The Genus Citrus This page intentionally left blank The Genus Citrus Edited by Manuel Talon Marco Caruso Fred G. Gmitter Jr. An imprint of Elsevier 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 © 2020 Elsevier Inc. 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 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: 978-0-12-812163-4 (print) ISBN: 978-0-12-812217-4 (online) For information on all Woodhead publications visit our website at https://www.elsevier.com/books-and-journals Publisher: Charlotte Cockle Acquisition Editor: Nancy Maragioglio Editorial Project Manager: Vincent Gabrielle Production Project Manager: Sojan P. Pazhayattil Cover Designer: Victoria Pearson Typeset by SPi Global, India Contents Contributors xiii 2.3.5 Early Pleistocene: Glacial maxima and the diversification 1 The citrus genome of mandarins 27 2.4 A new evolutionary framework for the Frederick G. Gmitter, Jr., Guohong Albert Wu, genus Citrus 27 Daniel S. Rokhsar, Manuel Talon Acknowledgments 28 1.1 Concept of genome 1 References 28 1.2 Citrus genomes 1 1.3 Genomes: Pure, admixed, and 3 Domestication and history domesticated 2 Xiuxin Deng, Xiaoming Yang, Masashi 1.3.1 Inference of pure and admixed Yamamoto, Manosh Kumar Biswas genome regions 2 1.3.2 Identification of the ancient 3.1 The taxonomy, cultivars, and genetic progenitor citrus species 4 origin of citrus 33 1.3.3 A whole-genome perspective of 3.1.1 The taxonomy and the true citrus citrus hybrids and admixtures 5 group 33 1.3.4 Comparative analyses of citrus 3.1.2 The genetic origin of some genomes: The example of hybrid citrus 36 evolution and domestication of 3.2 The cultivation history and distribution mandarins 5 of citrus 38 References 8 3.2.1 Ancient Chinese citrus 38 Further reading 8 3.2.2 Ancient citrus in Japan 41 3.2.3 Ancient citrus in India 44 2 The origin of citrus 3.2.4 The origin, spread, and introduction of citrus 46 Manuel Talon, Guohong Albert Wu, 3.2.5 The genetic diversity of Citrus 49 Frederick G. Gmitter, Jr., Daniel S. Rokhsar References 51 2.1 The mythological origin of citrus 9 2.2 The origin of citrus 9 4 Citrus taxonomy 2.2.1 The concept of citrus 9 Patrick Ollitrault, Franck Curk, Robert Krueger 2.2.2 Phylogeny of citrus pure species 10 2.2.3 Genealogy of cultivated citrus 11 4.1 The genus Citrus definition 57 2.2.4 Paleontology of citrus 13 4.1.1 The botanical treatment of the 2.2.5 Chronology of citrus speciation 15 genus Citrus 57 2.2.6 Biogeography of citrus 16 4.1.2 Phenotypical traits of the true Citrus 57 2.2.7 The center of origin of citrus 18 4.1.3 Reproductive biology, 2.3 Citrus radiation and evolution 21 cytogenetics and molecular data, 2.3.1 Citrus radiation 21 and the definition of the 2.3.2 Late Miocene: Global cooling genus Citrus 60 and the Southeast Asian radiation 22 4.2 The genus Citrus classifications; an 2.3.3 Dispersal routes of ancestral citrus 24 historical, biological, genetic, and 2.3.4 Early Pliocene: Wallacea phylogenomic perspective 62 orogeny and the dispersal of 4.2.1 The history of citrus botanical Australian limes 25 classifications 62 v vi Contents 4.2.2 1967–2017, from traditional 6 Citrus rootstocks taxonomy to phylogenomy: Kim D. Bowman, Johan Joubert 50 years to clarify the genetic organization of the genus Citrus 6.1 Introduction 105 and the origin of modern citrus 6.2 Reasons for a rootstock 105 varieties 64 6.3 Important rootstock attributes 106 4.2.3 The ancestral and admixture 6.4 Rootstock use by region 113 taxa 65 6.5 The major rootstocks 113 4.3 Phenotypic diversity structure strongly 6.6 Rootstock trends and future prospects 120 reflects evolutionary history 73 Acknowledgments 122 4.3.1 Reticulate evolution, apomixis, References 122 and the correlation between Further reading 127 the structures of genetic and phenotypic diversities in the 7 Traditional breeding Asian edible Citrus species 74 Marco Caruso, Malcolm W. Smith, Yann Froelicher, 4.3.2 Traits of the four Asian ancestral Giuseppe Russo, Frederick G. Gmitter, Jr. taxa of the edible Citrus 74 4.3.3 Traits of some modern citrus taxa 7.1 Introduction 129 resulting from admixture 76 7.2 Scion breeding 130 4.4 Conclusion 77 7.2.1 Somatic mutations and chimeras 130 References 77 7.2.2 Nucellar selections 132 7.2.3 Hybridization 134 5 Commercial scion varieties 7.2.4 Mutation breeding 138 7.3 Rootstock breeding 141 Graham H. Barry, Marco Caruso, 7.3.1 Objectives 141 Frederick G. Gmitter, Jr. 7.3.2 Conventional methods to 5.1 Pummelos/shaddocks generate new rootstocks 141 (Citrus maxima) 83 7.3.3 Propagation 141 5.1.1 Principal commercial pummelo 7.3.4 Phenotyping methods for varieties 83 diseases and abiotic stress 5.1.2 Pigmented pummelo resistance before field trials 142 varieties 84 7.3.5 Rootstock trials 143 5.1.3 Pummelo hybrids 85 7.4 Perspectives 143 5.2 Grapefruit (Citrus paradisi) 86 References 144 5.2.1 Principal commercial varieties 87 5.3 Lemons (Citrus limon) 89 8 Genomic breeding 5.3.1 Principal commercial varieties 89 Tokurou Shimizu 5.4 Limes (Citrus aurantiifolia and Citrus latifolia) 92 8.1 Introduction 149 5.5 Oranges (Citrus sinensis) 93 8.2 DNA markers 153 5.5.1 Sugar or acidless orange varieties 94 8.2.1 Types of DNA markers 153 5.5.2 Blood or pigmented orange 8.2.2 SSR and indel markers 153 varieties 95 8.2.3 SNP markers 154 5.5.3 Navel oranges 96 8.2.4 RFLP and CAPS markers 154 5.5.4 Common orange varieties 96 8.2.5 NGS-based high-throughput 5.6 Mandarins (Citrus reticulata) 97 genotyping 154 5.6.1 Principal commercial mandarin 8.3 Linkage mapping analysis toward MAS 155 varieties 98 8.3.1 Linkage-map construction using 5.6.2 Other mandarin hybrids of transferrable DNA markers 155 current or potential commercial 8.3.2 DNA-marker development for importance 102 monogenic traits 156 References 103 8.3.3 Polyembryony 156 Further reading 104 8.3.4 Fruit traits 156 Contents vii 8.3.5 Aroma 159 10.3.2 Secondary stem growth 204 8.3.6 Disease, stress resistance, and 10.3.3 Sprouting development 206 other traits 159 10.3.4 Factors affecting vegetative 8.4 MAS for complex traits 160 development 207 8.4.1 QTL analysis of complex traits 160 10.4 Leaf development 207 8.4.2 Linkage disequilibrium (LD) 10.4.1 Leaf abscission 209 analysis 160 10.5 Formation of the root system 211 8.4.3 Association mapping (AM) analysis 161 10.5.1 Development of the primary root 211 8.4.4 Genomic selection (GS) 161 10.5.2 Lateral root development 213 8.5 Future trends 163 10.5.3 Secondary root growth 213 References 163 10.5.4 Root distribution 214 10.5.5 Factors affecting root 9 Citrus biotechnology development 214 10.6 Trees of reduced size 215 Maria Antonietta Germanà, Pablo Aleza, 10.7 Control of vegetative development Jude W. Grosser, Manjul Dutt, Nian Wang, through the use of growth retardants 216 Jose Cuenca, Prabhjot Kaur References 216 9.1 Introduction 171 9.2 Micropropagation 171 11 Flowering and fruit set 9.3 Organogenesis and rooting 172 Manuel Agustí, Eduardo Primo-Millo 9.4 Gametic embryogenesis 174 9.5 Somaclonal variation 176 11.1 The process of flowering 219 9.6 Allotetraploids via somatic hybridization 176 11.2 Type of inflorescences 220 9.7 Somatic cybridization 178 11.3 Control of flowering 220 9.8 Molecular marker development for 11.3.1 Environmental control 220 Alternaria brown spot disease 178 11.3.2 Other factors affecting 9.9 Reducing juvenility via viral vectors 180 flowering 221 9.10 Genetic transformation of citrus 181 11.3.3 Control of flowering 224 9.11 Direct DNA incorporation into 11.4 Pollination and fertilization 224 citrus 181 11.5 Fruit set 225 9.11.1 Protoplast transformation 181 11.6 Parthenocarpy 226 9.11.2 Particle bombardment/biolistics 182 11.7 Endogenous regulation of fruit set 226 9.11.3 Agrobacterium-mediated 11.7.1 Influence of hormone levels 227 transformation of citrus 182 11.7.2 Competition for 9.12 CRISPR gene editing 183 photoassimilates 229 9.13 Concluding remarks 184 11.7.3 Interactions between References 184 hormones and photoassimilates 230 11.8 Factors affecting fruit set 231 10 Vegetative growth 11.8.1 Temperature 231 11.8.2 Irrigation 231 Eduardo Primo-Millo, Manuel Agustí 11.8.3 Nitrogen fertilization 231 10.1 Seed germination 193 11.8.4 Mineral deficiencies 232 10.1.1 Imbibition of water 193 11.8.5 Flowering intensity 232 10.1.2 Breathing 194 11.8.6 Position of the flower in 10.1.3 Protein synthesis 195 the tree 232 10.1.4 Mobilization of the reserves 11.9 Improvement of fruit set: Cultural contained in cotyledons 195 practices 233 10.1.5 Seedling development 199 11.9.1 The application of GA3 233 10.1.6 Polyembryony 201 11.9.2 Girdling or ringing 233 10.1.7 Juvenile characters 201 11.9.3 Treatment with GA3 10.2 Dormancy and vegetative activity 201 combined with girdling 234 10.3 Development of the canopy 202 11.9.4 Other practices that favor 10.3.1 Stem growth 202 fruit set 234 viii Contents 11.10 Fruit development 235 12.5 Color change during fruit 11.11 Factors affecting fruit development 236 development and ripening 255 11.11.1 Endogenous factors 236 12.5.1 Biochemical, molecular, and 11.11.2 Tree age 236 structural changes related to 11.11.3 Fruit position on the tree 236 chlorophylls and carotenoids 255 11.11.4 Foliar area 236 12.5.2 Environmental, nutritional, 11.11.5 Seed number 236 and hormonal cues affecting 11.11.6 Flowering intensity 236 chlorophylls and carotenoids 258 11.11.7 Competition among 12.5.3 General aspects of blood developing fruits 236 oranges during fruit 11.11.8 Environmental factors 237 development and ripening 260 11.11.9 Cultural practices 237 12.6 Preharvest drop impacts on and 11.12 Techniques to improve fruit size 238 determines, respectively, citrus 11.12.1 Pruning 238 fruit production and harvesting 11.12.2 Manual thinning 238 time 262 11.12.3 Chemical thinning 239 12.7 Transcriptome evolution during 11.12.4 Girdling or ringing 240 ripening: A next-generation view 263 11.13 Seed development 240 12.8 Future perspective: Basic knowledge References 241 and advanced techniques should Further reading 244 result in improved products 264 Author contribution 264 12 Fruit growth and development References 264 Francisco R. Tadeo, Javier Terol, María J. Rodrigo, 13 Citrus in changing environments Concetta Licciardello, Avi Sadka Christopher Vincent, Raphaël Morillon, 12.1 The long, complex, and intriguing Vicent Arbona, Aurelio Gómez-Cadenas journey from set fruitlets to ripe fruit 245 12.2 The fruit of citrus is a modified berry 13.1 Limitations to geographical expansion called hesperidium 246 of citrus 271 12.2.1 The fruit rind or peel provides 13.2 Predicted climate in citrus growing an interface of the fruit with regions 271 the external environment 246 13.2.1 Mediterranean climates 272 12.2.2 The fleshy pulp is composed of 13.2.2 Humid subtropics 272 segments, which contain the 13.2.3 Semiarid regions 272 juice vesicles 248 13.2.4 Overall climate trends in 12.2.3 Vascular system of the citrus fruit 249 citrus-producing regions 272 12.3 Citrus fruit dimensions are genetically 13.3 Citrus responses to climate- determined but are influenced by influenced environmental factors 273 environmental and cultural practices 249 13.4 Soil moisture 273 12.4 Metabolism and accumulation of 13.4.1 Optimal water requirements in carbohydrate and organic acids, citrus 273 determinants of fruit flavor quality 252 13.4.2 Flooding 275 12.4.1 The physiology and practical 13.4.3 Management of soil flooding aspects of carbohydrate and in citrus orchards 275 organic acid accumulation 252 13.4.4 Water deficit—Effects on crop 12.4.2 The genetic basis of BRIX productivity 275 and TA 252 13.4.5 Irrigation to mitigate water deficit 276 12.4.3 The biochemistry of 13.5 Soil salinity 276 carbohydrate and organic acid 13.5.1 Salinity effect on vegetative accumulation 252 and reproductive growth 277 12.4.4 Contribution of Omics 13.5.2 Salinity effects on mineral techniques to the nutrition 277 understanding of sugar 13.5.3 Salinity effects on citrus and acid metabolism and physiology 277 accumulation 254 13.5.4 Mitigation of salinity effects 278