Translational Genomics for Crop Breeding,Volume II: Abiotic Stress, Yield and Quality

Translational Genomics forCrop Breeding,Volume II: Abiotic Stress,Yield and Quality

Edited by

Rajeev K. VarshneyRoberto Tuberosa

This edition first published 2013 C© 2013 by John Wiley & Sons, Inc.

Editorial offices: 2121 State Avenue, Ames, Iowa 50014-8300, USAThe Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK9600 Garsington Road, Oxford, OX4 2DQ, UK

For details of our global editorial offices, for customer services and for information about how to apply for permission toreuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell.

Authorization to photocopy items for internal or personal use, or the internal or personal use of specific clients, is grantedby Blackwell Publishing, provided that the base fee is paid directly to the Copyright Clearance Center, 222 RosewoodDrive, Danvers, MA 01923. For those organizations that have been granted a photocopy license by CCC, a separatesystem of payments has been arranged. The fee codes for users of the Transactional Reporting Service areISBN-13: 978-0-4709-6291-6/ 2013.

Designations used by companies to distinguish their products are often claimed as trademarks. All brand names andproduct names used in this book are trade names, service marks, trademarks or registered trademarks of their respectiveowners. The publisher is not associated with any product or vendor mentioned in this book.

Limit of Liability/Disclaimer of Warranty: While the publisher and author(s) have used their best efforts in preparing thisbook, they make no representations or warranties with respect to the accuracy or completeness of the contents of this bookand specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. It is sold on theunderstanding that the publisher is not engaged in rendering professional services and neither the publisher nor the authorshall be liable for damages arising herefrom. If professional advice or other expert assistance is required, the services of acompetent professional should be sought.

Library of Congress Cataloging-in-Publication Data

Translational genomics for crop breeding. Volume II : abiotic stress, yield and quality / edited by Rajeev K. Varshney andRoberto Tuberosa.

p. cm.Includes bibliographical references and index.ISBN 978-0-470-96291-6 (cloth : alk. paper) – ISBN 978-1-118-72837-6 (epub) – ISBN 978-1-118-72842-0 (emobi) –

ISBN 978-1-118-72848-2 (ebook) – ISBN 978-1-118-72862-8 (epdf) 1. Crops–Genetic engineering. 2. Plantbreeding. 3. Plant genome mapping. 4. Crop improvement. I. Varshney, R. K. (Rajeev K.), 1973– II. Tuberosa, R.(Roberto)

SB123.57.T74 2013631.5′3–dc23

2013029686

A catalogue record for this book is available from the British Library.

Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be availablein electronic books.

Cover images: Background C© HelenStocker; Cornfield C© jess311; Corn on the cob C© Diane DiederichCover design by Matt Kuhns

Set in 10/12.5pt Times by Aptara R© Inc., New Delhi, India

1 2013

Contents

Foreword viiPreface ix

Chapter 1 Translational Genomics for Crop Breeding: Abiotic Stress Tolerance, Yield,and Quality, An Introduction 1Rajeev K. Varshney and Roberto Tuberosa

Chapter 2 Applying Genomics Tools for Breeding Submergence Tolerance in Rice 9Endang M. Septiningsih, Bertrand C. Y. Collard, Sigrid Heuer,Julia Bailey-Serres, Abdelbagi M. Ismail, and David J. Mackill

Chapter 3 Genomics Applications to Salinity Tolerance Breeding in Rice 31J. Damien Platten, Michael J. Thomson, and Abdelbagi M. Ismail

Chapter 4 Marker-Assisted Introgression of Major QTLs for Grain Yield UnderDrought in Rice 47Arvind Kumar, Shalabh Dixit, and Amelia Henry

Chapter 5 Molecular Breeding for Phosphorus-efficient Rice 65Sigrid Heuer, J.H. Chin, R. Gamuyao, S.M. Haefele, and M. Wissuwa

Chapter 6 Aluminum Tolerance in Sorghum and Maize 83Jurandir V. Magalhaes, Lyza G. Maron, Miguel A. Pineros,Claudia T. Guimaraes, and Leon V. Kochian

Chapter 7 Freezing Tolerance in the Triticeae 99Galiba Gabor, Eric J. Stockinger, Enrico Francia, Justyna Milc, Gabor Kocsy,and Nicola Pecchioni

Chapter 8 Molecular Breeding for Stay-Green: Progress and Challenges in Sorghum 125Vincent Vadez, Santosh Deshpande, Jana Kholova, Punna Ramu,and C. Tom Hash

Chapter 9 Genetic Improvement of Grain Quality in Japonica Rice 143Kiyosumi Hori and Masahiro Yano

Chapter 10 Biofortified Maize – A Genetic Avenue for Nutritional Security 161Raman Babu, Natalia Palacios, and BM Prasanna

v

vi CONTENTS

Chapter 11 Marker-Assisted Backcrossing Selection for High O/L Ratio inCultivated Peanut 177Padmalatha Koilkonda, Chikara Kuwata, Masanobu Fukami, Kenta Shirasawa,Koh Aoki, Satoshi Tabata, Makoto Hasegawa, Hiroyuki Kiyoshima,Shigeru Suzuki, Shigemi Sasamoto, Atsushi Kurabayashi, Hisano Tsuruoka,Tsuyuko Wada, and Sachiko Isobe

Chapter 12 Genomics-Assisted Breeding for Tomato Fruit Quality in the Next-GenerationOmics Age 193Matthew P. Kinkade and Majid R. Foolad

Chapter 13 Improvement of Yield per se in Sugarcane 211M. Gouy, S. Nibouche, J.Y. Hoarau, and L. Costet

Appendix I – Contributors 239

Appendix II – Reviewers 243

Index 245

Color plate section can be found between pages 82 and 83.

Foreword

ICRISAT’s mission is to reduce poverty, hunger,malnutrition, and environmental degradation inthe dryland tropics. To accomplish this, we needto address the challenges presented by popu-lation explosion and climate change and theirimpacts on agriculture.

Today about 70% of the food-insecure pop-ulation lives in developing countries, mostly assmall-scale and subsistence farmers, and theirpopulation growth is expected to triple by 2100.They eke out a living and feed themselves fromfood crops cultivated in degraded lands in anunequivocally warmer climate system.

To achieve global food security, the devel-opment of crop varieties that produce highyields in harsh climatic conditions will be akey strategy. Although several desirable traitshave been developed in crop species throughintegrated breeding practices, self-sufficiency infood grains and legumes per se has remained anelusive dream for poor people in the developingworld.

The knowledge generated through advancesin genomics during the past two decades hasenormous potential in advancing the quest forabiotic stress–tolerant crops in the arid and semi-arid regions of the world. Moreover, DNA-basedmarker technologies have increased the preci-sion in marker-assisted selection (MAS), therebyreducing the time for improving traits of inter-est. Genome sequence information for impor-tant crops like rice, sorghum, maize, soybean,

chickpea, pigeonpea, tomato, and so on is nowavailable to enable greater understanding of traitsthrough comparative studies. It is important tofurther translate available genome informationin crop breeding so that farming communitieswill be benefitted sooner than later.

Translational Genomics for Crop Breeding:Abiotic Stress, Yield and Quality, edited by Dr.Rajeev K. Varshney, our own ICRISAT scien-tist, and Professor Roberto Tuberosa from theUniversity of Bologna, Italy, provides a concretestep in this direction. It is the second of two vol-umes where the eminent editors have carefullyselected authors who are experts in translationalgenomics in crop breeding for different traits indifferent crop species to write the various chap-ters of this publication. These chapters provideexamples of translational genomics for enhanc-ing tolerance to abiotic stresses and quality traitsin a number of crops. I believe that such a book isvery timely, informative, and of such quality thatit will fill the gap that exists presently betweengenome science and crop breeding.

Through this publication, we hope the elusivedream of poor people in the developing worldwill sooner become a reality.

Hyderabad William D. DarDate: June 10, 2013 Director General,

ICRISAT

vii

Preface

Ever since the discovery about four decades agoof the first molecular tools to investigate DNAstructure and function, the science of genomicshas contributed tremendously to investigate thegenetic and functional basis of plant phenotypesand how this variability affects crop produc-tivity. More recently, further advances in high-throughput genotyping technologies and genomesequencing have accelerated gene discovery andallele mining and the application of this knowl-edge to crop improvement. This aspect of trans-lational genomics has also been referred to asgenomics-assisted breeding (GAB). Due to thecontinuous and coordinated efforts of the globalscientific community involved in crop improve-ment, in a number of cases GAB has become anintegral part of crop-breeding programs.

Although substantial efforts have been madein the past century to mitigate the negativeeffects of abiotic stresses on crop productivityand improve the nutritional quality of crops, theprogress achieved through conventional breed-ing approaches has been limited and will beinsufficient to meet the ever-growing needs ofhumankind in the next decades. Within thisdaunting scenario, the advances in genomicsduring the past decades provide new avenuesfor enhancing our understanding of the geneticbasis of complex traits while accelerating cropimprovement. While a good number of successstories have been completed or are in progressfor resistance to biotic stresses, GAB has lim-ited examples of success stories for the improve-ment of resistance to abiotic stresses, quality, and

yield per se. In view of the fast-growing needfor developing new cultivars with enhanced tol-erance to abiotic stresses, better quality and/orhigher yield, this volume compiles reviews fromleading authorities in their own fields of exper-tise while describing the progress and presentingideas for future applications.

The editors thank all the authors of the differ-ent chapters (Appendix I) for the skillful sum-maries of the research work in their area of exper-tise and in some cases for sharing unpublishedresults in order to make the articles as up to dateas possible. We also appreciate their cooperationin meeting the deadlines and in revising theirmanuscripts. While editing this book, the editorsalso received strong support from several col-leagues (Appendix II), who willingly reviewedthe manuscripts. Their constructive and criticalsuggestions have been very useful for improvingthe quality of manuscripts.

We are also grateful to colleagues and stafffrom our respective laboratories, who havehelped us complete the editing of this volumein parallel with their demanding responsibili-ties. In particular, Manish Roorkiwal, B. Man-jula, Pawan Khera, and Mahendar Thudi helpedRKV with the editorial work. RKV is thank-ful to his wife Monika for her constant encour-agement and support, and to Prakhar (son) andPreksha (daughter) for their love and coopera-tion. Similarly, RT is thankful to his wife Kayfor her patience and editorial contributions. RKVwould also like to extend his sincerest thanks toDr. William D. Dar, Director General, ICRISAT,

ix

x PREFACE

for his guidance and support in completing thisbook. The cooperation and help received fromJustin Jeffryes, Anna Ehler, Kelvin Matthews,Erin Topp of Wiley Blackwell, and ShikhaSharma of Aptara Corp. during various stagesof development and completion of this book arealso gratefully acknowledged. RKV would alsolike to mention that the book was edited duringthe tenure of RKV as Director, Center of Excel-lence in Genomics (CEG), ICRISAT, Hyder-abad (India), Theme Leader – Comparative andApplied Genomics (CAG), Generation Chal-lenge Programme (GCP) and Adjunct positionsat the University of Western Australia, CropsResearch Institute of Guangdong Academy ofAgricultural Sciences (GAAS), China and BGI-Hongkong Research Institute, China.

We hope that this book will be helpful anduseful as a ready guide to students, youngresearchers, crop specialists, breeders, and pol-

icy makers for contributing to the developmentof new cultivars more resilient to abiotic stressesand with a better nutritional quality. Lastly, wewould appreciate if the readers can point outany errors and give comments/suggestions, asthis would be useful for the future, revised andupdated editions.

Hyderabad, India (Rajeev K. Varshney)June 09, 2013

Bologna, Italy (Roberto Tuberosa)June 09, 2013

Chapter 1

Translational Genomics for Crop Breeding:Abiotic Stress Tolerance, Yield, and Quality,An IntroductionRajeev K. Varshney and Roberto Tuberosa

Abstract

In the context of global climate change and population explosion, feeding the world’s population andaddressing the issues of malnutrition, especially in developing countries, are daunting tasks beforethe global scientific community. The yield gains achieved through conventional breeding are notvery promising, as several abiotic stresses such as drought, salinity, cold, flooding, submergence, andmineral toxicity have been leading to significant yield losses and reducing the quality of produce.In recent years, advances in genomics research and next generation sequencing (NGS) technologieshave largely facilitated understanding and identifying gene networks that are involved in controllinggenetic variation for agronomically valuable traits in elite breeding populations. The availability ofgenome-sequence information, transcriptomic resources, molecular markers, and genetic maps formajor crops such as rice, maize, and sorghum have enabled adoption of genomics-assisted breeding(GAB) approaches, including marker-assisted backcrossing (MABC) and marker-assisted recurrentselection (MARS). Nevertheless, during the last decade significant genomic resources were alsodeveloped in less-studied crops and efforts are underway in deploying these genomic tools in breeding.Furthermore, the new bioinformatics approaches and decision-support tools developed are able toenhance the precision in selection and complement the success of GAB approaches.

This volume essentially focuses on the research on abiotic stress tolerance and the quality enhance-ment of agricultural produce. Further, this introductory chapter summarizes the key success storiesand lessons learned in the field of genomics tools for crop improvement. In addition, this chapteralso emphasizes the essence of deploying genome-wide association mapping and nested associationmapping (NAM), as well as genomic selection (GS) approaches for crop improvements, in the contextof the availability of a plethora of low-cost and high-throughput sequencing technologies.

Translational Genomics for Crop Breeding, Volume II: Abiotic Stress, Yield and Quality.Edited by Rajeev K. Varshney and Roberto Tuberosa.C© 2013 John Wiley & Sons, Inc. Published 2013 by John Wiley & Sons, Inc.

1

2 TRANSLATIONAL GENOMICS FOR CROP BREEDING

Introduction

Despite continuous efforts to improve agricul-tural crops, changes in climate in the past twodecades have had a tremendous influence oncrop production and productivity. Further, cli-mate changes will have a significant impact onthe food security of humankind, especially indeveloping countries (Lake et al. 2012). It isexpected that global temperatures will increaseabout 3◦C by 2100 (Schneider et al. 2007), achange that would drastically curtail global cropproduction. Additionally, other critical abioticstresses such as drought, salinity, cold, flood-ing, submergence, mineral toxicity, and so forthhamper the growth, development, yield, and seedquality of crops. In fact, these abiotic stressesrepresent the main cause of crop failure world-wide, curtailing average yields of all major cropsby more than 50%. Furthermore, the quantitativeinheritance and low heritability of resistance tothese stresses, coupled with a strong Genotypex Environment x Management interaction of theyield response of crops to abiotic stresses, greatlylimit a more accurate dissection and manipula-tion of such response. Since the world popula-tion is increasing at an alarming rate, minimiz-ing these losses is also a major concern for allnations, particularly those with a strong increasein food demand. Besides increasing the produc-tion potential, the nutritional quality of the pro-duce needs to be improved to avoid the malnutri-tion that billions are already facing, particularlyin developing countries (Muller and Krawinkel2005; Bouis et al. 2010).

In the context of rapidly growing demandfor the staples of our sustenance, conventionalbreeding programs are struggling to achieve theyield gain required to adequately meet the bur-geoning demand for food and plant-derived prod-ucts (Tester and Langridge 2010). Accordingly,genomics-assisted breeding (GAB, Varshneyet al. 2005) approaches are increasingly beingadopted to improve the accuracy and effective-ness of selection while allowing for the dissec-

tion of the traits controlling the adaptive responseof crops to unfavorable conditions. While avail-ability of molecular markers and genetic mapsare the prerequisites for GAB, several orphancrops, neglected at the global level but impor-tant for food security at the regional level, untilrecently lacked the genomic resources and plat-forms to implement GAB. However, in recentyears significant progress has been achievedin the development of genomic resources in anumber of orphan crops that have thus becomegenomic resource-rich crops (Varshney et al.2009, 2010). As a result, GAB activities includ-ing trait mapping and marker-assisted selection(MAS) methods, such as marker-assisted back-crossing (MABC) and marker-assisted recur-rent selection (MARS), are increasingly beingadopted in breeding programs for major cropsand have begun to be deployed in less-studiedcrops as well (Kulwal et al. 2012; Varshney et al.2012).

Volume I of this book series presents reviewsof genomics applications in crop breeding forbiotic stress resistance, while this volume (Vol-ume II) focuses on research endeavors in abioticstress tolerance and the enhancement of the qual-ity of agricultural produce. Four chapters in Vol-ume II deal with ongoing research on toleranceto submergence, salinity, drought, and phospho-rus (P) deficiency in rice. Another chapter dis-cusses work on cloning and molecular breed-ing work for aluminum toxicity in sorghum.Research on freezing tolerance, an importanttrait in the Western world, in wheat and barleyis summarized in another chapter. One chapter isfocused on molecular breeding efforts for stay-green tolerance, an important drought tolerancetrait in sorghum. Four chapters in the volumeare devoted to quality improvement traits in rice,maize, peanut, and tomato. In the last chapter,authors discuss advances in sugarcane genomicsand its applications for enhancing yields andongoing efforts in genomic selection (GS). Somehighlights of these chapters have been summa-rized in this introductory chapter.

TRANSLATIONAL GENOMICS FOR CROP BREEDING 3

Enhancing Tolerance to AbioticStresses in Rice

Submergence stress affects more than 15 Mhain lowland rice-growing areas of South andSoutheast Asia. Chapter 2 provides insightsinto the ongoing efforts at the InternationalRice Research Institute (IRRI), Manila, Philip-pines, to improve submergence tolerance in rice.Following the identification of Sub1 (Submer-gence1) locus and three ethylene responsive fac-tors (ERFs) in rice, Septiningsih and colleaguesreport the development of eight Sub1 varieties bythe IRRI, six of which are already widely grownin several countries.

More than 444 Mha of global rice-growingarea is affected by soil salinization (FAO, 2010).Soil salinization is a major problem in coastalareas of the regions where rice-based farmingpredominates. Reportedly rice yields are reducedby up to 50% when grown under moderate(6 dS/m) salinity levels (Ren et al. 2005). Thelosses due to soil salinization can be overcomeby soil reclamation or by improving salinity tol-erance in the crops. Efforts toward understandingthe genetic basis of the trait for crop improve-ment has revealed that several genes are inde-pendently involved in salinity tolerance at differ-ent stages of crop cycles. In Chapter 3, Plattenand colleagues provide an overview of genomicsapplications in enhancing salt tolerance in rice.

Drought is the major limiting factor to cropproduction, and cereals especially experiencevarious kinds of drought stresses, depending onthe timing and intensity of the water stress rel-ative to the reproductive stage of the crop. Inthe case of rice, in Asia about 34 Mha of rain-fedlowland rice and 8 Mha of upland rice (Huke andHuke 1997) are frequently subjected to droughtstress. Progress in developing high-yielding,drought-tolerant rice cultivars by conventionalbreeding has been slow, largely because of dif-ficulties in precisely defining the target environ-ment, complex interactions of drought tolerancewith environments and management practices,and lack of appropriate screening methodology.

However, during the past decade the availabilityof large-scale genomic resources and genomesequences have enabled the adoption of variousGAB approaches in rice (see Collard et al. 2008).These efforts are summarized in Chapter 4 byKumar and colleagues.

Sixteen essential elements are required forrice during the crop cycle. The major nutrientssuch as nitrogen (N), phosphorus (P), and potas-sium (K) are largely supplied as chemical fer-tilizers. The excess application of P, owing toits insoluble nature, leads to deficiencies of cop-per (Cu), iron (Fe), manganese (Mn), and zinc(Zn). Additionally, erosion of P-enriched soilsenhances eutrophication in fresh water (Wolf1996). Most of the rain-fed rice grown in Asiaand Africa is cultivated on problematic soils,especially when P becomes unavailable to thecrop as it adheres to soil particles. Hence, in thiscontext, development of crops with enhancedefficiency of P utilization and production ofhigher biomass is essential. Chapter 5 by Heuerand colleagues essentially discusses the issuesrelated to P deficiency in rice production. Fur-ther, the authors also highlight the need for theadoption of molecular breeding approaches andsummarize the molecular breeding efforts forenhancing P utilization efficiency in rice.

Enhancing Tolerance to AbioticStresses in Wheat and Barley

Freezing/cold tolerance in crop plants is mostimportant in the context of global climatechange. Freezing tolerance is important in tem-perate cereals such as wheat (Triticum spp.), bar-ley (Hordeum vulgare), and rye (Secale cereale).Long exposures of winter wheat and barley vari-eties to non-freezing cold temperatures (Dhillonet al. 2010) will accelerate flowering time (ver-nalization) and improve freezing tolerance (coldacclimation). In the case of wheat, Kobayashiet al. (2005) reported that Vrn-Fr1 controlsboth frost tolerance and vernalization. Chap-ter 6, by Gabor and colleagues, reports on thedevelopmental plasticity of these Triticeae crops