phytochrome and histone H2A.Z were identified as warm temperature sensors that are required for the adaptation of plant to temperature several degrees higher than the optimal growth temperature (Jung et al. 2016; Kumar and Wigge 2010). These two sensors might play key roles to regulate developmental alterations induced by high temperature, termed thermomorphogenesis (Box et al. 2015; Koini et al. 2009; Li et al. 2018). In contrast, Ca2+ channel localized in the plasma membrane and regulator of unfolded protein responses in the cytosol and endoplasmic reticulum (ER) have been proposed as sensors that can activate signals to protect plants against severe heat stress (Che et al. 2010; Finka et al. 2012; Howell 2013; Sugio et al. 2009; Wan and Jiang 2016). Functions of these heat stress sensors were associated with the early events that occurred within minutes or even seconds following the exposure of plants to heat stress: alteration in membrane fluidity, increased Ca2+ influx into the cytosol and accumulation of unfolded proteins (Horvath et al. 2012; Kollist et al. 2019; Li et al. 2018; Nievola et al. 2017; Niu and Xiang 2018). Although these sensors for warm temperature or heat stress are localized in different cellular components, integration of their functions was suggested in recent studies (Katano et  al. 2018b; Kataoka et al. 2017). Various types of plant’s responses to high temperature have been extensively studied. Especially, many researches have focused on strategies of plants to acclimate to heat stress. For example, plants possess the ability to adapt to abrupt temperature increases, referred as basal thermotolerance (Mittler et  al. 2012; Suzuki et  al. 2008). In addition, plants have the capacity to cope with lethal heat stress, when pre-exposed to sublethal heat stimuli followed by recovery under optimal

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temperature (Mittler et al. 2012). This acclimatory heat response, acquired thermotolerance, could be also essential for plants to maintain their growth and developmental processes under natural environments in which temperature gradually increases during the daytime. Furthermore, the significance of long-distance signaling in the acclimation of plants to heat stress has been also suggested in recent studies (Baxter et al. 2014; Gilroy et al. 2014; Suzuki et al. 2013a, b). When a small group of cells are locally exposed to heat stress, a long-distance signal can be propagated through the entire plant. Heat response mechanisms are then activated in the distal part of the plant which is not directly exposed to heat stress. This process of heat acclimation might be essential to prevent further damage to the whole plant (Baxter et al. 2014). Moreover, plants might possess specific heat response mechanisms that function in different types of organs or during different growth stages (Katano et al. 2018a, b; Suzuki and Katano 2018). For example, the development of reproductive organs is governed by specific mechanisms that might be distinct from those operating in leaves and roots development. Thus, it can be expected that different types of organs might differently tailor specific acclimationmachinery to adapt to heat stress (Katano et al. 2018b; Suzuki and Katano 2018). Responses of plants to warm temperature or heat stress are controlled by complex networks involving various signaling molecules, such as Ca2+, reactive oxygen species (ROS), nitric oxide (NO), plant hormones and transcriptional regulators as well as HEAT SHOCK PROTEINS (HSPs) (Katano et al. 2018b; Li et al. 2018; Mittler et al. 2012; Sun and Guo 2016; Wang et al. 2018). It is relatively easy to imagine that the networks of these signals might function downstream to high-­ temperature sensors. However, it remains unclear how high-temperature sensing mechanisms are integrated with downstream signaling networks. In addition, the mode of coordination among pathways regulated by different high-temperature sensors is still largely unknown. In this chapter, signaling networks involving high temperature sensors will be summarized. In addition, plastic signaling networks underlying various high-temperature responses will be addressed.

3.2  Sensing of Warm Temperature Mechanisms of high temperature sensing in plants have been uncovered by the researches focusing on the responses to a mild temperature increase that alter the growth patterns of plants (warm temperature, Fig.  3.1) and temperature increase that can cause damage to cells (heat stress, Fig. 3.2) (Box et al. 2015; Jung et al. 2016; Kumar and Wigge 2010; Koini et al. 2009; Li et al. 2018). In Arabidopsis, warm temperature several degrees above the optimal temperature induces thermomorphogenesis that is characterized by early flowering, enhanced elongation of hypocotyls and petioles, and decrease in stomatal density and leaf thickness (Box et al. 2015; Fernández et al. 2016; Koini et al. 2009; Li et al. 2018). It was demonstrated that these morphological alterations might be efficient to cooldown leaf temperature by increasing air space between the organs (Crawford

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Fig. 3.1  Signaling network involving transcription factors underlying warm temperature sensing mechanisms and their downstream pathways. Arrows indicate positive regulation. Dotted arrows indicate the transcription of genes. T-shape bars indicate negative regulation. ARF6, auxin response factor 6, BR6ox2, brassinosteroid 6 oxidase 2, BZR1, brassinazole resistant 1, COP1, constitutive photomorphogenic 1, CRY1, cryptochrome 1, CYT P450, cytochrome P450, ELF3, ETS-related transcription factor 3, HFR1, long hypocotyl in far-red 1, HY5, elongated hypocotyl 5, PIF4, phytochrome interacting factor 4, PHYB, phytochrome B, TAA1, tryptophan aminotransferase of Arabidopsis 1

et al. 2012). A decade ago, ACTIN RELATED PROTEIN 6 (ARP6) in Arabidopsis was proposed to be involved in sensing of warm temperature (Kumar and Wigge 2010). Forward genetics screening of a mutant with enhanced expression of HSF70 at low temperature identified the mutation of ARP6. This mutant deficient in ARP6 showed an early flowering phenotype under low temperature, which is similar to WT plants grown under warm temperature. ARP6 encodes a subunit of the SWi2/ snf2-Related 1 (SWR1) complex, an ATP-dependent chromatin remodeling protein complex which is necessary for the insertion of H2A.Z histone into nucleosomes instead of H2A (Deal et al. 2007; Kobor et al. 2004, Krogan et al. 2003; Mizuguchi et  al. 2004). Interestingly, the transcriptome of plants deficient in ARP6 grown under low temperature was similar to that of WT plants exposed to warm temperature. These results suggest that the expression of warm response genes can be modulated depending on the occupancy of H2A.Z histone in nucleosomes. Indeed, in WT plants, warm temperature can result in a decrease of H2A.Z occupancy in nucleosomes around the transcription start site of warm response genes, leading to enhanced transcription of them (Kumar and Wigge 2010). Although regulation of H2A.Z occupancy in nucleosomes is essential for warm temperature sensing in plants, H2A.Z itself might not function as a sensor that directly senses temperature increase. A recent study demonstrated that warm-induced eviction on H2A.Z is dependent of HSFA1s, suggesting that HSFA1s function upstream to H2A.Z (Cortijo et al. 2017).

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Fig. 3.2  Simplified model of signaling network underlying heat stress sensing mechanisms and their downstream pathways. Arrows indicate positive regulation. Dotted arrows indicate the transcription of genes. T-shape bars indicate negative regulation. This model only indicates key pathways of heat response pathways. Models including other components can be found in previous reviews. (Katano et al. 2018a, b; Li et al. 2018; Mittler et al. 2012). ABA, abscisic acid, APX, ascorbate peroxidase, BR, brassinolide, bZIP17/28, basic leucine zipper 17/28, CNGC, cyclic nucleotide-gated ion channel, ERF74, ethylene response factor 74, HSF, heat shock transcription factor, HSP, heat shock protein, MBF1c, multi-protein bridging factor 1c, NO, nitric oxide, RBOH, respiratory burst oxidase homolog, ROS, reactive oxygen species, SA, salicylic acid

PHYTOCHROME INTERACTING FACTOR 4 (PIF4) was also known to be a key regulator of thermomorphogenesis. Arabidopsis mutant deficient in PIF4 showed impairment of hypocotyl and petiole elongation under warm temperature (Koini et  al. 2009). A recent study proposed that PHYTOCHLOME B (PHYB) might function as a warm temperature sensor (Jung et al. 2016). PHYB activated by red light is known to phosphorylate PIF4, targeting it for degradation via 26S proteasome (Lorrain et al. 2008). Interestingly, warm temperature accelerates the conversion of PHYB from its active Pfr state to the inactive Pr state even under the dark, leading to activation of PIF4 that enhance cell elongation (Jung et  al. 2016). In addition, EARLY FLOWERING 3 (ELF3) was identified as a negative regulator of PIF4 by QTL analyses using various Arabidopsis accessions (Box et  al. 2015). Warm temperature inhibits the binding of ELF3 to the promoters of target genes, resulting in enhancement of PIF4 expression and following cell elongation (Box et al. 2015; Jung et al. 2016; Nomoto et al. 2012). However, it is still not clear if regulatory systems of ELF3 are involved in warm temperature sensing, because it takes hours to attenuate binding of ELF3 target gene promoters by warm temperature (Box et al. 2015; Li et al. 2018).

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3.3  P  athways that Function Downstream to Warm Temperature Sensing Following the sensing of warm temperature via mechanisms involving PHYB and PIF4, downstream pathways that enhance cell elongation can be activated (Fig. 3.1; Jung et al. 2016; Legris et al. 2016). Previous studies suggested the direct interaction of PIF4 with transcription factors involved in the regulation of hormone signaling. For example, PIF4 might directly interact with transcription factor AUXIN RESPONSE FACTOR 6 (ARF6) to regulate the expression of genes that are involved in hypocotyl elongation (Oh et al. 2014). BRASSINAZOLE RESISTANT 1 (BRZ1), a brassinosteroid (BR) responsive transcription factor, is also known to directly interact with PIF4 (Oh et al. 2012, 2014). Several target genes regulated by PIF4 were also identified in previous studies. Warm temperature can enhance the binding of PIF4 to the promoter of genes encoding auxin synthesis proteins, such as YUCCA 8 (YUC8), TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and CYTOCHROME P450, and activate their transcription (Franklin et al. 2011; Sun et al. 2012). In addition, PIF4 was also shown to bind to the promoter of DWARF4 (DWF4), BRASSINOSTEROID-6-OXIDASE 2 (BR6ox2) to promote their expression (Wei et al. 2017). These results suggest that PIF4 might play key roles to integrate auxin and BR signaling that enhance cell elongation in response to warm temperature. On the other hand, DELLA proteins that can be inhibited by gibberellic acid (GA) was shown to negatively regulate PIF4 and other hormone signaling. DELLA proteins might directly interact with PIF4, ARF6 and BZR1, and inhibit their DNA binding activity (Bai et al. 2012; Li et al. 2012; Lucas et al. 2008; Oh et al. 2014). Other negative regulators of PIF4 have been also proposed in previous studies. Blue light inhibits thermomorphogenesis via activation of CRY1 that directly interacts with and inhibits PIF4 (Ma et al. 2016). UV can also attenuate the accumulation of PIF4 protein (Yang et  al. 2005; Hayes et  al. 2017) via stabilization of inhibitory interacting protein LONG HYPOCOTYL IN FAR RED 1 (HFR1). Probably, UV might inhibit CONSTITUTIVELY PHOTOMORPHOGENETIC 1 (COP1), a ubiquitin ligase that promotes the degradation of HFR1. In addition, COP1 is known to be a negative regulator of ELONGATED HYPOCOTYL 5 (HY5) that might bind to the promoter of PIF4 and inhibit its transcription (Delker et al. 2014; Gangappa and Kumar 2017). Taken together, these results suggest that thermomorphogenesis regulated downstream of PHYB might be modulated by the coordination between several signaling involving hormones and chromophore-dependent pathways. As mentioned above, mechanisms that regulate the eviction of H2A.Z from the nucleosome is essential to promote early flowering under warm temperature (Kumar and Wigge 2010). Despite the existence of more than 300 genes involved in the regulation of flowering time, H2A.Z and SWR1 complex might be associated with only small sets of these flowering genes. H2A.Z might positively activate the expression of genes encoding FLOWERING LOCUS C (FLC), MADS AFFECTING FLOWERING 4 (MAF4) and MAF5 proteins (Choi et  al. 2005, 2007;

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Coleman-­Derr and Zilberman 2012; Deal et  al. 2007; Jarillo and Piñeiro 2015; March-Diaz et al. 2006). These proteins are known as transcription factors involved in the repression of the key floral accelerating genes encoding FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1) (Bouche et al. 2016). Nevertheless, the link between the eviction of H2A.Z at a warm temperature and the early flowering does not seem to be associated with repression of FLC, because FLC transcript was also shown to be elevated at warm temperatures (Gan et al. 2014). In addition, the flowering time of the mutants deficient in FLC, MAF4 or MAF5 did not resemble that of plants grown under warm temperature (Gu et  al., 2013), indicating that other regulators of flowering time could be responsible for the link between H2A.Z eviction and early flowering. Another mystery to be addressed is the integration of H2A.Z-dependent warm temperature response with heat stress response, because ARP6 was identified as a key regulator of H2A.Z occupancy in nucleosome by the mutant screening based on the enhanced expression of HSP70 (Kumar and Wigge 2010). Indeed, the involvement of H2A.Z-dependent mechanisms in the regulation of heat stress responses can be expected, because HEAT SHOCK TRANSCRIPTION FACTOR A1 (HSFA1), a key regulator of heat stress response was shown to function upstream to H2A.Z eviction mechanisms (Cortijo et al. 2017).

3.4  Sensing of Heat Stress Key factors associated with the events that occur within minutes or even seconds in response to heat stress were proposed as heat stress sensors (Fig. 3.2). Alterations in the membrane fluidity are known to be early events that occur during heat stress (Horvath et  al. 2012; Niu and Xiang 2018; Plieth et  al. 1999; Vigh et  al. 2007). Previous studies suggested that alterations in membrane fluidity trigger lipid signaling during heat stress (Niu and Xiang 2018; Horvath et al. 2012). Two signaling lipids, phosphatidylinositol (4,5)-bisphosphate (PIP2) and phosphatidic acid (PA), that are synthesized via the functions of phospholipase D (PLD) and phosphatidylinositol-­4-phosphate 5-kinase (PIPK), respectively (Mishkind et  al. 2009), were shown to rapidly accumulate in response to heat stress (Niu and Xiang 2018; Horvath et  al. 2012). PIP2 hydrolyzed by PHOSPHOLIPASE C (PLCs) releases diacylglycerol (DAG) and inositol 1,4,5-triphosphate (IP3), second messengers that activate Ca2+ release from organelles to cytosol under heat stress (Horvath et al. 2012; Zheng et al. 2012). PA is a key regulator of the PLC signaling pathway (Testerink and Munnik, 2005). It was previously demonstrated that PLC3 and PLC9 in Arabidopsis might contribute to the protection of plants against heat stress via regulation of small HSP (sHSP) and intracellular Ca2+ level (Zheng et al. 2012; Ren et al., 2017). An increase in cytosolic Ca2+ level is known as another early event that occurs within seconds or minutes in response to heat stress (Finka et  al. 2012; Li et  al. 2018; Mittler et al. 2012). CYCLIC NUCLEOTIDE GATED CHANNEL (CNGC)

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proteins that are localized in the plasma membrane have been proposed as a putative heat sensor in plants (Finka et al. 2012; Ward et al. 2009). Deficiency in CNGCb or CNGC2 in moss or Arabidopsis resulted in enhanced heat tolerance accompanied by a more rapid and higher increase in cytosolic Ca2+ in response to heat stress when compared to WT plants (Finka et al. 2012; Katano et al. 2018a). In animal cells, complex of multiple CNGCs forms a Ca2+ channel on the plasma membrane (Zheng and Zagotta 2004). Such CNGCs complex has not been identified in plant cells. However, it could be expected that deficiency in a CNGCb or CNGC2 might lead to altered conformations of Ca2+ channel and Ca2+ influx into the cytosol might be dysregulated in plant cells (Finka et al. 2012). CNGC6 also plays key roles to mediate heat-induced Ca2+ influx into the cytosol and regulation of HSPs expression (Gao et al. 2012). CNGC6 was shown to be activated by cytosolic cyclic adenosine monophosphate (cAMP) which can be rapidly increased within minutes following the exposure of plants to heat stress (Gao et al. 2012; Niu and Xiang 2018). These results suggest that CNGCs might function as heat sensors that govern Ca2+ influx into the cytosol. Roles of Ca2+ channel as heat sensors could be also supported by the findings that Ca2+ is required for the activation of ROS producing enzyme RESPIRATORY BURST OXIDASE HOMOLOGUES (RBOHs: Suzuki et  al. 2011a, b). Indeed, an increase in cellular ROS accumulation is also known to be an early event that can occur within seconds or minutes in response to heat stress (Yao et al. 2017). In addition, ROS might function as important signaling molecules that regulate the expression of several heat response genes and proteins (See below). Unfolded proteins generated by heat stress are toxic because they can form aggregates and disrupt normal cellular homeostasis (Li et al. 2018). Thus, mechanisms to sense unfolded proteins and maintain protein conformations are essential for plants to survive under heat stress. Accumulation of unfolded proteins are known to trigger specific stress responses, termed unfolded protein responses (UPR) in the cytosol and endoplasmic reticulum (CPR and ER-UPR, respectively). In previous studies, transcription factors that govern these unfolded protein responses have been proposed as heat sensors (Che et  al. 2010; Howell 2013; Sugio et  al. 2009). In response to heat stress or application of a chemical that induces ER-UPR (Tunicamycin), bZIP17 and bZIP28, ER membrane-anchored proteins, are dissociated from the ER and transferred to the Golgi apparatus. These proteins are then cleaved by SITE-1-PROTEASE (SP1) and SITE-2-PROTEASE (SP2) in the Golgi, translocated to the nucleus and function as transcription factors. In contrast to ER-UPR, CPR activates HSPs via functions of HSFs. Transcriptome analyses revealed that the majority of CPR-induced transcripts possess heat shock element (HSE), the target of HSF binding, in the promoter regions. Among HSFs, HSFA2 was identified as the main regulator of the CPR signaling pathways (Sugio et al. 2009). Chloroplasts and mitochondria are known to be highly sensitive to heat stress. Except for the plasma membrane, PSI and PSII in the chloroplasts and complex I/ III in the mitochondria are main sites of ROS generation, respectively (Miller et al. 2010; Niu and Xiang 2018; Suzuki et al. 2012). Under heat stress, an increase in lipid peroxidation products can result in damages on protein function as well as

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generation of  singlet oxygen (1O2) and superoxide radicals (O2·-) 1O2 and O2·− in photosystems (Niu and Xiang 2018; Yadav and Pospíšil 2012). In addition, heat stress also triggers retrograde signaling that is transduced from chloroplast to the nucleus (Wang et  al. 2018; Sun and Guo 2016). Previous studies suggested the involvement of 1O2 in the retrograde signaling regulated by EXECUTER 1 and EXECULTER 2 (EX1 and EX2) proteins under photooxidative stress (Prasad et al. 2016; Zhang et al. 2014). In future studies, it is necessary to further elucidate the roles of 1O2- dependent retrograde signaling in the heat stress responses. Heat stress also causes lipid peroxidation in the mitochondrion membrane (Bligny and Douce 1980; Caiveau et al. 2001), which inhibits the activity of cytochrome c oxidase (i.e complex IV) (Paradies et al. 1998). Inhibition of the electron transport in the respiratory chain induces the production of ROS that triggers mitochondrial retrograde signaling pathways (Niu and Xiang 2018). Because of high sensitivity to heat stress and the capacity of ROS generation, it could be possible that chloroplasts and mitochondria possess heat-sensing mechanisms. It should be necessary to uncover how these organelles can sense temperature increase.

3.5  P  athways that Function Downstream to Heat Stress Sensing 3.5.1  H  SFs- or MBF1c-Dependent Pathways to Protect Plants Against Heat Stress At least two pathways have been proposed as key mechanisms underlying heat stress responses in plants; pathways involving HSFs and HSPs, and networks regulated by MULTIPROTEIN BRIDGING FACTOR 1c (MBF1c) (Morimoto 1998; Suzuki et al. 2008; von Koskull-Doring et al. 2007). Pathways involving HSFs and HSPs are well-known pathways of heat stress responses that highly conserved in a broad range of organisms (Morimoto 1998; Suzuki et al. 2008; von Koskull-Doring et al. 2007). Plants possess complex, but, flexible networks of HSFs. HSFs act as transcriptional regulators that control the heat stress response by binding to a defined heat shock response element (HSE) in the promoter of heat response genes (Morimoto 1998; von Koskull-Doring et  al. 2007). The functional redundancy of multiple HSFs was revealed by the analyses of double, triple or quadruple mutants of HSFs (Liu et al. 2011; Nishizawa-Yokoi et al. 2011). Such a functional redundancy of HSFs, the key regulators of heat tolerance, could be essential for plants, as sessile organisms to survive under natural environments with highly fluctuating temperatures. In addition, previous studies suggested that different sets of HSPs might accumulate in different types of organs. For example, large HSPs such as HSP70, 90 and 101 highly accumulated in vegetative tissues, while, reproductive tissues mainly accumulate small HSPs under heat stress (Basha et al. 2012; Siddique et al. 2008). Probably, other pathways as well as HSFs

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might be required for the organ- specific patterns of HSPs accumulation. Indeed, tight links between HSFs and ROS signaling have been proposed in many studies (see below). In addition, organ- specific expression of ROS producing enzymes, RBOHs have been also proposed (Suzuki et al. 2011a). MBF1c was identified as another key regulator of heat tolerance in plants. MBF1c was found to directly interact with trehalose-6-phosphate synthase 5. In addition, transgenic plants overexpressing MBF1c showed enhanced accumulation of various soluble sugars (Suzuki et al. 2005). Thus, MBF1c might modulate carbohydrate metabolisms by regulating the synthesis of trehalose that functions as signaling molecule. Furthermore, it was demonstrated that binding of MBF1c to DNA might be essential for the protection of plants against heat stress (Suzuki et  al. 2011b). MBF1c might control the expression of at least 36 different heat-response transcripts, including DEHYDRATION RESPONSIVE ELEMENT-BINDING PROTEIN 2A (DREB2A) that is required for acclimation of plants to heat stress as well as drought (Schramm et al. 2008; Suzuki et al. 2011a, b). Pathway regulated by MBF1c was shown to function independently of mechanisms involving several major HSPs, such as HSP70, 90 and 101 (Suzuki et al. 2005, 2008). However, the integration of MBF1c with several HSFs has been also indicated in more recent studies (Li et al. 2018; Suzuki et al. 2011a). Further studies are therefore required to uncover how MBF1c- and HSFs-dependent pathways are coordinated in the regulation of heat responses in plants.

3.5.2  Signals Involving Ca2+, ROS and NO Uncovering signals that function together with networks of HSFs and HSPs can be a main avenue of recent researches focusing on heat stress responses in plants. It has been proposed that pathways involving Ca2+, ROS and NO signaling are tightly integrated with functions of HSFs (Katano et al. 2018b; Parankusam et al. 2017). For example, CNGC6 was proposed to mediate Ca2+ influx into the cytosol and expression of HSPs under heat stress (Gao et al. 2012). A more recent study demonstrated that CNGC6 might regulate the expression of HSPs via modulating NO signaling (Peng et al. 2019). CNGC2 might also regulate pathways involving HSPs, MBF1c and ROS scavenging enzymes, ASCORBATE PEROXIDASES (APXs), in growth stage-dependent manner (Katano et al. 2018a, b). Seedlings of Arabidopsis mutants deficient in CNGC2 showed enhanced heat tolerance accompanied by higher accumulation of HSPs, MBF1c and APXs compared to WT plants. In contrast to seedlings, the reproductive organs of these mutants exhibited higher sensitivity to heat stress accompanied by lower accumulation of MBF1c and HSP23.6 compared to WT plants. In addition, the accumulation of APX proteins was not upregulated in the flowers of these mutants. The differences in heat tolerance between seedlings and reproductive organs observed in plants deficient in CNGC2 might be due to the dysregulation of ROS homeostasis. Plants deficient in CNGC2 showed a slight increase of H2O2 in seedlings, but, a dramatic increase of H2O2 in

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flowers. A slight increase in H2O2 as signaling molecule might properly activate heat response signals in seedlings. Contrary, excess H2O2 could cause damages to flowers. These results suggest that mechanisms of Ca2+-dependent ROS homeostasis required for the protection of plants against heat stress might be different between seedlings and flowers. This hypothesis could be also supported by the finding that plants deficient in APX2 showed higher sensitivity to heat stress during seedlings, but, higher tolerance to heat stress in flowers (Suzuki et al. 2013a, b). It was reported that deficiency in CNGC2 resulted in a higher level of cytosolic Ca2+ (Finka et al. 2012). This increase in cytosolic Ca2+ could enhance ROS producing activity of RBOH proteins via binding to EF-hand motifs (Ogasawara et  al. 2008), leading to activation of further downstream signaling involving certain HSFs and MITOGEN-ACTIVATED PROTEIN KINASES (MAPKs) (Niu and Xiang 2018). The binding of free Ca2+ to CALMODULINs (CaMs) is also an essential process to enhance various heat response pathways (Poovaiah and Reddy 1993; Trewavas and Malho 1997). For example, Ca2+ and CaM were shown to bind S-NITROSOGLUTATHIONE REDUCTASE (GSNOR), an essential regulator of NO metabolism, to inhibit its activity and increase in NO level in cells, leading to enhanced heat tolerance in plants (Zhou et al. 2016; Xuan et al. 2010). In addition, CaM3 might bind to and activate CALMODULIN (CaM)-BINDING PROTEIN KINASE 3 (CBK3), as well as PROTEIN PHOSPHATASE 7 (PP7), to modulate DNA binding activity of HSFAs via regulation of its phosphorylation status (Liu et al. 2007; Liu et al. 2008; Reindl et al. 1997). Furthermore, CaM3 is also known as a regulator of other transcription factors such as MBF1c, WRKY39 and DREBs (Li et al. 2010, 2018; Mittler et al. 2012). Studies employing mutants deficient in CNGCs indicated that Ca2+ signaling could function upstream to ROS and NO signaling (Katano et al. 2018a; Peng et al. 2019). However, the hierarchy between Ca2+, ROS and NO signaling is still controversy. Seedlings of Arabidopsis mutants deficient in RBOHB and RBOHD were impaired in NO accumulation in response to heat stress (Wang et  al. 2014). The heat-sensitive phenotype of these mutants deficient in RBOHs was rescued by the application of NO donors or the overexpression of NO synthesis genes. Nevertheless, other studies reported that NO might act upstream to Ca2+ signals (de Pinto et al. 2015), although Ca2+ is required for the activation of RBOHs (Kadota et al. 2015; Ogasawara et al. 2008; Suzuki et al. 2011a, b). These results indicate the existence of a feedback loop to modulate Ca2+, ROS and NO signaling during heat stress. In addition, NO was also shown to modulate the activity of enzymatic and non-­ enzymatic antioxidant systems in plants under heat stress (Fancy et  al. 2017; Parankusam et al. 2017). Taken together these findings suggest that the signaling cascade involving Ca2+, ROS and NO might be tightly regulated to maintain the level of cellular ROS which can properly activate mechanisms to protect plant cells against heat stress. Furthermore, another possible role of this redox signaling could be stimulation of the binding of HSFs to target DNA (Hahn et al. 2011; Parankusam et al. 2017). Another plasma membrane-localized Ca2+ channel, ANNEXIN 1 (ANN1) might also contribute to the increase in cytosolic Ca2+ level in response to heat

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stress (Liao et  al. 2017; Richards et  al. 2014). However, ANN1 might not be responsible for the initial heat-induced increase of cytosolic Ca2+, because ANN1 can be activated following the CNGC-dependent increase in cytosolic Ca2+. It should be therefore necessary to address how Ca2+ signals activated via CNGCs and ANN1 can be integrated or coordinated in the regulation of heat responses in plants. ROS regulatory systems might be associated with signals from chloroplast, a major site of ROS production. 1O2 generated following lipid peroxidation of thylakoid membrane can enhance retrograde signaling involving EX1 and EX2 proteins (Prasad et al. 2016; Zhang et al. 2014) and might activate unfolded protein response in the chloroplast (Prasad et al. 2016; Zhang et al. 2014). Several proteins, such as SIGMA FACTOR BINDING PROTEIN 1 (SIB1), WRKY33 and WRKY40 are known as key factors that function downstream to EX1 and EX2 (Dogra and Li 2019). Retrograde signaling from chloroplast can be also initiated by the accumulation of the chlorophyll precursor, Mg-protoporphyrin IX (Mg-ProtoIX) (Woodson and Chory 2008) and regulated by the functions of GENOME UNCOUPLED 1 (GUM1) and ABA INSENSITIVE 4 (ABI4) (Woodson and Chory 2008). In addition, a previous study employing Chramydomonas reinhardtii demonstrated that Mg-ProtoIX can enhance the expression of HSP70 in the chloroplast and the cytosol (Niu and Xiang 2018). Although roles of the chloroplast retrograde signaling in heat stress response is still needed to be elucidated by further investigations, a recent study suggested the significance of chloroplast signals in the heat tolerance of plants. It was demonstrated that the heat tolerance of plants was maximized during the day (Dickinson et al. 2018). This light-dependent activation of the heat tolerance might be triggered by ROS signals, generated from the chloroplasts (Dickinson et  al. 2018). ROS derived from the chloroplast could diffuse into the nucleus (Expósito-Rodríguez 2017) and enhance the transcription activity of the HSFA1s, leading to the up-regulation of heat-responsive genes such as HSP70 (Dickinson et al. 2018). Although our knowledge of mitochondrial retrograde signaling is still poor compared to chloroplast retrograde signaling, the association of ROS regulatory systems with mitochondrial retrograde signaling was also reported in previous studies. When electron transport is disrupted by abiotic stresses, expression of transcript encoding ALTERNATIVE OXIDASE 1 (AOX1) can be enhanced to regulate ROS level in cells (Giraud et  al. 2009). ABI4, a common regulator of chloroplast and mitochondrial retrograde signaling, was shown to directly regulate the expression of transcript encoding AOX1 by binding to its promoter (Giraud et al. 2009). As mentioned above, chloroplast and mitochondria could be involved in heat stress sensing mechanisms, because these ROS producing organelles are highly sensitive to heat stress (Niu and Xiang 2018). It should be necessary to identify key structures or proteins that sense heat stress in these organelles in future studies. It should be also interesting how chloroplast and mitochondrial retrograde signaling are integrated under heat stress.

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3.5.3  Plant Hormone Signaling Various plant hormones are also known to be key regulators of heat stress responses, which are integrated with other pathways mentioned in the sections above. Integration of hormone signals with ROS regulatory systems during heat stress has been extensively studied (Alam et al. 2018; Nawaz et al. 2017; Sharma and Laxmi 2015). For example, ETHYLENE RESPONSE FACTOR 74 (ERF74) in Arabidopsis was shown to be a positive regulator of RBOHD (Yao et al. 2017). Transgenic plants expressing ERF74 demonstrated enhanced heat tolerance, whereas a deficiency in ERF74 resulted in the opposite phenotype. ERF74 might bind to the promoter of the gene encoding RBOHD and enhance its expression. Thus, it should be interesting to address how ethylene and Ca2+ signaling are integrated to activate RBOHD. Chlorophyll degradation is known as major responses that can be observed under heat stress (Abdelrahman et al. 2017). It could be a strategy of plants to prevent oxidative damage by attenuating the absorption of excess light energy under heat stress. However, excess bleaching of leaf colors can also negatively impact on plant growth and development under stressed conditions. Chlorophyll degradation is therefore needed to be strictly regulated (Abdelrahman et al. 2017). Ethylene is well known as a senescence promoting hormone during plant development and under abiotic stresses (Abdelrahman et al. 2017). Heat stress can enhance the production of ethylene that inhibits phosphorylation of ETHYLENE INSENSITIVE 2 (EIN2), resulting in cleavage of carboxyl-terminal of EIN2 fragment which translocated to the nucleus and enhances ETHYLENE INSENSITIVE 3 (Abdelrahman et  al. 2017; Chen et  al. 2010). EIN3 further enhances the expression of several downstream genes encoding transcription factors such as WRKY53, ETHYLENE RESPONSE FACTOR4 and 8 (ERF4 and 8) and EPITHIOSPECIFIER PROTEIN/ EPITHIOSPECIFYING SENESCENCE REGULATOR (ESP/ESR) (Abdelrahman et al. 2017; Kim et al. 2014; Li et al. 2013a, b). Abscisic acid (ABA) is another plant hormone that is well known to function together with ROS regulatory systems. An RNA-binding protein, FLOWERING CONTROL LOCUS A (FCA), regulates heat tolerance via interaction with ABA INSENSITIVE 5 (ABI5), a transcription factor known to regulate the expression of antioxidant genes (Lee et al. 2015). In addition, APX6 was shown to protect germinating seeds against abiotic stresses including heat stress via mediating cross-talk between ROS regulatory systems, ABA signaling, and auxin signaling (Chen et al. 2014). Furthermore, ABA can also enhance the expression of transcripts encoding antioxidant enzymes such as APX, CATALASE (CAT) and SUPEROXIDE DISMUTASE (SOD) under heat stress (Jajic et al. 2015). Although these findings demonstrated the significance of ABA in ROS scavenging, ABA also functions together with ROS signals to regulate heat response pathways. A previous study demonstrated that the H2O2-dependent induction of transcript encoding HSP70 might be mediated by the function of ABA (Li et al. 2014). In addition, temporal-­ spatial interaction between ROS and ABA is essential for the heat acclimation of plants (Suzuki et al. 2013a, b). Taken together, these results indicate that ABA might

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play key roles to modulate the heat response pathways via switching ROS producing and scavenging systems. Several lines of evidences supported the roles of cytokinin (CK) in the response of plants to heat stress. Transient increase in CK under heat stress might stimulate stomatal opening to enhance transpiration as protective mechanisms against elevated temperature (Dobra et al. 2015). In contrast to ethylene, CK was shown to attenuate heat-induced chlorophyll degradation to enhance heat tolerance in plants (Jespersen et  al. 2015; Skalák et  al. 2016). In addition, analyses of transgenic Arabidopsis plants expressing CK-biosynthesis gene encoding INOPENTYL TRANSFERASE (IPT) revealed that CK plays important roles in the enhancement of heat tolerance via regulation of cellular redox states, as well as regulation of stomatal movement and maintenance of photosynthetic machinery (Skalák et al. 2016). However, overexpression of CK-degrading enzyme, CK OXIDASE/ DEHYDROGENASE1 (CKX1), also resulted in the enhanced heat tolerance accompanied by up-regulation of genes encoding ROS scavenging enzymes including CAT1, CAT3 and SOD (Lubovská et al. 2014). These findings indicate that level of CK production and degradation should be balanced to modulate heat response mechanisms in plants. Brassinosteroid (BR) was also shown to play important roles in the maintenance of photosynthetic machinery and antioxidant capacity under heat stress. It was demonstrated that exogenous BR application resulted in enhanced RUBISCO activity and quantum efficiency in photosystem II and increased chlorophyll fluorescence under heat stress (Bajguz and Hayat 2009; Hayat et  al. 2010; Fariduddin et  al. 2014). These positive effects of exogenous BR application on heat stress responses in plants can be accelerated by combined application with salicylic acid (SA) (Nawaz et al. 2017). In addition, enhancement of antioxidant enzyme activities by exogenous BR application under heat stress have been also reported in various brassica species including Indian mustard and black mastered (Nawaz et  al. 2017). Despite its importance in heat tolerance in plants, detailed mechanisms underlying these BR-dependent heat stress responses are still largely unknown. Probably, the roles of chloroplast retrograde signaling in the regulation of BR-dependent pathways should be investigated, because of the involvement of BR in the maintenance of photosynthetic machinery. Furthermore, it should be necessary to investigate links between BR-dependent heat response and ER-UPR pathway. Indeed, a previous study demonstrated that BR signaling can be activated by the ER-UPR pathway (Che et al. 2010). Interestingly, exogenous BR application enhanced expression of the transcript encoding RBOH protein, leading to enhanced heat tolerance accompanied by an increase in apoplastic H2O2 accumulation, when combined with exogenous ABA (Zhou et al. 2014). Probably, BR might play as a bi-functional signaling hormone depending on the integrating hormones to reduce cellular ROS level preventing oxidative damages and to enhance ROS production activating acclimation pathways.

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3.5.4  I ntegration of Unfolded Protein Responses in Cytosol and Endoplasmic Reticulum (ER) In the ER-UPR pathway regulated by bZIP transcription factors, BR signaling, as well as chaperons, are essential for the acclimation responses of plants to abiotic stresses including heat stress (Che et al. 2010). In contrast, CPR pathways regulated by HSFA2 might involve HSPs and microRNAs (Katano et al. 2018b; Sugio et al. 2009). HSP70 and HSP90 were shown to be required for the regulation of the DNA-­ binding activity and stability of HSFs under heat stress (Hahn et al. 2011). In addition, miR156, which is controlled by HSFA2, was also shown to contribute to acquired thermotolerance by downregulating the expression of a transcript encoding SQUAMOSA-promoter binding like (SPL) transcription factor via post-­ transcriptional modification (Stief et al. 2014). A recent study proposed the relationship between these two UPR pathways under heat stress (Kataoka et al. 2017). Deficiency in bZIP28 resulted in enhanced accumulation of heat response proteins such as APXs, MBF1c and HSPs accompanied by a higher level of transcript encoding HSFA2 and accumulation of H2O2 under heat stress. These results suggest that deficiency in bZIP28 might be complemented by HSFA2-dependent pathways activated by H2O2 signaling (Fig. 3.3). In contrast to the mutant deficient in bZIP28, the mutant deficient in HSFA2 showed attenuated accumulation of APX proteins, confirming the requirement of HSFA2 in the regulation of APXs. In the HSFA2-dependent pathway, H2O2 might function upstream to HSFA2, because certain HSFs were proposed to function as molecular sensors of H2O2 and regulate the expression of oxidative stress response genes (Miller and Mittler 2006). In addition, the expression of transcript encoding HSFA2 was shown to be highly responsive to H2O2 (Davletova et al. 2005). Furthermore, mutant deficient in HSFA2 also showed lower expression of transcript encoding bZIP28 under heat stress compared to WT plants (Kataoka et al. 2017), suggesting that HSFA2 might be required for the expression of bZIP28. Thus, CPR and ER-UPR pathways might be integrated via ROS signaling under heat stress.

Fig. 3.3  Possible integration between CPR and ER-UPR pathway. When bZIP28 is deficient in Arabidopsis plants, pathways rounded by dotted circle might complement the deficiency in bZIP28 (Kataoka et al. 2017). APX, ascorbate peroxidase, bZIP28, basic leucine zipper 28, HSFA2, heat shock transcription factor A2, HSP, heat shock protein

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3.6  Conclusions In this chapter, high-temperature sensing mechanisms function in different organelles and various signaling pathways that might function downstream of these sensing mechanisms were summarized, and the complexity of high-temperature response pathways was clearly indicated. In the natural environment, it is almost impossible to expect that when plants are exposed to temperature increase. In addition, mechanisms underlying heat tolerance were shown to be different depending on the types of organs and developmental stages (Katano et  al. 2018a, b). Furthermore, main high-temperature sensing mechanisms function in plant cells are also different depending on temperature (i.e. warm temperature and heat stress). Thus, such very complicated systems involving multiple sensing mechanisms might be essential for plants to flexibly acclimate to fluctuating temperature in the natural environment. Recent studies also demonstrated that different sets of transcripts were up-regulated following the exposure to the different durations of heat stresses (Wang et al. 2019; Li et al. 2019). We can also therefore expect that multiple heat-­ sensing mechanisms could be differently coordinated depending on the timing. Indeed, several major events including Ca2+ signaling, ROS production, HSP accumulation and growth alterations can be occur in different timing during heat stress (Li et al. 2018). Mechanisms underlying responses of plants to various types of heat stresses have been addressed in a previous review (Katano et al. 2018a, b). Many players commonly function in the different types of heat stress responses, but, the mode of coordination between these players can be different depending on temperature, timing and types of organs or tissues (Katano et al. 2018a, b). Probably, one of the most important processes in the heat acclimation in plants might be the modulation of cellular ROS level, because they can function as either toxic or signaling depending on the amount (Mittler 2017). Based on the previous findings, we can suggest that Ca2+, NO, ABA and CK might be the hub to switch the cellular signaling between production or scavenging of ROS. Previous studies demonstrated the possible existence of a feedback mechanism to modulate Ca2+, NO and ROS signaling (Katano et al. 2018a, b). In addition, ABA was shown to be involved in both scavenging and production of ROS during heat stress (Jajic et al. 2015; Li et al. 2014). Although warm temperature or heat stress might be sensed by different mechanisms, we still cannot ignore the possible links between responses to warm temperature and heat stress. The links between these high-temperature responses could be supported by the significance of HSFA1, a key regulator of the heat stress response, in the high temperature-induced eviction of H2A.Z histone (Cortijo et al. 2017). It should be therefore necessary to address how functions of different high-­temperature sensors are integrated into the regulation of warm temperature and heat stress responses. Another important question to be addressed in future studies is how do chloroplast and mitochondria sense high temperature. It could be expected that these organelles might play key roles in high-temperature sensing, because of their

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high sensitivity to temperature increase. As mentioned above, signals involved in heat stress response were shown to be activated by retrograde signaling from these organelles. In future studies, key structures or proteins that might sense temperature changes in these organelles need to be elucidated.

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Gu X, Le C, Wang Y, Li Z, Jiang D, Wang Y, He Y (2013) Arabidopsis flc clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat Commun 4:1947 Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755 Hayat S, Hasan SA, Hayat Q, Ahmad A (2010) Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239:3–14 Hayes S, Sharma A, Fraser DP, Trevisan M, Cragg-Barber CK, Tavridou E, Fankhauser C, Jenkins GI, Franklin KA (2017) UV-B perceived by the UVR8 photoreceptor inhibits plant thermomorphogenesis. Curr Biol 27:120–127 Horvath I, Glatz A, Nakamoto H, Mishkind ML, Munnik T, Saidi Y, Goloubinoff P, Harwood JL, Vigh L (2012) Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog Lipid Res 51:208–220 Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499 Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants (Basel) 4:393–411 Jarillo JA, Piñeiro M (2015) H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J 83:96–109 Jespersen D, Yu J, Huang B (2015) Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in relation to heat-induced senescence in creeping bentgrass. PLoS One 10:e0123744 Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JC, Schafer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354:886–889 Kadota Y, Shirasu K, Zipfel C (2015) Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56:1472–1480 Katano K, Kataoka R, Fujii M, Suzuki N (2018a) Differences between seedlings and flowers in anti-ROS based heat responses of Arabidopsis plants deficient in cyclic nucleotide gated channel 2. Plant Physiol Biochem 123:288–296 Katano K, Honda K, Suzuki N (2018b) Integration between ROS regulatory systems and other signals in the regulation of various types of heat responses in plants. Int J Mol Scis 19:3370 Kataoka R, Takahashi M, Suzuki N (2017) Coordination between bZIP28 and HSFA2 in the regulation of heat response signals in Arabidopsis. Plant Signal Behav 12:e1376159 Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, Nam HG, Woo HR, Lim PO (2014) Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J Exp Bot 65:4023–4036 Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, Link AJ, Madhani HD, Rine J (2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2:E131 Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413 Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasjarvi J, Mittler R (2019) Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci 24:25–37 Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, Ding H, Haw RA, Pootoolal J, Tong A, Canadien V, Richards DP, Wu X, Emili A, Hughes TR, Buratowski S, Greenblatt JF (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12:1565–1576 Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

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Chapter 4

From Beneficial Bacteria to Microbial Derived Elicitors: Biotecnological Applications to Improve Fruit Quality Beatriz Ramos-Solano, Ana Garcia-Villaraco Velasco, Enrique Gutiérrez-­ Albanchez, Jose Antonio Lucas, and Javier Gutierrez-Mañero

Abstract  Food security is the global goal set by the UN in which enough and high-­ quality food should be available for any person at all times to live a healthy life. Increasing productivity has gone through several milestones in terms of selecting varieties, mineral plant nutrition or transgenic plants. However, additional efforts need to be made to further increase productivity, especially in low-quality soils. Among the new actions to take is to turn the plant into an active player in production, not a passive element that just absorbs nutrients. At that point, the microorganisms that inhabit plant roots become relevant actors since plants select those that best meet their needs in a given environment by releasing different molecules through the root, selecting efficient collaborators. Therefore, isolated strains become active materials to improve plant nutrition and/or trigger plant metabolism to develop biofertilizers and/or biostimulants for agriculture. The application of active strains to different crops has proved to be effective to increase yield. However, the systemic changes induced in plant metabolism affect many processes, at the metabolic and gene expression level, affecting secondary metabolism pathways. Expression of core and regulatory genes is activated, resulting in modification of secondary metabolites profiles. When these secondary metabolites target human receptors, they are termed bioactives; hence, fruits from plants that have been stimulated contain more bioactives and hold a higher potential benefit for health. Isolation of bacterial determinants (elicitors) from effective strains

B. Ramos-Solano (*) · A. Garcia-Villaraco Velasco · J. A. Lucas · J. Gutierrez-Mañero Group of Biotechnology of the Plant-Microbiome Interaction, Facultad de Farmacia, Universidad San Pablo-CEU Universities, Madrid, Spain e-mail: [email protected] E. Gutiérrez-Albanchez Group of Biotechnology of the Plant-Microbiome Interaction, Facultad de Farmacia, Universidad San Pablo-CEU Universities, Madrid, Spain Biobab R&D S.L.Calle Patones, s/n - Parcela 28.3 - P.I. Ventorro del Cano, 28925, Alcorcón (Madrid), Spain © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_4

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able to target specific genes of interest in plants is a challenging approach to improve fruit quality, and at the same time, trigger plant defense reducing the need for chemical inputs during production. A case study blackberry illustrates bacterial strain and elicitors effects on fruit quality. Keywords  PGPR · Elicitors · Berry · Phenolic compunds · Flavonols · Anthocyanins · Yield

4.1  Introduction Food security is the global goal set by the UN as the moment in which “enough and high-quality food should be available for any person at all times to live a healthy life”. The demand for food is expected to increase by 70–100% by 2050, when the world population is expected to reach 10,000 million, hence increasing concerns about food security worldwide (Lindgren et al. 2018). This becomes an extremely challenging goal as climate change is decreasing the arable and productive cropping areas, not only increasing abiotic stress conditions like nutrient and water limitation, salinity, temperature…(http://www.fao.org/3/a-­i5199e.pdf) but also favoring pathogen spreading and susceptibility, therefore compromising plant growth (Ning et al. 2017). Along with humankind history, the feeding population has been the limiting factor for human activity and wellbeing. The first revolution in this line was the moment when humans were able to grow edible plants and became sedentary; from there on, increasing productivity to feed themselves became the greatest concern and major advances were made on selecting varieties over time. Next, the Green revolution associated with the Haber-Bosch process and mineral nutrition in the 1800’s, marked a milestone in terms of increasing productivity-boosting the plant’s productive potential, which was further improved in the 1900’s by high yield seeds and phytochemicals to end up nowadays with genetically modified plants. Great advances have been done with GMO plants, that still has a limit because limited gene targets can be dealt with in a single plant, either targetting chemical resistance or pathogen resistance or salinity resistance. Crop yield may be controlled by the application of chemicals or gene modification approaches plus gene breeding technologies but all involve active human intervention, considering plants as passive elements that respond to this intervention. However, additional and more affordable efforts need to be made to further increase productivity, especially in low-­ quality soils. Among the new actions to take is to explore the potential of the plant to be an active part of the process, not a passive element that just absorbs nutrients and suffers from pathogen outbreaks. At that point, the microorganisms that inhabit plant roots become relevant actors on the scene, as they have evolved with plants along

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time, providing help to improve plant adaptation to adverse environmental conditions (Galicia-Campos et  al. 2020). Plants select those microorganisms that best meet their needs in a given environment by releasing different molecules through the roots, recruiting the most efficient collaborators (Narasimhan et al. 2003). Plant-­ microbe interaction involves microbial molecules (elicitors) and plant receptors when we consider the relationship plantwise, and the opposite when it is considered bacterialwise. Therefore, management of the interkingdom communication appears as an excellent tool to boost plant physiology and food quality. In this game, isolation of effective beneficial strains or bacterial derived molecules (elicitors) to improve plant nutrition, and/or trigger plant metabolism to develop biofertilizers, and/or biostimulants for agriculture is of paramount importance. This chapter presents the general physiological processes of plant metabolism to grow and deal with changing conditions along their life cycle. Then, the plant targets that microorganisms can modulate, contributing to enhanced plant fitness will be reviewed, as well as how these modifications result in improved quality and beneficial human health potential of plant-based foods, naturally enriched in beneficial molecules (bioactives), by bacterial modulation of plant metabolism. The hypothesis is illustrated with a case study on blackberries treated with a bacterial strain and derived raw metabolic and structural elicitors, and effects of potential benefits for human health.

4.2  P  lant Fitness. Growth and Mechanisms for Adaptation to Stress. Factors Limiting Growth As photoautotrophs, plants obtain their carbon sources from the energy of light through photosynthesis, and they also need to absorb nutrients which are available in soils and, above all, they depend on water availability for survival, so plants are endowed with mechanisms to provide all these, and elements to coordinate developmental processes, like plant growth regulators (Fig.  4.1). Since plants are sessile organisms, they are fixed to the soil for life where seeds germinate and have depicted physiological processes to successfully overcome stress situations (Oh et al. 2009). The most limiting factor of plant growth is water. Water limitation may be due directly to low water availability or to soil conditions in which salinity is high, thus also creating a serious problem for the plant. The mechanisms to overcome water shortage in plants involve control of ion homeostasis, control of reactive oxygen species (ROS) balance, osmolyte synthesis and hormonal control of stomatal closure by abscisic acid and changes concomitant to ethylene synthesis upon stress signal that always results in growth arrest (Fricke et  al. 2006; Ilangumaran and Smith 2017). Soil nutrients are limited or show a limited availability for plants. In agriculture, nutrients are usually provided through external chemical fertilizers to crops, being extremely high in intensive agricultural practices to guarantee high yield and

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Fig. 4.1  Plant physiological mechanisms for growth and adaptation

quality. The use of chemical fertilizers, which are expensive and create environmental problems, is highly extended and yet in recent decades, increased fertilizer inputs are no longer correlated with crop yields increases, revealing a low efficiency in nutrient use and, hence, a great environmental risk (Zhang et al. 2010). Due to the sessility of plants, they have to cope with changing conditions, for which they have to adapt to a most versatile metabolism, leading to a plethora of different metabolites, suitable to overcome each adverse condition (Oh et al. 2009). According to biosynthetic origin and structure, three great groups of secondary metabolites have been defined: terpenes, phenolic compounds and alkaloids. Despite being called secondary metabolism, plants have it due to its role in adaptation, since it includes (i) structural molecules basic for plant growth like phytosterols or aromatic amino acids, or (ii) molecules with a primary physiological role, like carotenoids in light-harvesting, or plant growth regulators, like abscisic acid or gibberellins. This secondary metabolism is inducible upon specific factors, and plays a key role in adaptation, involving modification of the expression of certain genes for specific responses, leading to different metabolic profiles concomitant to genetic modifications (Gutierrez-Albanchez et al. 2020). Also part of this secondary metabolism, plants have an innate immunity system, started by adverse conditions and always mediated by increases in ROS levels. Plant innate immunity is based on receptors able to detect invasion. Traditionally, plant innate immunity has been described as a two-stage process. The first stage involves

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plant membrane receptors able to recognize specific molecular patterns from pathogens (PAMPS; Pathogen Associated Molecular Patterns), nemathodes (NAMPs; Nematode Associated Molecular Patterns), danger signals started by the plant itself (DAMPs; Danger Associated Molecular Patterns), or any microbe irrespective of their pathogenic capacity (MAMPs; Microbe Associated Molecular Patterns). Upon completing this first stage, the second stage takes place with the onset of the response known as PTI or MTI (PAMP-triggered Immunity or MAMP-­triggered immunity). However, many pathogenic microbes are able to inject effectors in the plant’s cytosol to block the PTI/MTI response, enhancing the chances of a successful invasion. To overcome this secondary attack, plants have developed specific receptors to these effectors able to trigger a new defensive response, this way being more intense and known as ETI (Effector-triggered immunity) (Gust et al. 2017; Alhoraibi et al. 2019). Plant membrane receptors involved in PTI response are known as pattern recognition receptors (PRR), and share a few traits in their general structure, as leucine rich repeated domains (LRR) for ligand binding. In view of the above, it is evident that one of the plant responses is started outside the plant and the second starts inside the organism. Recently, all molecular patterns able to trigger an immune response in the plant (PAMPs, MAMPs, DAMPs…) have been placed in the danger signal group (DA; Danger signal); extracellular immunogenic pattern (ExIP) and intracellular immunogenic pattern (InIP) are the terms coined to describe where the danger signal is perceived, and extracellular triggered immunity (ExTI) and intracellular triggered immunity (InTI) to refer to the place where the response is initiated. Although the increase in ROS was only accepted for pathogen stress at first, it is now widely accepted that this behaviour is valid both for biotic and abiotic stress (Miller et al. 2017; Qi et al. 2017). Irrespective of the bacterial determinant and the plant response, ROS mediate signal transduction, leading to gene expression changes and concomitant defense molecule synthesis and systemic responses (Fig. 4.2).

Fig. 4.2  Plant defense pathways triggered by beneficial and pathogenic microorganisms associated with systemic defense

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ROS are unavoidable by-products of cellular metabolism and in addition, they behave as signaling molecules for many processes involved in plant growth, development and stress responses (Reczek and Chandel 2015). Under normal growth conditions, ROS homeostasis is maintained at low levels. However, environmental stimuli may disrupt this homeostasis, resulting in a ROS burst (Sharma et al. 2012). The supply of carbon skeletons to all these metabolic pathways relays on photosynthesis. It is of utmost importance that the process is very efficient, however, it creates high oxidative conditions in cells. As a result of excess, ROS accumulation membrane oxidation and disruption of the photosystems occur, resulting in severe cellular damage (Vranova 2002), compromising photosynthetic efficiency. So plants have designed antioxidant mechanisms to overcome oxidative stress: enzymatic and non-enzymatic antioxidants. The enzyme pool of antioxidants involves superoxide dismutase (SOD) which converts superoxide radicals (O2·−) into H2O2, which is subsequently converted into H2O by ascorbate peroxidase (APX) and catalase (CAT). All three enzymes play major roles in scavenging O2·− and H2O2 (Willekens et al. 1997). The non-enzymatic pool of antioxidant components such as ascorbate, glutathione, carotenoids, tocopherols and phenolic compounds (including flavonoids and anthocyanins) contribute to the protection against ROS (Halliwell 2006). It becomes evident at this point that ROS are a common factor to balance organic matter synthesis and plant adaptative responses, evidencing that growth and adaptation need to be balanced (Ning et  al. 2017). Furthermore, the compounds listed as the non-ezymatic pool of antioxidants are plant metabolites synthetized through the complex pathways of secondary metabolism, connecting with the adaptative role of this secondary metabolism (Fig. 4.3).

4.3  The Multifactor Solution: PGPR The term Plant growth-promoting rhizobacteria (PGPR) was coined by Kloepper in 1981 to define free-living beneficial bacteria that enhanced plant growth. From there on, many studies have contributed to the development of this topic revealing the many ways that PGPR contribute to plant fitness. These bacterial strains are isolated from the rhizosphere where plants release carbon sources through the exudates, selecting those individuals that provide benefits to the plant upon colonization (Pongsilp et al. 2016). Among the benefits that PGPR provide plants with are improving plant nutrition, production of biostimulating phytohormones and peptides, suppressing plant diseases or stimulating plant metabolism to improve defense (Ramos Solano et al. 2008; Pieterse et al. 2014). Production of plant growth regulators such as auxin, cytokinin and gibberellin delivered right into the roots and therefore, affecting hormonal balance, has been demonstrated to affect plant growth, an effect that is more marked when a physiological combination of plant growth regulators is provided (Zahir et  al. 2004; Gutierrez-Mañero et al. 1996). In the area of plant nutrition, hormonal effects of PGPR lead to the increased root surface, allowing greater nutrient absorption

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Fig. 4.3  Metabolic network involving ROS in photosynthetic plant cells. ROS are naturally formed as a photosynthetic by-product, although ROS levels increase upon stress conditions. Under mild stress, ROS serve as signaling molecules to start signal transduction towards an adaptative response involving activation to secondary metabolism. As they must be kept at physiological levels, plants are endowed with ROS scavenging systems to bring ROS levels to a basal state. Upon high stress, ROS levels dramatically increase and this may cause oxidative damage if scavenging systems are not enough

leading to increased growth (Gutierrez-Mañero et  al. 1996), but PGPR can also release compounds able to mobilize nutrients that limit plant growth, like iron by the means of siderophores, or phosphate by releasing P-mobilizing enzymes or activating nutrient mineralization contributing to better nutrition (Pieterse et al. 2014). The effect on growth promotion and improvement of plant fitness by PGPR is due to more than one target being simultaneously triggered by the PGPR (Illangumaran and Smith 2017) that results more efficient than providing only nutrients or only plant growth regulators. Likewise, PGPR can improve the general fitness of the plant by increasing photosynthesis rate and/or efficiency (García-Cristobal et  al. 2015) or decreasing oxidative stress by lowering photosynthetic pigments (Galicia-­ Campos et al. 2020). All these increases in plant nutrition lead to improved productivity, meeting one of the definitions of food security, which is the amount of food. The use of PGPR with this aim is of special relevance for countries under development that usually have soils with low productivities, as it has been shown that PGPR performs best when the conditions are challenging (Ramos-Solano et al. 2006, 2014). What is yet

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to be achieved is the second part of food security referring to the quality of foods, in which systemic induction is involved. Two phenomena, known as Induced Systemic Tolerance (IST) (Qin et al. 2016) and Induced Systemic Resistance (ISR) (van Loon et al. 1998), are accepted among the general defense mechanisms in plants against biotic and abiotic stress, both mediated by ROS control. However, one of the most relevant effects of specific PGPR is their ability to trigger a systemic response, activating the plant’s secondary metabolism (Algar et al. 2014; Gutierrez-Mañero et al. 2012). Upon plant recognition of bacterial determinants (MAMPs or PAMPs), by pattern-recognition receptors (PRRs) (Henry et al. 2012), the defense response is initiated, resulting in an increased defensive capacity of the entire plant called Induced Systemic Resistance (ISR) (Pieterse et al. 2014). Upon root colonization, the plant activates its metabolism, acquiring a potentiated defensive capacity without concomitant induction of specific defense genes, a phenomenon termed priming, which is accepted today as an intrinsic part of induced resistance; furthermore, the specific metabolic changes that take place upon root colonization have been termed as priming fingerprint (Mauch-Mani et  al. 2017) and involves expression of specific proteins (Pieterse et al. 2014). This interaction involves a bacterial determinant that binds a specific receptor and triggers a determined plant response. Two different branches can be activated, the salicylic acid (SA) branch and the jasmonic/ethylene acid (JA/ET) branch (Van Loon et al. 1998). When ISR was first described, it was believed that the SA-mediated pathway was used exclusively by pathogens, triggering Systemic Acquired Resistance (SAR), while the JA/ET branch was limited to PGPR (Pieterse et  al. 1998). Furthermore, it was believed that beneficial microbes would only use the JA/ ET pathway, although evidence confirms the capacity to trigger either pathway or both simultaneously (Domenech et al. 2007; Barriuso et al. 2008), and this depends on the determinants (MAMPs) able to trigger a response on the plant species under study (Bonilla et  al. 2014; Gutierrez-Albanchez et  al. 2017). There is increasing evidence of the crosstalk between these pathways and the involvement of other plant growth regulators in defense (Vos et al. 2015). Further to this reasoning, the interaction involves plant receptors to specific bacterial molecules. These bacterial molecules are termed elicitors, and these can be obtained directly from structural features of bacterial strains, like LCOs (lipochitinoligosaccharides), flagellins, or metabolites released to culture media along with growth, all being potential MAMPs. Among the biotic elicitors, proteins, polysaccharides or volatile compounds can be found, and they can be microorganism metabolites or structural molecules, either from a pathogenic or non-pathogenic microorganism (Wiesel et al. 2014). Furthermore, bacterial elicitors are also able to trigger simultaneously the existing metabolic pathways for defense (Martin-Rivilla et al., 2019). As secondary metabolic pathways lead to a number of metabolites, and some happen to trigger human receptors improving human health, elicitors can be used to enrich edible plants in certain metabolites creating healthier fruits (Garcia-Seco et  al., 2015), the so- called functional foods. Furthermore, if they are used in

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Fig. 4.4  Hypothesis of plant elicitation with beneficial bacteria and derived molecules to improve secondary metabolism and yield in berries

medicinal plants, higher yields will be obtained in agronomic production (Bonilla et al. 2014) and these can be also applied in cell cultures (Gutierrez Mañero et al. 2012) or edible foods (Algar et al. 2012; Capanoglu 2010). Based on the above facts, the working hypothesis from our group is to use beneficial bacteria or parts of the same (elicitors) as a tool to trigger plant metabolism in the field production to increase crop yield and fruit quality, by causing a mild biotic stress in the plant, that smoothly and constantly triggers secondary metabolism to achieve constant concentrations of bioactives in the edible fruits (Fig. 4.4). The ability of many beneficial bacteria to trigger plant metabolism in different species has been reported and there is increasing evidence of bacterial derived elicitors with the same effect on different plant species like soybean or St. John’s wort (Algar et al. 2012; Gutierrez Mañero et al. 2012). To support the value of this strategy a summary of studies carried on in blackberry follows below. Blackberry (Rubus ssp.) was selected as it is a minority crop according to a surface area devoted to this plant worldwide, despite its high added value in the market, where it is considered a commodity (Kaume et al. 2012). As a consequence of this low surface, no specific phytochemical products are available in the market and our working hypothesis fitted in  local growers to enhance the plant’s metabolism for defense and increase yield.

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4.4  Case Study: Blackberry To study blackberry metabolism, field-grown blackberry plants were inoculated with a beneficial bacteria strain (Pseudomonas fluorescens N21.4), aiming to trigger flavonoid biosynthesis as part of an induced systemic response. Fruits were studied in three states along with maturation, carrying on a bioactive characterization and studying core and regulatory gene expression. As a result, flavonoids concentration increased in the fruit along with maturation over the non-inoculated controls, and edible fruits showed enhanced levels of kempferol-3-rutinoside and epicatechin; expression of core and regulatory genes was consistent with metabolic profile, being the target genes chalcone isomerase (RuCHI) and flavonol synthase (RuFLS), associated to enhanced accumulation of anthocyanins, catechins, and flavonols in developing fruits of blackberry (García-Seco et al. 2015). This study made us wonder if all flavonols and anthocyanins were synthesized in fruits. A thorough transcriptomic and metabolomic analysis in leaves and fruits revealed that flavonols were synthesized in leaves and then translocated to fruits to provide substrates for the massive anthocyanin biosynthesis that takes place thereupon ripening (Gutierrez-Albanchez et  al. 2017), consistent with the mobility of flavonoids through the plant (Biała and Jasinski 2018). We further demonstrated that Bacillus amyloliquefaciens strain QV15 was also able to trigger the flavonol-anthocyanin pathway in blackberry, but targetting different genes, namely the core-gene encoding flavonol-3-hydroxilase (RuF3H) in leaves and fruits, and the regulatory gene encoding the transcription factor RuMYB5 controlling the pathway, significantly overexpressing both genes (Gutierrez-Albanchez et al. 2020). Interestingly, the trial suffered a sudden powdery mildew outbreak, so we were able to demonstrate that the systemic induction caused by the bacillus strain also stimulated blackberry defensive metabolism, protecting plants over 80% as compared to non-inoculated controls. Also as a result of this trial, the priming fingerprint of this strain was established, by comparing the response to QV15 of two different plants: blackberry in field conditions and Arabidopsis in controlled conditions, which were further challenged by different pathogens. As a result, the priming fingerprint induced by QV15 was defined by a decrease in ROS scavenging enzymes’ activity in pre- and post-pathogen-challenged plants, an increase in glucanase and chitinase activity after pathogen challenge, and a significant increase in the expression of PR1 (Gutierrez-Albanchez et al. 2018). The transcriptome analysis carried out in blackberry leaves revealed an activation of photosynthesis, protection of chlorophyll breakdown, and active defense based on specialized proteins. After all these changes in the plant’s physiology, an increase in phenolics (flavonols and anthocyanins) in blackberries was expected but it didn’t happen. We found a general decrease in flavonols and anthocyanins as compared to controls when a rough quantitative analysis was done although the UHPLC-MS/TOF analysis indicated a marked increase in kempferol-3-rutinoside and decreases in quercetin-derivatives suggesting that the reprogramming induced by QV15 goes beyond the analyzed metabolites (Gutierrez-Albanchez et al. 2020).

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An interesting conclusion of these studies is that two strains from different genera are able to trigger blackberry metabolites, targetting different genes of the flavonol-­anthocyanin pathway and yet, they both increase kempferol derivatives, suggesting a pivotal role for this flavonol in coordinating plant adaptation (Gutierrez-­ Albanchez et  al. 2020). This behaviour has been shown by Martin-Rivilla et  al. (2020) with Pseudomonas fluorescens N21.4 and further mimicked by its metabolic elicitors in blackberry leaves. Following these succesful field trials, we wondered if we would be able to mimic the response triggered by these two strains with their elicitors, as these are usually effective at lower concentrations and are easier to deliver in regular agronomic management. Therefore, another experiment in blackberry was undertaken in order to explore the ability of bacterial elicitors to mimic the systemic effects of QV15 delivered by soil drench, trying leaf application also. First, bacterial elicitors were obtained from 24 h cultures by centrifugation of the culture media to separate cells from metabolic products. Metabolic products (metabolic elicitors) were diluted in water and delivered by foliar spray; dilution was prepared to match the concentration of root inocula. The cell pellet was suspended in the same volume used for metabolic elicitors, autoclaved, constituting the structural elicitors; these were diluted to match the concentration of root inocula and delivered by foliar spray. The root inoculated with bacteria was kept as a positive control and non-inoculated controls were also in the trial. Each treatment consisted of 60 plants, arranged in 3 replicates of 20 plants each. Treatments were delivered every 2 weeks through a 6 month period. Samples (leaves and fruits) were taken at the peak of fruiting (month 5) when photosynthesis was measured. In leaves, photosynthetic pigments (chlorophylls and carotenes), antioxidant enzymes (SOD and APX) and the antioxidants total phenols, total flavonols and total anthocyanins were measured; the same analysis was done in fruits. Fruit yield was recorded. Data were analyzed by one way ANOVA and LSD posthoc test. Methods are described in detail in Gutierrez et al. (2017). The main results are summarized in Fig. 4.5; this presentation of data provides an overview of the plant response at a glance, to evidence the multitarget effects provided by PGPR, which is the purpose of this chapter. The first question to solve was to determine the effectiveness of leaf delivery as compared to roots. This can be evidenced in production, which is increased by QV15, and slightly by metabolic elicitors, and decreased by structural elicitors (Fig. 4.6a). Accumulated production per plant was 2.2% higher in QV15 inoculated plants (Fig. 4.6b); although statistically non-significant, it represents a nice commercial increase of 11.148 kg per ha, since plant density is 5000 plants/ha. The most relevant result related to crop yield is the increase in C fixation registered both under the strain delivered through the roots, as well as by structural and metabolic elicitors showing that they have triggered photosynthesis, probably improving Calvin cycle yield. However, only the strain itself triggers the net photochemical quenching (PQ) and results in increased fruit yield. Despite the significant increases in the number of flowers detected no significant increases were recorded for elicitors, probably due to the metabolic reprogramming upon elicitation

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Fig. 4.5  Summary of results. Green cells indicate significantly higher values than controls; red cells indicate significantly lower than controls; and empty cells represent no changes to control. Data were calculated from 3 replicates of 20 plants each. One-way ANOVA with replicates (3) and LSD as posthoc test was done; significance (p  20), so that the concentration of mineral N is decreased by the development of microbial biomass.

6.3  Effect of Organic Matter on Plants 6.3.1  Effect on Nutritional Status and Growth The enhancement of soil microbial biomass as a consequence of long term compost addition (Baldi et al. 2010, 2018), for example, stimulated nutrient mineralization in soil-improving plant nutritional status and total nutrient removal at the end of the orchard life (Table 6.6). In detail, the yearly application of compost at 10 t ha−1 for 14  years has increased macronutrient in the plant with values similar to mineral fertilization (Table 6.6). The increase of soil microbial biomass not only raises nutrient soil availability but also contributes to preventing the loss of mineral N and other nutrients by slowing the release of nutrients. A long-term field experiment on peach demonstrated that in the soil profile of 0.00–0.80 m depth, mineral N (sum of nitrate and ammonium) pool concentration ranged between 1 and 28 mg kg−1 showing a similar trend for all treatments. Only occasionally the application of compost at 10  t  ha−1 and mineral fertilization caused significant peaks of mineral N; however, it is interesting to note that the maximum N concentration was in those periods (late spring, early and late summer) of intense N absorption by plants (Toselli et al. 2019). Besides the effect of increased microbial activity, also the presence of humic acids in organic amendments is able to increase the availability of micronutrients (Nardi et al. 2002) and promote Fe acquisition (Chen and Aviad 1990; Pinton et al. 1999; Nardi et al. 2002) and nutrient uptake (Nardi et al. 2002) by plants.

Table 6.6  Effect of compost application on total nutrient content in peach trees after 14 years of amendment application Treatment Untreated control Mineral Compost low rate (5 t ha-1) Compost high rate (10 t ha-1) Significance

N g plant−1 360 b 587 a 403 b 568 a **

P

K

Ca

Mg

133 b 149 b 142 b 167 a *

325 417 343 435 n.s.

996 b 1262 a 947 b 1224 a *

107 b 135 a 107 b 137 a *

Within the same column, values followed by the same letter are not statistically different according to Student Neuman Keul test (P ≤ 0.05). n.s., *, **: effect not significant or significant at P ≤ 0.5 and P ≤ 0.01, respectively

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As a matter of fact, in the soil of the river Po Valley (Italy), leaf concentration-­ response to increasing compost application rate changes according to the nutrients. Leaf Ca (Fig.  6.2d), Cu (Fig.  6.3a), Fe (Fig.  6.3b) and Mn (Fig.  6.3c) increased linearly with the rate; leaf K (Fig. 6.2c) increased until 20 t ha−1, then it stabilized with a higher application rate. Leaf N (Fig.  6.2a) and Mg (Fig.  6.2e) and Zn (Fig.  6.3d) did not respond to the rate of compost, while leaf P decreased with increasing compost rate (Fig. 6.2b). A number of reports show that the application of organic matter induces a positive effect on plant growth. For instance, compost significantly enhanced strawberry

Fig. 6.2  Effect of compost application rate on leaf macronutrient concentration in commercial nectarine trees. R2 = correlation coefficient. DW, dry weight

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Fig. 6.3  Effect of compost application rate on leaf micronutrient concentration in commercial nectarine trees. R2 = correlation coefficient. DW, dry weight

(Wang and Lin 2002) and nectarine growth (Bravo et al. 2012; Sorrenti et al. 2019; Baldi et al. 2018); sludge induced a significant enhancement of apple plant growth (Bozkurt et  al. 2010); compost and compost+biochar positively influenced apple tree growth with more evident effect in the combination of the two amendments (Safaei Khorram et al. 2019). The application of compost, olive mill wastewater and cover crop with legumes increased olive growth (Chehab et al. 2019). The use of dried fungal biomass, vinasse and animal sewage promoted apple tree above and below ground growth and enhanced the final number of fruit (Polverigiani et  al. 2014). Compost, vermicompost and peat-compost mixture at planting increased apple tree growth in a clay soil from Israel (Gur et al. 1996) and sandy soil from USA (Peryea and Covey 1989). Similar results at planting were also observed when cow and chicken manures were applied (Van Schoor et al. 2009).

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Nonetheless many researches evidenced the positive effects of compost; there are also several studies that reports negative effects of compost application on seed germination (Tiquia 2010; Aslam and VanderGheynst 2008) and plant growth (von Glisczynski et al. 2016), mainly due to N immobilization by microbial competition (Hodge et  al. 2000) and to the release of phytotoxic compounds (Tiquia 2010). Organic amendments can, indeed, release a wide range of inhibitory compounds, like short-chain organic acids, tannins and phenols, mainly when not properly stabilized (Bonanomi et al. 2011); consequently, it is vital to supply amendments opportunely stabilized during the production process.

6.3.2  Effect on Yield and Fruit Quality The supply of mineral nutrients (De Brito et  al. 1995), the improvement of soil structure and water retention capability (Serra-Wittling et al. 1996), the enhancement of soil microbial and enzymatic activities (Garcıa-Gil et  al. 2000), and the control of soilborne pathogens (Bonanomi et al. 2010) are considered the main reasons of the improvement of plant yield, as a response of organic matter applications. This response is often observed even in absence of differences in leaf nutrient concentration, supporting the hypothesis that nutrient status is not the main cause of different yields (Roussos et al. 2017). An increase of fruit yield as a consequence of organic matter addition was observed in strawberry (Arancon et al. 2004; Mahadeen 2009; Wang and Lin 2002), apple (Bozkurt et al. 2010), sour cherry (Angin et al. 2012; Aslantas et al. 2013) and wine grape (Liu et al. 2016). In the latest case, the authors hypothesize that growth responses reflected the ability of humic acids, present in vermicompost, to act as plant growth regulators. Contrasting results on the effect of organic fertilization on fruit quality and nutraceutical value are reported in the literature (Prange 2015). Several evidences report a positive effect of organic fertilization on crop quality, including fruit color, weight, size, total sugars and anthocyanin contents in dates fertilized with chicken manure and cow dung (Marzouk and Kassem 2011). Strawberry fertilized with compost increased fructose, glucose, sucrose, total sugars and organic acid concentration (Wang and Lin 2002). Sweet cherry (Tan et al. 2018) and apple (Amarante et al. 2008; Peck et al. 2006) fertilized with organic amendment increased soluble sugar and total acidity. However, opposite results were reported in apple (Amiri and Fallahi 2009) and kiwi fruit (Amodio et  al. 2007). An excess of N available for plants was considered the main reason for the reduction of vitamin C concentration in fruits (Lee and Kader 2000). A similar response can describe the second-degree function response of fruit firmness and soluble solid concentration in nectarine to increasing compost application rate with the highest values found as a response to 20 t ha−1 (Fig. 6.4). While the fruit firmness is related to fruit maturation that can be delayed by the increase of N availability soluble solid concentration is the result of a balance between fruit and shoot competition for C. The best results in term of C partitioning to the fruit can be achieved with a compost application rate of 20 t ha−1.

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Fig. 6.4  Effect of compost application rate on soluble solid concentration and fruit firmness. R2 = correlation coefficient. SSC, soluble solid concentration

6.4  Biofertilizers Plant performances not only depens on soil available nutrients, but also on microorganism that live in agricultural soils; while some of them are detrimental, others have positive effects on plant, in term of growth (roots and aerial parts), root uptake, and tolerance to pathogen diseases (Glick et  al. 1998). Recently, the use of bio-­ fertilizers, together with the supply of organic matter has gained more importance due to the higher concern on crop sustainability and the preservation of soil quality. The term “bio-fertilizer” has been recently introduced to define a fertilizer (organic or mineral) that contains living cells of different types of beneficial microorganisms (Mohammadi and Sohrabi 2012). including bacteria, cyanobacteria, fungi (yeast, molds, mycorrhizae) and actinomycetes (Bora et al. 2016) with indirect or direct effects on growth promotion (Vessey 2003). Indirect mechanisms occur when they reduce or prevent the negative effects of abiotic and biotic stresses, through antibiotic production, nutrient and space competition and synthesis of lysing enzymes against phytopathogenic organisms (Lucy et al. 2004; Príncipe et al. 2007). Direct mechanisms include the synthesis of easily available compounds for plants (phytohormones, ammonia, etc.) and the solubilization of nutrients (Glick et  al. 1998; Vessey 2003; Lucy et al. 2004; Príncipe et al. 2007; Ahmad et al. 2008). The mechanisms of action of bio-fertilizers can be divided in five classes, according to different effects on plant growth: (1) increase of root surface area; (2) increase

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of the availability of nutrients in the rhizosphere through N2 fixation, nutrient solubilisation and production of siderophores (Glick et al. 1998); (3) establishment of a symbiotic relationship among microorganisms and host plant; (4) reduction of the proliferation of pathogens; (5) combination of actions (Persello-Cartieaux et  al. 2003; Vessey 2003; Van Loon 2007). Biofertilizers can fix yearly 20–200  kg  N  ha−1, can solubilize phosphorous (Richardson 2001; Artursson et al. 2006), in the range of 30–50 kg P ha−1, and K (Kumar et al. 2016), and mobilize P, Zn and Fe to varying extent (Bora et al. 2016). One of the mechanisms developed is the release of organic acids (such as oxalic, citric, butyric, malonic, lactic, succinic, malic, gluconic, acetic, glyconic, fumaric, adipic, and 2-ketogluconic), and the decrease of rhizosphere pH (Kim et al. 1998; Richardson 2001). In the literature, there are a number of papers dealing with the employment of bio-fertilizers in fruit crops. Root-applied combinations of Bacillus spp. and Microbacter increased cumulative yield, fruit weight and nutrient acquisition of apple Granny Smith in Turkey (Karlidag et al. 2007). The use of yeast in combination with beneficial bacteria promoted an increase of yield in the Topaz apple variety (Mosa et al. 2016). Beneficial microbial, including Azotobacter chroococcum, Pseudomonas spp. and mycorrhizal fungi (Glomus fasciculatum) improved kiwifruit crop (Khachi et  al. 2015). Leaf-applied N-fixing-bacteria-Azotobacter, Azospirillum and Beijerinkia were effective in promoting mulberry leaf yield for silkworm rearing and cocoon production (Sudhakar et al. 2000). A positive effect on cherry and apricot yield, vegetative growth and leaf nutrient concentration was also found in response to flower and/or foliar application of Pseudomonas (strain BA-8) and Bacillus (strain OSU-142) alone or in combination (Esitken et al. 2006). Similar results of floral and foliar application of Pseudomonas and Bacillus were also obtained on apple cv. Starkrimson and Granny Smith grown in Turkey (Pirlak et al. 2007). The positive effect was related to the N2-fixing capacity of both bacteria strains along with specific positive activity on auxin (OSU-142) and zeatin (BA-8) hormone production. The foliar fixation of N enhanced shoot growth and induced a greater uptake of nutrients from the soil (Esitken et al. 2006). Growth promoting hormones such as auxin and cytokines, on the other hand, are effective in stimulating cell division and fruit growth (Esitken et al. 2006). Mycorrhizal inoculation with Glomus epigaeum, G. mosseae and Gigaspore calospora increased height, root length, number of leaves and dry weight of micro propagated pomegranate (Singh et al. 2012) plantlets. Similar results were obtained in apple (Sharma and Bhutani 1998) and peach (Wu et al. 2011). Moreover, mycorrhizal inoculation was found to improve the nutritional status of peach seedling (Wu et al. 2011). Pear plants of the cv. Gola inoculated with Azotobacter and Azospirillum showed a greater uptake of NO3−, NH4+, H2PO4, K+ and Fe2+ (Mohammadi and Sohrabi 2012) and a higher vegetative growth (Azotobacter), fruit yield and quality (Kumar et al. 2013), indicating that chemical fertilization inputs can be reduced when plant growth-promoting rhizobacteria (PGPR) are applied to plants.

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The combined effect of Bacillus, strain M3 in combination with strain OSU-142 increased yield, growth and nutrition of raspberry plant under organic growing conditions (Orhan et al. 2006). In addition, these two strains were able to solubilize phosphates and to increase organic matter mineralization through the process of acidification, chelation and exchange reactions in plant growth media. Bio-fertilizer inoculation with Pseudomonas flourescence was found to significantly improve fruit quality, yield, weight, and soluble solid concentration and juice volumes of Washington navel orange (Shamseldin et al. 2010); while inoculation with Azospirillum brasilence did not significantly improve yield and fruit quality. P. flourescence was also able to reduce growth and diffusion of soil nematode more than A. brasilence (Shamseldin et al. 2010). On the other hand on strawberry, none of the individual microorganisms from each species or their mixture showed growth-promoting-effects in more than two experiments and dual inoculation was not more effective than the single one (Vestberg et al. 2004). The concentration of the beneficial microorganisms in bio-fertilizers should allow the colonization of the rhizosphere at a sufficient population density to produce their beneficial effect (Bloemberg and Lugtenberg 2001). In apple (Kardilag et al. 2007) and sweet cherry (Esitken et al. 2006), a positive effect was obtained using 109  CFU (colony forming units) ml−1. However, IAA-producing-PGPR should not be applied over the 106 CFU ml−1, because they can trigger ethylene-­ mediated negative effects (Persello-Cartieaux et al. 2003). Although the number of beneficial microorganisms declines rapidly in the rhizosphere after inoculation, their effects usually last throughout the growing season (Lucy et al. 2004). The correct management of fertilization is the first mean to increase soil beneficial microorganism; for example, the use of organic fertilizers stimulates microorganism proliferation (Mohammadi and Sohrabi 2012). In addition, the use of endophytic efficient genotypes that can easily adapt to soil conditions is able to promote plant growth (Compant et al. 2005; Forchetti et al. 2007; Príncipe et al. 2007).

6.5  Conclusions The application of organic matter could, besides increasing fruit tree performances, be a useful tool to improve soil organic C stock and fertility in intensive agriculture systems. Soil acts as a C reservoir playing an important role in the mitigation of climate change. Soils of agroecosystems can have an important C sink capacity: it was estimated that an increase of soil organic carbon of 4‰ every year can balance anthropogenic CO2 emissions (Lal et  al. 2015). Most of the organic amendment derives from the recycling of waste reducing, thus, the cost of disposal and landfill management. The challenge of future research will be the identification, for each soil, of the organic amendments that can maximize C stock and, at the same time, allow a sufficient release of mineral nutrients to sustain orchard yields and plant performances minimizing eventual detrimental effects.

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Chapter 7

Evaluation of Turbulence Stress on Submerged Macrophytes Growing in Lowland Streams Using H2O2 as an Indicator Takashi Asaeda, M. Harun Rashid, L. Vamisi Krishna, and M. Rahman

Abstract  Submerged macrophytes are subjected to a vast array of stresses in natural waters. Since each stress factor has a different mechanism of affecting the plants, it is often difficult to evaluate the total level of stress acting on the macrophytes. Therefore, using environmental factors to devise a common index for assessing the magnitude of the stress acting on submerged macrophytes is necessary. It is well known that environmental stresses intensify the generation of reactive oxygen species (ROS) in plant tissue, among which H2O2 is the major component. Thus, the possibility of using the concentration of H2O2 in the plant tissue as an indicator of the environmental stress was investigated. Although the flow velocity is one of the strongest stress factors of submerged macrophytes in a natural stream, the solar radiation also contributes to the generation of ROS through the photosynthetic process. Therefore, derivation of the stress component due to the flow velocity and solar radiation is particularly important. The total H2O2 concentration level is approximately given by the sum of the H2O2 concentration generated by each stressor. The antioxidant activities increased proportionally with the H2O2 concentration; however, there was a delay in the response of the antioxidant activities. The comparison of the fractions of the H2O2 concentration due to the light and velocity stresses reveal that the oxidative stress from the solar radiation and flow turbulence

T. Asaeda (*) Hydro Technology Institute, Tokyo, Japan Institute for Studies of the Global Environment, Sophia University, Tokyo, Japan Research and Development Center, Ibaraki, Japan Department of Environmental Science, Saitama University, Saitama, Japan e-mail: [email protected] M. H. Rashid · L. V. Krishna · M. Rahman Department of Environmental Science, Saitama University, Saitama, Japan © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_7

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are the dominant stressors in this natural stream. These results also indicate that the H2O2 concentration in submerged macrophytes can be considered a suitable index of the environmental stresses. Keywords  Flowing water · Hydrogen peroxide · Oxidative stress · Photoinhibition · Reactive oxygen species · Submerged macrophytes · Turbulence

Abbreviations APX Ascorbate peroxidase ATP Adenosine triphosphate CAT Catalase Chl Chlorophyll H2O2 Hydrogen peroxide POX peroxidase PSII Photochemical system II ROS Reactive oxygen species

7.1  Introduction The chapter aims to discuss the interconnection between the processes of stress-­ related reactive oxygen species (ROS) production and the macrophyte biomass formation, H2O2 as a common indicator for evaluating each environmental stress level, then evaluated the effect of flow velocity in a normal stream under solar radiation, and finally proposed a methodology for obtaining the distribution and potential biomass of macrophytes as a function of the dominant environmental stress. The distribution of submerged macrophytes is an important characteristic of natural streams and may have either a positive or negative effect on river management. Natural stream channels have various types of environmental stresses, such as flow velocity (Bornette and Puijalon 2011; Ellawala et  al. 2013), temperature (Santamaria 2002; Panda and Khan 2004; De Silva and Asaeda 2017a), pH (Nimptsch and Pflugmacher 2007), and anoxic sediment (Zaman and Asaeda 2013; Pal et al. 2014), which together control the biomass distribution of macrophytes. Under normal channel conditions, without stresses such as salinity, temperature, and chemical compounds, the flow velocity is one of the dominant stressors and thus affects the distribution of habitats and biomass in the river channel (Franklin et al. 2008). There have been many studies conducted on the macrophyte tolerance of flow velocity. The relationship between the mechanical strength of the plant body and

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drag force (Bal et al. 2011; Puijalon et al. 2011) and the uprooting and flow velocity (Puijalon et al. 2008) are important factors that simultaneously determine whether the plant body can endure the flow velocity. Additionally, the growth rate is affected by the flow velocity (Chambers et al. 1991). In high flow velocity, more favorable plant morphologies are formed by the suitable balance of hormones (Ke and Li 2006). These concepts, based on hydrodynamics, describe the macrophyte-tolerant mechanical conditions in running water. However, since these concepts are based on the instantaneous balance of external force and strength, it is difficult to generalize the suppression level in the field with various environmental stresses. The understanding of the suppression level of macrophyte growth among environmental stresses requires a common indicator with which to evaluate the stress level. In macrophyte bodies, ROS are inevitably formed by the leakage of electrons onto O2 from the electron transport activities of chloroplasts, mitochondria, peroxisome, plasma membranes, etc. or as a byproduct of various metabolic pathways localized in different cellular compartments (Nakano and Asada 1981; Asada 2006). In high concentrations, all ROS are extremely harmful to organisms; thus, macrophytes have various defense mechanisms to reduce ROS (Gill and Tuteja 2010; Suzuki et al. 2012). The generation of ROS is enhanced when the macrophytes are subjected to high environmental stresses, and a state of oxidative stress occurs when the level of ROS exceeds the amount controllable by the natural defense mechanisms (Gill and Tuteja 2010). Under oxidative stress, the excessive ROS poses a threat to the cells by causing peroxidation of the lipids, oxidation of the proteins, damage to the nucleic acids, enzyme inhibition, activation of the programmed cell death pathway, and ultimately leads to death of the cells (Gechev et al. 2006). At the same time, ROS are well known second messengers in a variety of cellular processes, including tolerance to environmental stresses, to avoid oxidative injury (Apel and Hirt 2004; Sharma et al. 2012). ROS are intensively generated in chloroplast by the activity of photosynthesis, when plants are exposed to light (Ohnishi et al. 2005; Asada 2006; Foyer and Noctor 2009; Poulson and Thai 2015). Therefore, in natural waters, solar radiation is a possible important stressor during the daytime, although it has not shown to have a strong effect in previous laboratory experiments. Even though flow velocity is a very important environmental factor for running water macrophytes, the responses of macrophytes to flow velocity in the field have not much elucidated. Flow velocity in a natural channel is divided into two components: mean flow velocity, which is the average velocity during a certain period, and turbulence, the fluctuating deviation from the mean flow velocity. Mean flow exerts a tension stress on the plant body in the flow direction, while turbulence creates a fluctuating force in continuously changing directions. In recent studies, it was elucidated that turbulence is more stressful to the macrophyte body than mean flow is (Atapaththu and Asaeda 2015).

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7.2  Dominant Stressors in the Natural Water In streams and rivers, flow velocity regulates macrophyte growth (Puijalon et  al. 2011), indicating that it is one of the dominant stressors. Atapaththu and Asaeda (2015) conducted laboratory experiments and reported that the turbulence intensity was more stressful for the macrophytes than the mean flow and that the turbulence intensity induced much greater oxidative stresses. Turbulence is always associated with the mean flow in natural running water since the Reynolds number generally exceeds the critical value. In a natural channel, however, the turbulence intensity has a different trend from the mean flow velocity, depending on the conditions of the river channel, such as bottom surface roughness and the complexity of the channel morphology (Blanckaert and Graf 2001; Roy et al. 2004). The present results indicate that the H2O2 concentration in the plant tissue had a significantly higher correlation with the ambient turbulence intensity than the mean flow velocity, confirming that the oxidative stress of the plant is attributed to the turbulence rather than the mean flow in the natural channel. These results are consistent with those of previous laboratory experiments. In a natural river channel, the mean surface velocity is normally applied to the representative velocity scale for the macrophyte growth (Biggs 1996; Kemp et al. 2000). This might be reasonable for the flow velocity in a relatively uniform channel; however, in order to generalize the relation for different types of channels, particularly in riffle and pool systems, the turbulence intensity should be selected instead of the mean flow velocity as a reference for the velocity scale. Solar radiation is generally more intense in nature than in laboratory experiments. Reactive oxygen species are intensively generated in chloroplast during photosynthesis when plants are exposed to high amounts of light. Therefore, in natural waters, solar radiation also becomes a strong stressor for the submerged macrophytes, and oxidative stress is generated intensively during the daytime. The temperature of natural water periodically varies depending on the seasons, while further fluctuations follow the daily meteorological conditions and the water characteristics upstream. In addition, the water temperature is generally rising due to the recently climatic change. In the present study, the temperature variation was also a strong stressor on the submerged macrophytes, although it was not as influential as the solar radiation or turbulence (De Silva and Asaeda 2017b; Asaeda et al. 2020). In natural streams without other location-specific stressors, the turbulence intensity, solar radiation and temperature generally have strong effects on the growth of submerged macrophytes.

7.3  Effect of Temperature on ROS and Antioxidant Activities The effect of temperature on the generation rate of the ROS and antioxidant activities were also investigated in the laboratory experiments. E. densa plants were cultured in four tanks similar to those of the previous experiments, except in this

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experiment light was continuously provided for the entire duration. After an acclimatization period (2 months from the date of planting), the temperature regimes of the tanks were set to 10, 15, 25 and 30  °C, respectively. 7  days after setting the temperature of the tanks, E. densa tissues were sampled for the chemical analyses (De Silva and Asaeda 2017b). To assess the effect of temperature regimes on H2O2 in the E. densa tissue, the following empirical equation was developed from the results obtained in the temperature experiment:

H 2 O2  0.316  Temp  16.25

where H2O2 is the concentration of H2O2 (μmol ·g−1FW) in the E. densa tissue and Temp is the temperature (°C) of the growth medium (Hoagland’s solution). The H2O2 concentration is a representative value of ROS, catalase (CAT), ascorbate peroxidase (APX) and peroxidase (POX) activities, and the concentration of the photosynthetic pigments, chlorophyll-a (Chl-a) and chlorophyll-b (Chl-b), and carotenoid were analyzed for the sampled E. densa tissues from both experiments (Fig. 7.1a,b).

7.4  E  ffects of Photosynthesis on the H2O2 and Antioxidant Activities Superoxide ions, generated at PSII during photosynthesis are converted to H2O2 by the activity of superoxide dismutase (Scarpeci et al. 2008), and H2O2 finally decomposes into water and oxygen by the activities of APX, CAT, POD, etc. (Mittler 2002; Caverzan et al. 2012). When submerged macrophyte E. densa was subjected to a dark exposure experiments, the H2O2 concentration in the E. densa plant tissues was the lowest (2 μmol · g−1 FW) after 30 min of the darkness treatment, and then later increased (Fig.  7.2a). When E. densa was under continuous light, the ROS were generated during photosynthesis and simultaneously scavenged by the antioxidant activities (Fig. 7.2b). After initiation of the darkness exposure, the H2O2, which was intensively generated by the photosynthesis during the light period, is scavenged by the slowly responding antioxidant activities, though H2O2 is generated by other stressors at a lower rate. Thus, the H2O2 concentration decreases and have the lowest concentration within 30 min, when the generation rate of the H2O2 balances with the antioxidant activities. In the prolonged darkness, however, although the H2O2 concentration starts to increase, antioxidant activities do not increase at the same rate, leading to a further increase in the H2O2 concentration. Therefore, it seems that the H2O2 concentration after 30 min of darkness corresponds to the environmental stress level exclusively due to the effect of photosynthesis. The excessive amount of H2O2 concentration in the samples under continuous light over the H2O2 concentration in the samples that underwent the 30 min of dark

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corresponds to the effect of photosynthesis and correlates with the concentration from samples under the continuous light (Fig. 7.3).

7.5  T  he Indicator of the Fractions of Stresses Associated with the Turbulence Stresses The level of the H2O2 concentration from the samples under continuous light has a higher deviation with respect to the turbulence intensity than the samples treated with 30 min of darkness (Fig. 7.4a, b). The H2O2 concentration, after removing the amount corresponding to the stressful temperature exposure and photosynthesis, has a relatively unique relationship with the turbulence intensity. The trend was similar to the result of the oscillating grid laboratory experiment, where the amount of H2O2 in the macrophyte tissue was proportional to the root mean square velocity of the turbulence (Asaeda and Rashid 2017). This indicates that the total H2O2 concentration is the linear integration of the amount produced by the different stressors, and the level of these different stresses are evaluated separately, in practice, by the respective H2O2 concentrations (Asaeda et al. 2020).

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The difference between the light and dark treatment experiments corresponds to the amount generated by the light stress, which widely varies in approximately 2 ~ 10 μg H2O2 · g−1 FW. The variation in the solar radiation intensity during the day is reflected in the H2O2 concentration. The intercept value of the dark treatment experiment, 2–3  μg H2O2 · g−1 FW, given in Fig.  7.4(b) is the sum of the other stresses and normal metabolisms, except for the temperature change. The value was nearly the same as that of the laboratory experiment (Asaeda et al. 2017). Therefore, in the daytime, the total amount of H2O2 generated in the plant tissues is primarily the sum of the amount generated by the environmental stress plus the amount generated during photosynthesis. This process can be generalized with the following simple equation (Asaeda et al. 2020).



H 2 O2  Total   H 2 O2 Photosyntheis,Metabolism    H 2 O2  Environmental stress



(7.1)

Although there might be some interactions between the different environmental stressors (Rivero et al. 2014), it is possible to separate the stress levels by their share of the H2O2 concentration (Mitter 2002; Asaeda et al. 2021).

7.6  Stress Patterns of the Changing Light Intensity The response of the ROS generation to the environmental stress is relatively fast compared to that of the antioxidant activities. Under natural conditions, the solar radiation intensity frequently changes. Therefore, there is a time lag between the current level of the ROS, which corresponds to the current condition of the environmental stressors and that of the antioxidant activities that reflects the earlier conditions. The difference in the response time differentiates the variation pattern of the ROS concentration in macrophyte tissues from those of the environmental stress. As the environmental stress level increases, the antioxidant activities are insufficient to scavenge the ROS, consequently increasing the ROS activities; however, as the environmental stress level decreases, the excessive antioxidant activities reduce the ROS activities to a lower level. The slower buffering capacity of the antioxidant activities, in comparison to the generation of the H2O2 due to environmental stressors, affects the daily variation in the H2O2 concentration. The H2O2 concentration increases in the daytime until 15:00, and it decreases thereafter, followed by a decrease in the antioxidant activities. After the sun sets, the H2O2 generation is lower than the daytime values; the H2O2 is scavenged considerably by the antioxidant enzymes and further decreases in concentration.

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7.7  E  ffect of the Water Turbulence on the Structural Components of the Macrophyte Tissues Cellulose and lignin substantially increase with turbulence intensity. These compounds contribute to the stiffness of the cell wall and are not used for metabolism. In highly turbulent flow, such as in shallow water with a high velocity flowing over a gravelly bed, with high mechanical stresses, plants allocate more resources to increase cellulose and lignin components, although the plant growth is repressed. In contrast, in deeper water, where turbulence intensity is relatively low, plants allocate more resources for biomass production rather than cell strength. H2O2 is involved in lignin synthesis by the reproduction of cell wall by catalase (Elster and Heuple 1976; Paradakis and Roubelaski-Angelaskis 1999), thus a high concentration of H2O2 in a high-turbulence zone likely contributes to the synthesis of a large amount of lignin.

7.8  Biomass The E. densa biomass had a positive correlation with the chlorophyll-a concentration, regardless of the river and season. The chlorophyll-a concentration slightly decreased during the 30-min dark treatment in some tests (Fig. 7.5a), however, the deviation from the continuous light condition was small. Most likely, it takes a longer period than 30 min to reduce the concentration with a significant margin. The chlorophyll-a and H2O2 concentrations show a linear negative relationship (Fig. 7.5a). The enhanced ROS generation in the plant tissue from turbulence damages the biomolecules of the organelle, including the ATP synthesize machinery associated with chlorophyll-a (Szechynska-Hebda and Karpinski 2013). Under these types of conditions, chlorophyll-a cannot utilize the light energy to its maximum capacity and the excess light energy due to the reduction of the electron demand in the electron transport chain further enhances the generation of ROS. Macrophyte biomass is a function of the accumulated photosynthetic products, which are dependent on the chlorophyll-a concentration, and the respiration loss. Since the average light intensity was similar among the rivers and study sections, the biomass had a positive correlation with the chlorophyll-a concentration. In the river channel, the chlorophyll-a concentration in the macrophyte tissue decreased following the decrease in the light intensity and increase in the turbulence intensity, which in turn decreased the biomass. With increasing depth, the light intensity decreases. Additionally, at deeper depths, the macrophytes reduce the turbulence intensity by their own biomass. Thus, by growing at deeper depths, they reduce the high light intensity and thus the destruction of the photosynthetic apparatus, and they also reduce the ROS generation. Thus, at deeper depths in the river channels, the macrophytes produce greater biomass than they would at shallower depths. In this study, the biomass of E. densa has a high correlation with depth, providing the largest biomass at 100  cm deep (Fig.  7.6). Since the depths of observed

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sections of these rivers were relatively shallow, the large biomass was always observed in the deepest zones. The observed light intensity at the depth was ~100 μmol · m−2 · s −  1, which equals to the estimated value using the attenuation coefficient of light in the water of these rivers, ~0.03 cm−1. E. densa profusely grow with this light intensity and can produce a large biomass.

7.9  Conclusion Submerged macrophytes are exposed to various abiotic stressors in natural rivers, although the contributions of each stressor are rarely evaluated. H2O2 is one of the reactive oxygen species that are generated due to the environmental stress level. The total concentration of H2O2 in the plant tissues is an indicator of the environmental stress level that the plant is exposed to. The dominant stressors in the field are the flow velocity, intensive solar radiation, and temperature. For the flow, the turbulence rather than the mean flow velocity is the main component that generates H2O2, and there is a linear relationship between the turbulence and H2O2 concentration. The ROS are intensively generated during photosynthesis, and the daytime solar radiation is another dominant stressor in the natural waters. The ROS are scavenged by the antioxidant activities, but there is a time lag between the H2O2 generation and the antioxidant activities, and the antioxidant activities slow the H2O2 concentration in the plant tissues. The generation of the ROS is more prominent than the antioxidant activities during the most intensive period of solar radiation. The chlorophyll-a concentration in the plant tissues has a negative relation with the H2O2 concentration. In a natural river, these processes result in a nearly linear increase in the E. densa biomass with increasing depth, down to a sufficient light intensity. Acknowledgements  A grant-in-aid, Scientific Research (b) (15H04045) (19H02245) from Japan Society for the Promotion of Science, Development Grant for River Management Technology from the Ministry of Land, Infrastructure, Transportation and Tourism, Japan, and River Found from River Foundation of Japan supported this study.

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Chapter 8

Opportunities of Revegetation and Bioenergy Production in Marginal Areas Agustina Branzini and Marta S. Zubillaga

Abstract  Production and use of bioenergy must be a priority in order to satisfy the critical necessity to diversify the primary energy sources. Renewable energy sources, such as bioenergy became an interesting strategy to develop as the urgency of greenhouse gases (GHGs) emission increases. To respond these needs and considering that the environmental control of post closure landfills is a requisite, the reinsertion of these sites into its environment is a challenge. There are different strategies to reinsert final disposal site, such as landscape integration, social use or renewable energy generation. In fact, considering bioenergy production, C4 species are grown as energy crops proposed for restructured energy system. This chapter intends to recognize the positive consequence of revegetation strategy with bioenergy purpose in a landfill on their post closure stage. In a bioeconomy framework this is an innovative experience since the use of the post-closure landfill area for the production of biomass crops as a clean energy source. Keywords  Biomass · Soil · Closed landfill · Rehabilitation · Bioenergy

8.1  Global Solid Waste Generation Globally, there is an increasing of waste generation rates. According to World Bank information (2021), the world generated 2.01 billion tons of municipal solid waste annually (0.74 kg person per day), which was approximately 38% higher than that reported in 2016 (Los Angeles Times 2016). In effect, is projected an increase by

A. Branzini (*) · M. S. Zubillaga Department of Fertility and Fertilizers, School of Agronomy, University of Buenos Aires, Buenos Aires, Argentina e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_8

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70% of annual waste generation from 2016 to 2050 (Kaza et al. 2018a, b). In fact, the World Bank has predicted that the above figure is likely to rise to nearly 4 billion tons by the year 2100 (Los Angeles Times 2016). This trend can be explained as a result of different aspects such as population growth, increased in living standard and industrialization amongst others. In view of regional waste generation, Asia, Pacific region and Europe are the continents that generate more waste annually, being this generation over 300 million tons. Instead, North America, Latina America and The Caribbean and Africa, generate less than 300 million tons of waste annually (Kaza et al. 2018a, b) (Fig. 8.1). There is a positive correlation between waste generation lifestyle and income level. However, there is dissimilarity in waste generation projection between countries. In high-income countries, daily per capita is projected to increase by 19% in 2050 and in low- and middle-income countries, it is expected that this increase be a 40% or more (Kaza et al. 2018a, b). As well, waste composition varies across income levels, reflecting diverse patterns of consumption. This variation mainly occurs due to density and moisture content of waste (Kumar 2020), and then social and economic development, such as energy sources and climatic zones are the most important aspects influenced in waste composition. In most cases, this composition defined waste collection and how it is disposed. Usually, municipal solid waste classification includes organic and inorganic current (Hoornweg and Bhada-Tata 2012). Highest proportion of municipal solid waste in high-income countries is inorganic materials compared with low-income countries that the primary constituents of waste are degradable organic matter and paper (Kumar 2020). In waste management terms, weight and volume are two important parameters to consider. Although organics and inert

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Fig. 8.1  Regional waste generation annually, according The World Bank 2021

20%

25%

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decrease, paper and plastics increases as a country’s affluence increases, prevailing waste volumes (Hoornweg and Bhada-Tata 2012).

8.2  Nonhazardous Waste Treatment Management of municipal solid wastes is a large challenge for local governments. As the future of resources is planned, local governments increased the implementation of integrated waste management concept. At first, this management practice comprises reduction of wastes generation and then, in waste stream, the recovery of generated waste for recycling or composting. It also includes energy recovery as viable environmental management and secures landfilling practices (EPA 2019a, b). However, the World Bank’s report (2018) indicated that more than 30% of municipal solid waste is managed in an environmentally inappropriate manner. In fact, in low income countries, over 90% of waste is mismanaged (Kaza et al. 2018a, b). This increases emissions and disaster risk, which affects the poor disproportionately. Another data associated with this social-economic impact is that waste management costs comprise 20% of municipal budgets on average (Kaza et al. 2018a, b). Consequently, in worldwide, the most common treatment for nonhazardous waste is land disposal method (Butt et al. 2014; Aleya et al. 2019). The use of landfill sites for disposal municipal waste is until perceived as a suitable practice in many developed countries as long as highly engineered facilities are implemented (EPA 2019a, b). Since landfills are the most used and worldwide spread method of municipal solid waste disposal (Wong et al. 2015; Koda et al. 2017), most of the world’s non-engineered landfills are located in Africa, Latin America and Asia with direct impact on the public and environmental health (Mavropoulos and Newman 2015). However, Vaccaro et al. (2019) suggest that contaminants concentration from landfills in these continents may be more influenced by local conditions, consumption patterns and the waste management behaviors of people. The International Solid Waste Association (ISWA) assumed that landfills receive almost 40% of the world’s waste that serve for 3–4 billion people approx. Therefore, disposal of municipal solid waste in these sites comprises different environmental risks and increases concerns about negative impacts on human health, such as air, soil and groundwater contamination, risk of fires, bad odors and poor quality of lifestyle in the surroundings (ISWA 2021; Adamcová et al. 2017). In effect, as landfills may contain a wide diversity of contaminants, management strategies must be developed in order to reduce any storage-related risk of contamination (Morris and Barlaz 2011; Gibbons et  al. 2014; Bichet et  al. 2016; Ben Salem et  al. 2017). Certainly, the three major environmental challenges associated with landfills sustainable management are the reduction of greenhouse gas emissions, mitigation of soil and groundwater contamination, and reduction of odor (Lamb et al. 2014). Currently, in most worldwide countries, municipal solid waste collection, transport and final disposal is one of the major problems of urban and rural environment. Inadequate final disposal of waste is one of the challenges for achieving

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sustainability development around the world. Thus, municipal solid waste management solutions must be financially and technically feasible, socially acceptable and environmentally responsive within the current legal framework of each region. Since landfill consequences includes contamination of ecosystems, climate change and public health problems, solid waste management issue is the biggest challenge to governments of small and large cities (Hussein et al. 2018).

8.3  Landfills Restoration. Postclosure Use The “active life” of each landfill site is the period of operation which waste is received for disposal. This period begins with the initial waste receipt and ends with achievement of closure actions. Closure is the process during which a landfill site is no longer accepts waste and prepares for post-closure maintenance according to an approved monitoring plan. Landfill sites must be closed in agreement with applicable protocols and local regulations in effect at the time (CalRecycle 2018). To close landfill sites, once it reaches its capacity, it is covered with a 45  cm compact layer to prevent infiltration and erosion, thus improving the establishment of a vegetation cover. However, many old landfills over the world have not been managed, because local authorities often do not have the expertise, resources or required personnel to implement proper management (Szabó et al. 2017). That’s the reason why in many cases, contamination from inappropriate landfill closure continues even after decades of disuse (Madon et  al. 2019). In that sense, after the landfill is closed, it is necessary a long-term monitoring of gas and leachate composition and its essential its restore to contain the contaminants. These activities have become essential in order to (i) certify that the contamination potential of leachates decreases over time, and to (ii) support authorities in selection the precise method for removal of contaminants (Grisey and Aleya 2016). The most important actions in post-closure care for municipal solid waste landfills consist of groundwater monitoring, leachate collection and treatment, gas recapture and management, final cover maintenance and risk assessment (Vesilind et al. 2001; Caldwell 2004; Tansel et al. 2008). Rate and duration of leachate and gas production from closed landfill sites are defined by diverse factors such as waste characteristics, microclimate, landfill design and closure strategies (Lee and Jones-­ Lee 1993; Tansel et al. 2007). It is recommended that a post-closure of landfills care period be 30  years for municipal solid wastes. According to EPA (2016), this post-closure care period could be modifying by local government guidelines on a site-specific basis. A closed landfill site is considered stable when it no longer represents a risk to human health and the environment. However, there are currently no specific technical criteria for the systematic assessment of the stability of closed landfills that, in turn, facilitate an objective determination of the modification of the 30  year post-closure care period in each landfill case (Tansel et al. 2008; Sizirici et al. 2011). Into this reality, is challenging to decide when extend or reduce the post-closure care period.

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On the basis that municipal solid waste landfills are habitually located in proximity to urban areas, there is an interest to transform them in productive lands through its redevelopment (Hard et al. 2019). The use of post-closed landfill should be compatible with the processes that this will suffer over time and the protection measures installed, as well as the follow-up and post-closure maintenance tasks (Lobo García de Cortázar et al. 2016). In order to restore post-closed landfill, technical, energetic, ecological, economic and social aspects determine the possibilities of its future use. As opportunities that arise from adequate planning, the implementation of innovative technologies and the emergence of new businesses associated with sustainable alternatives stand out. These opportunities are fundamental to achieve the transition towards renewable energies and face the challenge of adapting to the bioeconomy (Bolan et al. 2013). Thus, there are different strategies to deal with the recovery and reinsertion of a closed final disposal site, with varied experiences around the world. With regard to the reinsertion of these sites, it could be mention landscape integration with wildlife refuge, recreational park, agricultural cultivation, commercial use or the energy park (solar, wind), which could be grouped into natural areas (NA), social use (SU) and renewable energy generation (RE). Through a biometric analysis carried out previously, these 3 categories of post-closure landfills were implemented in different parts of the world (Fig. 8.2). In fact, a closed landfill site could be reused for various purposes in function to community needs; then is interesting consider combination between maintenance and the use of landfill such as the development of biomass and bio waste recycling facility (Vesilind et al. 2001; Morris 2005). North America 12 10 8 6 4 2

Asia

NA

0

SU

RE

Latin America

Europe

Fig. 8.2  Participation of different parts of the world in definition of closed landfill uses

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The interest in landfill redevelopment for productive purposes has been explored in different studies with a wide spectrum of results and also has several potential concerns associated to green use. In the UK, Green et al. (2014) found that sites where historic landfills have been reused for grazing have exposure levels below tolerable ones, being safe for the animals, however the animals could be exposed to higher metal ingestion rates than would be expected from rural conditions. Another study in Eritrea informed that crops grown in landfill site improved the fertility of soils but it had alarming concentrations of heavy metals (Tesfai and Dresher 2009). Conversely, Gworek et al. (2016) studied heavy metal concentrations in soil, plants, and water in the surrounding area of a Polish municipal solid waste landfill and observed that concentrations were similar to natural concentrations offsite. In general, the cover soil for closure landfill sites is collecting form adjacent areas up to 100 m depth. The resultant soil often has poor nutrient contents and low moisture, which could limit plant growth after the waste recovery (Song and Lee 2010). Another limitation is that on occasion this cover soil does not present seed bank to enables natural revegetation after closure and seed dispersal from surrounding areas could be limited if the landfill is to large (Song 2018). Therefore, selected species for revegetation must have arid-adapted characteristics, be heavy in weight, have wind resistance, and stock sufficient energy for the initial growth to survive at the environment. Furthermore, it is important to consider that as landfill surface is relatively has low nutrient contents (Song and Lee 2010) plants could showed poor rates both in germination and seedling survivals. It is important to mention that although the selected species could be popular for revegetation, the landfill has a unique condition. In a revegetation study located in South Korea (Song 2018), native plant species were selected to apply to the landfill soil for hyroseeding experiments. Each species was selected by their lifeform, features and colors, with perennial species being preferred. Results of this study showed that all species presented higher than 50% germination rates, with Brassica campestris and Dianthus sinensis L. showing 100% germination. However, they mentioned that poor soil condition was the reason for not adapted plants to landfill conditions. Biological rehabilitation of anthropic constructed areas including landfills (Shen et al. 2008) may be effected by traditional methods of plant covering or use of the hydroseeding technology (Głażewski and Makowski 1993). The method of hydroseeding has been performed for revegetation and refers to the application of seeds and supplementary materials such as fertilizers and organic amendments. Also, seeding hydromixtures could be made of the sewage sludge from the communal treatment plants and compost from liquid manure. Projects included in diverse use categories are an opportunity to front of the bioeconomy challenges, since they argument to an increase in renewable energies, contributing to the diversification of the energy matrix and its environmental benefits.

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8.4  Bioenergy as Strategy in Closed Landfill The global energy supply is dominated by fossil fuels since the dawn of the industrial revolution to the present-day. Coal, oil and gas are the primary energy drivers globally (World Bioenergy Association 2019). Although primary energy supply from renewables has increased by 48% since 2000, an energy transition is necessary. This transition is a trail to transformation of the global energy sector from fossil-based to zero-carbon by the second half of this century (IRENA 2021). Having an extensive energy mix is most likely to be the best manner to achieve energy and climate change targets (Welfle et al. 2014). The trail to energy transformation is beginning since around 19% of the global energy demand is met through renewable sources, out of which, modern renewable contributes up to 10% (Edrisi and Abhilash 2016). In fact, bioenergy is the largest renewable energy source globally that could help mitigate climate change, provide energy security and also promote rural development (Das et  al. 2020). In 2017, biomass had an important participation in renewable energy supply, representing 70% of the total renewable supply. However, it is important to note that in developing countries, is the traditional use of biomass for cooking and heating, the most important source that contribute of biomass supply globally. The availability of a diversity of feedstock and residues to produce solid, liquid and gaseous biofuels for use in electricity, heat and transportation profits bioenergy development around the world. In fact, with the increasing use of modern biomass solutions like wood pellets, biogas and liquid biofuels, contribution of modern bioenergy sources will be a major part in the future renewable energy mix (World Bioenergy Association 2019). In several regions around the world, the role of bioenergy is relatively important or has an enormous potential to have developed. In Africa, 96% of all renewable energy supply is contributed by biomass and in other continents such Asia, America and Europe this biomass participation is closely to 60%, evidencing an energy mix (Fig. 8.3). First generation energy crops are a significant alternative to generate modern bioenergy. However, there is a common disapproval in their use, since they occupy land that is needed for food production. Nevertheless, the world has a great deal of marginal land that is unfavorable for food production and is now unused (Jones et al. 2015). In this sense, the International Energy Agency has projected that to 2030 the global energy demand could be provided from the bioenergy crops grown sustainably on non-arable lands (Metzger and Huttermann 2009; Skevas et al. 2014). There are several estimations of the bioenergy potentials using marginal lands, ranging from ~30–1000 EJ y−1 of primary energy, being the global primary bioenergy potential in the range of 130–270 EJ y−1 for 2050 (Haberl et al. 2010; Haberl et al. 2011). Considered marginal land potentially available for bioenergy in different worldwide regions, Cai et al. (2011) who evaluated combinations of areas of abandoned, marginal land and areas defined as mixed crop and natural vegetation land, demonstrate that these areas ranged between 320 and 702 Mha but increased to 1107 Mha

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Africa Amercias

16%

1%

Asia Europe

20%

Oceania

22% 41%

Fig. 8.3  Total primary energy supply of renewables in continents in 2017

if were included grassland, scrubland and savannas with marginal productivity. Marginal lands are candidates for growing dedicated energy crops such as perennial grasses and woody crops, but there is necessary a wide examination on ecosystem services. Some field data indicate that ecosystem services vary with the type of marginal land, management and perennial species. Developed of energy crops on marginal lands can reduce water and wind erosion, sequester soil C between, rehabilitate contaminated or compacted soils, and improve biodiversity (Blanco-­ Canqui 2016). There are several plant species which have shown potential to be used as bioenergy crops (Li et al. 2008) and have the capacity of grow in marginal lands. In particular, C4 grass species could be grown successfully on marginal lands as they have the potential to develop on poor soils (where food crops cannot produce profitability) as a result of lower nutrient requirements and better water use efficiencies (Stewart et  al. 2009; Fargione et  al. 2010; Iqbal et  al. 2015). The lignocellulosic crops can provide environmental benefits such as reducing greenhouse gases, mitigating erosion and improving soil fertility (Zegada-Lizarazu et  al. 2010). These perennial energy grasses may provide the entire aboveground biomass and have the capacity to regenerate from their roots or buds at the plant base, offer the utmost potential for energy plantation on landfills. That’s the reason why do not require replanting for long periods of time (Pandey 2017) (Fig. 8.4). According to different authors, numerous species that have been considered as bioenergy crops may be suitable to perform well in phytocapping in landfills (Nixon et al. 2001; Angelini

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•Prosopis juliflora •Popular •Salix

•Jatropha curcas •Pongamia pinnata •Azaractica indica •Ricinus communis

Biodiesel

Biomass

Energy crops in landfill

Ethanol •Miscanthus giganteus •Panicum sp •Cnaryreedgrass •Arundo donax

Biogas •Pennisetum purpureum •Saccharum •Erianthus arundinaceum •Sorghum bicolor

Fig. 8.4  Bioenergy sources obtained from potential energy crops. (Adopted from Pandey 2017)

et  al. 2005; Lamb et  al. 2014). These species include Panicum virgatum (switch grass), Miscanthus spp. (miscanthus) and Pennisetum purpureum (Napier grass), amongst others species (Johannessen et al. 1999). Panicum genus of grasses has high forage production, with fast establishment and regrowth because of its root system, can be used to enhance soil structural quality (Bogdan 1977) and could be growth in a closed municipal solid waste landfill. While landfill sites create a specific environment with an unstable composition of species, Panicum acted as a late specie in succession and stable specie in plant community (Vaverková et al. 2019). Miscanthus genus is originated from South Asia with a high photosynthetic potential under temperate field conditions (Naidu and Long 2004). Miscanthus giganteus produces biomass yield higher than 17 t ha−1 y−1 (Christian et al. 2008) or even 25 t ha−1 after 3 years of cultivation (Zub and Brancourt-Hulmel 2010). The mainly use of Miscanthus giganteus biomass is for biofuel material but applications for paper production particularly writing and printing papers, animal litter, and biomaterials are also effective (Wanat et al. 2013) because its thermal decomposition begins at a lower temperature and occurs at a higher rate compare to wood species. One of its characteristics to use in closed landfill sites is the adaptation and the tolerance to contaminated ecosystems (Arduini et al. 2006; Fernando and Oliveira 2004). Diverse studies demonstrated that when Miscanthus giganteus grows in contaminated soils has a mechanism of tolerance, an antioxidant capacity, and shows a low transference to its aerial parts (García et al. 2010; Barbu et al. 2010).

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There is evidence that the grass Pennisetum purpureum had an important survival rate, being irrigated with pure leachate from landfill (Erdogan et al. 2008) and also can growth and accumulate great quantities of heavy metals from soil landfill (Vongdala et al. 2018). In Argentina, Cittadino et al. (2016) found that the survival rate of 240 specimens of Pennisetum purpureum planted on Villa Dominico closed landfill was 100%. The plantation sowed a slow or null growth in the first month, then a linear growth was observed until mid-April, at which time the plants began to reach their maximum heights (> 260 cm), averaging 221 cm ± 39 cm. It is important to remark that while landfill final cover cannot be considered as a traditional soil, pennisetum could adapt to landfill environment and grow in it. This author affirms that his species meets the basic premises that must accomplish a bioenergy crop. The use of non-productive lands like landfills and nonedible plants like P. purpureum for the production of biomass as a source of energy production is a model to replicate. The main weakness of this alternative is that it presents high initial costs of implantation, which are made of rhizomes. Whereas each project is site-specific, plants are usually selected based on rehabilitation strategy of landfill, environmental conditions, the role of the vegetative cover, the depth of plant roots, agricultural species requirements, long-term maintenance requirements, and costs to implementation that rehabilitation strategy (EPA 2019a, b). Although a variety of plant species can be used on a landfill surface, native plants are recommended when possible. In order to save the weakness associated to this alternative, native plants found in the surrounding natural areas will have superior chance of success, require the minimum maintenance and are the most cost-effective in the long term. Ideally, revegetation of landfill sites will create natural conditions that encourage re-population by native animal species and that are consistent with the surrounding land (EPA 2019a, b). Also, the correct strategy selection for production of bioenergy from C4 species is necessary to achieve economic efficiency.

8.5  Conclusion In order to comply with Sustainable Development Goals, the greatest challenge for the next years is to achieve a decrease in solid waste generation through prevention, reduction, reuse, and recycling. However, as currently landfills continue to be an option widely used worldwide, its rehabilitation in a post-closure phase is a necessary process to accomplish its reintegration into the surrounding environment. The most important issue is that a closed landfill site can be reused for many purposes which serve the community needs. Thus, since closed landfill sites creates a specific environment with diverse plant species, sometimes with risky effects for the surrounding ecosystems, agriculture and humans, selection of species for its future revegetation is important, in order to facilitate specific plant succession and no risk for community. Particularly, in revegetation projects of closed landfills by

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energy crops, should be evaluate all ecosystem services and economic viability due species tolerant to adverse climatic, soil, and environmental conditions. It is important remark that the post-closure use of landfills and management options will be based on the bioeconomy framework allow the development of strategies that contemplate new technological and productive paradigms.

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Chapter 9

Biochar Behaviour and the Influence of Soil Microbial Community Ihuoma N. Anyanwu, Chinedum U. Nwajiuba, Emmanuel B. Chamba, Victor Omoni, and Kirk T. Semple

Abstract  Biochar–soil microbiota interactions may occur within a short or long period of time after application, and the behaviour of biochar could determine their impacts on soil. In comparison, modifications in soil microbiota function, structure, biomass and/or ecosystemic function following biochar application could translate to changes in soil fertility leading to positive and/or negative impacts. Amendment of soil with biochar has been evaluated globally as a means of improving soil health, fertility and increase soil microbial biomass. However, little is known about the mechanisms through which biochar modulates soil microbial activity or implications of these interactions. This review unravels possible interactions that may occur during soil–biochar contact time and the impacts on soil microbial function. Furthermore, the paper discusses interactions between biochar and microbial groups (such as bacteria, fungi, nematode, archaea, enzymatic activities), and elucidates possible factors that may influence biochar–microbiota behaviour in the soil environment. It also considers the implications for the associated biota and feasibility of applying biochar in weathered soils and/or contaminated land remediation. Finally, the review highlights knowledge gaps and future research directions. Keywords  Biochar · Soil · Behaviour · Microbiota · Interaction

I. N. Anyanwu (*) Department of Biological Sciences, Alex Ekwueme Federal University Ndufu-Alike, Abakaliki, Nigeria Lancaster Environment Centre, Lancaster University, Lancaster, UK C. U. Nwajiuba Department of Agriculture, Alex Ekwueme Federal University Ndufu-Alike, Abakaliki, Nigeria E. B. Chamba CSIR-Savana Agricultural Research Institute, Tamale, Ghana V. Omoni · K. T. Semple Lancaster Environment Centre, Lancaster University, Lancaster, UK © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 D. K. Gupta, J. M. Palma (eds.), Plant Growth and Stress Physiology, Plant in Challenging Environments 3, https://doi.org/10.1007/978-3-030-78420-1_9

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9.1  Introduction Biochar ‘charcoal for soil application’ is produced by pyrolysis of biomass feedstocks under zero or low-oxygen concentrations (