Rice chemistry and technology [Fourth edition] 9780128115084, 0128115084

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Rice

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Rice Chemistry and Technology

Fourth Edition

Edited by

Jinsong Bao College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

Woodhead Publishing is an imprint of Elsevier The Officers’ Mess Business Centre, Royston Road, Duxford, CB22 4QH, United Kingdom 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, OX5 1GB, United Kingdom Copyright © 2019 AACCI. Published by Elsevier Inc. in cooperation with AACC International. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the Publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither AACCI nor the Publisher, nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-811508-4 For information on all Woodhead Publishing publications visit our website at https://www.elsevier.com/books-and-journals

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Contents

List of contributors Preface to the fourth edition Preface to the third edition Preface to the second edition Preface to the first edition 1

2

3

4

Origin, taxonomy, and phylogenetics of rice Xin Wei and Xuehui Huang 1. Natural genetic variation in rice 2. Taxonomy and phylogenetics of rice 3. Domestication of cultivated rice References

xi xv xvii xix xxi 1 1 5 11 19

Gross structure and composition of the rice grain Bienvenido O. Juliano and Arvin Paul P. Tua~no 1. Structure of the rice grain 2. Gross composition of grain parts and milling fractions 3. Changes during rice grain filling Acknowledgments References

31

Rice starch Jinsong Bao 1. Constituents of rice starch 2. The structural levels of starch 3. Starch functional properties 4. Starch biosynthesis 5. Future challenges Acknowledgments References

55

Rice proteins and essential amino acids Taiji Kawakatsu and Fumio Takaiwa 1. Seed storage proteins 2. Essential amino acids

31 39 42 48 48

55 57 67 72 88 94 94 109 109 115

vi

Contents

3.

5

6

7

Conclusion Acknowledgments References

123 123 124

Rice lipids and rice bran oil Chuan Tong and Jinsong Bao 1. Classification, structure, and content of rice lipids 2. Environmental and other factors affecting rice lipid composition 3. Genetic basis of rice lipids 4. Relationships between rice lipids and grain quality 5. Rice bran oil 6. Health benefits of RBO 7. Future prospects Acknowledgments References

131

Rice minerals and heavy metal(oid)s Gareth J. Norton 1. Content of elements in rice grains 2. Natural variation for grain element content 3. Transgenic approaches for altering grain element content 4. Currently released cultivars 5. Concluding statement References

169

Rice vitamins Subhrajyoti Ghosh, Karabi Datta and Swapan K. Datta 1. Vitamin A 2. Vitamin B1 3. Vitamin B2 4. Vitamin B3 5. Vitamin B5 6. Vitamin B6 7. Vitamin B7 8. Vitamin B9 9. Vitamin B12 10. Vitamin C 11. Vitamin D 12. Vitamin E 13. Vitamin K 14. Conclusions and future prospects Acknowledgments References

195

131 137 140 144 154 158 160 160 160

169 176 181 186 187 187

196 199 201 201 202 202 204 204 205 206 207 207 209 210 210 211

Contents

8

9

10

11

12

vii

Rice phenolics and other natural products Yafang Shao and Jinsong Bao 1. Phenolics 2. Genetics of phenolics 3. Other natural products 4. Future challenges 5. Conclusion References

221

Rice end-use quality analysis Christine J. Bergman 1. Physical properties 2. Functional properties 3. Biochemical properties 4. General techniques 5. Future research References

273

Rice milling quality Jinsong Bao 1. Laboratory assessment of milling quality 2. Criteria for milling quality 3. Factors affecting milling quality 4. Genetics of milling quality 5. Breeding of milling quality 6. Future challenges Acknowledgments References

339

Rice appearance quality Hao Zhou, Peng Yun and Yuqing He 1. Definition, classification, and diversity of rice appearance quality 2. Grain shape and rice yield 3. Effects of grain chalkiness on rice milling and eating quality 4. Genetic bases of rice grain shape 5. Genetic bases of rice grain chalkiness 6. Genetic improvement of rice appearance quality 7. Major issues and prospects in studies on rice appearance quality References

371

Rice cooking and sensory quality Christian Mestres, Aurélien Briffaz and Dominique Valentin 1. Consumer demand and sensory evaluation 2. Understanding cooking behavior and cooking quality 3. Future challenges References

385

222 249 253 257 259 260

277 285 301 312 317 317

340 341 344 353 363 364 365 365

371 373 373 373 377 378 380 380

385 400 417 418

viii

13

14

15

16

Contents

Impact of climate change on rice grain quality Lianxin Yang and Yunxia Wang 1. Experimental approaches for investigating rice response to climate change 2. Milling quality 3. Appearance quality 4. Cooking and eating quality 5. Protein and its components 6. Concentration and bioavailability of elements 7. Future perspectives Acknowledgments References

427

Biotechnology for rice grain quality improvement Jinsong Bao 1. Omics technologies 2. Marker-assisted selection 3. Transgenic breeding 4. Genome editing technology 5. Future trends Acknowledgment References

443

Postharvest technology: rice drying Griffiths G. Atungulu and Sammy Sadaka 1. Fundamental principles of rice drying 2. Grain bin fans 3. Rice drying systems 4. Recent developments in alternative drying technologies for rice 5. Impacts of drying on milled rice quality Acknowledgments References

473

Postharvest technology: rice storage and cooling conservation Griffiths G. Atungulu, R.E. Kolb, J. Karcher and Z. Mohammadi Shad 1. Terminology and processes definition 2. Rice storage systems 3. Aging of rice during storage 4. Effects of storage on the sensory and physicochemical properties of rice 5. Conclusions Acknowledgments References

517

428 428 430 432 434 435 437 437 438

443 454 456 462 463 464 464

474 483 492 501 507 513 513

518 529 544 544 550 551 552

Contents

17

18

19

ix

Rice noodles Zhan-Hui Lu and Lilia S. Collado 1. Noodles in Asian diet 2. Raw material characterization 3. Processing of rice noodles 4. Trends in product development References

557

Rice in brewing Masaki Okuda, Sachiko Iizuka, Yan Xu and Dong Wang 1. Rice in sake production 2. Rice in Huangjiu production References

589

Utilization of rice hull and straw Yu-Fong Huang and Shang-Lien Lo 1. Characteristics 2. Adsorbents 3. Biofuels 4. Other uses 5. Future challenges References

627

Index

557 558 566 578 581

589 612 620

628 630 637 649 653 653 663

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List of contributors

Griffiths G. Atungulu Department of Food Science, University of Arkansas Division of Agriculture, Fayetteville, AR, United States Jinsong Bao College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China Christine J. Bergman Food Science and Nutrition, Food & Beverage and Event Management Department, University of Nevada Las Vegas, Las Vegas, NV, United States Aurélien Briffaz Qualisud, Univ Montpellier, CIRAD, Montpellier SupAgro, Université d’Avignon, Université de La Réunion, Montpellier, France; CIRAD/ QualiSud, Cotonou, Bénin Lilia S. Collado Institute of Food Science and Technology, College of Agriculture and Food Science, University of the Philippine Los Banos, College, Laguna, Philippines Karabi Datta Lab of Translational Research on Transgenic Crops, Dept. of Botany, University of Calcutta, Kolkata, India Swapan K. Datta Lab of Translational Research on Transgenic Crops, Dept. of Botany, University of Calcutta, Kolkata, India Subhrajyoti Ghosh Lab of Translational Research on Transgenic Crops, Dept. of Botany, University of Calcutta, Kolkata, India Yuqing He National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China Yu-Fong Huang Graduate Institute of Environmental Engineering, National Taiwan University, Taipei, Republic of China Xuehui Huang College of Life and Environmental Sciences, Shanghai Normal University, Shanghai, China Sachiko Iizuka

National Research Institute of Brewing, Higashihiroshima, Japan

Bienvenido O. Juliano Philippines J. Karcher

Philippine Rice Research Institute Los Ba~nos, Laguna,

FrigorTec GmbH, Hummelau, Amtzell, Germany

xii

List of contributors

Taiji Kawakatsu Division of Biotechnology, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Japan R.E. Kolb FrigorTec GmbH, Hummelau, Amtzell, Germany Shang-Lien Lo Graduate Institute of Environmental Engineering, National Taiwan University, Taipei, Republic of China Zhan-Hui Lu Guelph Research and Development Centre, Agriculture and Agri-Food Canada, Guelph, ON, Canada Christian Mestres CIRAD/QualiSud, Fe34398, Montpellier, France; Qualisud, Univ Montpellier, CIRAD, Montpellier SupAgro, Université d’Avignon, Université de La Réunion, Montpellier, France Z. Mohammadi Shad Department of Food Science, University of Arkansas Division of Agriculture, Fayetteville, AR, United States Gareth J. Norton School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom Masaki Okuda

National Research Institute of Brewing, Higashihiroshima, Japan

Sammy Sadaka Department of Biological and Agricultural Engineering, University of Arkansas Division of Agriculture, University Avenue, Little Rock, AR, United States Yafang Shao

China National Rice Research Institute, Hangzhou, China

Fumio Takaiwa Division of Biotechnology, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Japan Chuan Tong Food Science Institute, Zhejiang Academy of Agricultural Sciences, Hangzhou, China Arvin Paul P. Tua~ no Institute of Human Nutrition and Food, College of Human Ecology, University of the Philippines Los Ba~ nos, Laguna, Philippines; Department of Chemistry, College of Humanities and Sciences, De La Salle Health Sciences Institute, Dasmari~ nas, Philippines; Former Supervising Science Research Specialist, Philippine Rice Research Institute Los Ba~ nos, Laguna, Philippines Dominique Valentin INRA, UMR 1324 Centre des Sciences du Gout et de l’Alimentation, Universite de Bourgogne, UMR Centre des Sciences du Gout et de l’Alimentation, Dijon, France Yunxia Wang College of Environmental Science and Engineering, Yangzhou University, Yangzhou, China Dong Wang

Jiangnan University, Wuxi, China

Xin Wei College of Life and Environmental Sciences, Shanghai Normal University, Shanghai, China

List of contributors

Yan Xu

xiii

Jiangnan University, Wuxi, China

Lianxin Yang Jiangsu Key Laboratory of Crop Genetics and Physiology/ Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, China Peng Yun National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China Hao Zhou National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

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Preface to the fourth edition

Rice (Oryza sativa L.) is recognized not only as a food security crop that feeds over half the global population but also as a source of essential and unique nutritional and functional properties vital for our health and well-being. Rice grain quality improvement remains a central objective of rice breeding programs worldwide. Rice quality is a primary determinant of its market price and consumer acceptance. For these reasons, scientific and technological advances in the field of rice grain quality need to be regularly summarized and updated in an easily accessible and authoritative form. This fourth edition of Rice: Chemistry and Technology updates the previous three monographs, with emphasis on three features in rice grain quality research. The first feature reflects a new emphasis on nutritional value and health benefits of rice. Each compositional component of the rice grain, major and minor, has been described in its own individual chapter. The second feature is the advancement of understanding of the rice grain chemistry through integration with knowledge from the fields of genetics and molecular biology. In addition to new insights into varietal differences, genetics of chemical components and their regulation at the molecular level during seed development have now been well characterized. Finally, the third feature, biotechnology as a new tool, has been comprehensively and well applied in rice grain quality research, providing the impetus for further improvement of rice grain quality. As a multiauthored work, each chapter of this monograph has been written by one or more experts on the subject. Although extensive and up-to-date references are included in each chapter, a single monograph cannot exhaustively cover all historical references and themes in the field. Readers are encouraged to continue to refer to the previous editions of this work, which cover other themes and the older literature in more detail. I would like to thank all the contributors for their time and talent in writing the chapters. I dedicate this monograph to the Godfather of Rice Chemistry, Dr. Bienvenido O. Juliano, who passed away in February 2018, soon after he submitted chapter 2 for this edition. Finally, I would like to thank my wife, Yan Hong, and my son, Ziran Bao, for their patience and understanding during the preparation of the monograph. Jinsong Bao

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Preface to the third edition

Rice has taken center stage this last decade, not only as an important provider of nourishment for the world’s population but as a grain now recognized as having many unique nutritional and functional attributes with potential to be captured in a multitude of value-added food and nonfood applications. Basic, up-to-date knowledge of rice chemistry and technology is needed to guide the research that will develop new applications and lead rice into the coming decades. The third edition of Rice: Chemistry and Technology updates the 1985 monograph, with emphasis on current developments. The book presents, in a single work, comprehensive overviews covering topics ranging from the rice plant and varieties to rice structure and composition and the functionality of its components. Postharvest processing technologies for drying, storage, and milling and those for making traditional and new value-added products are discussed in detail. New nutritional findings are presented. A multiauthored work, each chapter of the monograph has been written by one or more authorities on the subject. The authors have styled their chapters as overviews, with extensive bibliographies directing the reader to the primary literature. This monograph is intended to be an addition to your collection and not a replacement for the second edition, which covers the older literature in more detail. I wish to thank the authors for their time and talent in writing the chapters. The authors and I acknowledge and dedicate this monograph to the godfather of the rice world, Bienvenido O. Juliano, whose contributions to the field have guided our research. You paved the way for us, Ben, and we thank you. Elaine T. Champagne

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Preface to the second edition

Rice is the principal food cereal in tropical Asia, where 90% of the world’s rice crop is grown and consumed. Significant progress in the chemistry and technology of rice in the last decade has prompted the Publications Committee of the American Association of Cereal Chemistry (AACC) to revise its Monograph No. 4, Rice: Chemistry and Technology, edited by Dave Houston and published in 1972. The present monograph updates the 1972 monograph, with emphasis on developments in the 1970s and 1980s. Chapters on parboiling and milling emphasize the Asian situation, since the status in the United States and Europe is adequately discussed in published chapters. Extrusion-cooked rice foods and rice noodles are emphasized, as well as Japanese convenience foods. Rice straw is included because of the current interest in biomass utilization. All chapters on technology and processing were contributed by authorities on the subject. Contributors were encouraged to emphasize varietal differences and possible topics for future research. As editor, I elected to write most of the chemistry chapters and those on by-products and residue, to minimize overlap and maximize coverage of the interfaces between the chemistry and structure of the rice grain and its technological properties. This monograph was mainly planned, written, and edited in 1983e84 during my sabbatical leave from the International Rice Research Institute (IRRI). I wish to thank the contributors for their time and talent in writing the chapters; R. Don Sullins, then chairman of the AACC Publications Committee, for his assistance and support; M. S. Swaminathan, Director General of IRRI, for approving my leave; the Southeast Asian Research Center for Agriculture for providing me a visiting professorship and office space; the IRRI Department of Communications and Publications for graphics and photography; the IRRI library staff for rechecking literature citations; Daisy Herrero for typing the manuscripts; and my research colleagues in the Cereal Chemistry Department for reviewing my chapters. Finally, I wish to thank my wife, Linda, and my children for their patience and understanding during the preparation of the monograph. B.O.J.

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Preface to the first edition

Rice, as one of the two major food cereals, providesdtogether with a comparable amount of wheatda large proportion of the total nourishment of the world’s population. However, reported research on rice chemistry and technology has lagged markedly behind that reported for wheat. Moreover, the available information on rice other than on its culture has remained largely scattered in contrast to that for wheat, which has been well collected and summarized. The present monograph, the fourth in the monograph series sponsored by the American Association of Cereal Chemists, attempts to minimize this disparity. The book has two major aims: to collect and present for the first time in a single work an ordered, coherent, and informative series of reviews on rice chemistry and technology; and to provide an extensive bibliography that will permit direct access to the primary literature. This combination offers useful data to all connected with the handling, processing, or sale of rice and its by-products, as well as to any individual seeking information on rice composition or technology. A third, minor, aim is to use predominantly the metric system of measurement in accordance with its extensive scientific acceptance and the worldwide trend toward its general adoption. As a multiauthored work, the monograph has the advantage that each chapter is presented by an authority on the subjectdand some disadvantages that inevitably accompany this type of publication. The dedicated efforts of the authors have provided the values to be found in this volume; errors and omissions must be attributed to the editor, who welcomes all corrections and suggestions for improving any possible later edition. Credit for initiating this work belongs to the Monograph Committee of the Association and to Past President Byron Miller and Executive Vice-President Raymond J. Tarleton, who put the plan into effect. My particular thanks go to Director of Publications Merrill J. Busch, and to Assistant Editor Carolyn M. Light and her able proofreading and typesetting coworkers, who diligently, patiently, and cooperatively handled the multitude of details in preparing this work for publication. I thank also my wife, Twylla, not only for her aid but especially for her sustained forbearance during preparation of the monograph. D.F.H.

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Origin, taxonomy, and phylogenetics of rice

1

Xin Wei, Xuehui Huang College of Life and Environmental Sciences, Shanghai Normal University, Shanghai, China

Rice, generally referred to as Asian cultivated rice (Oryza sativa L.), is one of the most important staple crops, feeding almost half of the world population. It is widely cultivated around the world and mainly in Asia. Domesticated rice has played a central role in human nutrition and culture during the past 10,000 years. The domestication of rice is one of the most important technological innovations in Asian history, significantly supporting the formation of two of the four ancient civilizations. There is no doubt that rice is one of the most important influential crops in Asia. However, the origin and the domestication processes of cultivated rice have been debated for decades, which is inconsistent with the important position of rice. In this chapter, we discuss recent genetic and archaeological work that reveals the origin, taxonomy, and phylogenetics of rice, and we describe the genomic research into the domestication of subspecies of rice. The development of genomic methods provides a clear picture of the domestication of rice and will certainly benefit the rice functional genomics studies and molecular breeding in the future.

1. Natural genetic variation in rice 1.1

Geographic distribution of rice and its phenotypic diversity

Nowadays rice is widely planted in more than 120 countries across the world, from 35 S to 53 N, with a concentration in tropical and subtropical areas of Asia. From 2010 to 2014, the world harvest area of rice was 163 million hectares per year, led by India, China, Indonesia, Bangladesh, and Thailand with a combined 67% of total (FAO, 2014). The planting area of rice increased approximately 42% in the last 50 years and is still increasing gradually. The increased planting area was mainly in Southeast and South Asia (about 75%), led by India, Indonesia, Thailand, China, and Vietnam. China and India are the biggest rice production countries, which produced approximately 50% of the world’s rice. Rice is mainly grown in the Yangtze River basin, southeast coastal area, and northeast area of China. The planting region of rice in northeast area increased quickly in the last decades. The Gangetic Plain and coastal areas are the major rice production areas in India. More than 400,000 rice accessions have been collected in the public germplasm repositories. The large germplasm resources conservation center of rice includes the International Rice Research Institute (>100,000 rice accessions), National Crop Rice. https://doi.org/10.1016/B978-0-12-811508-4.00001-0 Copyright © 2019 AACCI. Published by Elsevier Inc. in cooperation with AACC International. All rights reserved.

2

Rice

Genebank of China (>80,000), National Plant Germplasm System of United States Department of Agriculture (USDA, >18,000), and National Bureau on Plant Genetic Resources of India (>60,000). These accessions show various phenotypes and many agronomic traits, such as heading date, plant height, seed shape, pericarp color, and grain weight. Take the seed color for example, it could be white, red, black, brown, purple, or green. Rice is classified into two subspecies by their grain shapes and texture: indica and japonica. Generally, indica is long grain, relatively less sticky, with less amylopectin, while japonica is short grain and more sticky. Besides seed shape and texture, indica and japonica show significant differences in plant height, leaf shape, leaf color, plant type, awn length, density of glume pubescence, germinating rate, cold tolerance, lodging resistance, disease resistance, seed shattering, tiller number, and many other agronomic traits. Compared to indica, the japonica varieties have shorter plant height, shaper leaf shape, light leaf color, strong cold tolerance, strong lodging resistance, are nonshattering, but have lower tiller number, slower germinating rate, are sensitive to rice blast, have long and dense glume pubescence and long awn in some varieties. Differences between nonsticky (indica) and sticky (japonica) rice are even documented in Chinese literature as early as AD 100 (Matsuo et al., 1997). Indica varieties are concentrated in the mostly submerged region in South Asia and Southeast Asia, while japonica varieties are mainly grown in the fields with less water, such as northern latitudes of East Asia, upland areas of Southeast Asia, and high elevations in South Asia. The planting area of japonica is about 13 million hectares, less than 10% of the total. Most japonica is grown in China (about 60%), and over 80% of it is in Northeast China, East China, and Yunnan-Guizhou Plateau.

1.2

IRGSP and OMAP

To meet the projected food demands of growing populations, the world rice production must increase by 30% over the next 20 years. The utilization of biotechnology and molecular breeding to increase the rice yield potential and yield stability is particularly important, in which a high quality reference rice genome sequence is much required. The International Rice Genome Sequencing Project (IRGSP), established in 1998, set the power of sequencing groups from 10 nations to draw a complete precise map of the rice genome (Nipponbare, a japonica cultivar). The IRGSP released a high-quality finished genome sequence of japonica rice in 2005. The rice genome is the first completely sequenced monocot plant genome and the second plant genome after Arabidopsis (a dicot). The highly accurate and public IRGSP sequence opened the door for functional characterization of the rice genome and permitted rice geneticists to identify the genes underlying complex agronomic traits. Based on the rice genome, understanding of the biological function of rice genes and the genetic improvement of rice production and quality has been greatly facilitated. Through comparative analyses, the domestication and evolution research of rice and other cereal crops was also largely promoted (Paterson et al., 2004; Salse et al., 2008; Wang et al., 2005; Yu et al., 2005). Benefiting from the high quality genome and other research for rice, such as the smallest genome of the major cereals, dense genetic maps and relative ease of genetic

Origin, taxonomy, and phylogenetics of rice

3

transformation, rice has been developed to be one of the model species for molecular and genetic research in plants. The complete japonica rice genome that was released by IRGSP adopted the cloneby-clone approach (International Rice Genome Sequencing Project, 2005). Before that, draft genome sequences of indica (93-11) and japonica (Nipponbare) were acquired by a whole-genome shotgun method and released in 2002 (Goff et al., 2002; Yu et al., 2002). These draft maps of the rice genome sequences have laid a solid foundation for studying the differences among subspecies of rice. Rice (O. sativa) belongs to the genus Oryza, which consists of two cultivated (O. sativa and O. glaberrima) and 22 wild species (Ge et al., 1999). Based on the karyotype and molecular analysis, Oryza is divided into four complexes, including O. sativa, O. officinalis, O. ridleyi, and O. meyeriana. Ten genome types (A, B, BC, C, CD, E, F, G, HJ, and HK) are recognized in the rice genus. Each genome type contains one to eight species. The two cultivated species and six wild relatives are classified as AA genome diploid species. The other 17 wild species are clustered into another nine genome types. Compared with cultivated rice, the wild rice species generally show a stronger tolerance to drought, salt, disease, and insect stresses as well as higher nutrient-absorption activity. The wild rice species can offer a largely valuable resource of superior genes to the genetic improvement of the cultivated rice. The Oryza Map Alignment Project (OMAP) began in 2005, aiming to better investigate the wild species of rice. The OMAP initially planned to sequence the genomes of African cultivated rice and 11 wild species by constructing bacterial artificial chromosome (BAC) libraries, constructing physical maps and aligning them to the IRGSP genome sequence (Wing et al., 2005). The ambitious goal of OMAP is to construct a genome research platform for evolution, domestication, polyploidy, development, and gene network of the genus Oryza and genetic improvement of rice.

1.3

Large-scale resequencing and genomic variation

Sanger dideoxy enzymatic DNA sequencing technology was developed in 1977, making automated and large-scale sequencing possible, which is widely used to obtain information on genes, genetic variation, and gene function for biological and medical research. It also played significant roles in the genome sequencing of humans, Drosophila, Arabidopsis, rice, and other important species. However, the exorbitant cost and laborious work limited the use of Sanger sequencing in the ultra-large-scale genome sequencing. Therefore, the high-throughput sequencing technology, also known as next-generation sequencing (NGS), began to be developed in the end of 1990s, and three mainstream NGS platforms, including Illumina/Solexa, Roche/454, and ABI/SOLiD sequencing were released from 2005 to 2006. These sequencing technologies greatly decreased the financial and time costs of DNA and RNA sequencing, and revolutionized genomics and molecular biology research. In the last decade, more than 200 animal and plant genomes were successfully sequenced by NGS. As a selffertilizing diploid species with a small completed high-quality genome, the genomics and functional genomics studies of rice have been greatly enhanced by using NGS (Guo et al., 2014).

4

Rice

Combination of the completed high-quality rice genome and NGS technology brought us to a new era of whole genome resequencing. Whole genomeresequencing of rice means that the individuals are sequenced by NGS without genome assembly, but through short-read alignment. Genomic variations, including structure variation (SV), insertions/deletions (InDels), copy number variations (CNVs), and single nucleotide polymorphisms (SNPs), between the sequenced individuals and the reference genome, are assayed by aligning the short-sequence reads against the reference genome. It is used to identify genomic variation in key germplasm and recombinant populations. Based on the information from whole genome resequencing, rice researchers have characterized numerous genomic variations, identified many quantitative trait loci (QTLs) with high mapping resolution, and developed new molecular breeding systems. One japonica elite cultivar, Koshihikari, was sequenced by NGS with 15.7 genome coverage in depth, and 67,051 SNPs were identified and used in the definition of the pedigree haplotypes of closely related japonica cultivars (Yamamoto et al., 2010). Forty accessions of cultivated rice and 10 accessions of wild rice (O. rufipogon and O. nivara) were resequenced. In total, 6,496,456 SNPs, 808,000 InDels, 94,700 SVs, and 1676 CNVs were identified (Xu et al., 2012). A large population of Chinese landraces (517 accessions) was resequenced with approximately one-fold coverage. By aligning to the rice reference genome, a total of 3,625,200 nonredundant SNPs were identified, resulting in an average of 9.32 SNPs per kb, with 167,514 SNPs located in the coding regions of 25,409 annotated genes. A high-density SNP map and haplotype map (HapMap) of the rice genome was constructed (Huang et al., 2010). Subsequently, the population was extended to a larger and more diverse sampled950 worldwide rice cultivars. In the genic regions, 4,109,366 nonsingleton SNPs and 191,476 nonredundant InDels ranging from 1 bp to 376 bp in size were identified (Huang et al., 2012b). The authors investigated the worldwide rice population structure and constructed a neighbor-joining tree involving five divergent groups: indica, aus, temperate japonica, tropical japonica, and intermediate, which were consistent with the five distinct groups detected by previous research (Garris et al., 2005). After that, 533 represented rice accessions were resequenced and combined with the 950 sequenced germplasms, in which a total of 6,551,358 high-quality SNPs with the minor allele of each SNP shared by at least five accessions were identified (Xie et al., 2015). The 3000 Rice Genomes Project released sequenced genomes of a core collection of 3000 rice accessions from 89 countries with an average sequencing depth of 14X, and about 20 million rice SNPs were identified (Alexandrov et al., 2015). Based on genome-wide SNP analysis, genomic changes associated with the breeding effect in the indica subspecies were identified. These whole genome resequencing studies revealed relationships among landraces and modern varieties of rice, and genetic diversity that can be used for breeding programs in rice.

1.4

Rice germplasm resources for breeding

A strong genetic bottleneck was generated during the domestication and modern breeding of rice. It was estimated that cultivated rice lost more than 75% of the genetic

Origin, taxonomy, and phylogenetics of rice

5

diversity found in the wild progenitors (Zhu et al., 2007). The superior genes or alleles that contribute to yield, disease resistance, and drought tolerance might be lost in the modern rice varieties because of the genetic drift through bottleneck effects. Future rice improvement needs the genetic variation from traditional varieties and related wild species to cope with the many biotic and abiotic stresses that challenge rice production around the world. However, the wild species are threatened with extinction as their habitats are destroyed by human disturbance and the traditional landraces are being lost as the farmers prefer high-yield commercial varieties. Thus, rice scientists make their efforts for the collection of rice germplasm resources worldwide. For instance, the International Rice Genebank of IRRI held more than 127,000 rice accessions and 4600 wild relatives in the beginning of 2017 (The International Rice Genebank: http://irri.org/our-work/research/genetic-diversity). These rice germplasm resources are indispensable genetic resources for further improvement of cultivated rice varieties. With the development of NGS, rice genome variation and regulatory genes of important agronomic traits (e.g., plant height, flowering time, grain yield, grain quality, and stress resistance) have been exploited. Genome-wide superior alleles that improve the rice yield and quality have been detected in the rice germplasm resources. The collected and conserved rice germplasm resources are the most important strategic resource for rice breeding.

2. Taxonomy and phylogenetics of rice 2.1

Phylogenetics of wild rice (AA-group in Oryza genus)

The genus Oryza is classified into 10 genomes comprising 24 species (two cultivated and 22 wild). The two cultivated species and six wild relatives belonged to O. sativa complex are classified as AA genome diploid species, including Asian cultivated rice (O. sativa), African cultivated rice (O. glaberrima), common wild rice (O. rufipogon), annual wild rice (O. nivara), Barth’s rice (O. barthii), longstamen rice (O. longistaminata), Australian wild rice (O. meridionalis), and South American wild rice (O. glumaepatula). The geographical distributions of these eight species are totally different: O. sativa is grown all around the world with a concentration in Asia, O. rufipogon and O. nivara mainly distribute in Asia, O. glaberrima is concentrated in West Africa, O. barthii and O. longistaminata are found in tropical Africa, O. meridionalis is in Australia, and O. glumaepatula is in South America. Generally, the O. sativa, O. glaberrima, O. nivara, O. barthii, and O. meridionalis are annual species whereas the others are perennial species. However, a perennial form O. meridionalis was found in Australia recently (Sotowa et al., 2013). Based on the morphology, geographic distribution, and levels of partial sterility in F1 hybrid, O. rufipogon and O. nivara were supposed to be progenitor species of O. sativa while O. barthii might be the ancestor of O. glaberrima. Phylogenetic relationships of species in the genus Oryza have been well analyzed by molecular approaches, including chloroplast DNA (Chen et al., 1993; Dally and Second, 1990; Kumagai et al., 2010), nuclear restriction fragment length polymorphism (RFLP)

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(Wang et al., 1992), two microsatellites (Akagi et al., 1998), two nuclear genes and a chloroplast gene (Ge et al., 1999), multilocus in nuclear genome (Zhu et al., 2007), 53 nuclear genes and 16 intergenic regions (Zhu et al., 2014), and chloroplast genomes (Wambugu et al., 2015). These phylogenetic analyses supported the morphological and crossing results. To lay the foundation for the comprehensive genome comparison and construct a convincing phylogenetic tree of the AA-genome Oryza species, the IRGSP, OMAP, and other genome sequencing projects were funded to provide high-quality genome research and generate a large array of publicly available genomic resources. Genome-sequencing of O. rufipogon, O. glaberrima, and O. longistaminata was completed by OMAP in 2012, 2014, and 2015, respectively (Huang et al., 2012c; Wang et al., 2014; Zhang et al., 2015), and the other genomes will be released in the near future. These genomes provide the opportunity to compare the genomes and elucidate the convincing phylogenetic relationships of all AA-group species. Based on 2305 one-to-one, single-copy orthologous genes from these genomes, the robust phylogeny of these species was constructed (Zhang et al., 2014). The evolutionary relationships are consistent with the calculated phylogeny of all AA-genome Oryza species in previous study (Zhu et al., 2014). Using the large gene set, the divergence times between AA and FF genomes was dated 35.3 million years (Myr). The divergence time between O. barthii and O. glaberrima is 0.26 Myr, and the divergence time between O. sativa and O. nivara is 1.2 Myr (Zhang et al., 2014).

2.2

Phylogenetics of Asian cultivated rice

As a predominantly autogamous species, gene flow of Asian cultivated rice is restricted. Because of fewer opportunities for cross-pollination, the phylogeny of rice may be affected by the natural distribution of the ancestral species, as well as domestication and artificial selection. As a result, the geographically or ecologically distinct groups of rice, indica and japonica subspecies, which are mainly grown in tropical Asia and temperate East Asia, respectively, are expected to show greater genetic differentiation than that in the outcrossing species. At all levels of analysis, including morphological, physiological, and molecular, the differences between the indica and japonica subspecies are quite significant (Oka and Morishima, 1982). To define the phylogeny of Asian cultivated rice, molecular markers have been used in the phylogenetic analysis from three decades ago. Using 15 isozyme loci, 1688 traditional rices from Asian rice were classified into six groups. The two largest groups were regarded as indica and japonica, the two minor ones was regarded as aus and Basmati rice, and the satellite ones were restricted to some deepwater rices in Bangladesh and Northeast India (Glaszmann, 1987). After that, RFLP was used in the phylogenetic analysis of rice (Nakano et al., 1992; Zhang et al., 1992), and the differentiation of indica and japonica was detected. A sample of 234 accessions of rice was genotyped at 169 nuclear simple sequence repeats (SSRs) and two chloroplast loci, five divergent groups were detected, corresponding to indica, aus, aromatic, temperate japonica, and tropical japonica rice (Garris et al., 2005). A core collection

Origin, taxonomy, and phylogenetics of rice

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of USDA world rice collections, including 1763 accessions representing all rice collections, was genotyped using 72 genome-wide SSR markers, and the results showed that the collection consisted of 35% indica, 27% temperate japonica, 24% tropical japonica, 10% aus, and 4% aromatic (Agrama et al., 2010). The drought-tolerant, early maturing aus, which is grown in Bangladesh during the summer season, is a minor group that has generally been considered to be indica ecotype. Aromatic, such as basmati from Pakistan, is highly praised for its fragrance and quality. Tropical japonica, also is named javanica initially, is grown in the high-elevation areas of Southeast Asia. Both aromatic and tropical japonica have a close relationship with temperate japonica. Later, microarrays were used in the population structure analysis of rice. The resequencing microarrays, which consist of 100 Mb of the unique fraction of the reference genome, were used to construct the phylogeny of 20 diverse varieties and landraces rice (McNally et al., 2009). In total, 160,000 nonredundant SNPs were detected. The phylogenetic tree revealed three distinct groups, with temperate japonica, tropical japonica, and aromatic closely allied in one group and the other groups correlating with aus and indica types. Another Affymetrix SNP array containing 44,100 SNPs was applied in the genotyping of a rice diversity panel consisting of 413 inbred accessions of O. sativa collected from 82 countries (Zhao et al., 2011). The five subpopulations indica, aus, temperate japonica, tropical japonica, and aromatic were clearly clustered based on the top four principal components analysis. These results were in agreement with previous SSR and SNP analysis (Agrama et al., 2010; Ali et al., 2011; Garris et al., 2005; Zhao et al., 2010). With the development of NGS, whole-genome resequencing was used in the phylogenetic analysis of rice. Resequencing of 950 worldwide rice germplasms (Huang et al., 2012b) showed that the worldwide rice collection has five distinct groups: indica, aus, temperate japonica, tropical japonica, and intermediate. Among these subpopulations, indica and aus were within the indica subspecies, whereas temperate japonica and tropical japonica were clustered into the japonica subspecies. The tropical japonica and aus accessions were not found in the traditional Chinese landraces. Subsequently, another rice collection containing 533 accessions was sequenced. Combined with the 950 sequenced germplasms, a total of 6,551,358 high-quality SNPs were identified. The population structure analysis revealed six distinct groups: indica I, indica II, temperate japonica, tropical japonica, aus, and an intermediate group (Xie et al., 2015). Most Chinese indica (71%) was divided into indica I group. The indica II group contained most of the accessions from the IRRI (95%), many accessions from Southeast had parentage of IRRI varieties, and some elite varieties bred in China with an IRRI variety parent.

2.3

Differentiation between indica and japonica subspecies

Rice consists of two subspecies: indica and japonica. The distinction of the two subspecies has been documented in ancient Chinese books since the Han dynasty (Oka, 1988). Reproductive isolation, which is the most important standard to define the species or subspecies, is observed in the F1 of the indica and japonica cultivars (about

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70% F1 sterility). Besides that, significant differentiation is found in morphological characteristics (Morishima and Oka, 1981), isozyme data (Glaszmann, 1987), DNA markers (Mackill, 1995; Ni et al., 2002; Zhang et al., 1992), and genomes (Feltus et al., 2004; Huang et al., 2008). The IRGSP sequenced a japonica cultivar (Nipponbare) using a BAC-based strategy (International Rice Genome Sequencing Project, 2005), and the Beijing Genomics Institute used a shotgun approach to sequence an indica variety (Yu et al., 2002). The availability of genomes of the two rice subspecies offers the opportunity to compare the genomics. Based on the alignment of the draft genomes of indica and japonica, 408,898 DNA polymorphisms were discerned, including 384,341 SNPs and 24,557 single-base Indels (Feltus et al., 2004). On average, the polymorphism rate was 1.70 SNPs/kb and 0.11 Indel/kb. The distribution across the genome of the SNPs was not random, with 328 contigs that had high polymorphism rates and 237 contigs that had a low level of polymorphism. Comparative genomic analysis also detected 2041 transposon insertion polymorphisms (TIPs) between the two subspecies genomes (Huang et al., 2008). TIPs represented more than 50% of large insertions and deletions (>100 bp) in the rice genome and generated approximately 14% of the genomic DNA sequence. Genome resequencing of the indica and japonica populations generated numerous genomic variations that can be applied in the investigation of differentiation between the two subspecies. More than 500 Chinese rice landraces with approximately onefold-coverage genome sequencing (Huang et al., 2010) were studied. A total of 3,625,200 nonredundant SNPs were identified and used in the construction of phylogenetic relationships. On the basis of the neighbor-joining tree, 373 typical indica and 131 typical japonica landraces were identified. Sequence diversity (p) was estimated at 0.0024, 0.0016 and 0.0006 for all samples, indica and japonica, respectively, suggesting that the indica landraces have much higher genetic diversity than the japonica landraces. The population-differentiation statistic (Fst) between the indica and japonica landraces was estimated at 0.55, much higher than in human populations (Consortium, 2003) and a typical oilcrop, sesame (Wei et al., 2015). The high Fst value indicated a very strong population differentiation of indica and japonica. Further analysis of the highly differentiated SNPs revealed that 367,081 SNPs were nearly fixed and 127,729 SNPs were completely fixed. The completely fixed SNPs had a smaller proportion in the coding region. In total, 53 genes that had large-effect completedifferentiation SNPs were identified, which might be related in the differentiation of the two subspecies.

2.4

Rice taxonomy is changing in modern breeding

Previous phylogeny and population analysis revealed five main groups of rice: indica, aus, aromatic, temperate japonica, and tropical japonica rice (Garris et al., 2005; Huang et al., 2010, 2012b). Genome-wide SNPs further divided indica group into indica I and indica II groups (Xie et al., 2015). The phylogeny of rice strongly related to

Origin, taxonomy, and phylogenetics of rice

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the distribution of different groups. Indica I is mainly from South China, indica II is from Southeast Asia, temperate japonica is grown in Northeast Asia, aus is grown in South Asia, while aromatic is distributed in South Asia and Middle Asia. The population structure of rice might result from the adaptation of climate and light conditions in different areas. Most traditional rice, or named landraces, could be clustered into the five groups. For instance, Huang et al. (2010) sequenced 517 Chinese landraces and analyzed the phylogeny based on all identified SNPs. The results showed that 97.5% (504 of 517) accessions could be clearly divided into indica or japonica and only 13 intermediate landraces were detected. Because of the distinct geographic distribution of the five rice groups, crosses of different groups rarely occurred. The intermediate landraces might result from occasional crossing between indica and japonica. Modern breeding of rice, crossing of different rice cultivars and artificially selecting the outstanding progenies according to their phenotypes, began approximately 100 years ago. It has greatly improved the agronomic and economic characteristics of rice varieties, including yield, biotic and abiotic tolerance, eating quality, adaptability, and a number of other agronomic traits. Green Revolution, which largely improved the yield of rice varieties in the 1960s, successfully introduced the semidwarf traits into many modern-bred varieties. The breeding of the “three-line system” of hybrid rice efficiently utilized heterosis of rice. Based on the hybrid breeding, superior traits from maintainer lines (indica I) and restorer lines (indica II) were combined in the hybrid rice and resulted in much higher (>20%) yield in 1970se1980s. Meanwhile, the genome constitution of the ancestors of modern rice has been great changed by the modern breeding. According to the estimation of linkage disequilibrium from SNP alleles and determination of haplotype diversity from consecutive alleles, polymorphisms in the haplotype blocks were found to be reduced in several chromosomal regions and the haplotype blocks became less diverse over time as a result of the breeding process (Yonemaru et al., 2012). However, new polymorphisms were also generated across the genome during the breeding process. Additionally, Xie et al. (2015) identified that most Chinese rice landraces are divided into indica I, whereas the varieties bred by IRRI are clustered in indica II. The taxonomy of rice had been changed by modern breeding. Because of the distinct distribution and partial reproductive isolation of indica and japonica, large gene flow between indica and japonica was rare in the landraces. However, high heterosis performance is observed from the hybrid of indica and japonica. Pioneer breeders have made great efforts to create high-yield hybrid rice and inbred rice varieties by crossing different lines of indica and japonica as well as performing successive selection. A large number of elite hybrid varieties, including 1439 indicaindica type, 38 japonica-japonica type, and 18 indica-japonica type, were resequenced and genome aligned (Huang et al., 2015b). The result revealed that the genomes of varieties generated from indica-japonica crosses were strikingly different from that of indica-indica- and japonica-japonica-type varieties. Genetic bottleneck, which results from domestication and modern breeding, is detected to be severe in rice. More than 75% of the genetic diversity in wild rice

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was lost (Zhu et al., 2007). Some favorite genes or alleles that constituted the wild rice genome and contributed to strong biotic and abiotic tolerance cannot be found in current rice varieties. Numerous genes or alleles that are involved in the tolerance of cold, flood, drought, and salt stresses in wild rice have been identified (Ma et al., 2016; Mishra et al., 2016; Niroula et al., 2012; Singh et al., 2015). Meanwhile, numerous genes contributing to the resistance of rice blast, bacterial blight, bacterial leaf streak, and brown planthopper also were detected in wild rice (Du et al., 2009; Gu et al., 2005; Qu et al., 2006; Song et al., 1995; Wang et al., 2015). Breeders have successfully introduced these superior genes or alleles from wild rice into cultivated rice and significantly improved the tolerance of abiotic stresses and resistance of the biotic stresses of modern rice varieties. The Xa21 gene, the first important functional gene identified from wild rice (O. longistaminata) and which showed highly resistance of rice blast disease, had been widely used in marker-assisted rice breeding (Luo et al., 2012). The brown planthopper resistance gene, Bph14, was the first cloned insect resistance gene. It is isolated from O. officinalis, and also was introduced into bred varieties (Li et al., 2006b). Introducing these genes from wild rice not only enhanced the phenotypic performance of new bred cultivars but also dynamically changed the genomic component of modern varieties and produced a profound effect on the rice taxonomy.

2.5

Hybrid rice from indica-japonica crosses

Hybrid rice is bred from two significant different parents with heterosis in yield. The first hybrid rice variety was created by three-line hybrid system and released in the 1970s in China. The Chinese breeders successfully transferred the male sterility gene from wild rice to generate the cytoplasmic genetic male-sterile line. The malesterile line was reproduced by crossing with the maintainer line, and the hybrid rice was produced by the combination of restorer line and male-sterile line. Using this technology system, the first generation of hybrid rice varieties produced 15%e20% higher yields than inbred rice varieties of the same growth duration. The annual harvest areas of hybrid rice in China has increased from 0.14 million hm2 to about 15 million hm2 in the last four decades, accounting for about 50% of the total rice planting areas. The exploitation of hybrid rice has met the increased demand for rice in China and Southeast Asia. Although scientists realized that exploitation of indica/japonica heterosis can heighten the level of hybrid rice yield, few indica-japonica hybrid rice varieties have been bred. In the collection of w1500 hybrid rice varieties (Huang et al., 2015), the group of indica-japonica crosses has a higher level of heterozygosity (45.1%) than that of indica-indica crosses (21.8%) and japonica-japonica crosses (15.8%). By calculating the genetic effects of heterozygous alleles on heterosis, the results showed that effective pyramiding of rare superior alleles with positive dominance in hybrids led the higher yield. Thus, the heterotic phenomenon that the hybrids from indica-japonica crosses out yield other hybrids in different environments might result from the introduction of superior alleles between indica and japonica. With the discovery of low-frequency favorite alleles in indica and japonica, better performance of indica-japonica hybrid rice can be expected in the future.

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3. Domestication of cultivated rice 3.1

Domestication traits and related genes

Domestication is usually referred to as a sustained multigenerational process of conscious selective breeding in which humans convert wild animals and plants into predictable livestock and crops. It has contributed to one of the greatest revolutions in human historydthe transition from gathering foods from the wild to producing them in farms. Charles Darwin had recognized that the domestication mainly happened in some desirable traits of the domestic species (Darwin, 1868). The domestication of animals mostly occurred in the genes that controlled behavior, while the domestication of plants significantly influenced the genes related to ripening or shattering, plant architecture, timing of germination, seed size, and adaptation. Unlike the improvement traits of domestic plants, the domestication traits are generally fixed in the initial domestication and appear in all individuals and populations. Cultivated rice significantly differs from its wild ancestor, O. rufipogon, in the morphology and environment adaptation. The most noticeable domestication traits of cultivated rice are lack of seed shattering, erect growth, annual habit and loss of seed dormancy. Other domestication traits of rice consist of seed coat color, flowering time, plant height, seed length, seed width, awn length, and eating quality. A large number of genes that are related to these domestication traits have been identified. Loss of seed-shattering habit is considered to be the most critical event in rice domestication. One layer between pedicel and spikelet at the base of rice seed is observed in wild rice and some indica varieties, resulting in a stronger seedshattering phenotype. Based on the linkage mapping, two independent research groups identified two genes, sh4 and qSH1, that caused loss of seed shattering in all rice and japonica rice, respectively (Konishi et al., 2006; Li et al., 2006a). The sh4 was detected from the recombination population derived between indica and O. nivara, explaining 69% variation on the reduction of grain shattering in cultivated rice (Li et al., 2006a). Similarly, qSH1 was detected from the Kasalath (a typical aus cultivar) and Nipponbare (a temperate japonica cultivar) population, explaining 68.6% of the total variation in the population. Further analysis showed that the nonshattering sh4 allele had a single origin and was fixed in all rice cultivars by artificial selection during the domestication of rice (Zhang et al., 2009). Selection on the nonshattering qSH1 allele mainly distributed in japonica and was rare in indica. The results are consistent with the fact that japonica varieties have a greater hard-to-shatter level than indica varieties. Another significant domestication event of rice is the transition from the prostrate growth of wild rice to the erect growth of cultivated rice. The PROG1 gene that encodes a single Cys2-His2 zinc-finger protein and controls tiller angle and number of tillers of rice was identified from the ancestral wild rice O. rufipogon (Jin et al., 2008; Tan et al., 2008). The mutant allele, prog1, in cultivated rice led to smaller tiller angle, greater tiller number, and erect growth. Sequence comparison of indica and japonica variations revealed that all erect growth rice varieties had the same SNPs and Indels, implying that the favored prog1 allele might have been singly originated and strongly selected during rice domestication (Tan et al., 2008).

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Other important domesticated genes that were related to the domestication traits include but not limited to Rc (Sweeney et al., 2006), Bh4 (Zhu et al., 2011), Waxy (Olsen and Purugganan, 2002; Qiao et al., 2012; Wang et al., 1995), TAC1 (Jiang et al., 2012; Yu et al., 2007), qSW5/GW5 (Shomura et al., 2008; Weng et al., 2008), Sdr4 (Sugimoto et al., 2010), Sd1 (Asano et al., 2011; Sasaki et al., 2002), OsLG1 (Ishii et al., 2013; Zhu et al., 2013), An-1 (Luo et al., 2013), LABA1 (Gu et al., 2015; Hua et al., 2015), and GAD1 (Jin et al., 2016). Unlike the domesticated alleles of sh4 and prog1 genes that were fixed in all cultivated rice, domestication of these genes exist in a large range of variations in rice. Rc, which encodes a basic helixeloopehelix transcription factor, conditioned the rice seed coat color change from red to white pericarp (Sweeney et al., 2006). The domesticated rc allele, which had a 14 bp deletion, has not been selected in all cultivated rice accessions. Similar to the qSH1 gene, domestication of TAC1 (plant architecture related), OsLG1 (panicle architecture related), and qGW5 (seed width related) were mainly domesticated in japonica (Huang et al., 2009; Ishii et al., 2013; Konishi et al., 2006; Shomura et al., 2008; Yu et al., 2007). Selection of the photoperiod genes, such as Hd1, Ehd1, Hd3a, Ghd7, Ghd8, and DTH2, extends the distribution of rice from tropical and subtropical area to temperate area, resulting in rice changing from a regional plant to a worldwide plant (Takahashi et al., 2009; Wei et al., 2010; Wu et al., 2013; Xue et al., 2008).

3.2

Recent studies on domestication processes

Domestication process is one of the most fundamental questions of crop research. The domestication of many crops has been illuminated by genetic, biochemical, and molecular evidence, such as maize, wheat, and tomato. For rice, the most important crop, the domestication was not clearly demonstrated. It is generally accepted that cultivated rice was domesticated from the wild relative rice in Asia about 10,000 years ago. However, the four basic questions of rice domesticationdthe ancestor, geographic origin, domestication time, and the number of domestication timesdall have been argued for a long time (Kovach et al., 2007; Sang and Ge, 2007a, 2007b; Sweeney and McCouch, 2007). The puzzle of rice domestication mainly related to the complex population structure of rice. Rice consists of two subspecies: indica and japonica. Recent genomic analysis revealed that the two subspecies could be further divided into five groups: indica, aus, temperate japonica, tropical japonica, and aromatic. The debates about the single or multiple domestication events and the geographic origin of rice are both closely related to indica and japonicadWere indica and japonica domesticated from one or two distinct populations of wild rice? Which subspecies was domesticated first? Where are the starting domestication areas of indica and japonica? Two major hypotheses were proposed in rice domestication: the first one is that indica and japonica had a single origin in one area; the other is that the subspecies or five groups have multiple origins in geographically distinct regions from different wild ancestor populations. The single origin hypothesis was popular before the application of biochemistry and genetic markers in the rice domestication research. It suggested that O. sativa was domesticated from O. rufipogon or O. nivara directly and then

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diverged into two subspecies (Chang, 1976; Oka and Morishima, 1982), or indica was domesticated firstly and then japonica was derived from indica (Ting, 1957). The isozymes, RFLPs, SNPs, transposons analysis of natural populations showed that indica and japonica were domesticated from indica-like and japonica-like O. rufipogon (Cheng et al., 2003; Londo et al., 2006; Rakshit et al., 2007; Second, 1982; Sun et al., 2002; Wei et al., 2012). With the development of NGS, genome sequences and genome-wide variations of wild and cultivated rice were used in the rice domestication study and enabled us to evaluate the hypotheses in the genomics level. Sixty-six accessions of indica, japonica, and O. rufipogon were resequenced with 1.5X genome coverage per accession. The genomic analysis supported a history of independent origin of indica and japonica from wild rice. However, some low-diversity regions in the genomes originated only once in one population and spread across all cultivars through introgression and human selection (He et al., 2011). Two O. rufipogon accessions were genome sequenced and the genomes were compared with that of cultivated rice. The results provided evidence of the independent domestication of japonica and indica with gene flow from japonica to indica (Yang et al., 2012). In total, 630 gene fragments on chromosomes 8, 10, and 12 from 40 cultivated rice and 17 wild relative accessions were sequenced. Using patterns of SNPs, 20 putative selective sweeps in cultivated rice were identified and a single domestication origin of rice was supported by the demographic modeling (Molina et al., 2011). Although similar strategies were used in the research of Molina et al. (2011) and He et al. (2011), two opposite conclusions were obtained. This result might relate to the small size of samples used in these studies. To make an accurate and comprehensive study of domestication, a large scale of samples from a broad distribution region was required. To investigate the population structure of Oryza rufipogon, 42 genome-wide sequence-tagged sites were used to survey 108 O. rufipogon accessions throughout the native range of the species. Two genetically distinct O. rufipogon groups, Ruf-I and Ruf-II, were identified. Ruf-I showed genetic similarity with indica, whereas Ruf-II was not found to be closely related to cultivated rice varieties. The results support the hypothesis of a single origin of rice and that indica was domesticated firstly (Huang et al., 2012a). Subsequently, genome sequences of 446 geographically diverse accessions of the wild rice species O. rufipogon (including O. nivara), and from 1083 cultivated indica and japonica varieties, were generated and a comprehensive map of rice genome variation was constructed (Huang et al., 2012c). The O. rufipogon population was clustered into three groups: Or-I, Or-II, and Or-III by 5 million SNPs. In total, 55 selective sweeps that have occurred during domestication were identified. In-depth analyses of the domestication sweeps and genome-wide patterns reveal that japonica was first domesticated from Or-III, and that indica was subsequently developed from crosses between japonica rice and wild rice in Or-I (also called O. nivara). One study (Civan et al., 2015) suggested a multiple-origin model hypothesizing japonica, indica, and aus having three separate origins with independent domestications (but was argued by Huang and Han, 2016). Recently, a new model that suggested that different rice subspecies had separate origins but only one domestication was constructed by comparing the genomes of wild and cultivated rice (Choi et al., 2017), consistent with the previous study (Huang et al., 2012c).

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For the ancestor of O. sativa, both O. rufipogon and O. nivara were considered as the progenitors of rice (Grillo et al., 2009; Khush, 1997; Vaughan et al., 2008). O. rufipogon is perennial, photoperiod sensitive, and largely cross-fertilized; it is widely distributed from South China to North Australia. O. nivara is an annual wild relative of rice, which is mainly found in South and Southeast Asia (Zhou et al., 2008). It was derived from O. rufipogon about 0.16 million years ago associated with an ecological shift from a persistently wet to a seasonally dry habitat (Liu et al., 2015; Zheng and Ge, 2010). Chen et al. (1993) detected a deletion in chloroplast DNA in 137 cultivars and 117 strains of wild rice from various countries. The result revealed that indica and annual type of O. rufipogon (also named O. nivara) had the deletion while japonica and perennial type of O. rufipogon had the nondeletion, suggesting that indica might have a close relationship to O. nivara. The genomics research supported that O. nivara had a closer relationship to indica. Xu et al. (2012) resequenced 40 accessions of cultivated rice and 10 accessions of O. rufipogon and O. nivara. With the 6.5 million SNPs, phylogenetic analysis showed that indica and japonica had a close relationship to O. nivara and O. rufipogon, respectively. Huang et al. (2012c) also identified that indica came from the cross of japonica and Or-I (mainly O. nivara). Thus, the genomic results showed that O. nivara might be the main ancestor of indica, whereas japonica was domesticated only from O. rufipogon. Based on these genome studies, a model that might be close to the truth of rice domestication was constructed (Fig. 1.1). Some mutations that related to shattering,

Oryza rufipogon in South China

Domestication

Oryza rufipogon in South Asia

Cross

Cross

Ancient japonica

Oryza nivara and O. rufipogon in South Asia

Domestication

Proto indica

indica

Proto aus

Domestication

japonica

Domestication

Aus

Figure 1.1 The domestication model of cultivated rice. The genomes of rice and wild rice are indicated by ovals in different colors. Red (light gray in print version): indica and Oryza rufipogon in South Asia. Blue (dark black in print version): japonica and O. rufipogon in South China. Purple (light black in print version): Aus, Oryza nivara and O. rufipogon in South Asia. Genes are indicated by different shapes. Square: genes from the South Asia O. rufipogon genome. Triangle: genes from the South China O. rufipogon genome. Hexagon: the initial domesticated genes in ancient japonica. Diamond: genes from O. nivara genome. Circle: domesticated genes.

Origin, taxonomy, and phylogenetics of rice

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tilling angle, and seed coat color were discovered in the O. rufipogon from South China and fixed in the ancient japonica. When the ancient japonica spread to South Asia, it was crossed with O. rufipogon in the local region. Thus, proto indica and proto aus that carried domesticated genes were developed, respectively. Finally, with long time artificial selections, indica, japonica, and aus varieties were generated and the domestication alleles were fixed in modern rice. The genomics research was further used in the domestication research of the small groups of rice, including aus, aromatic, and tropical japonica (Wang et al., 2016); more in-depth investigations will be needed to understand the detailed domestication and introgression events in these rice groups.

3.3

Geographic origin and domestication timing

Geographic origin and domestication timing were two of the basic questions of rice domestication. Generally, crop was domesticated from the areas that have the wild relative species. Nowadays, wild relative species O. rufipogon and O. nivara distribute in South Asia, Southeast Asia, and South China. In the very beginning, because of the finding of wild relative rice and the rich varieties of local rice, O. sativa was supposed to be domesticated from India (Vavilov, 1951). Later, Ting (1957) detected wild rice in South China and argued that rice was domesticated from southern China. Another single-origin hypothesis of rice domestication supposed that rice was domesticated in a broad geographic range spanning eastern India, Indochina, and portions of southern China (Khush, 1997). However, these conjectures were proposed based on the distribution of wild rice and the morphological diversity of cultivated rice. The archaeological evidence and genetic data of rice domestication have accumulated quickly in the last decades. Phytolith, the fossil of rice, has been found in several archaeological sites in Asia. Among the phytoliths, those found in middle and lower regions of the Yangtze River were accepted to be the earliest by most archaeologists. The rice phytoliths preserved in Diaotonghuan in Jiangxi Province and Shangshan in Zhejiang Province were detected to be from 10,000 years ago (Jiang and Liu, 2006; Zhao, 1998). The nonshattering rice appeared about 6600 to 8000 years ago in Tianluoshan and Jiahu archaeological sites (Fuller et al., 2009; Zhao, 2010). This evidence suggested that rice cultivation begun about 8000 years ago in the middle and lower regions of the Yangtze River of China and the key domestication trait of nonshattering was subsequently fixed at about 7000 years ago (Gross and Zhao, 2014). In India, rice was cultivated and appears to have been a staple food by 5000 years ago (Fuller, 2011). Therefore, the archaeologists stated that the middle and lower regions of the Yangtze River should be one of the geographic origin centers of rice cultivation (Fuller et al., 2009; Vaughan et al., 2008; Zong et al., 2007). The geneticists used biochemical and molecular markers to investigate the phylogenetic relationship of O. sativa and wild rice from the 1980s (Londo et al., 2006; Second, 1985; Wei et al., 2012). With the constructed phylogeny, the areas that the ancestral wild rice population were identified to be from were the geographic origin regions of O. sativa. Second (1985) used 24 isozymes to screen 181 Oryza plants and found that indica and japonica had the closest relationship to O. rufipogon

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from China and South Asia, respectively. Londo et al. (2006) detected the SNPs in one chloroplast DNA (atpB-rbcL) and two nuclear genes (SAM and p-VATPase) on 362 samples of O. sativa and O. rufipogon. Phylogeographic analysis supported that indica was domesticated within a region south of the Himalaya mountain range, likely eastern India, Myanmar, and Thailand, whereas japonica was domesticated from southern China. Wei et al. (2012) selected 100 accessions of cultivated rice and 111 accessions of wild rice in China to examine the relationship between O. sativa and O. rufipogon and thereby infer the domestication and evolution of rice in China through sequence analysis of six gene regions. The results indicated that both indica and japonica were domesticated from Southern China and the Pearl River basin near the Tropic of Cancer, and was the domestication center of O. sativa in China. Huang et al. (2012c) sequenced 446 accessions of O. rufipogon and 1083 accessions of O. sativa. Analysis of genome-wide SNPs and domestication sweeps showed that japonica was domesticated from Pearl River Valley in Southern China, and that indica came from crosses of ancestral japonica and wild rice in South Asia. In fact, fossils of cultivated rice have also been recently found in Southern China in several archaeological sites, including Yuchanyan (Boaretto et al., 2009), Niulandong (Gong et al., 2007), Shixia (Zhang et al., 2007), Jiuwuhoushan (Zhang et al., 2008), and Pingtouling (Liu et al., 2010). Among these archaeological sites, Yuchanyan is recognized as the oldest archaeological site of cultivated rice in China. It is located in Daoxian County, Hunan Province, and is estimated to be w13,000 to 18,000 years old (Boaretto et al., 2009). Thus, fossil evidence of ancient cultivated rice found in Southern China also strongly supports the hypothesis that cultivated rice may have been domesticated in Southern China and then spread worldwide. Molina et al. (2011) performed molecular clock analysis of the domestication time and indica-japonica splitting time. They dated the origin of rice domestication at about 8200 to 13,500 years ago, and the splitting of japonica and indica at 3900 to 6700 years ago. Thus, combined with the archaeological evidence and genetic analysis, Gross and Zhao (2014) supposed that japonica was domesticated from South China at 8000 years ago, and completely domesticated indica appeared in Ganges Plains in India until the domesticated japonica arrived and hybridized with it about 4000 years ago. Choi et al. (2017) estimated that the domestication of japonica rice began at w13,100 to 24,100 years ago. Although much effort had been made on rice domestication, some concerns still continue because a precise estimate of the domestication time is very difficult in both genetic studies and archaeological research. Moreover, gene flow from O. sativa to the wild rice was identified recently, indicating that the wild rice populations should be considered a hybrid swarm, and thus domestication research based on the genomics of wild rice, especially that between indica and O. nivara, might have been affected (Wang et al., 2017).

3.4

The case for the domestication of African rice

The African cultivated rice (O. glaberrima), one of the two cultivated species of the genus Oryza, is now confined almost exclusively to West Africa (Vaughan et al., 2008).

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By comparison to Asian cultivated rice (O. sativa), grain yield and eating quality of O. glaberrima are not desirable (Sarla and Swamy, 2005). However, it is well adapted to the cultivated condition in West Africa and is tolerant to the abiotic and biotic stresses, such as drought, salinity, waterlogging, iron, pests, and diseases (Linares, 2002; Wang et al., 2014). By introducing superior genes from O. glaberrima genomes into O. sativa, the improvement of O. sativa could be expected. Although the crossing of O. glaberrima and O. sativa is difficult, progenies have were successfully generated in the mid-1990s (Jones et al., 1997). QTLs contributing to grain quality, yield, and disease resistance had been identified from the O. sativa  O. glaberrima populations (Aluko et al., 2004; Gutierrez et al., 2010; Li et al., 2004). Unlike the complex history of domestication in O. sativa, the domestication process of O. glaberrima was identified very early (Linares, 2002; Sweeney and McCouch, 2007; Vaughan, 1989). There are two AA genome rice species grown in Africa: O. barthii and O. longistaminata. O. longistaminata is a perennial species found in much of sub-Saharan Africa. O. barthii is an annual species grown widely in Africa. Although O. longistaminata and O. barthii distributed in the same habit of some regions in Africa, archaeological evidence suggested that O. glaberrima was first domesticated from O. barthii in the inland delta of the Upper Niger River about 2000 to 3000 years ago (Portéres, 1962; Choi et al., 2017). It is documented that O. glaberrima was domesticated from 300 BC to 200 BC in Mali (Mcintosh, 1994). From 1998 to 2001, a large quantity of African rice grains was recovered from the site of Dia, in the middle Niger Delta. Based on dimensions of the rice grains, they were presumed to be domesticated plants. The accelerator-based mass spectrometry C-14 dating of the rice revealed that it was domesticated about 2500 to 2800 years ago (Murray, 2004). Genetic data, including isozymes, SSRs, and SNPs, unequivocally demonstrated that O. glaberrima had a close relationship to O. barthii (Second, 1982; Semon et al., 2005; Zhu and Ge, 2005). The accessions of O. glaberrima were sequenced recently (Sakai et al., 2011; Wang et al., 2014). The genome sequence of O. glaberrima provides the opportunity to deepen the understanding of the domestication of African cultivated rice at the genomics level. Resequencing of 20 accessions of O. glaberrima and 94 accessions of O. barthii revealed that O. glaberrima was domesticated from O. barthii in a single region along the Niger River (Wang et al., 2014). Artificial selection of O. glaberrima was detected at a genome-wide scale, including the orthology of qSh1, Sd1, Dep1, and Rc genes that had been domesticated in O. sativa (Wang et al., 2014). Sequence comparison of three nonshattering genes, OsSh1, qSh1, Sh4, revealed distinct SNPs in these genes of O. sativa and O. glaberrima, supporting the independent domestication of O. glaberrima and O. sativa (Wang et al., 2014). The nonshattering genes Sh3 and GL4 were identified in O. glaberrima recently (Win et al., 2016; Wu et al., 2017). The domestication of O. glaberrima was at least 6000 years later than O. sativa. The ancestral population of O. barthii was also much smaller than that of O. rufipogon and O. nivara. The short domestication time and a strict origin of the gene pool might result in the weakness yield and seed quality of O. glaberrima as well as less genetic diversity. Asian cultivated rice was introduced into West Africa after the initial domestication by the Portuguese as early as the middle of the 16th century (Portéres, 1962).

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Asian-cultivated rice was grown side by side with O. glaberrima in Africa and replaced a large proportion of the planting area of O. glaberrima. The introduction of O. sativa into the O. glaberrima range added a new dynamic to the evolution of African-cultivated rice. Based on SSR detection, genetic analysis identified that part of O. glaberrima has introgressed genes from O. sativa (Semon et al., 2005). This gene flow from O. sativa to O. glaberrima was confirmed by genomic analysis, but in a very low frequency (Huang et al., 2015a).

3.5

Genetic mapping of domestication genes

Understanding the domestication of a crop will guide future breeding efforts (Morrell et al., 2011). The identified domesticated genes will be valuable resources for genetic improvement of rice. With great effort from rice researchers, a large number of rice domestication genes that underlying important agronomic traits have been identified in the last two decades (Doi et al., 2004; Jin et al., 2008; Konishi et al., 2006; Li et al., 2006a; Sweeney et al., 2006; Tan et al., 2008; Wang et al., 1995; Wei et al., 2010; Yano et al., 2000; Yu et al., 2007). Some of the domesticated genes were domesticated in the initial stage of rice domestication and fixed in all descendant rice, such as Sh4 and PROG1 (Jin et al., 2008; Li et al., 2006a), whereas some of them were mainly selected in one group. For instance, DEP1 and TAC1 were only domesticated in japonica (Huang et al., 2009; Yu et al., 2007). Generally, the genetic mapping of rice domestication genes was based on linkage mapping with biparental population. For linkage mapping, different kinds of biparent population had been used for the gene identification. Sh4, a transcription factor that greatly reduced shattering in O. sativa, was mapped from a large F2 population (w12,000) derived between O. sativa and O. nivara (Li et al., 2006a). PROG1, a zinc-finger nuclear transcription factor that controlled aspects of wild rice plant architecture, was also mapped from a large population (>3000) derived from Teqing (a rice variety) and a near-isogenic line that developed from chromosome segment substitution line of Teqing and O. rufipogon (Jin et al., 2008). GAD1, an EPIDERMAL PATTERNING FACTOR-LIKE peptide, regulating grain number, grain length, and awn development, was mapped from an F2 population with 4250 individuals derived from a cross between 93-11 and O. rufipogon (Jin et al., 2016). By measuring the ratio of the genetic diversity in wild rice to that in cultivated rice across the rice genome, Huang et al. (2012c) identified 60 loci in indica, 62 in japonica, and 55 in the full population to be the selective sweep loci of rice. These loci were supposed to be involved in the rice domestication and introgression. The most well-characterized domestication genes, including Bh4, PROG1, sh4, qSW5, and OsC1, were among the 55 loci detected in the full population. Some other famous domestication genes, qSH1, Waxy and Rc, were only detected in the japonica. However, many other selective sweep loci in rice genome have not been clearly elucidated. These genes that have not been identified might be related to several typical domestication traits, such as seed dormancy, germination rate, and perennial. To clone these domestication genes, new mapping population methods and technologies may be developed and used in the future. Chromosome segment substitution lines, near-isogenic lines, and

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nested association mapping populations of wild rice and different O. sativa groups can be developed. GWAS using whole-genome sequencing might identify new domesticated genes influencing agronomic traits (Yano et al., 2016). Combined genome-wide association study (GWAS) with gene expression and metabolism was successfully used in the identification of genes related in the tomato domestication (Huang and Han, 2016). Genome-editing technologies using CRISPR/Cas system are greatly needed in the quick validation of the identified rice domestication genes and their functional variants that underlie the significant agronomic traits.

References Agrama, H.A., Yan, W., Jia, M., Fjellstrom, R., Mcclung, A.M., 2010. Genetic structure associated with diversity and geographic distribution in the USDA rice world collection. Natural Science 02, 247e291. Akagi, H., Yokozeki, Y., Inagaki, A., Fujimura, T., 1998. Origin and evolution of twin microsatellites in the genus Oryza. Heredity 81, 188e197. Alexandrov, N., Tai, S., Wang, W., Mansueto, L., Palis, K., Fuentes, R.R., Ulat, V.J., Chebotarov, D., Zhang, G., Li, Z., Mauleon, R., Hamilton, R.S., McNally, K.L., 2015. SNP-Seek database of SNPs derived from 3000 rice genomes. Nucleic Acids Research 43, D1023eD1027. Ali, M.L., Mcclung, A.M., Jia, M.H., Kimball, J.A., Mccouch, S.R., Georgia, C.E., 2011. A rice diversity panel evaluated for genetic and Agro-morphological diversity between subpopulations and its geographic distribution. Crop Science 51, 2021e2035. Aluko, G., Martinez, C., Tohme, J., Castano, C., Bergman, C., Oard, J.H., 2004. QTL mapping of grain quality traits from the interspecific cross Oryza sativa  O. glaberrima. Theoretical and Applied Genetics 109, 630e639. Asano, K., Yamasaki, M., Takuno, S., Miura, K., Katagiri, S., Ito, T., Doi, K., Wu, J., Ebana, K., Matsumoto, T., Innan, H., Kitano, H., Ashikari, M., Matsuoka, M., 2011. Artificial selection for a green revolution gene during japonica rice domestication. Proceedings of the National Academy of Sciences of the United States of America 108, 11034e11039. Boaretto, E., Wu, X., Yuan, J., Bar-Yosef, O., Chu, V., Pan, Y., Liu, K., Cohen, D., Jiao, T., Li, S., Gu, H., Goldberg, P., Weiner, S., 2009. Radiocarbon dating of charcoal and bone collagen associated with early pottery at Yuchanyan Cave, Hunan Province, China. Proceedings of the National Academy of Sciences of the United States of America 106, 9595e9600. Chang, T.T., 1976. The origin, evolution, cultivation, dissemination, and diversification of Asian and African rices. Euphytica 25, 425e441. Chen, W.B., Nakamura, I., Sato, Y.I., Nakai, H., 1993. Distribution of deletion type in cpDNA of cultivated and wild rice. Japanese Journal of Genetics 68, 597e603. Cheng, C., Motohashi, R., Tsuchimoto, S., Fukuta, Y., Ohtsubo, H., Ohtsubo, E., 2003. Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Molecular Biology and Evolution 20, 67e75. Choi, J.Y., Platts, A.E., Fuller, D.Q., Hsing, Y.L., Wing, R.A., Purugganan, M.D., 2017. The rice Paradox: multiple origins but single domestication in Asian rice. Molecular Biology and Evolution 34, 969e979.

20

Rice

Civan, P., Craig, H., Cox, C.J., Brown, T.A., 2015. Three geographically separate domestications of Asian rice. Nature Plants 1, 15164. Consortium, T.I.H., 2003. The International HapMap project. Nature 426, 789e796. Dally, A.M., Second, G., 1990. Chloroplast DNA diversity in wild and cultivated species of rice (Genus Oryza, section Oryza). Cladistic-mutation and genetic-distance analysis. Theoretical and Applied Genetics 80, 209e222. Darwin, D., 1868. The Variation of Animals and Plants under Domestication. John Murray, London. Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., Yano, M., Yoshimura, A., 2004. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes & Development 18, 926e936. Du, B., Zhang, W., Liu, B., Hu, J., Wei, Z., Shi, Z., He, R., Zhu, L., Chen, R., Han, B., He, G., 2009. Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proceedings of the National Academy of Sciences of the United States of America 106, 22163e22168. Feltus, F.A., Wan, J., Schulze, S.R., Estill, J.C., Jiang, N., Paterson, A.H., 2004. An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Research 14, 1812e1819. Fuller, D.Q., 2011. Funding plant domestication in the indian subcontinent. Current Anthropology 52, S347eS362. Fuller, D.Q., Qin, L., Zheng, Y., Zhao, Z., Chen, X., Hosoya, L.A., Sun, G.P., 2009. The domestication process and domestication rate in rice: spikelet bases from the Lower Yangtze. Science 323, 1607e1610. Garris, A.J., Tai, T.H., Coburn, J., Kresovich, S., Mccouch, S., 2005. Genetic structure and diversity in Oryza sativa L. Genetics 169, 1631e1638. Ge, S., Sang, T., Lu, B.R., Hong, D.Y., 1999. Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proceedings of the National Academy of Sciences of the United States of America 96, 14400e14405. Glaszmann, J.C., 1987. Isozymes and classification of Asian rice varieties. Theoretical and Applied Genetics 74, 21e30. Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B.M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W.L., Chen, L., Cooper, B., Park, S., Wood, T.C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R.M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., Briggs, S., 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92e100. Gong, Z.T., Chen, H.Z., Yuan, D.G., Zhao, Y.G., Wu, Y.J., Zhang, G.L., 2007. The temporal and spatial distribution of ancient rice in China and its implications. Chinese Science Bulletin 52, 1071e1079. Grillo, M.A., Li, C., Fowlkes, A.M., Briggeman, T.M., Zhou, A., Schemske, D.W., Sang, T., 2009. Genetic architecture for the adaptive origin of annual wild rice, oryza nivara. Evolution 63, 870e883. Gross, B.L., Zhao, Z., 2014. Archaeological and genetic insights into the origins of domesticated rice. Proceedings of the National Academy of Sciences of the United States of America 111, 6190e6197.

Origin, taxonomy, and phylogenetics of rice

21

Gu, K., Yang, B., Tian, D., Wu, L., Wang, D., Sreekala, C., Yang, F., Chu, Z., Wang, G.L., White, F.F., Yin, Z., 2005. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435, 1122e1125. Gu, B., Zhou, T., Luo, J., Liu, H., Wang, Y., Shangguan, Y., Zhu, J., Li, Y., Sang, T., Wang, Z., Han, B., 2015. An-2 encodes a cytokinin synthesis enzyme that regulates awn length and grain production in rice. Molecular Plant 8, 1635e1650. Guo, L., Gao, Z., Qian, Q., 2014. Application of resequencing to rice genomics, functional genomics and evolutionary analysis. Rice 7, 4. Gutierrez, A.G., Carabali, S.J., Giraldo, O.X., Martinez, C.P., Correa, F., Prado, G., Tohme, J., Lorieux, M., 2010. Identification of a Rice stripe necrosis virus resistance locus and yield component QTLs using Oryza sativa  O. glaberrima introgression lines. BMC Plant Biology 10. He, Z., Zhai, W., Wen, H., Tang, T., Wang, Y., Lu, X., Greenberg, A.J., Hudson, R.R., Wu, C.I., Shi, S., 2011. Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genetics 7, e1002100. Hua, L., Wang, D.R., Tan, L., Fu, Y., Liu, F., Xiao, L., Zhu, Z., Fu, Q., Sun, X., Gu, P., Cai, H., Mccouch, S.R., Sun, C., 2015. LABA1, a domestication gene associated with long, barbed awns in wild rice. Plant Cell 27, 1875e1888. Huang, X.H., Han, B., 2016. Rice domestication occurred through single origin and multiple introgressions. Nature Plants 2. Huang, X.H., Kurata, N., Wei, X.H., Wang, Z.X., Wang, A., Zhao, Q., Zhao, Y., Liu, K.Y., Lu, H.Y., Li, W.J., Guo, Y.L., Lu, Y.Q., Zhou, C.C., Fan, D.L., Weng, Q.J., Zhu, C.R., Huang, T., Zhang, L., Wang, Y.C., Feng, L., Furuumi, H., Kubo, T., Miyabayashi, T., Yuan, X.P., Xu, Q., Dong, G.J., Zhan, Q.L., Li, C.Y., Fujiyama, A., Toyoda, A., Lu, T.T., Feng, Q., Qian, Q., Li, J.Y., Han, B., 2012c. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497e501. Huang, X., Lu, G., Zhao, Q., Liu, X., Han, B., 2008. Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Plant Physiology 148, 25e40. Huang, P., Molina, J., Flowers, J.M., Rubinstein, S., Jackson, S.A., Purugganan, M.D., Schaal, B.A., 2012a. Phylogeography of Asian wild rice, Oryza rufipogon: a genome-wide view. Molecular Ecology 21, 4593e4604. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J., Fu, X., 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics 41, 494e497. Huang, X., Wei, X., Sang, T., Zhao, Q., Feng, Q., Zhao, Y., Li, C., Zhu, C., Lu, T., Zhang, Z., Li, M., Fan, D., Guo, Y., Wang, A., Wang, L., Deng, L., Li, W., Lu, Y., Weng, Q., Liu, K., Huang, T., Zhou, T., Jing, Y., Li, W., Lin, Z., Buckler, E.S., Qian, Q., Zhang, Q.F., Li, J., Han, B., 2010. Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genetics 42, 961e967. Huang, X.H., Yang, S.H., Gong, J.Y., Zhao, Y., Feng, Q., Gong, H., Li, W.J., Zhan, Q.L., Cheng, B.Y., Xia, J.H., Chen, N., Hao, Z.N., Liu, K.Y., Zhu, C.R., Huang, T., Zhao, Q., Zhang, L., Fan, D.L., Zhou, C.C., Lu, Y.Q., Weng, Q.J., Wang, Z.X., Li, J.Y., Han, B., 2015b. Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nature Communications 6, 6258. Huang, X., Zhao, Q., Han, B., 2015a. Comparative population genomics reveals strong divergence and Infrequent introgression between Asian and African rice. Molecular Plant 8, 958e960.

22

Rice

Huang, X., Zhao, Y., Wei, X., Li, C., Wang, A., Zhao, Q., Li, W., Guo, Y., Deng, L., Zhu, C., Fan, D., Lu, Y., Weng, Q., Liu, K., Zhou, T., Jing, Y., Si, L., Dong, G., Huang, T., Lu, T., Feng, Q., Qian, Q., Li, J., Han, B., 2012b. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genetics 44, 32e39. International Rice Genome Sequencing Project, 2005. The map-based sequence of the rice genome. Nature 436, 793e800. Ishii, T., Numaguchi, K., Miura, K., Yoshida, K., Thanh, P.T., Htun, T.M., Yamasaki, M., Komeda, N., Matsumoto, T., Terauchi, R., Ishikawa, R., Ashikari, M., 2013. OsLG1 regulates a closed panicle trait in domesticated rice. Nature Genetics 45, 462e465, 465e1-2. Jiang, L., Liu, L., 2006. New evidence for the origins of sedentism and rice domestication in the Lower Yangzi River, China. Antiquity 80, 355e361. Jiang, J., Tan, L., Zhu, Z., Fu, Y., Liu, F., Cai, H., Sun, C., 2012. Molecular evolution of the TAC1 gene from rice (Oryza sativa L.). J Genet Genomics 39, 551e560. Jin, J., Hua, L., Zhu, Z., Tan, L., Zhao, X., Zhang, W., Liu, F., Fu, Y., Cai, H., Sun, X., Gu, P., Xie, D., Sun, C., 2016. GAD1 encodes a Secreted peptide that regulates grain number, grain length, and awn development in rice domestication. Plant Cell 28, 2453e2463. Jin, J., Huang, W., Gao, J.P., Yang, J., Shi, M., Zhu, M.Z., Luo, D., Lin, H.X., 2008. Genetic control of rice plant architecture under domestication. Nature Genetics 40, 1365e1369. Jones, M.P., Dingkuhn, M., Aluko/Snm>, G.K., Semon, M., 1997. Interspecific Oryza sativa L.  O. glaberrima Steud. progenies in upland rice improvement. Euphytica 94, 237e246. Khush, G.S., 1997. Origin, dispersal, cultivation and variation of rice. Plant Molecular Biology 35, 25e34. Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T., Yano, M., 2006. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392e1396. Kovach, M.J., Sweeney, M.T., Mccouch, S.R., 2007. New insights into the history of rice domestication. Trends in Genetics 23, 578e587. Kumagai, M., Wang, L., Ueda, S., 2010. Genetic diversity and evolutionary relationships in genus Oryza revealed by using highly variable regions of chloroplast DNA. Gene 462, 44e51. Li, J., Xia, M., Qi, H., He, G., Wan, B., Zha, Z., 2006b. Marker-assisted selection for Brown planthopper (Nilaparvata lugens stal) resistance genes Bph14 and Bph15 in rice. Scientia Agricultura Sinica 39, 2132e2137. Li, J., Xiao, J., Grandillo, S., Jiang, L., Wan, Y., Deng, Q., Yuan, L., Mccouch, S.R., 2004. QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African (O. glaberrima S.) rice. Genome 47, 697. Li, C., Zhou, A., Sang, T., 2006a. Rice domestication by reducing shattering. Science 311, 1936e1939. Linares, O.F., 2002. African rice (Oryza glaberrima): history and future potential. Proceedings of the National Academy of Sciences of the United States of America 99, 16360e16365. Liu, Z.H., Zheng, T.Y., Chen, Y.D., Xiang, A.Q., 2010. Analyses on Re-examining several methods of biological researches for ancient cultivated rice. Journal of Guangxi University for Nationalities 16, 13e23. Liu, R., Zheng, X.M., Zhou, L., Zhou, H.F., Ge, S., 2015. Population genetic structure of Oryza rufipogon and Oryza nivara: implications for the origin of O. nivara. Molecular Ecology 24, 5211e5228. Londo, J.P., Chiang, Y.C., Hung, K.H., Chiang, T.Y., Schaal, B.A., 2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proceedings of the National Academy of Sciences of the United States of America 103, 9578e9583.

Origin, taxonomy, and phylogenetics of rice

23

Luo, J., Liu, H., Zhou, T., Gu, B., Huang, X., Shangguan, Y., Zhu, J., Li, Y., Zhao, Y., Wang, Y., Zhao, Q., Wang, A., Wang, Z., Sang, T., Wang, Z., Han, B., 2013. An-1 encodes a basic helix-loop-helix protein that regulates awn development, grain size, and grain number in rice. Plant Cell 25, 3360e3376. Luo, Y.C., Sangha, J.S., Wang, S.H., Li, Z.F., Yang, J.B., Yin, Z.C., 2012. Marker-assisted breeding of Xa4, Xa21 and Xa27 in the restorer lines of hybrid rice for broad-spectrum and enhanced disease resistance to bacterial blight. Molecular Breeding 30, 1601e1610. Ma, X., Feng, F., Wei, H., Mei, H., Xu, K., Chen, S., Li, T., Liang, X., Liu, H., Luo, L., 2016. Genome-wide association study for plant height and grain yield in rice under contrasting moisture regimes. Frontiers in Plant Science 7, 1801. Mackill, D.J., 1995. Classifying japonica rice cultivars with RAPD markers. Crop Science 35, 889e894. Matsuo, T., Futsuhara, Y., Kikuchi, F., Yamaguchi, H., 1997. Science of the Rice Plant. Food and Agriculture Policy Research Center, Tokyo. Mcintosh, S.K., 1994. Excavations at Jenné-jeno, Hambarketolo, and Kaniana (Inland Niger Delta, Mali), the 1981 Season. University of California Press. McNally, K.L., Childs, K.L., Bohnert, R., Davidson, R.M., Zhao, K., Ulat, V.J., Zeller, G., Clark, R.M., Hoen, D.R., Bureau, T.E., Stokowski, R., Ballinger, D.G., Frazer, K.A., Cox, D.R., Padhukasahasram, B., Bustamante, C.D., Weigel, D., Mackill, D.J., Bruskiewich, R.M., Ratsch, G., Buell, C.R., Leung, H., Leach, J.E., 2009. Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proceedings of the National Academy of Sciences of the United States of America 106, 12273e12278. Mishra, S., Singh, B., Panda, K., Singh, B.P., Singh, N., Misra, P., Rai, V., Singh, N.K., 2016. Association of SNP haplotypes of HKT family genes with salt tolerance in indian wild rice germplasm. Rice 9. Molina, J., Sikora, M., Garud, N., Flowers, J.M., Rubinstein, S., Reynolds, A., Huang, P., Jackson, S., Schaal, B.A., Bustamante, C.D., Boyko, A.R., Purugganan, M.D., 2011. Molecular evidence for a single evolutionary origin of domesticated rice. Proceedings of the National Academy of Sciences of the United States of America 108, 8351e8356. Morishima, H., Oka, H.I., 1981. Phylogenetic differentiation of cultivated rice, XXII. Numerical evaluation of the indica-japonica differentiation. Japanese Journal of Breeding 31, 402e413. Morrell, P.L., Buckler, E.S., Ross-Ibarra, J., 2011. Crop genomics: advances and applications. Nature Reviews Genetics 13, 85e96. Murray, S.S., 2004. Searching for the origins of African rice domestication. Antiquity 78, 99e107. Nakano, M., Yoshimura, A., Iwata, N., 1992. Phylogenetic study of cultivated rice and its wild relatives by RFLP. Rice Genetics Newsletter 9, 132e134. Ni, J., Colowit, P.M., Mackill, D.J., 2002. Evaluation of genetic diversity in rice subspecies using microsatellite markers. Crop Science 42, 601e607. Niroula, R.K., Pucciariello, C., Ho, V.T., Novi, G., Fukao, T., Perata, P., 2012. SUB1Adependent and -independent mechanisms are involved in the flooding tolerance of wild rice species. Plant Journal 72, 282e293. Oka, H., 1988. Indica-japonica differentiation of rice cultivars. In: Oka, H.I. (Ed.), Origin of Cultivated Rice. Japan Scientific Societies Press, Tokyo. Oka, H., Morishima, H., 1982. Phylogenetic differentiation of cultivated rice. XXIII. Potentiality of wild progenitors to evolve the indica and japonica types of rice cultivars. Euphytica 31, 41e50. Olsen, K.M., Purugganan, M.D., 2002. Molecular evidence on the origin and evolution of glutinous rice. Genetics 162, 941e950.

24

Rice

Paterson, A.H., Bowers, J.E., Chapman, B.A., 2004. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proceedings of the National Academy of Sciences of the United States of America 101, 9903e9908. Port Res, R., 1962. Berceaux Agricoles Primaires Sur Le continent Africain. The Journal of African History 3, 195e210. Qiao, W.H., Chen, Y.T., Wang, R.S., Wei, X., Cao, L.R., Zhang, W.X., Yang, Q.W., 2012. Nucleotide diversity in gene and validation of single nucleotide polymorphism in relation to amylose content in Chinese Microcore rice germplasm. Crop Science 52, 1689. Qu, S., Liu, G., Zhou, B., Bellizzi, M., Zeng, L., Dai, L., Han, B., Wang, G.L., 2006. The broadspectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 172, 1901e1914. Rakshit, S., Rakshit, A., Matsumura, H., Takahashi, Y., Hasegawa, Y., Ito, A., Ishii, T., Miyashita, N.T., Terauchi, R., 2007. Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theoretical and Applied Genetics 114, 731e743. Sakai, H., Ikawa, H., Tanaka, T., Numa, H., Minami, H., Fujisawa, M., Shibata, M., Kurita, K., Kikuta, A., Hamada, M., Kanamori, H., Namiki, N., Wu, J., Itoh, T., Matsumoto, T., Sasaki, T., 2011. Distinct evolutionary patterns of Oryza glaberrima deciphered by genome sequencing and comparative analysis. Plant Journal 66, 796e805. Salse, J., Bolot, S., Throude, M., Jouffe, V., Piegu, B., Quraishi, U.M., Calcagno, T., Cooke, R., Delseny, M., Feuillet, C., 2008. Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20, 11e24. Sang, T., Ge, S., 2007a. Genetics and phylogenetics of rice domestication. Current Opinion in Genetics & Development 17, 533e538. Sang, T., Ge, S., 2007b. The puzzle of rice domestication. Journal of Integrative Plant Biology 49. Sarla, N., Swamy, B.P.M., 2005. Oryza glaberrima: a source for the improvement of Oryza sativa. Current Science 89, 955e963. Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., Ishiyama, K., Saito, T., Kobayashi, M., Khush, G.S., Kitano, H., Matsuoka, M., 2002. Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416, 701e702. Second, G., 1982. Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Japanese Journal of Genetics 57, 25e57. Second, G., 1985. Evolutionary relationships in the Sativa group of Oryza based on isozyme data. Genetics Selection Evolution 17, 1e26. Semon, M., Nielsen, R., Jones, M.P., Mccouch, S.R., 2005. The population structure of African cultivated rice oryza glaberrima (Steud.): evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation. Genetics 169, 1639e1647. Shomura, A., Izawa, T., Ebana, K., Ebitani, T., Kanegae, H., Konishi, S., Yano, M., 2008. Deletion in a gene associated with grain size increased yields during rice domestication. Nature Genetics 40, 1023e1028. Singh, B.P., Jayaswal, P.K., Singh, B., Singh, P.K., Kumar, V., Mishra, S., Singh, N., Panda, K., Singh, N.K., 2015. Natural allelic diversity in OsDREB1F gene in the Indian wild rice germplasm led to ascertain its association with drought tolerance. Plant Cell Reports 34, 993e1004. Song, W.Y., Wang, G.L., Chen, L.L., Kim, H.S., Pi, L.Y., Holsten, T., Gardner, J., Wang, B., Zhai, W.X., Zhu, L.H., Fauquet, C., Ronald, P., 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804e1806.

Origin, taxonomy, and phylogenetics of rice

25

Sotowa, M., Ootsuka, K., Kobayashi, Y., Hao, Y., Tanaka, K., Ichitani, K., Flowers, J.M., Purugganan, M.D., Nakamura, I., Sato, Y.I., Sato, T., Crayn, D., Simon, B., Waters, D.L.E., Henry, R.J., Ishikawa, R., 2013. Molecular relationships between Australian annual wild rice, Oryza meridionalis, and two related perennial forms. Rice 6. Sugimoto, K., Takeuchi, Y., Ebana, K., Miyao, A., Hirochika, H., Hara, N., Ishiyama, K., Kobayashi, M., Ban, Y., Hattori, T., Yano, M., 2010. Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proceedings of the National Academy of Sciences of the United States of America 107, 5792e5797. Sun, C., Wang, X., Yoshimura, A., Doi, K., 2002. Genetic differentiation for muclear, mitochondrial and chloroplast genomes in common wild rice (O. rufipogon Griff.) and cultivated rice (O. sativa L.). Theoretical and Applied Genetics 104, 1335e1345. Sweeney, M., Mccouch, S., 2007. The complex history of the domestication of rice. Annals of Botany 100, 951e957. Sweeney, M.T., Thomson, M.J., Pfeil, B.E., Mccouch, S., 2006. Caught red-handed: rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18, 283e294. Takahashi, Y., Teshima, K.M., Yokoi, S., Innan, H., Shimamoto, K., 2009. Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proceedings of the National Academy of Sciences of the United States of America 106, 4555e4560. Tan, L., Li, X., Liu, F., Sun, X., Li, C., Zhu, Z., Fu, Y., Cai, H., Wang, X., Xie, D., Sun, C., 2008. Control of a key transition from prostrate to erect growth in rice domestication. Nature Genetics 40, 1360e1364. Ting, Y., 1957. The origin and evolution of cultivated rice in China. Acta Agron Sinica 8, 243e260. Vaughan, D.A., 1989. The Genus Oryza L. Current Status of Taxonomy. IRRI, Manila. Vaughan, D.A., Lu, B.-R., Tomooka, N., 2008. The evolving story of rice evolution. Plant Science 174, 394e408. Vavilov, N.I., 1951. The Origin, Variation, Immunity and Breeding of Cultivated Plants. Ronald Press. Wambugu, P.W., Brozynska, M., Furtado, A., Waters, D.L., Henry, R.J., 2015. Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Scientific Reports 5, 13957. Wang, Z.Y., Second, G., Tanksley, S.D., 1992. Polymorphism and phylogenetic relationships among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theoretical and Applied Genetics 83, 565e581. Wang, X., Shi, X., Hao, B., Ge, S., Luo, J., 2005. Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytologist 165, 937e946. Wang, H.R., Vieira, F.G., Crawford, J.E., Chu, C.C., Nielsen, R., 2017. Asian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated rice. Genome Research 27, 1029e1038. Wang, H., Xu, X., Vieira, F.G., Xiao, Y., Li, Z., Wang, J., Nielsen, R., Chu, C., 2016. The power of Inbreeding: NGS-based GWAS of rice reveals convergent evolution during rice domestication. Molecular Plant 9, 975e985. Wang, M., Yu, Y., Haberer, G., Marri, P.R., Fan, C., Goicoechea, J.L., Zuccolo, A., Song, X., Kudrna, D., Ammiraju, J.S., Cossu, R.M., Maldonado, C., Chen, J., Lee, S., Sisneros, N., DE Baynast, K., Golser, W., Wissotski, M., Kim, W., Sanchez, P., Ndjiondjop, M.N., Sanni, K., Long, M., Carney, J., Panaud, O., Wicker, T., Machado, C.A., Chen, M., Mayer, K.F., Rounsley, S., Wing, R.A., 2014. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nature Genetics 46, 982e988.

26

Rice

Wang, C.L., Zhang, X.P., Fan, Y.L., Gao, Y., Zhu, Q.L., Zheng, C.K., Qin, T.F., Li, Y.Q., Che, J.Y., Zhang, M.W., Yang, B., Liu, Y.G., Zhao, K.J., 2015. XA23 is an Executor R protein and confers broad-spectrum disease resistance in rice. Molecular Plant 8, 290e302. Wang, Z.Y., Zheng, F.Q., Shen, G.Z., Gao, J.P., Snustad, D.P., Li, M.G., Zhang, J.L., Hong, M.M., 1995. The amylose content in rice endosperm is related to the posttranscriptional regulation of the waxy gene. Plant Journal 7, 613e622. Wei, X., Liu, K., Zhang, Y., Feng, Q., Wang, L., Zhao, Y., Li, D., Zhao, Q., Zhu, X., Zhu, X., Li, W., Fan, D., Gao, Y., Lu, Y., Zhang, X., Tang, X., Zhou, C., Zhu, C., Liu, L., Zhong, R., Tian, Q., Wen, Z., Weng, Q., Han, B., Huang, X., Zhang, X., 2015. Genetic discovery for oil production and quality in sesame. Nature Communications 6, 8609. Wei, X., Qiao, W.H., Chen, Y.T., Wang, R.S., Cao, L.R., Zhang, W.X., Yuan, N.N., Li, Z.C., Zeng, H.L., Yang, Q.W., 2012. Domestication and geographic origin of Oryza sativa in China: insights from multilocus analysis of nucleotide variation of O. sativa and O. rufipogon. Molecular Ecology 21, 5073e5087. Wei, X., Xu, J., Guo, H., Jiang, L., Chen, S., Yu, C., Zhou, Z., Hu, P., Zhai, H., Wan, J., 2010. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiology 153, 1747e1758. Weng, J., Gu, S., Wan, X., Gao, H., Guo, T., Su, N., Lei, C., Zhang, X., Cheng, Z., Guo, X., Wang, J., Jiang, L., Zhai, H., Wan, J., 2008. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Research 18, 1199e1209. Win, K.T., Yamagata, Y., Doi, K., Uyama, K., Nagai, Y., Toda, Y., Kani, T., Ashikari, M., Yasui, H., Yoshimura, A., 2016. A single base change explains the independent origin of and selection for the nonshattering gene in African rice domestication. New Phytologist 213. Wing, R.A., Ammiraju, J.S., Luo, M., Kim, H., Yu, Y., Kudrna, D., Goicoechea, J.L., Wang, W., Nelson, W., Rao, K., Brar, D., Mackill, D.J., Han, B., Soderlund, C., Stein, L., Sanmiguel, P., Jackson, S., 2005. The oryza map alignment project: the golden path to unlocking the genetic potential of wild rice species. Plant Molecular Biology 59, 53e62. Wu, W., Liu, X., Wang, M., Meyer, R.S., Luo, X., Ndjiondjop, M.N., Tan, L., Zhang, J., Wu, J., Cai, H., Sun, C., Wang, X., Wing, R.A., Zhu, Z., 2017. A single-nucleotide polymorphism causes smaller grain size and loss of seed shattering during African rice domestication. Nature Plants 3, 17064. Wu, W., Zheng, X.M., Lu, G., Zhong, Z., Gao, H., Chen, L., Wu, C., Wang, H.J., Wang, Q., Zhou, K., 2013. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proceedings of the National Academy of Sciences of the United States of America 110, 2775e2780. Xie, W., Wang, G., Yuan, M., Yao, W., Lyu, K., Zhao, H., Yang, M., Li, P., Zhang, X., Yuan, J., Wang, Q., Liu, F., Dong, H., Zhang, L., Li, X., Meng, X., Zhang, W., Xiong, L., He, Y., Wang, S., Yu, S., Xu, C., Luo, J., Li, X., Xiao, J., Lian, X., Zhang, Q., 2015. Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. Proceedings of the National Academy of Sciences of the United States of America 112, E5411eE5419. Xu, X., Liu, X., Ge, S., Jensen, J.D., Hu, F., Li, X., Dong, Y., Gutenkunst, R.N., Fang, L., Huang, L., Li, J., He, W., Zhang, G., Zheng, X., Zhang, F., Li, Y., Yu, C., Kristiansen, K., Zhang, X., Wang, J., Wright, M., Mccouch, S., Nielsen, R., Wang, J., Wang, W., 2012. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nature Biotechnology 30, 105e111. Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C., Li, X., Zhang, Q., 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics 40, 761e767.

Origin, taxonomy, and phylogenetics of rice

27

Yamamoto, T., Nagasaki, H., Yonemaru, J., Ebana, K., Nakajima, M., Shibaya, T., Yano, M., 2010. Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms. BMC Genomics 11, 267. Yang, C.C., Kawahara, Y., Mizuno, H., Wu, J., Matsumoto, T., Itoh, T., 2012. Independent domestication of Asian rice followed by gene flow from japonica to indica. Molecular Biology and Evolution 29, 1471e1479. Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473e2484. Yano, K., Yamamoto, E., Aya, K., Takeuchi, H., Lo, P.C., Hu, L., Yamasaki, M., Yoshida, S., Kitano, H., Hirano, K., Matsuoka, M., 2016. Genome-wide association study using wholegenome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nature Genetics 48, 927e934. Yonemaru, J., Yamamoto, T., Ebana, K., Yamamoto, E., Nagasaki, H., Shibaya, T., Yano, M., 2012. Genome-wide haplotype changes produced by artificial selection during modern rice breeding in Japan. PLoS One 7, e32982. Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Huang, X., Li, W., Li, J., Liu, Z., Li, L., Liu, J., Qi, Q., Liu, J., Li, L., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Zhang, J., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Ren, X., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Wang, J., Zhao, W., Li, P., Chen, W., Wang, X., Zhang, Y., Hu, J., Wang, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Li, G., Liu, S., Tao, M., Wang, J., Zhu, L., Yuan, L., Yang, H., 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79e92. Yu, B., Lin, Z., Li, H., Li, X., Li, J., Wang, Y., Zhang, X., Zhu, Z., Zhai, W., Wang, X., Xie, D., Sun, C., 2007. TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant Journal 52, 891e898. Yu, J., Wang, J., Lin, W., Li, S., Li, H., Zhou, J., Ni, P., Dong, W., Hu, S., Zeng, C., Zhang, J., Zhang, Y., Li, R., Xu, Z., Li, S., Li, X., Zheng, H., Cong, L., Lin, L., Yin, J., Geng, J., Li, G., Shi, J., Liu, J., Lv, H., Li, J., Wang, J., Deng, Y., Ran, L., Shi, X., Wang, X., Wu, Q., Li, C., Ren, X., Wang, J., Wang, X., Li, D., Liu, D., Zhang, X., Ji, Z., Zhao, W., Sun, Y., Zhang, Z., Bao, J., Han, Y., Dong, L., Ji, J., Chen, P., Wu, S., Liu, J., Xiao, Y., Bu, D., Tan, J., Yang, L., Ye, C., Zhang, J., Xu, J., Zhou, Y., Yu, Y., Zhang, B., Zhuang, S., Wei, H., Liu, B., Lei, M., Yu, H., Li, Y., Xu, H., Wei, S., He, X., Fang, L., Zhang, Z., Zhang, Y., Huang, X., Su, Z., Tong, W., Li, J., Tong, Z., Li, S., Ye, J., Wang, L., Fang, L., Lei, T., Chen, C., Chen, H., Xu, Z., Li, H., Huang, H., Zhang, F., Xu, H., Li, N., Zhao, C., Li, S., Dong, L., Huang, Y., Li, L., Xi, Y., Qi, Q., Li, W., Zhang, B., Hu, W., et al., 2005. The Genomes of Oryza sativa: a history of duplications. PLoS Biology 3, e38. Zhang, Q., Maroof, M.A., Lu, T.Y., Shen, B.Z., 1992. Genetic diversity and differentiation of indica and japonica rice detected by RFLP analysis. Theoretical and Applied Genetics 83, 495e499. Zhang, W.X., Xiang, A.Q., Qiu, L.C., Xiao, D.F., 2007. Research on the husks ancient rice in the Shixia Ruins. Journal of South China Agricultural University 28, 20e23.

28

Rice

Zhang, W.X., Xiang, A.Q., Qiu, L.C., Yao, J.H., 2008. Studies on Bi-peaked Tubercles and Signs of hull of ancient rice from the Jiuwuhoushan site in the Reaches of the Xinghua river in Fengkai,Guangdong Province. Chinese Journal of Rice Science 22, 103e106. Zhang, Y., Zhang, S., Liu, H., Fu, B., Li, L., Xie, M., Song, Y., Li, X., Cai, J., Wan, W., Kui, L., Huang, H., Lyu, J., Dong, Y., Wang, W., Huang, L., Zhang, J., Yang, Q., Shan, Q., Li, Q., Huang, W., Tao, D., Wang, M., Chen, M., Yu, Y., Wing, R.A., Wang, W., Hu, F., 2015. Genome and comparative transcriptomics of African wild rice Oryza longistaminata provide insights into molecular mechanism of Rhizomatousness and self-Incompatibility. Molecular Plant 8, 1683e1686. Zhang, L.B., Zhu, Q., Wu, Z.Q., ROSS-Ibarra, J., Gaut, B.S., Ge, S., Sang, T., 2009. Selection on grain shattering genes and rates of rice domestication. New Phytologist 184, 708e720. Zhang, Q.J., Zhu, T., Xia, E.H., Shi, C., Liu, Y.L., Zhang, Y., Liu, Y., Jiang, W.K., Zhao, Y.J., Mao, S.Y., Zhang, L.P., Huang, H., Jiao, J.Y., Xu, P.Z., Yao, Q.Y., Zeng, F.C., Yang, L.L., Gao, J., Tao, D.Y., Wang, Y.J., Bennetzen, J.L., Gao, L.Z., 2014. Rapid diversification of five Oryza AA genomes associated with rice adaptation. Proceedings of the National Academy of Sciences of the United States of America 111, E4954eE4962. Zhao, Z., 1998. The Middle Yangtze region in China is one place where rice was domesticated: phytolith evidence from the Diaotonghuan Cave, Northern Jiangxi Antiquity 72, 885e897. Zhao, Z., 2010. New data and new issues for the study of origin of rice agriculture in China. Archaeological & Anthropological Sciences 2, 99e105. Zhao, K., Tung, C.W., Eizenga, G.C., Wright, M.H., Ali, M.L., Price, A.H., Norton, G.J., Islam, M.R., Reynolds, A., Mezey, J., Mcclung, A.M., Bustamante, C.D., Mccouch, S.R., 2011. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Communications 2, 467. Zhao, K., Wright, M., Kimball, J., Eizenga, G., Mcclung, A., Kovach, M., Tyagi, W., Ali, M.L., Tung, C.W., Reynolds, A., Bustamante, C.D., Mccouch, S.R., 2010. Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS One 5, e10780. Zheng, X.-M., Ge, S., 2010. Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara). Molecular Ecology 19, 2439e2454. Zhou, H.F., Zheng, X.M., Wei, R.X., Second, G., Vaughan, D.A., Ge, S., 2008. Contrasting population genetic structure and gene flow between Oryza rufipogon and Oryza nivara. Theoretical and Applied Genetics 117, 1181e1189. Zhu, Q., Ge, S., 2005. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytologist 167, 249e265. Zhu, B.F., Si, L., Wang, Z., Zhou, Y., Zhu, J., Shangguan, Y., Lu, D., Fan, D., Li, C., Lin, H., Qian, Q., Sang, T., Zhou, B., Minobe, Y., Han, B., 2011. Genetic control of a transition from black to straw-white seed hull in rice domestication. Plant Physiology 155, 1301e1311. Zhu, Z., Tan, L., Fu, Y., Liu, F., Cai, H., Xie, D., Wu, F., Wu, J., Matsumoto, T., Sun, C., 2013. Genetic control of inflorescence architecture during rice domestication. Nature Communications 4, 2200. Zhu, T., Xu, P.Z., Liu, J.P., Peng, S., Mo, X.C., Gao, L.Z., 2014. Phylogenetic relationships and genome divergence among the AA- genome species of the genus Oryza as revealed by 53 nuclear genes and 16 intergenic regions. Molecular Phylogenetics and Evolution 70, 348e361.

Origin, taxonomy, and phylogenetics of rice

29

Zhu, Q., Zheng, X., Luo, J., Gaut, B.S., Ge, S., 2007. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Molecular Biology and Evolution 24, 875e888. Zong, Y., Chen, Z., Innes, J.B., Chen, C., Wang, Z., Wang, H., 2007. Fire and flood management of coastal swamp enabled first rice paddy cultivation in east China. Nature 449, 459e462.

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Gross structure and composition of the rice grain

2

~o 2, 3,4 Bienvenido O. Juliano 1 , Arvin Paul P. Tuan 1 Philippine Rice Research Institute Los Ba~nos, Laguna, Philippines; 2Institute of Human Nutrition and Food, College of Human Ecology, University of the Philippines Los Ba~nos, Laguna, Philippines; 3Department of Chemistry, College of Humanities and Sciences, De La Salle Health Sciences Institute, Dasmari~nas, Philippines; 4Former Supervising Science Research Specialist, Philippine Rice Research Institute Los Ba~nos, Laguna, Philippines

Knowledge of the grain structure is important in understanding the physical and chemical properties of the rice grain, which is consumed mainly as boiled, whole milled rice. The various tissues differ drastically in structure, composition, and function; and the cells show compartmentalization of nutrients. The structure and gross composition of the rice grain have been reviewed by Bechtel and Pomeranz (1980), Juliano and Bechtel (1985), Champagne et al. (2004), and Juliano (2007).

1. Structure of the rice grain 1.1

Hull

The mature rice grain is harvested as a covered grain (rough rice or paddy), in which the caryopsis (brown rice) is enclosed by a tough siliceous hull (husk) (Juliano and Aldama, 1937; Juliano, 2007) (Fig. 2.1). The caryopsis is enveloped by the hull, composed of two “modified” leaves (lemmae): the palea (dorsal) and the larger lemma (ventral). The palea and lemma are held together by two hook-like structures. The shape of the mature caryopsis and its ridges corresponds to the shapes of the lemma and palea. The outer surface of the hull possesses trichomes that fit between longitudinal rows of endosperm cells. Some varieties have an awn attached to the tip of the lemma. The cells of the hull are highly lignified and brittle. Mean hull weight is about 20% of the rough rice weight, with values ranging from 16% to 28%. The rice hull provides protection to the caryopsis. The tightness of the hull, or the ability of the lemma and palea to hook together without gaps, has been related to the grain’s resistance to insect infestation during storage. The hull also protects the grain from fungi infestation, as the dehulled grain can readily be colonized by Aspergillus spp. Both lemma and palea consist of four structural layers: (1) an outer epidermis of highly silicified cells, the outer surface of which is sinuous and coated with a thick cuticle, among which trichomes are found; (2) sclerenchyma or hypoderm fibers two or three cell layers thick, possessing lignified cell walls; (3) crushed, spongy Rice. https://doi.org/10.1016/B978-0-12-811508-4.00002-2 Copyright © 2019 AACCI. Published by Elsevier Inc. in cooperation with AACC International. All rights reserved.

32

Rice

Awn Lemma Palea

Ventral Pericarp Seed coat Nucellus Aleurone layer

Hull

Dorsal

Inner endosperm

Starchy endosperm

Subaleurpone layer Embryo

Scutellum Epiblast Plumule Radicle

Rachilla

Sterile lemmae

Figure 2.1 Longitudinal section of indica rice grain. Redrawn by A.V R. Albino based on Juliano, J.B., Aldama, M.J., 1937. Morphology of Oryza sativa Linnaeus. Philippine Agriculturist 26, 1e134, Juliano, B.O., 2007. Structure and gross composition of the rice grain. In: Juliano, B.O. (Ed.), Rice Chemistry and Quality. Philippine Rice Research Institute, Mu~noz, Nueva Ecija, Philippines, pp 21e45.

parenchyma cells, some elongated with a rather wavy outline, and some short or quadrilateral; and (4) an inner epidermis of generally isodiametric cells (Juliano and Aldama, 1937). The lemma has five distinct but poorly developed vascular bundles, whereas the palea has three.

1.2

Pericarp, seed coat, and nucellus

The caryopsis itself is a single-seeded fruit, wherein the pericarp is fused to the seed (composed of seed coat, nucellus, endosperm and embryo). Inside the hull and covering the endosperm and embryo of the mature rice grain are three distinct layers of crushed cells that make up the caryopsis coat: the pericarp, seed coat (tegmen), and nucellus (Fig. 2.1). The pericarp is the mature, ripened ovary wall, which undergoes extensive degeneration during caryopsis development (Bechtel and Pomeranz, 1980). It consists of several layers of crushed cells that are about 10 mm thick, and it has a single vascular bundle on the dorsal side. The outer surface of the pericarp has an undulating appearance and a thin cuticle (Bechtel and Pomeranz, 1977).

Gross structure and composition of the rice grain

33

Next to the pericarp is a single layer of crushed cells, the seed coat or tegmen (Fig. 2.1). The seed coat has a thick cuticle (0.5 mm) located on the inner side of the crushed cells (Bechtel and Pomeranz, 1977). It corresponds to the inner layer of the inner integument (Juliano and Aldama, 1937). Pigments in colored rices are usually in the pericarp or the seed coat, which explains varietal differences in pigment retention on milling. Abutting the seed coat cuticle is another thick cuticle (0.8 mm), that of the crushed nucellar cells (Fig. 2.1). The nucellus in mature rice is about 2.5 mm thick (including the cuticle). The bond between the seed coat and nucellar cuticle is weak, which results in their separation during tissue handling and preparation (Bechtel and Pomeranz, 1977).

1.3

Aleurone layer

The aleurone layer, the outermost layer of the endosperm (triploid tissue), differs in both morphology and function from the starchy endosperm. It may be 1e7 cells thick and is thicker on the dorsal (back) than along the lateral (side) and ventral (front, embryo side) surfaces. Varieties differ in the thickness of the aleurone layer; coarser or bolder, short-grain rices tend to have more cell layers than do slender, long-grain rices (Hoshikawa, 1967c). The aleurone layer completely surrounds the rice grain and the outer side of the embryo. It is tightly bound to the underlying cells of the starchy endosperm and to most of the embryo. Two types of aleurone cells are reported (Bechtel and Pomeranz, 1977; Zheng et al., 2017). Those of the first type, around the starchy endosperm, are cuboidal and are densely packed cytoplasm. Here, two storage structures are prominent: aleurone grains (protein bodies [PBs] or aleurins) and lipid bodies (spherosomes) (Fig. 2.2). Aleurone grains are membrane-bound and contain globoids, which are 1e3 mm phytate storage bodies (Tanaka et al., 1973). Globoids prepared in 1.25e1.35 g/mL density media are spherical particles about 2e3 mm in diameter. Lipid bodies are apparently not bound by a typical bilayer membrane, are homogeneous, and are able to fuse with one another following mechanical damage of the grain. However, Takano (1993) reported that rice bran spherosomes (1e3 mm) have a monomolecular phospholipid membrane and need prior phospholipase D action on the membrane phosphatidylcholine before lipase can react on the intact spherosomes. Surface proteins called oleosins maintain the integrity of seed oil bodies by negatively charged repulsion and steric hindrance (Chuang et al., 1996). Rice oleosins have isoelectric point of pH 6.2 and are present in 16 and 18 kDa isoforms. Rice oil bodies lose their integrity on trypsin treatment. Other organelles of the aleurone layer include the nucleus, mitochondria, endoplasmic reticulum, vesicles, and plastids. Plastids are bound by a double membrane and are unique in that they possess invaginations that form vesicles and tubules of cytoplasm within the plastid. The second type of aleurone cells that surround the embryo has been termed the modified aleurone layer. It differs substantially from the other aleurone cells in that the modified cell has less densely packed cytoplasm, is rectangular, has fewer and

34

Rice

Figure 2.2 TEM section of aleurone layer of Caloro rice, showing aleurone grains (Ag, protein bodies) with globoid inclusions (G), lipid droplets (L, spherosomes), nucleus (N), and cell wall (C). Reprinted with permission from Bechtel, D.B., Pomeranz, Y., 1977. Ultrastructure of the mature ungerminated rice (Oryza sativa) caroypsis. The caryopsis coat and aleurone cells. American Journal of Botany 64, 966e973, courtesy of the late D.B. Bechtel, 2003.

smaller lipid bodies, lacks aleurone grains, has numerous vesicles, and has filament bundles (Bechtel and Pomeranz, 1977; Zheng et al., 2017).

1.4

Embryo

The embryo (germ) is extremely small and located at the ventral side at the base of the grain. It is bounded on the side by a single aleurone layer and by the fibrous cellular remains of the pericarp, seed coat, and nucellus, i.e., the caryopsis coat (Bechtel and Pomeranz, 1977). The starchy endosperm borders the inner edge of the embryo. The two major parts of the embryo are the scutellum (cotyledon) and embryonic axis. The C-shaped embryonic axis is separated from the starchy endosperm by the scutellum proper. The scutellum contains globoid-rich particles resembling aleurone grains (Tanaka et al., 1977). Three appendages of the scutellum partly sheath the coleoptile; a ventral scale and two lateral scales protect the upper half of the axis. In longitudinal section, the outlines of the embryonic leaves (plumule) and the embryonic primary root (radicle) are seen joined together by a short stem (mesocotyl). The lower half of the embryonic axis is sheathed by the epiblast, an upper extension of the coleorhiza. The coleorhiza surrounds the radicle and is continuous with the scutellum proper (Bechtel and Pomeranz, 1978a). The radicle consists of the root

Gross structure and composition of the rice grain

35

cap, root apex, epidermis, and subepidermal region (hypodermis), cortex, endodermis, pericycle, and provascular tissue. The radicle is separated from the plumule by a small region of parenchyma cells and interconnecting tissues, the mesocotyl. The plumule is sheathed and protected by a cone-shaped coleoptile. Coleoptile cells are also rich in protein and lipid bodies (Buttrose and Soeffky, 1973). Ultrastructure studies on the rice embryo have suggested that, based on contained storage reserves, parenchyma cells belong to three classes: (1) cells having electrondense inclusions (globoids) in PBs and having numerous lipid bodies scattered throughout the cytoplasm, therefore probably storage cells; (2) cells having PBs, with or without electron-dense and peripheral lipid bodies, primarily epidermal; and (3) cells lacking PBs and having peripheral lipid bodies (Bechtel and Pomeranz, 1978a).

1.5

Endosperm

The starchy endosperm is divided into two regions: (1) The subaleurone layer, i.e., the two outermost cells located just beneath the aleurone layer; and (2) the central region consisting of the rest of the starchy endosperm. The starchy endosperm consists of thin-walled parenchyma cells, usually elongated radially on cross-sectional view, and filled with compound starch granules and some PBs (Fig. 2.2). The cells toward the flattened or lateral sides are polygonal and slightly elongated (length: width ratio [L/W] ¼ 0.7e1.4); or those that extend from the ventral to the dorsal side are greatly elongated in the dorsiventral direction (L/W ¼ 0.2e1.0) (Little and Dawson, 1960). Generally, the radiating dimensions of these cells are shorter in long-grain rices than in medium- or short-grain rices. A central core of small cells has an isodiametric shape and ranges in size from 45 mm  50 mm to 80 mm  105 mm, corresponding to a cell area of 2250e8400 mm2. Grain of cultivars may have 12e22 cells in the dorsal radius, 10e18 cells in the ventral radius, 10e17 cells in the lateral radius, and 103e256 cells in the longitudinal axis (Nagato and Kono, 1963; Hoshikawa, 1968). The cell contents are mainly large, polygonal compound starch granules (3e9 mm in diameter) surrounded by density stained proteinaceous material localized in small pockets of PBs (Del Rosario et al., 1968; Bechtel and Pomeranz, 1978b) (Fig. 2.3). The subaleurone layer has smaller starch granules but is richer in PBs and lipid bodies. Bechtel and Pomeranz (1978b) found three types of membrane-bound PBs in the subaleurone layer, but only one type in the central region of mature rice (Bechtel and Juliano, 1980) (Fig. 2.4). Large spherical PBs, common to both regions, measure 1e2 mm in diameter, display concentric rings and/or radial rays, have electron-dense centers, are susceptible to pepsin hydrolysis, and are only partly digested by alkaline protease (pronase). The small spherical PBs of the subaleurone region measure 0.5e0.75 mm in diameter, have concentric rings and/or radial rays, but are completely digested by pepsin and pronase. The third type of PB of the subaleurone region is crystalline; they display a crystal lattice, are rounded, are composed of small angular components, measure 2e3.5 mm in diameter, are removed completely by pepsin, and are somewhat resistant to pronase degradation under conditions that are optimal with regard to pH for

36

Rice

Figure 2.3 Light microscopy (at low [a] and high [b] magnifications) of subaleurone layer of high-protein BPI-76 grain stained with mercuric chloride-bromphenol blue, showing stained protein bodies (p. b.) and unstained compound starch granules (s. g.). Reprinted from Del Rosario, A.A.R., Briones, V.V.P., Vidal, A.A. J., Juliano, B.O.O., 1968. Composition and endosperm structure of developing and mature rice kernel. Cereal Chemistry 45, 225e235.

Large spherical

Crystalline

Compound starch granule

Protein bodies

Small spherical 1 µm

Figure 2.4 TEM section of the subaleurone layer of IR26 developing rice endosperm showing the three types of protein bodies: large and small spherical PB I and segmented crystalline PB II. Reillustrated by J.B. Labita based on Bechtel, D.B., Juliano, B.O., 1980. Formation of protein bodies in the starchy endosperm of rice (Oryza sativa L.). A re-investigation. Annals of Botany 45, 503e509.

Gross structure and composition of the rice grain

37

the two enzymes. The crystalline PB corresponds to the crystalline segmented PB in the developing rice grain (Harris and Juliano, 1977; Bechtel and Juliano, 1980) and to the homogeneous type of PB (PB II, rich in glutelin, alkali-soluble protein) of Tanaka et al. (1980). Using immunocytochemical procedures, Barber et al. (1998) reported that prolamin and glutelin may not be exclusively confined to PB I and PB II, respectively. In other cereal endosperms, PBs are mainly of the prolamin type. Chalky portions are present in the endosperm of some nonwaxy rices. When the chalky region extends to the center of the endosperm and the edge of the ventral side, this is called a white core. An opaque region at the middle of the ventral (embryo) side is called a white belly or abdominal white. A long white streak on the dorsal side is called a white back. The chalkiness has been shown to be due to loose packing of starch granules in the region (Del Rosario et al., 1968) (Fig. 2.5). Scanning electron microscopy (SEM) confirms that starch granules are loosely packed, somewhat spherical, and simple in chalky regions of nonwaxy endosperm. In “crumbly” rice, many of the granules are well rounded on one or more faces (Evers and Juliano, 1976). The soft regions contribute to grain breakage during milling. High temperature during ripening favored japonica rice grain chalkiness (Ishimaru et al., 2009). The effect of high ambient temperature on the structure and composition of the developing rice endosperm, particularly chalk, was recently reviewed (Sreenivasulu et al., 2015). Waxy rices have an opaque endosperm. Histochemical studies show that the starch granules are compound and closely arranged, except on the ventral side

Figure 2.5 Light microscopy (at low [a] and high [b] magnifications) of crosssections of the center of Taichung Native 1 white-core milled rice stained with fast green-iodine. Lightly stained area corresponds to the white core. Reprinted from Del Rosario, A.A.R., Briones, V.V.P., Vidal, A.A. J., Juliano, B.O.O., 1968. Composition and endosperm structure of developing and mature rice kernel. Cereal Chemistry 45, 225e235.

38

Rice

(Del Rosario et al., 1968; Evers and Juliano, 1976; Zheng et al., 2017). SEM shows that waxy rice starch has micropores on the inside surface of the single starch granules (granola) and hollows on the outer surface of compound granules; these are absent in the endosperm of nonwaxy rice (Watabe and Okamoto, 1960). A small cavity has been observed at the center of each granulum in the compound waxy starch granule (Utsunomiya et al., 1975). The weight distribution of the various parts of the rice caryopsis is 1%e2% pericarp, 4%e6% aleurone plus seed coat, 2%e3% embryo, and 89%e94% starchy endosperm. A rice sample had 6.5% pericarp, seed coat, nucellus, and aleurone; 2.0% scutellum; 1.0% embryo; and 90.5% endosperm. The caryopsis of two shortgrain rices had 3.3% and 3.8% germ, 6.6% and 10.2% caryopsis coat plus aleurone layer, and 90.0% and 85.5% starchy endosperm, respectively. The weight distribution in the embryo fraction as a percentage of brown rice was 0.26% epiblast, 0.18% coleorhiza, 0.34% plumule, 0.18% radicle, and 1.2%e1.4% scutellum.

1.6

Milling fractions

Dehulling separates the hull (husk) from the brown rice or caryopsis. The ability of the palea and lemma to hook together without gaps differs among rices. Although a tight hull may provide storage protection to the grain, it may make such rices more difficult to dehull. Abrasive milling removes the outer maternal tissues, producing milled or polished or white rice, and the by-products (coproducts) rice bran and polish. The bran contains more of the pericarp, seed coat, nucellus, aleurone layer, and germ than the polish, which contains relatively more starchy endosperm. The bran is darker than the polish. Usually 10% by weight of brown rice is removed during milling. Bran and polish consist of fragments derived from the pericarp, seed coat, and nucellus, together with the greater portion of the aleurone layer, part of the subaleurone layer of the starchy endosperm, and the germ. They may be adulterated by hull fragments. Bran removal amounts to 5%e9% of the rough rice milled; commonly, the amounts are in the upper range (8%e9%), with the lowest values occurring in countries where the degree of milling is regulated. In addition, polish or white bran amounts to 2%e3% of the rough rice. Assuming 20% hull and 80% brown rice in rough rice, these values correspond to 6%e11% bran and 2.5%e3.8% polish in brown rice. Rice milling rates, representing the weight recovery of milled rice from rough rice, range from 0.60 to 0.73 in various rice-producing countries. Milled rice is slightly smaller in size than brown rice. Its outer surface is smooth, nonglistening, and waxy white. Each of the flat surfaces has two inconspicuous parallel ridges. The contents of some of the surface endosperm cells are exposed as a result of removal of the cell walls. Part of the scutellum adheres to the endosperm in milled rice. Shallow ridges on the brown rice surface are preferable to deep ridges or convolutions, particularly for pigmented grains, because bran removal is then most effective at lower degrees of milling. At all stages of milling (1%e6% bran removal from brown rice), abrasion is more severe on the protruding ridges than in the grooves, on the ventral region than on the dorsal, and in the median portion than at the distal

Gross structure and composition of the rice grain

39

portions of the grain (Srinivas and Desikachar, 1974). At 6% bran removal, residual pericarp, tegmen, and aleurone are still present in the grooves and dorsal pit of milled rice. The density of milled rice ranges from 1.43 to 1.46 g/mL, and the bulk density from 0.78 to 0.85 g/mL.

2. Gross composition of grain parts and milling fractions Rice starch is discussed in Chapter 3, rice proteins in Chapter 4, rice lipids in Chapter 5, rice minerals in Chapter 6, rice vitamins in Chapter 7, and rice phenolics and other natural products in Chapter 8. Utilization of rice hull is discussed in Chapter 19. Hence, these items they are not covered in this chapter. Brown rice has the lowest protein content and total dietary fiber among cereal grains, and the highest content of starch and available carbohydrates (USDA, 2016) (Table 2.1). It has the highest energy content next to oat. Removal of the inedible hull reduces the fiber content of brown rice. Its low dietary fiber content caused the delay in having the United States Food and Drug Administration consider brown rice as a whole grain, which usually requires 10% content of dietary fiber in the grain. In brown rice, all nonstarch constituents are concentrated in the bran fraction, and the endosperm (milled rice) is richest in starch. Lipid bodies are concentrated in the embryo and the aleurone layer, and also in the subaleurone layer; hence, the energy level is highest in the bran, followed by brown rice, and then milled rice (Table 2.2) (Juliano and Bechtel, 1985; Champagne et al., 2004). Nutrient composition and genetic diversity in rice were reviewed by Kennedy and Burlingame (2003). Protein content is slightly higher in brown rice than in milled rice because of the higher protein level in the bran (Table 2.2). Crude fat, crude ash, crude fiber, and total dietary fiber are also higher in brown than milled rice, being concentrated in the bran fraction. Sugars, phytic acid, and phenolics are also higher in brown rice. Pigments are located in the pericarp. Black or purple rice has more phenolics (0.6% anthocyanins) than red rice (0.2% proanthocyanidins) but nonpigmented brown rice has 40 g matured in 16e21 DAF, and those with 1000-grain wt < 18 g matured in 11e12 DAF (IRRI, 1978). Medium-size-grain rices (1000-grain wt of 20e30 g), however, had grain-filling periods that varied widely from 11 to 21 DAF. The active grain-filling period would be about 4 d shorter, since the endosperm starch is first seen by 4 DAF only. Pericarp, seed coat, and nucellus. At fertilization, the rice caryopsis consists of a mature embryo sac surrounded by the nucellus, the inner integument, the outer integument, and the pericarp. Before anthesis, the pericarp has both an inner and an outer epidermis. The outer epidermal cells remain rectangular, but the inner ones become highly elongated and pressed by the integuments during caryopsis development. Pericarp cells enlarge rapidly as the fruit increases in size, and by 4 DAF, the pericarp cells are in a state of degeneration characterized by an electron-lucent and

Gross structure and composition of the rice grain

43

disorganized cytoplasm (Bechtel and Pomeranz, 1980). The degeneration of the pericarp continues, with cell elongation and loss of starch from the chloroplasts. The final fate of the pericarp is the collapse and crushing of the cell layers, such that it loses thickness as the seed enlarges. The pericarp reaches its mature state at about 21 DAF. The inner and outer integuments of rice consist initially of two layers of cells each at anthesis (Juliano and Aldama, 1937). The outer integument (testa) degenerates and is absent in the 5-day (d) grain. The inner integument (tegmen) elongates and undergoes extensive structural changes. The outer layer also degenerates, and the cuticle is secreted on the inner side of the inner integument. These structures of the tegmen form the seed coat of the mature rice grain. After fertilization, the inner layers of the nucellus undergo rapid degeneration (collapse) as the endosperm forms a thin layer around the embryo sac vacuole. Ultimately, the nucellar epidermal cells also degenerate and are crushed between the aleurone layer of the endosperm and the inner seed coat. Their fusiform hexagonal shape and ribs of wall-thickening are structural adaptations to resist the compressional forces during the latter stage of grain filling (Ellis and Chaffey, 1987). Embryo. The embryo consists of 2e13 cells during the first 24 h after the pollination. Differentiation of the coleoptile, coleorhiza, and scutellum begins on the third day. The plumule and the enclosing coleoptile are present in the 5-d grain. The vascular system of the scutellum becomes evident in the 6-d grain. Differentiation of the embryo is complete by at least 13 DAF and not later than 20 DAF. The embryo gains the capacity to germinate at about 6e7 DAF (Navasero et al., 1975). At 16 DAF, the embryo cells are filled with lipid bodies and contain prominent vacuoles that have accumulated substantial amounts of protein deposits (Krishnan and White, 1997). Antibodies raised against rice endosperm a-globulin and against glutelin cross-react with minor embryo proteins, but the most abundant storage proteins (g-globulins) of rice embryos do not react with these antibodies. PBs of the embryo are morphologically distinct from endosperm PB I and PB II. Aleurone layer. The aleurone layer begins to differentiate at the dorsal area during 3 DAF and is fully developed at 7 DAF. Some simple starch granules may be observed in the aleurone cells of the immature grain, but they are absent in the mature grain. Although aleurone cells can differentiate as early as 4 DAF, secretion of reserves into aleurone cells does not begin until 8 DAF; although reported to be morphologically complete at 14 DAF (Hoshikawa, 1967b), aleurone grains do not mature until 21 DAF (Bechtel and Juliano, unpubl. data). Endosperm. The first division of the endosperm triple fusion occurs 3e3.5 h after pollination, and nuclear division follows at a rate faster than that of the differentiating embryo. The endosperm has 50e80 nuclei by 24 h after pollination. By 3 DAF, a multinucleated layer of the endosperm has formed at the periphery of the embryo sac. By 4 DAF, cell membrane formation has occurred, starting from the embryonic end and extending to the entire peripheral tissue, and layers of 2 cells have formed. The embryo sac becomes filled with endosperm cells by 5 DAF. Cell division is essentially complete by 9 DAF; the aggregate number of endosperm cells is about 180,000 in Japanese variety Yoneshero (Hoshikawa, 1967a). Total endosperm cells range from 83,100 to 231,800 in different varieties (Hoshikawa, 1968).

44

Rice

After fertilization, the rice caryopsis develops much faster along the longitudinal than the transverse axis. It attains full length at 4 DAF, maximum width at 14 DAF, and maximum thickness at 21 DAF (Del Rosario et al., 1968). Grain dry weight increases and reaches optimum value at 28-d sample. The actual period of dry matter accumulation is 14e18 DAF. The consistency of the endosperm goes through progressive changes termed milky, dough, yellow, and mature. Compound starch granules are first noticed in the endosperm cells at 4 DAF (Del Rosario et al., 1968; Harris and Juliano, 1977). The compound granule originates from a single amyloplast. The granules increase in size first and fastest at the center of the endosperm (Zheng et al., 2017). Granules in the exterior cell layers increase in size more slowly and are always smaller than those in the interior cells. The starch in the subaleurone layer, adjacent to the aleurone layer, is the most delayed, with the final size of the compound granule as small as 10 mm. The size of the granule increases most rapidly during the period 10e18 DAF. In the center of the endosperm, the compound granules reach maximum size (39 mm in major diameter) by 15 DAF, corresponding to 10 d of starch granule formation. Individual starch granules may increase in mean size from 3.3 to 6.3 mm during grain development (Briones et al., 1968). The starch granules increase in size and the spherical granules become polygonal as IR29 waxy grains attain maturity (Murugesan et al., 1992). Based on the progress of endosperm translucency, the completion of ripening is earlier in the central, apical, and ventral regions than in peripheral, basal, and dorsal portions, respectively. Waxy endosperm appears as translucent as that of nonwaxy endosperm above 18% moisture content (MC). However, some 26 waxy varieties differ in MC during grain desiccation, such that endosperm opacity is first observed, the Japanese “ryokka” phenomenon, and is classified into 15.5% MC (to 18%) (Watabe and Okamoto, 1960). High night ripening temperature increased the size of starch granules (Liu et al., 2017). Harris and Juliano (1977) reported the presence of PBs, particularly in the subaleurone layer, by 7 DAF, confirming earlier light microscopy studies (Del Rosario et al., 1968). Bechtel and Juliano (1980) first observed PB I by 4 Daf, Pb II by 6 DAF, and small spherical PBs by 14 DAF. Krishnan and White (1997) verified the presence of prolamin in PB I and of glutelin and globulin in PB II. Using immunodetection (Palmer et al., 2015), deposition of arabinoxylans and b-glucans coincided with the start of grain filling. Pectin was detected in both endosperm and maternal tissue. A rhamnogalacturonan I was detected in endosperm cell walls from 12 DAF. Galactan was detected at the earliest stages of the development of endosperm cell walls and arabinan occurred from 8 DAF until maturity. The genetic networks involved in the regulation of endosperm initiation, cell cycle regulation, aleurone layer specification, starch synthesis, storage protein accumulation and endosperm size, and correlation between embryo and endosperm were reviewed by Zhou et al. (2013). The proper size balance between embryo and endosperm is genetically regulated (Nagasawa et al., 2017). Translocation of nutrients. The pathway by which assimilates are transported to the developing caryopsis involves the single vascular bundle at the dorsal region of the pericarp through the long-distance pathway of the phloem (Oparka and Gates, 1981;

Gross structure and composition of the rice grain

45

Hoshikawa, 1984; Juliano and Bechtel, 1985). Assimilates then traverse a shortdistance pathway between the terminal sieve elements of the pericarp vascular bundles, moving to the pigment strand (nuclear projection) cells, which have numerous plasmodesmata, and on to the nucellus (Oparka and Gates, 1981). By 12 DAF, the nucellus extends about halfway around the circumference of the IR2153-338-3 endosperm. On the ventral half, the nucellus is partially crushed by the enlarging endosperm, and the cuticular layers lie in contact with the upper thickened wall of the aleurone layer. Assimilates probably move predominantly from the vascular bundle to the nucellus, which is rich in plasmodesmata. However, plasmodesmata are absent between the nucellus and the aleurone layer. Since transfer cells are absent in rice, the mitochondria that are regularly aligned in the aleurone and subaleurone layers of the caryopsis may function as part of a solute transport system (Oparka and Gates, 1981; Krishnan et al., 1998). In developing Koshihikari grain, the generation of the nucellar epidermis follows closely the completion of starch accumulation: 20 DAF at the ventral side, 25 DAF at the lateral sides, and 30 DAF at the dorsal side, in succession. Water distribution in the developing Koshihikari rice caryopsis by nuclear magnetic resonance microimaging supports the hypothesis that water flows from the pericarp vascular bundle onto the nucellus (Horigane et al., 2001). Thus, PBs are deposited at the periphery of the endosperm caused by the radial pattern of cell development and the proximity of peripheral endosperm cells to the nucellar epidermis (Ellis and Chaffey, 1987). Structural differences in aleurone cells and subaleurone cells in the dorsal and ventral parts of the rice caryopsis might be related to nutrient absorption and translocation (Zheng et al., 2017). The phloem sap collected by an insect laser technique from the uppermost internode of variety Kantou 1 week after anthesis contained 574 mM sucrose as the only sugar detected, and 125 mM total amino acids (Hayashi and Chino, 1990). Plant sap is rich in soluble silicic acid (Yoshihara et al., 1979).

3.2

Compositional changes

Endosperm starch is derived mainly from the photosynthesis after flowering, hence the high correlation between yield and solar radiation during panicle formation through grain filling. By contrast, grain protein comes mainly from translocation of accumulated plant nitrogen (N) at flowering (Perez et al., 1973). Although yield response was earlier reported for split N applied before flowering, recent studies indicate some increase in both yield and protein content from late N applied around flowering, because available soil N becomes deficient during the panicle formation stage (Perez et al., 1996). With tropical hybrids, application of N at flowering increases leaf N concentration and the photosynthetic rate of flag leaves, and significantly improves grain filling percentage and grain yield, but not in inbreds (Peng et al., 1998). Organic rice had lower protein content than ordinary rice treated with inorganic N fertilizer at Los Ba~nos (Tua~ no et al., 2011). Likewise, grain phytic acid content decreased with increase in nitrogen fertilizer application (Ning et al., 2009).

46

Rice

Starch properties. Free sugars (sucrose, glucose, maltooligosaccharides, fructose, and nonsucrosyl fructose) were maximum at about 9 DAF in IR28 and waxy IR29, coinciding with the maximum rate of starch accumulation (Singh and Juliano, 1977) (Fig. 2.6). The blue value of nonwaxy starch increased, reflecting an increase in AC, but waxy IR29 decreased in AC from 2.5% to 1.5% during maturation. AC increased from 9% at 5 DAF to 18.5% at 17 DAF in Taichung 65 nonwaxy japonica rice (Asaoka et al., 1985). Changes in the properties of starch granules were studied for both waxy IR29 (Murugesan et al., 1992) and nonwaxy (Hizukuri et al., 1995) rice. At 7, 11, 15, and 30 DAF, the iodine affinity, blue value, and maximum wavelength of iodinestained solutions of the starches and their isoamylolysates, the b-limits, and the 16 14

Weight (mg) IR28

Starch/grain

12 10 8 6 4

Free sugars/10 grains

2 0 2

1

IR1100–128–1 Soluble protein/ 5 grains (IR8)

Crude protein/grain

Free amino N/100 grains

0 6

Starch lipids/100 grains

IR42

4

Free lipids/10 grains

2 0 6

12

18 24 Days after flowering

30

Figure 2.6 Accumulation of starch, free sugars, crude and soluble protein, free amino N, and free and starch-bound (fat-by-hydrolysis) lipids during rice grain ripening. Adapted from Juliano, B.O., 2007. Structure and gross composition of the rice grain. In: Juliano, B.O. (Ed.), Rice Chemistry and Quality. Philippine Rice Research Institute, Mu~ noz, Nueva Ecija, Philippines, pp 21e45.

Gross structure and composition of the rice grain

47

intrinsic viscosity of the starches were largely constant during grain development of IR29. The data suggest that only complete molecules are packed into granules. With intermediate-AC IR64 and high-AC IR42 at 7, 11, and 30 DAF, the AC of the starch increased, the molecular weight and degree of branching of amylose increased slightly, and the mean chain length and b-amylolysis limit of amylopectin did not change (Hizukuri et al., 1995). Only IR64 starch showed an increase in iodine affinity, intrinsic viscosity, and amount of long-chain component of amylopectin, but starch properties of IR42 remained nearly constant. This again implies that the individual molecules complete their structure rapidly after initiation of synthesis. In an international germplasm collection, high night temperature during ripening decreased AC of lowand intermediate-AC rices, but increased AC of high-AC rices (Chen et al., 2008), in agreement with earlier studies (Resurreccion et al., 1977; Larkin and Park, 1999). Starch of chalky nonwaxy grains is reported to contain less AC (more amylopectin of shorter chain length) than translucent grains (Patindol and Wang, 2003). Proteins and lipids. Free amino acids increased in developing grain up to 8e12 DAF and then decreased (Cruz et al., 1970) (Fig. 2.6). Ribonucleic acid (RNA) content also increased and leveled off by 16 DAF. Protein content increased progressively up to 16 DAF or later (Palmiano et al., 1968). Glutelin and globulin (salt-soluble protein) began to accumulate by 5 DAF, and prolamin by 10 DAF (Yamagata et al., 1992). Glutelin reached a maximum at 11 DAF, but prolamin and globulin continued to increase up to 18 DAF. The molar ratio of glutelin to prolamin was 1.7 at 10 DAF, and the ratio steadily decreased to 1.2 at 25 DAF because of the increased synthesis and accumulation of prolamin, specifically during the latter stages of seed development (Li and Okita, 1993). High night temperature during ripening is reported to increase the ratio of PB II/PB I in Japanese rice (Ashida et al., 2013). RNA increased progressively to 8e12 DAF, then decreased and leveled off. Soluble protein was maximum at 10 DAF (Baun et al., 1970). Nonstarch lipids increased up to 12 DAF, but starch lipids (fat by hydrolysis) increased up to 20 DAF in developing IR42 grain (Choudhury and Juliano, 1980) (Fig. 2.6). Neutral lipids were accumulated up to 16 DAF, but phospholipids and glycolipids were already optimum by 10e12 DAF. In Japanese rice, decreasing ripening temperature decreased oleic acid in crude fat progressively, but increased linoleic acid (Taira et al., 1979). Lipids and oleosins were accumulated concomitantly in maturing rice seeds (Wu et al., 1998). Others. Highest level of proanthocyanidin in developing red rice is reported at the milk stage (Jiamyangyuen et al., 2017). Soluble and bound phenolic acids and antioxidant activity of rice hull decreased during grain development (Butsat et al., 2009). Ferulic acid was the major soluble phenolic acid, followed by p-coumaric acid. The major aroma compound in the rice grain is 2-acetyl-1-pyrroline (Buttery et al., 1982). Draining the rice fields in northern Thailand during grain development contributed to high 2-acetyl-1-pyrroline level in Khao Dawk Mali 105 grain (Yoshihashi et al., 2004). Increased soil salinity also increased 2-acetyl-1-pyrroline in three fragrant French rice varieties (Gay et al., 2010). Silicon fertilization also increased 2-acetyl-1pyrroline and proline contents of aromatic rice grain (Mo et al., 2017). About half of

48

Rice

the 2-acetyl-1-pyrroline is proposed to be in free form (volatile) and the rest in form bound to the starch and only released on cooking (Yoshihashi et al., 2005). Knowledge of the structure and distribution of nutrients in the rice grain is important in explaining rice grain quality properties.

Acknowledgments We acknowledge Anneth Vanessa R. Albino and Hanz Cez R. Albino for redrawing Fig. 2.1 and Jacob B. Labita for further editing Fig. 2.1 and Fig. 2.4. We thank Ralph Joseph A. Santos and Shera Joyce E. Marcelo who assisted in the typing of the manuscript.

References Asaoka, M., Okuno, K., Sugimoto, Y., Fuwa, H., 1985. Developmental changes in the structure of endosperm starch of rice (Oryza sativa L.). Agricultural & Biological Chemistry 49, 1973e1978. Ashida, K., Araki, E., Maruyama-Funatsuki, W., Fujimoto, H., Ikegami, M., 2013. Temperature during grain ripening affects the ratio of type II/type I protein body and starch pasting properties of rice (Oryza sativa L.). Journal of Cereal Science 57, 153e159. Barber, D.L., Lott, J.N.A., Yang, H., 1998. Immunocytochemical reactions to intact protein bodies in rice (Oyza sativa L.) using antibodies to purified fractions of some rice polypeptides. Journal of Cereal Science 27, 1e81. Baun, L.C., Palmiano, E.P., Perez, C.M., Juliano, B.O., 1970. Enzymes of starch metabolism in the developing rice grain. Plant Physiology 46, 429e434. Bechtel, D.B., Juliano, B.O., 1980. Formation of protein bodies in the starchy endosperm of rice (Oryza sativa L.). A re-investigation. Annals of Botany 45, 503e509. Bechtel, D.B., Pomeranz, Y., 1977. Ultrastructure of the mature ungerminated rice (Oryza sativa) caroypsis. The caryopsis coat and aleurone cells. American Journal of Botany 64, 966e973. Bechtel, D.B., Pomeranz, Y., 1978a. Ultrastructure of the mature ungerminated rice (Oryza sativa) caryopsis. The germ. American Journal of Botany 65, 78e85. Bechtel, D.B., Pomeranz, Y., 1978b. Ultrastructure of the mature ungerminated rice (Oryza sativa) caryopsis. The starchy endosperm. American Journal of Botany 65, 684e691. Bechtel, D.B., Pomeranz, Y., 1980. The rice kernel. In: Pomeranz, Y. (Ed.), Advances in Cereal Science and Technology 3. American Association in Cereal Chemists, Inc, St Paul, MN, pp. 73e113. Blakeney, A.B., Matheson, N.K., 1984. Some properties of the stem and pollen starches of rice. Starch/St€arke 36, 265e272. Briones, V.P., Magbanua, L.G., Juliano, B.O., 1968. Changes in physicochemical properties of starch of developing rice grain. Cereal Chemistry 45, 351e357. Buttery, R.G., Ling, L.C., Juliano, B.O., 1982. 2-Acetyl-1-pyrroline: an important aroma component of cooked rice. Chemistry and Industry (London) 958e959. Butsat, S., Weerapreeyakul, N., Siriamornpun, S., 2009. Changes in phenolic acids and antioxidant activity in Thai rice husks at five growth stages during grain development. Journal of Agricultural and Food Chemistry 57, 4566e4571.

Gross structure and composition of the rice grain

49

Buttrose, M.S., Soeffky, A., 1973. Ultrastructure of lipid deposits and other contents in freezeetched coleoptile cells of ungerminated rice grains. Australian Journal of Biological Sciences 26, 357e364. Champagne, E.T., Wood, D., Juliano, B.O., Bechtel, D.B., 2004. The rice grain and its gross composition. In: Champagne, E.T. (Ed.), Rice Chemistry and Technology, third ed. American Association of Cereal Chemists, Inc, St. Paul, MN. Chen, M.H., Bergman, C., Pinson, S., Fjellstrom, R., 2008. Waxy gene genotypes. Associations with apparent amylose content and the effect by the environment in an international rice germplasm collection. Journal of Cereal Science 47, 536e545. Choudhury, N.H., Juliano, B.O., 1980. Lipids in developing and mature rice grain. Phytochemistry 19, 1385e1389. Chuang, R.L.C., Chen, J.C.F., Chu, J., Tzen, J.T.C., 1996. Characterization of seed oil bodies and their surface oleosin isoforms from rice embryos. Journal of Biochemistry 120, 74e81. Cruz, L.J., Cagampang, G.B., Juliano, B.O., 1970. Biochemical factors affecting protein accumulation in the rice grain. Plant Physiology 46, 743e747. Del Rosario, A.R., Briones, V.P., Vidal, A.J., Juliano, B.O., 1968. Composition and endosperm structure of developing and mature rice kernel. Cereal Chemistry 45, 225e235. Ellis, J.R., Chaffey, N.J., 1987. Structural differentiation of the nucellular epidermis in the caryopsis of rice (Oryza sativa). Annals of Botany 60, 671e675. Evers, A.D., Juliano, B.O., 1976. Varietal differences in surface ultrastructure of endosperm cells and starch granules of rice. Starch/St€arke 28, 160e166. Finocchiaro, F., Ferrari, B., Gianinetti, A., 2010. A study of biodiversity of flavonoid content in the rice caryopsis evidencing simultaneous accumulation of anthocyanins and proanthocyanidins in a black-grained genotype. Journal of Cereal Science 51, 28e34. Gay, F., Maraval, I., Roques, S., Gunata, Z., Boulanger, R., Audebert, A., Mestres, C., 2010. Effect of salinity on yield and 2-acetyl-1-pyrroline content in the grains of three fragrant rice cultivars (Oryza sativa L.) in Camargue (France). Field Crops Research 117, 154e160. Harris, N., Juliano, B.O., 1977. Ultrastructure of of endosperm protein bodies in developing rice grains differing in protein content. Annals of Botany 41, 1e5. Hayashi, H., Chino, M., 1990. Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant and Cell Physiology 31, 247e251. Henry, R.J., 1985. A comparison of the non-starch carbohydrates in cereal grains. Journal of the Science of Food and Agriculture 36, 1243e1253. Hizukuri, S., Takeda, Y., Juliano, B.O., 1995. Structural changes of non-waxy starch during development of rice grains. In: Meuser, F., Manners, D.J., Seibel, W. (Eds.), Progress in Plant Polymeric Carbohydrate Research, Berlin 1992. Behr’s Verlag GmbH & Co, Hamburg, Germany, pp. 38e43. Horigane, A.K., Engelaar, W.M.H.G., Murayama, S., Yoshida, M., Okubo, A., Nagata, T., 2001. Visualisation of moisture distribution during development of rice caryopsis (Oryza sativa L.) by nuclear magnetic resonance imaging. Journal of Cereal Science 33, 105e114. Hoshikawa, K., 1967a. Studies on the development of endosperm in rice. I. Process of endosperm tissue formation. Nippon Sakumotsu Gakkai Kiji 36, 151e161. Hoshikawa, K., 1967b. Studies on the development of endosperm in rice. IV. Differentiation and development of the aleurone layer. Nippon Sakumotsu Gakkai Kiji 36, 216e220. Hoshikawa, K., 1967c. Studies on the development of endosperm in rice. V. The number of aleurone cell layers, its varietal difference and the influence of environmental factors. Nippon Sakumotsu Gakkai Kiji 36, 221e227.

50

Rice

Hoshikawa, K., 1968. Studies on the development of endosperm of rice. IX. Size and shape of endosperm and number of endosperm cells in foreign rice varieties. Nippon Sakumotsu Gakkai Kiji 37, 87e96. Hoshikawa, K., 1984. Development of endosperm tissue with special reference to the translocation of reserve substances in cereals. III. Translocation pathways in rice endosperm. Nippon Sakumotsu Gakkai Kiji 53, 153e162. Irakli, M.N., Samaridou, V.F., Katsantonies, D.N., Biliaderis, C.G., Papadoyannis, I.N., 2016. Phytochemical profiles and antioxidant capacity of pigmented and non-pigmented genotypes of rice (Oryza sativa L.). Cereal Research Communications 44, 98e110. IRRI (International Rice Research Institute), 1978. Annual Report for 1977. IRRI, Manila, Philippines, pp. 13e26, 73e81. Ishimaru, T., Horigane, A.K., Ida, M., Iwasawa, N., San-oh, Y.A., Nakajono, M., Nishizawa, N.K., Masumura, T., Kondo, M., Yoshida, M., 2009. Formation of grain chalkiness and changes in water distribution in developing rice caryopses grown under high-temperature stress. Journal of Cereal Science 50, 166e174. Jiamyangyuen, S., Nuengchamnong, N., Ngamdee, P., 2017. Bioactivity and chemical components of Thai rice at five stages of grain development. Journal of Cereal Science 74, 136e144. Juliano, B.O., 2007. Structure and gross composition of the rice grain. In: Juliano, B.O. (Ed.), Rice Chemistry and Quality. Philippine Rice Research Institute, Mu~ noz, Nueva Ecija, Philippines, pp. 21e45. Juliano, B.O., Bechtel, D.B., 1985. The rice grain and its gross composition. In: Juliano, B.O. (Ed.), Rice Chemistry and Technology, second ed. American Association of Cereal Chemists, Inc, St. Paul, MN, pp. 17e57. Juliano, J.B., Aldama, M.J., 1937. Morphology of Oryza sativa Linnaeus. Philippine Agriculturist 26, 1e134. Kennedy, G., Burlingame, B., 2003. Analysis of food composition data on rice from a plant resources perspective. Food Chemistry 80, 589e596. Krishnan, H.B., White, J.A., 1997. Protein body formation and immunocytochemical localization of globulins and glutelins in developing rice (Oryza sativa L.) embryos. Crop Science 37, 932e939. Krishnan, S., Samson, N.P., Ebenezer, G.A.I., Dayanandan, P., 1998. Structural and chemical changes in developing and mature rice grains. In: Chataigner, J. (Ed.), Rice Quality: A Pluridisciplinary Approach. Nottingham, UK, 1997. Cahiers Options Meditterraneennnes 24:CD-rom. International Center for Advanced Mediterranean Agronomy Studies, Montpellier, France. Larkin, P.D., Park, W.D., 1999. Transcript accumulation and utilization of alternate and non-consensus splice sites in rice granule-bound starch synthase are temperature-sensitive and controlled by a single-nucleotide-polymorphism. Plant Molecular Biology 40, 719e727. Li, X., Okita, T.W., 1993. Accumulation of prolamines and glutelins during rice seed development: a quantitative evaluation. Plant and Cell Physiology 34, 385e390. Little, R.R., Dawson, E.H., 1960. Histology and histochemistry of raw and cooked rice kernels. Food Research 25, 611e622. Liu, J., Zhao, Q., Zhou, L., Cao, Z., Shi, C., Cheng, F., 2017. Influence of environmental temperature during grain filling period on granule size distribution of rice starch and its gelatinization properties. Journal of Cereal Science 76, 42e55.

Gross structure and composition of the rice grain

51

Mo, Z., Lei, S., Ashraf, I., Khan, I., Li, Y., Pan, S., Duan, M., Tian, H., Tang, Z., 2017. Silicon fertilization modulates 2-acetyl-1-pyrroline content, yield formation and grain quality of aromatic rice. Journal of Cereal Science 75, 17e24. Murugesan, G., Hizukuri, S., Fukuda, M., Juliano, B.O., 1992. Structure and properties of waxy-rice (IR29) starch during development of the grain. Carbohydrate Research 223, 235e242. Nagasawa, N., Hibara, K., Heppard, E.P., Vander Velden, K.A., Luok, S., Beatty, M., Nagato, I., Sakai, H., 2017. GIANT EMBRYO encodes CYP78A13, required for proper size balance between embryo and endosperm in rice. The Plant Journal 75, 592e605. Nagato, K., Kono, Y., 1963. On the grain texture of rice. 1. Relation among hardness distribution, grain shape and structure of endosperm tissue of rice kernel. Nippon Sakumotsu Gakkai Kiji 32, 181e189. Nantiyakul, N., Furse, S., Fisk, I.D., Tucker, G., Gray, D.A., 2013. Isolation and characterization of oil bodies from Oryza sativa bran and studies of their physical properties. Journal of Cereal Science 57, 141e148. Navasero, E.P., Baun, L.C., Juliano, B.O., 1975. Grain dormancy, peroxidase activity and oxygen uptake in Oryza sativa. Phytochemistry 14, 1899e1902. Ning, H., Liu, Z., Wang, Q., Lin, Z., Chen, S., Li, G., Wang, S., Ding, Y., 2009. Effect of nitrogen fertilizer application on grain phytic acid and protein concentrations in japonica rice and its variation with genotypes. Journal of Cereal Science 50, 49e55. Oparka, K.J., Gates, P., 1981. Transport of assimilates in the developing caryopsis of rice (Oryza sativa L.). Ultrastructure of the pericarp vascular bundle and its connections with the aleurone layer. Planta 151, 561e573. Palmer, R., Cornuault, V., Marcus, S.F., Knox, J.P., Shewry, P.R., Tosi, P., 2015. Comparative in situ analysis of cell wall polysaccharide dynamics in developing rice and wheat grain. Planta 241, 669e685. Palmiano, E.P., Almazan, A.M., Juliano, B.O., 1968. Physicochemical properties of protein in developing and mature rice grain. Cereal Chemistry 45, 1e12. Patindol, J., Wang, Y.-J., 2003. Fine structure and physicochemical properties of starches from chalky and translucent rice kernels. Journal of Agricultural and Food Chemistry 51, 2777e2784. Peng, S., Yang, J., Garcia, F.V., Laza, R.C., Visperas, R.M., Saico, A.L., Chaveza, Q., Virmani, S.S., 1998. Physiology-based crop management for yield maximization of hybrid rice. In: Virmani, S.S., Siddiq, E.A., Muralidharan, K. (Eds.), Advances in Hybrid Rice Technology. International Rice Research Institute, Manila, Philippines. Perez, C.M., Cagampang, G.B., Esmama, B.V., Monserrate, R.U., Juliano, B.O., 1973. Protein metabolism in leaves and developing grains of rices differing in grain protein content. Plant Physiology 51, 537e542. Perez, C.M., Juliano, B.O., Liboon, S.P., Alcantara, J.M., Cassman, K.G., 1996. Effect of late nitrogen fertilizer application on head rice yield, protein content, and grain quality. Cereal Chemistry 73, 556e560. Resurreccion, A.P., Hara, T., Juliano, B.O., Yoshida, S., 1977. Effect of temperature during ripening on grain quality of rice. Soil Science & Plant Nutrition 23, 109e112. Resurreccion, A.P., Juliano, B.O., Tanaka, Y., 1979. Nutrient content and distribution in milling fractions of rice grain. Journal of the Science of Food and Agriculture 30, 475e481. Shao, Y., Xu, F., Sun, X., Bao, J.S., Beta, T., 2014. Identification and quantification of phenolic acids and anthocyanins as antioxidants in bran, embryo and endosperm of white, red and black rice kernels (Oryza sativa L.). Journal of Cereal Science 59, 211e218.

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Rice

Singh, R., Juliano, B.O., 1977. Free sugars in relation to starch accumulation in developing rice grain. Plant Physiology 59, 417e421. Sreenivasulu, N., Butardo Jr., V.M., Misra, G., Cuevas, R.P., Anacleto, R., Kavi Kishor, P.B., 2015. Designing climate-resilient rice with ideal grain quality suited for high-temperature stress. Journal of Experimental Botany 66, 1737e1748. Srinivas, T., Desikachar, H.S.R., 1974. Removal of bran and aleurone layer at different points on the surface of rice grain during progressive milling. Journal of Food Science & Technology 11, 83e84. Taira, H., Taira, H., Fujii, K., 1979. Influence of cropping season on lipid content and fatty acid composition of lowland non-glutinous brown rice. Nippon Sakumotsu Gakkai Kiji 48, 371e377. Takano, K., 1993. Mechanism of lipid hydrolysis in rice bran. Cereal Foods World 38, 695e698. Tanaka, K., Yoshida, T., Asada, K., Kasai, Z., 1973. Subcellular particles isolated from aleurone layer of rice seeds. Archives of Biochemistry and Biophysics 155, 136e143. Tanaka, K., Ogawa, M., Kasai, Z., 1977. The rice scutellum. II. A comparison of scutellar and aleurone electron-dense particles by transmission electron microscopy including energydispersive X-ray analysis. Cereal Chemistry 54, 684e689. Tanaka, K., Sugimoto, T., Ogawa, M., Kasai, Z., 1980. Isolation and characterization of two types of protein bodies in the rice endosperm. Agricultural & Biological Chemistry 44, 1633e1639. Tua~ no, A.P.P., Xu, Z., Castillo, M.B., Mamaril, C.P., Manaois, R.V., Romero, M.V., Juliano, B.O., 2011. Content of tocols, g-oryzanol, and total phenolics and grain quality of brown rice and milled rice applied with pesticides and organic and inorganic nitrogen fertilizer. Philippine Agricultural Scientist 94, 211e216. USDA (United States Department Of Agriculture), 2016. Agricultural Research Service nutrient Database Laboratory USDA. In: National Nutrient Database for Standard Reference Release 28 (May 2016). USDA ARS, Beltsville, MD. Utsunomiya, H., Yamagata, M., Doi, Y., 1975. Scanning electron microscopy of the endosperm of cereal crops. IV. Starch cell layer of imperfect grain of rice (nonglutinous) and glutinous rice. Yamaguti Daigaku Nogakubu Gakujutsu Hokoku 26, 19e44. Vidal, V., Pons, B., Brunnschweiller, J., Handshin, S., Rouau, X., Mestres, C., 2007. Cooking behavior of rice in relation to kernel physicochemical and structural properties. Journal of Agricultural and Food Chemistry 55, 336e346. Wada, T., Lott, J.N.A., 1997. Light and electron microscopic and energy dispersive Xeray microanalysis studies of globoids in protein bodies of embryo tissues and th aleurone layer of rice (Oryza sativa L.) grains. Canadian Journal of Botany 75, 1137e1147. Watabe, T., Okamoto, H., 1960. Experiments on the “ryokka“ phenomenon in glutinous rice plant (in Japanese). Science Report Kyoto Prefectural University of Agriculture 12, 1e5. Wu, L.S.H., Wang, L.-D., Chen, P.-W., Chen, L.-J., Tzen, J.T.C., 1998. Genomic cloning of 18 kDa oleosin and detection of triacylglycerols and oleosin isoforms in maturing rice and postgerminative seedlings. Journal of Biochemistry 123, 386e391. Yamagata, H., Nomura, T., Arai, S., Tanaka, K., 1992. Nucleotide sequence of a cDNA that encodes a rice prolamin. Bioscience, Biotechnology and Biochemistry 56, 537. Yoshida, S., 1981. Fundamentals of Rice Crop Science. International Rice Research Institute, Los Ba~nos, Philippines. Yoshihara, T., Sogawa, K., Pathak, M.D., Juliano, B.O., 1979. Soluble silicic acid as a sucking inhibitory substance in rice against the brown planthopper (Delphacidae, Homoptera). Entomologia Experimentalis et Applicata 26, 314e322.

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Yoshihashi, T., Nguyen, T.T.H., Kabaki, N., 2004. Area dependency of 2-acetyl-1-pyrroline content in an aromatic rice variety, Khao Dawk Mali 105. Japan Agricultural Research Quarterly 38, 105e109. Yoshihashi, T., Huong, N.T.T., Surojanametakul, V., Tungtrakul, P., Varanyanond, W., 2005. Effect of storage conditions on 2-acetyl-1-pyrroline content in aromatic rice variety, Khao Dawk Mali 105. Journal of Food Science 70, S34eS37. Zheng, Y., Zing, D., Wei, H., Xu, Wu, Y., Gu, Y., Wang, Z., 2017. Structure observation of rice endosperm tissues (in Chinese). Chinese Journal of Rice Science 31, 81e98. Zhou, S., Yin, L., Xue, H., 2013. Functional genomics based understanding of rice endosperm develolpment. Currrent Opinion in Plant Biology 16, 236e246.

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Rice starch Jinsong Bao College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

3

Starch is the most abundant composition in the rice grain. It constitutes 72%e82% of the dry weight of brown rice grain (Frei et al., 2003) and approximately 90% of milled rice grain (Fitzgerald, 2004). Starch is mainly composed of amylose and amylopectin, which are composed of the same basic glucan polymers but with different length and degree of branching. Amylose is essentially a linear molecule via a-1,4-glucosidic linkages with very few a-1,6-glucosidic linkages, while amylopectin contains linear chains of various lengths. Starch determines the eating and cooking properties of rice grains, or at least contributes to them through interactions with other components in the rice endosperm (proteins, lipids, water) or through interactions with other ingredients used to process the rice (Fitzgerald, 2004). The amylose content, the molecular structure of each fraction, and physicochemical properties all contribute to the performance of the rice grain. During the past decade, our understanding of starch biosynthesis pathway and structure of starch have greatly improved (Blennow et al., 2013; Fijita, 2014; Jeon et al., 2010; Nakamura, 2015, 2018; Pfister and Zeeman, 2016; Tetlow and Emes, 2017), making it a real possibility that starch structure can be manipulated to target starches for desired eating quality as a staple food, and to assist in identifying novel and potential applications in food and nonfood industries (Fijita, 2014; Fitzgerald, 2004; Nakamura, 2015, 2018). In this chapter, we update the information on rice starch structure, functional properties, and biosynthesis described in the previous versions (Juliano, 1985; Fitzgerald, 2004), but we mainly focus on the new advances made in the last decade.

1. Constituents of rice starch 1.1

Amylose and amylopectin

The major constituents of starch are amylose and amylopectin. Amylopectin is a highly branched molecule with the branch points being a-(1,6) bonds. Amylopectin is generally the major component of starch, constitutes 65%e85% of the matter in the starch granules, but in the waxy mutants, the amylopectin content can even reach 100% (Hanashiro, 2015). Amylose essentially consists of long-chained a-1,4 linked glucose molecules, but it also may contain a few a-1,6 branch points. The linear nature confers unique properties on amylose, among which is the ability to form complexes with iodine. The formation of the iodine-amylose complex provides the method to determine the apparent amylose content (AAC) in the starch sample (Perez and

Rice. https://doi.org/10.1016/B978-0-12-811508-4.00003-4 Copyright © 2019 AACCI. Published by Elsevier Inc. in cooperation with AACC International. All rights reserved.

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Juliano, 1978). The difference between AAC and true amylose content results from the amount of long branch chains of amylopectin, which can also develop color with iodine. AAC in waxy rice is lower than 2%, whereas common rice has an AAC ranging from very low (5%e12%), low (12%e20%), intermediate (20%e25%) to high (25%e33%) (Bao et al., 2006a; Wani et al., 2012). The AAC of amylose extender (ae) mutant can be as high as 35% (Yano et al., 1985). At present, there are no rice genotypes that approach the AAC of amylomaize (i.e., 70%) (Bao and Bergman, 2018). AAC also differs in rice subspecies; indica rice varies more greatly than japonica subspecies. Indica rice has all kinds of AAC classes, but the normal japonica rice generally has low to intermediate AAC. Both indica and japonica rice have waxy rice. Rice AAC also varies with the influences of environments, such as growth location, climatic and soil conditions, during grain development. The ambient temperature during grain filling is an important factor affecting the AAC of rice grain. It is well known that rice that flowers and matures at lower temperatures will be higher in AAC.

1.2

Minor constituents

The difference between rice starch and flour is that most of the native proteins and lipids in the flour have been removed. The protein content of milled rice in a germplasm collection reportedly ranged from 4.5% to 15.9% (Kennedy and Burlingame, 2003). Lipids exist in rice at much lower amounts. Therefore, isolation of starch from rice mainly involves techniques to remove proteins. The majority of rice protein is alkaline soluble, and so alkaline steeping method is commonly used in industry and research to produce rice starch with good recovery, low residual protein content and low damaged starch content (Hogan, 1967; Yang et al., 1984; Lumdubwong and Seib, 2000). The goal for the protein content of isolated rice starch is generally 0.5% or less (Bao and Bergman, 2018). Starch isolated by the alkaline steeping method yielded 73%e85% starch (dry basis), 0.07%e0.42% residual protein, and 0.07%e2.6% damaged starch (Yang et al., 1984). Lumdubwong and Seib (2000) applied a commercial alkaline protease to isolate rice starch from wet-milled rice flour, yielding 95% starch on a dry basis with 0.52% residual protein content and 2.1% damaged starch content. Wang and Wang (2004) reported that neutral protease treatment in combination with high-intensity ultrasound resulted in a starch yield of 79.8%e86.7% with 0.50%e0.96% residual protein content and 0.98%e1.87% damaged starch content. The protein (typically 0.1%e0.7%) in starch is mostly the granule-bound starch synthase 1 (GBSS1) that makes amylose, but also other amylopectin-synthesizing enzymes, such as other starch synthases (SSs), and starchbranching enzymes (BEs) (Pfister and Zeeman, 2016). Besides proteins, other minor constituents including lipids, phosphorus, and trace elements, are commonly found in the isolated rice starch (Champagne, 1996). Nonwaxy rice contains 0.3%e0.4% bound lipids, while waxy rice starch contains less of this fraction (0.03%) (Morrison et al., 1984; Morrison and Azudin, 1987). The formation of an amylose-lipid complex (sometimes referred to as starch-lipid or phospholipids) was reported by Morrison et al. (1993) in intact starch using a solid-state nuclear magnetic resonance technique. The composition of total starch lipids in

Rice starch

57

nonwaxy rice starch has an average of 32% free fatty acids and 68% lysophospholipids (LPLs) including lysophosphatidyl choline (LPC) and lysophosphatidylethanolamine (LPE) (Morrison et al., 1984). A single-step extraction with 75% n-propanol (8 mL/0.15 g) heated at 100
C for 2 h, combined with liquid chromatography mass spectrometry (LCMS) is effective in the analysis of starch lipids in milled rice (Liu et al., 2014a). Across nonwaxy rice genotypes, total LPC and total LPE ranged from 4727.1 to 7685.2 mg/g, and from 882.8 to 1809.5 mg/g, respectively (Tong et al., 2014a). Some low phytic acid mutants may alter the starch phospholipid profiles in rice endosperm (Tong et al., 2017). Phosphorus plays an extremely important role in starch functional properties, such as, paste clarity, viscosity consistency, and paste stability. Phosphorus in starch is mainly present in two forms: phospholipids and phosphate monoesters. In nonwaxy rice starch, phosphorus is mainly in the form of phospholipids, whereas in waxy rice, phosphorus is present as starch phosphate monoesters (Lim et al., 1994; Jane et al., 1996). Starch phosphate monoesters are products of starch phosphorylation, a general phenomenon existing naturally in the plant kingdom. The reaction of phosphorylation is catalyzed by the glucan-water dikinase (GWD), which is a necessary process during the degradation of the transitory starch in plants. Starch phosphate monoesters in native rice starches are primarily found in amylopectin, and only a trace is found in amylose. About 80%e90% phosphate monoester in rice starch is on the C6 of glucose units (Tabata et al., 1975; Jane et al., 1996). Overexpression of the potato GWD in rice (japonica, cv Zhonghua 11) resulted in the transgenic rice with the glucan-6-phosphate (G-6-P) and glucan-3-phosphate (G-3-P) contents, approximately 9 and 1 times higher, respectively, compared to control lines (Chen et al., 2017).

2. The structural levels of starch Starch structure is complex but can be divided into multiple structural levels (Gilbert et al., 2013; Tran et al., 2011; Li and Gilbert, 2018) (Fig. 3.1).

2.1

Level 1

Level 1 describes individual linear chains of starch molecules, where anhydroglucose units are linked together by a(1 / 4)-glycosidic bonds (Li and Gilbert, 2018). Rice amylopectin has characteristics of chain-length distribution profile, which varies in different rice genotypes. Hizukuri (1986) and Kobayashi et al. (1986) indicated that the structure of amylopectin can be generalized in terms of its types of chains (A, B, and C), which differ in length. The A-chains (unbranched) are linked to B-chains and do not carry any other chains; the B-chains (B1eB4) carry one or more A-chains and/or B-chains; and the C-chain has the reducing end of the molecule (Fig. 3.1). Amylopectin chain-length distributions (CLDs) after hydrolysis with isoamylose can be characterized by fluorophore-assisted carbohydrate electrophoresis (FACE) (Wu et al., 2014; Li and Gilbert, 2018), high-performance anion exchange

58

Rice

Amorphous B chain

Crystalline Amorphous

A chain

Crystalline

Individual branch Level 1

Amylopectin

Amylose

Level 2

Semi-crystalline lamellae Level 3

Crystalline 2 μm

Amorphous

Growth rings

Starch granules

Grains

Level 4

Level 5

Level 6

Figure 3.1 The structural levels of starch. Adapted from Tran, T.T.B., Shelat, K.J., Tang, D., Li, E., Gilbert, R.G., Hasjim, J., 2011. Milling of rice grains. the degradation on three structural levels of starch in rice flour can be independently controlled during grinding. Journal of Agricultural and Food Chemistry 59, 3964e3973; Li, H., Gilbert, R.G., 2018. Starch molecular structure: the basis for an improved understanding of cooked rice texture. Carbohydrate Polymers 195, 9e17, with modifications.

chromatography (HPAEC) (Wong and Jane, 1997; Li and Gilbert, 2018), capillary electrophoresis (Nakamura et al., 2002), mass spectrometry (MALDI-TOF; Grimm et al., 2003) and HPLC-GPC combined with multiangle laser-light scattering and refractive index detectors (MALLS-RI) (Chen and Bergman, 2007) (Fig. 3.2). The weight-based chain-length distribution of fa (degree of polymerization (DP) 6e12), fb1 (DP 13e24), fb2 (DP 25e36), and fb3 (DP > 36) by HPAEC were 18.07%e24.71%, 45.01%e55.67%, 12.72%e14.05%, and 10.80%e20.72%, respectively, among 14 rice genotypes (Kong et al., 2015a). The average chain length in rice amylopectin was DP 16.34e17.76 (Kong et al., 2015a). The molar-based chain-length distribution of rice amylopectin fa (DP 6e12), fb1 (DP 13e24), fb2 (DP 25e36), and fb3 (DP > 36) by FACE were 22.8%e24.4%, 50.1%e53.6%, 9.9%e11.4%, and 11.4%e15.5%, respectively, for some rice starch mutants (Zhou et al., 2018). The average chain length in these amylopectins was DP 21.0e22.4 (Zhou et al., 2018). Villareal et al. (1997) demonstrated that some high-amylose rice varieties have an additional fraction B4, with a weight percent of approximately 1%.

Rice starch

59

(A) 1600

1400

1200

nA

1000

800

600

400

200

0 0

13

26

39

52

65

87

91

104

117

130

143

156

169

61

66

182

195

Minutes

(B) 7

Peak area (%)

6 5 4 3 2 1 0 6

11

16

21

26

31

36

41

46

51

56

71

Degree of polymerization Figure 3.2 The chain-length distribution of rice amylopectin determined by high-performance anion exchange chromatography system equipped with an enzyme column reactor and pulsed amperometric detector (A) and the relative area percent of different chains (B).

The chain-length distributions of the debranched rice starches can also be characterized by size-exclusion chromatography (SEC). For debranched rice starches, three peaks were found in the SEC weight distribution (Fig. 3.3A) (Zhou et al., 2018), two peaks at DP w 16 and 40 are short and long amylopectin chains (Fig 3.3B), whereas

(A) 1.2 GM01

Wde (logX) (arb. units)

1

GM03 0.8

GM04 GM05

0.6

GLA4 0.4 0.2 0 1

(B)

10

100

1000

10000

X

1.2

Wde (logX) (arb. units)

1 GM01

0.8

GM03 AP1

GM04

0.6

GM05

0.4

GLA4 AP2

0.2 0 1

100

10 X

(C)

Wde (logX) (arb. units)

0.25

GM01

0.2

GM03

0.15

GM04 GM05

0.1

GLA4

AM 0.05

0 100

1000

X

10000

Figure 3.3 SEC of the debranched rice starches. (A) SEC weight chain-length distributions (CLDs), w(log X), of debranched rice starches, and (B) an enlargement of the amylopectin region as a function of DP X; and (C) an enlargement of the amylose region as a function of DP X. All CLDs were normalized as a function of the highest peak to yield the same area under the curve in order to avoid the effect of different sample concentrations. AM stands for the amylose peak, and AP1 and AP2 are the amylopectin peaks. GLA4 is an indica high AAC rice, and others are mutants induced from GLA4 (Zhou et al., 2018).

Rice starch

61

Table 3.1 The structural parameters obtained from SEC weight CLDs1 Sample2

XAM

hAM

XAP1

hAP1

XAP2

hAP2

GLA4

2546  161a

0.136  0.006c

17  0a

1

41  0a

0.625  0.004b

GM01

2446  19a

0.137  0.003c

17  0a

1

41  0a

0.622  0.003b

GM03

2067  94a

0.208  0.009a

15  0a

1

40  0a

0.464  0.001c

GM04

2146  49a

0.203  0.007a

16  0a

1

40  0a

0.452  0.010c

GM05

2502  59a

0.179  0.007b

16  0a

1

41  0a

0.646  0.001a

Mean  standard deviation was calculated from duplicate measurements. GLA4 is an indica high AAC rice, while others are mutants induced from GLA4 (Zhou et al., 2018). Values with different letters in the same column are significantly different at P 100) and short-chain amylopectin chains (average DP17) were negatively and positively correlated with paste breakdown, respectively. However, Vandeputte et al. (2003) using a more diverse set of rice starches, including 5 waxy and 10 nonwaxy starches, found no significant correlation between amylopectin chain-length distribution and PV, BD, SB, and CPV. As with many apparently confusing situations in cereal chemistry, a study is needed that evaluates the association between amylopectin and amylose characteristics (i.e., content and structure) and starch pasting properties across a set of samples that are representative of the world’s germplasm (Bao and Bergman, 2018). The pasting viscosity of rice starch is also affected by various environmental factors, including air temperature, atmospheric carbon dioxide, light, water, and soil

68

Rice

240

CPV

Temperature profile

90 PV

75 120 HPV

Temperature (ºC)

Viscosity (RVU)

180

60 60 PT 45 0 0

3

6 9 Time (min)

12

15

Figure 3.7 The rapid visco-analyzer (RVA) pasting properties of rice starch. CPV, cold paste viscosity; HPV, hot paste viscosity; PT, pasting temperature; PV, peak viscosity. The secondary parameters of breakdown (BD), setback (SB) and consistency (CS) viscosities can be calculated as PV-HPV, CPV-PV, and CPV-HPV, respectively.

nutrients. By comparing the starch physicochemical properties of rice grown in different locations, significant differences were found in the pasting viscosities (Bao et al., 2004a; Cameron et al., 2007; Xu et al., 2004). Bao et al. (2004a) reported that CPV, SB, BD, and peak time (Ptime) of viscosity parameters were mainly affected by genotype, whereas PV and HPV were mainly affected by environmental factors. Tong et al. (2014b) reported genotype was the main factor in determining PV, HPV, CPV, BD, SB, CS, and PT of viscosity parameters. AAC and several pasting viscosity parameters had significant correlation with LPLs (Tong et al., 2015). However, using partial correlation analysis to exclude the effect of AAC, CPV and individual LPLs were positively correlated, while BD, CS, and other individual LPLs were negatively correlated, suggesting that naturally occurring individual LPLs can contribute to the pasting properties, either independently or in combination with amylose.

3.2

Thermal (gelatinization) property

Gelatinization is the disruption of molecular orders within the starch granule manifested in irreversible changes in properties such as granular swelling, native crystallite melting, loss of birefringence, and starch solubilization, which can be determined with

Rice starch

69

a differential scanning calorimetry (DSC). DSC measures the gelatinization parameters of onset (To), peak (Tp), and conclusion (Tc) temperatures, and enthalpy (DH) of gelatinization (Fig. 3.8). The GT determines the time required for cooking. For milled rice grain, the GT can be measured indirectly by the degree of disintegration of milled rice soaked in a KOH solution (Little et al., 1958). This test is called the alkaline spreading value and is evaluated using a 1e7 scale proportionate to the amount of disintegration. Values of 2e3, 4e5, and 6e7 represent high, intermediate, and low GT (Simpson et al., 1965). AAC and GT combination for each rice accession is not in a random feature, but may be under genetic control (Fig. 3.9) (Bao et al., 2004b; Yang et al., 2014; Li et al., 2017b). For the low-AAC rice accessions (AAC 26

12.5e15

16e17

III

HA: Soft

>26