Tai Lieu Chat Luong Plant Pathogen Resistance Biotechnology Plant Pathogen Resistance Biotechnology Edited by David B Collinge Copyright © 2016 by John Wiley & Sons, Inc All rights reserved Published by John Wiley & Sons, Inc., Hoboken, New Jersey Published simultaneously in Canada No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per‐copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) 750‐8400, fax (978) 750‐4470, or on the web at www.copyright.com Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) 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(800) 762‐2974, outside the United States at (317) 572‐3993 or fax (317) 572‐4002 Wiley also publishes its books in a variety of electronic formats Some content that appears in print may not be available in electronic formats For more information about Wiley products, visit our web site at www.wiley.com Library of Congress Cataloging‐in‐Publication Data Names: Collinge, D.B (David Brian), editor Title: Plant pathogen resistance biotechnology / David B Collinge Description: Hoboken, New Jersey : John Wiley & Sons, [2016] | Includes bibliographical   references and index Identifiers: LCCN 2015049842 | ISBN 9781118867761 (cloth) Subjects: LCSH: Plant biotechnology | Plants–Disease and pest resistance–Molecular aspects |   Phytopathogenic microorganisms Classification: LCC TP248.27.P55 P568 2016 | DDC 630–dc23 LC record available at http://lccn.loc.gov/2015049842 Set in 10/12pt Times by SPi Global, Pondicherry, India Cover credit: Getty/LeitnerR 10 9 8 7 6 5 4 3 2 1 1 2016 To Andrea, Mikkel and Jakob Tak for jeres støtte Contents List of Contributors xiii Foreword xix Acknowledgments xxv Chapter The Status and Prospects for Biotechnological Approaches for Attaining Sustainable Disease Resistance David B Collinge, Ewen Mullins, Birgit Jensen and Hans J.L Jørgensen 1.1 Introduction 1.2 Factors to consider when generating disease‐resistant crops 1.3 Opportunities to engineer novel cultivars for disease resistance 10 1.4 Technical barriers to engineering novel cultivars for disease resistance 13 1.5 Approaches for identification and selection of genes important for disease resistance 14 1.6 Promising strategies for engineering disease‐resistant crops 15 1.7 Future directions and issues 15 References16 Part I: Biological Strategies Leading Towards Disease Resistance Chapter Engineering Barriers to Infection by Undermining Pathogen Effector Function or by Gaining Effector Recognition Ali Abdurehim Ahmed, Hazel McLellan, Geziel Barbosa Aguilar, Ingo Hein, Hans Thordal‐Christensen and Paul R.J Birch 2.1 Introduction 2.2 Plant defence and effector function 21 23 23 24 vii viii contents 2.3 Strategies for engineering resistance 33 2.4 Perspective 42 References43 Chapter Application of Antimicrobial Proteins and Peptides in Developing Disease‐Resistant Plants Ashis Kumar Nandi 51 3.1 Introduction 51 3.2 Biological role of PR‐proteins 52 3.3 Antimicrobial peptides 56 3.4 Regulation of PR‐protein expression 57 3.5 Biotechnological application of PR‐protein genes in developing improved crop plants 60 3.6 Future directions 61 Acknowledgement63 References63 Chapter Metabolic Engineering of Chemical Defence Pathways in Plant Disease Control Fred Rook 71 4.1 Introduction 71 4.2 Present status of metabolic engineering in the control of plant disease 73 4.3 Metabolic engineering: technical challenges and opportunities 78 4.4 The outlook for metabolically engineering of disease resistance in crops 83 References85 Chapter Arabinan: Biosynthesis and a Role in Host‐Pathogen Interactions Maria Stranne and Yumiko Sakuragi 91 5.1 Introduction 91 5.2 Biosynthesis and modification of arabinan 94 5.3 Distribution of arabinan in different tissues and during development 96 5.4 Role of arabinan in plant growth and development 98 5.5 Roles of arabinan degrading enzymes in virulence of phytopathogenic fungi 99 5.6 Roles of arabinan in pathogen interactions 101 5.7 Conclusion 103 References103 Chapter Transcription Factors that Regulate Defence Responses and Their Use in Increasing Disease Resistance Prateek Tripathi, Aravind Galla, Roel C Rabara and Paul J Rushton 109 6.1 Introduction 6.2 Transcription factors and plant defence 6.3 AP2/ERF transcription factors 6.4 bZIP transcription factors 109 110 111 113 400 Plant Pathogen Resistance Biotechnology incremental improvements to cultivars has led to rapid advances in plant breeding for disease resistance (Brown, 2015) and should be equally effective in biotech programmes 20.10 Biotech innovation and genetic diversity The exploitation of GM technology has been greatly inhibited by the virtual embargo on the cultivation of GM crops in most of Europe and the excessive cost of conducting the trials required for regulatory approval, both in Europe and elsewhere (Wulff et al., 2011) Only the largest companies have the resources needed to achieve regulatory approval for even one GM construct As a consequence, the relatively few plant GM products that have come to market have been “blockbuster” products from the largest transnational corporations This has two strongly adverse consequences for disease control Firstly, the agricultural biotechnology industry does not benefit from the creativity of individual inventors and small investors which has been such a powerful driver of progress in other sectors such as information technology Secondly, diversity in R‐genes within fields, in different cultivars and between different geographical areas is a crucial feature of sustainable disease control in crops (Brown, 2015; Mundt, 2014) The monoculture system of industrialized agri­ culture, in which each field is sown with an essentially uniform cultivar, allows virulent pathogen genotypes to spread very rapidly in “founder events”, causing formerly useful R‐genes to become ineffective (Brown and Hovmøller, 2002) Effective R‐genes will be no more durable if they are introduced into crop improvement programmes by biotech rather than breeding (Brown, 2015) The durability of disease resistance will be enhanced if farming systems move away from the simplified monoculture that charac­ terizes much food production in industrialized countries and, instead, re‐incorporates some of the complexities of natural ecosystems that reduce the rate of parasites’ adaptation to their hosts (Brown, 2015) In a world which needs to feed a growing population, it should be possible to incorporate new dis­ coveries into the technology of food produc­ tion Achievement of durable disease control will require the best available technology to be integrated into a more complex, less uniform farming system 20.11 Conclusion Little of the regulation which, at least in Europe, has stifled innovation in plant bio­ technology has benefitted human health or the environment A more rational policy would have numerous benefits for disease control It would encourage the use of diverse R‐genes instead of channelling investment into blockbuster products It would permit selected constructs to be tested in diverse genetic backgrounds It would allow selection of cultivars in which fitness penalties of R‐genes are mitigated by reas­ sortment of the genetic background It would make it possible for small companies to develop innovative ways of controlling crop diseases These technologies can then be exploited in more ecologically diverse agricultural systems to achieve the goal of durable disease control (Brown, 2015) Acknowledgement The author’s work is supported by the BBSRC Biotic Interactions 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xvii, xviii, 6, 7, 9, 10, 13, 16, 40, 52, 53, 85, 99, 113–117, 131–147, 178, 194, 220, 223, 263, 279, 281, 288, 292, 293, 323–325, 330, 348, 351 see also drought tolerance abscisic acid (ABA), xviii, 7, 10, 40, 52, 96, 131, 135, 173, 249, 324 adoption (of GM), 163, 166, 263, 275, 282, 285, 290, 295–300, 302, 308, 309, 312, 330, 388 ADR1, 390 Agrobacterium, 33, 132 A radiobacter, 348 A tumefaciens, 4, 40, 139, 279, 280, 348 A vitis, 198 Agrobacterium‐mediated transformation, 13, 172, 180, 183, 185, 187, 227, 231, 233–234, 250–252, 279 agrochemicals (chemical control), 11, 83–85, 147, 158, 165, 173, 184, 193, 195, 197, 198, 202, 221, 222, 228, 245–246, 264, 286–287, 298, 308, 319, 321, 322, 325, 330–331, 334, 341–342, 354–355, 355, 356–357 agroecology, 400 Albugo spp., 29 alkaloid, 71, 72, 78–79, 320 allele, 171, 177, 178, 194, 256, 323, 330, 366, 370–380, 387, 392–396, 399 Almond (Prunus dulcis), 203 Alternaria spp., 60 A alternata, 5, 138 A brassicae, 62 A brassicicola, 55, 117 A dauci, 357 A radicina, 357 A solani, 74 ankyrin repeat, 114, 395 antibiotic resistance, 181, 234, 235, 251, 310 antifungal protein (AFP), 57, 62, 257, 258, 260, 262 antimicrobial compounds, 31–32, 40, 42, 61, 85, 110, 146–147, 246, 249, 264 antimicrobial protein/peptide, 51–63, 117–119, 254, 259, 264, 281, 320 Antirrhinum majus, 84 APD1, 58 apotosis, 8, 110 see also programmed cell death (PCD) apple (Malus domestica), 55, 83, 96, 99, 100, 252, 299, 376 arabidopsides, 329 Arabidopsis histidine kinase (AHK), 41 see also receptor‐like protein kinases Arabidopsis (thaliana), 9, 10, 14, 30, 31, 40, 53, 62, 69, 77, 80, 93, 94, 98, 102, 109, 113, 117, 134, 178, 248, 255, 281, 311, 322, 326, 333, 346, 368, 370, 372, 373, 375, 389–397 arabinan, 91–103 arabinoxylans, 91, 92 Argentina, 275–283 developments, 278, 279 land cultivated with GM crops, 277 transgenic crops (approved), 275–276, 276–277, 277 ash (Fraxinus spp.), Aspergillus aculeatus, 98 A flavus, 62 A niger, 196 A giganteus, 257, 258, 260 Plant Pathogen Resistance Biotechnology, First Edition Edited by David B Collinge © 2016 John Wiley & Sons, Inc Published 2016 by John Wiley & Sons, Inc 405 406 index autophagy, see also programmedcell death (PCD) auxin, 29, 32, 38, 114, 131, 135–136, 138, 138, 139, 140, 142, 142–144, 198, 202, 223, 231, 233, 249, 346 avirulence (Avr) gene/protein, 6, 7, 9, 23–43, 56, 60, 110, 137, 138, 140, 173, 175, 175, 176, 177–179, 183, 185, 253, 257, 377, 385–387 avocado (Persea americana), 311 Bacillus spp., 227, 325, 344, 346 Bacillus circulans, 257 B cereus, 221 B lentimorbus, 221 B subtilis, 100, 357 B thuringiensis (and BT toxins, cry genes), 73, 221, 223, 227, 232, 290, 296, 305 bacterial blight/leaf streak, 176, 246, 249, 253, 262 see also Xanthomonas oryzae BAK1, 28, 31, 132, 137, 174 bal, 390, 391 banana (Musa spp.), 5, 11, 62, 83, 160, 287, 288, 376 barley (Hordeum vulgare), 9, 13, 30, 33, 35, 54, 56, 57, 62, 76, 115, 200, 201, 250, 252, 287, 288, 289, 292, 333, 352, 365, 367, 369–372, 375, 379, 380, 389, 390, 396, 397, 398, 399 benefits (of GM crops), 119, 158, 164, 165, 261, 291, 295, 307 benzo(1,2,3)thiadiazole‐7‐carbothioic acid S‐methyl ester (BTH), 321–323, 326, 328–333 β‐1,3‐glucanase, 5, 23, 31, 55, 62, 92, 92, 99, 112, 178, 249, 253, 254, 255, 320 β‐1,4‐glucanase, 201, 204 β‐aminobutyric acid (BABA), 322, 323–327, 328, 329, 332–333 bioantagonism, 324 biofilms, 204 bioinformatics, 51, 85, 177, 209, 312, 342, 373–375, 380 biological control, xvii, xx, 2, 158, 221, 326, 334, 341–357 biological control agent (BCA), 341–357 biological control benefits, 325 biotechnology, 305, 307–309, 312 biotechnology deregulation, needs and procedures, 172, 187, 280, 282, 400 biotic stress, 10, 13, 113–117, 123, 131–147, 178, 220, 223, 264, 320, 323–326, 328, 329, 330, 343–344, 375 biotrophy, 3, 4, 5, 6, 8, 10, 15, 16, 32, 40, 41, 53–59, 133–136, 139, 195, 195, 219, 249, 264, 320, 323, 326, 387, 390, 395 Bipolaris sorokiniana, 3, 117 Black Sigatoka, 5, 11, 12, 83 see also Mycosphaerella fijiensis blast, rice, 30, 73, 245–246, 249, 253, 260, 323, 331 see also Magnaporthe oryzae Blumeria graminis f.sp hordei, 3, 4, 30, 54, 56, 389, 390, 398 see also powdery mildew B.g f.sp secalis, 397 B.g f.sp tritici, Bois noir, 198 Botryosphaeria spp., 197 see also grapevine wood pathogens Botrytis cinerea (teleomorph Botryotinia fuckeliana), 3–5, 15, 17, 37, 40, 55, 62, 74, 76, 80, 84, 93, 96, 99–103, 117, 135, 137–139, 195, 196–197, 200, 310, 312, 391 see also grey mould BR1, 101, 144 see also BAK1 Brassica oleracea, 54, 62 Brassica spp., 356 brassinosteroids, 7, 53, 131, 136–137, 249 browning of potatoes, 281 BT‐maize, xviii, 12–13, 296–300, 305 bunch rot see Botrytis Burkholderia glumae, 34–35, 246 callose, 7, 23, 31, 55, 74, 91, 101, 110, 132, 135, 137, 174, 178–179, 196, 221, 320, 327, 389 calmodulin, 6, 7, 58, 145, 221 camalexin, 71, 73, 77 canola see rape Capsicum annum (pepper), 12, 55 Capsicum spp (peppers), 55, 160–161 capsidiol, 40, 137 cassava (Manihot esculenta), 161, 309, 311, 313, 376 cassava mosaic disease, 311 cecropin, 62, 209, 257, 258 CEL 1, 372–374 Cercospora arachidicola, 62 C nicotianae, 54, 393 C zeina, 312 C coffeicola, 224 CERK1, 30 see also receptor‐like protein kinases Cf‐9, 30, 39, 392 chemical control see agrochemicals chemical defence, 8, 71–85, 132 chitin, 24, 27, 30, 37 chitinase, 5, 12, 23, 62, 83, 110–112, 178, 200, 223, 224, 249, 253, 254–257, 320, 343, 349, 351–352 chromatin remodelling, 111, 330 cisgenesis, 179, 199, 252 see also intragenesis citrus, 164, 203, 224, 279, 280–281, 376 citrus canker, 281 see also Xanthomonas climate change, xvii, 1, 146–147, 157, 222, 295 Clonostachys rosea, 344, 352, 353, 355–357 Clustered Regulatory Interspaced Short Palindromic Repeats (CRISPR), xix, 15, 16, 35, 81, 120, 121, 261 Cochliobolus carbonum, 100 C miyabeanus, 249 cocoa (Theobroma cocoa), 54, 59, 219 index 407 coexistence, 263, 297, 300 coffee (Coffea arabica (Arabica) and C canephora), 13, 78, 203, 217–236, 299 coffee leaf rust, 1–2, 219–222 see also Hemileia vastatrix coiled‐coil (CC) domain, 27–28, 388, 391 Colletotrichum graminicola, 40, 77 C kahawae, 221 C orbiculare, 55 corn see barley; maize; wheat corn borers, 298, 300, 309 coronatine, 6, 7, 117, 134, 138, 140 cotton (Gossypium spp.), xix, 59, 62, 73, 118, 227, 275, 276, 277, 278, 285–290, 290, 292, 295, 297, 300, 301, 305, 306, 307, 308, 309, 312, 354 Cpr1, 392–393 crop/plant breeding, 146, 147, 158, 162, 165, 171–173, 177, 179, 184, 187, 194, 198–200, 211, 220, 225–227, 235, 253, 262, 280, 282, 305, 333, 354, 376 cross‐resistance, 145 crosstalk, 131, 135, 145 crown gall, 139, 198, 202, 285, 348 see also Agrobacterium Cry toxin/genes, 223, 227, 232, 234–235, 290, 296, 299, 300 cuticle, 7, 92, 92–93, 132, 319, 320 cutinase, 92, 320 cysteine‐rich protein kinase (CRK), cytochrome P450, 77, 79, 201, 378 cytokinins (CK), xviii, 6, 7, 10, 30, 40, 131, 137–138, 147, 249, 346 damage‐associated molecular patterns/immunity (DAMPs), 25, 132, 247 see also immunity defence‐no‐death (DND), 220 defensins, 57, 62, 134, 249, 254–255 degrading enzymes, xix, 3, 4, 6, 7, 38, 51, 94, 99, 102, 103, 174, 197, 201, 204, 206, 207, 209, 223, 247, 320, 343, 349, 352 deletion mutations, 36, 81, 185, 366, 370, 371, 378, 379 DELLA proteins, 134, 136, 143, 334 Dickeya spp., D zeae, 246 see also soft rot DNA methylation, 111, 231–232, 330, 368, 390, 396 DNA pool, 367–368, 369, 374, 375 double‐stranded RNA (dsRNA), 4, 5, 159, 258 downy mildews, 3, 28, 33, 195, 196, 198, 199, 368, 387, 391 see also Hyaloperonospora; Peronospora; Plasmopara Drechslera tritici‐repentis, drought tolerance, 279, 281–282 economic impact, 278 economic/income benefits, 85, 278, 290, 302, 308, 312, 386, 387 ecoTILLING, 375, 379–380 EDS5, 58, 59 effectors, 3, 4, 5, 6, 9, 23–43, 60, 109, 132, 137, 138, 140, 173, 174, 175–177, 179, 185, 196, 202, 247, 253, 258, 260, 261, 326, 385 effector‐triggered immunity (ETI), 8–9, 23–43, 60, 109, 114, 133, 134, 173, 174, 246, 250, 321, 385 see also immunity EF–Tu receptor (EFR), 24, 33, 132 see also receptor‐ like protein kinases eIF4E, 161, 162, 377, 379 elicitors, 6, 24, 30–31, 39, 96, 102, 139, 247, 258, 321, 322, 326, 327, 332–334, 392 elicitors endogenous, 247, 322, 324 ENDO I, 372 endophyte, xvii, 3, 203, 222, 325 epigenetic, 63, 146, 231, 234, 328–330, 334, 393 Erwinia, 280 see also Dickeya; Pectobacterium E carotovora, 37, 280 E chrysanthemi, 246 Erysiphe cichoracearum, 93 see also powdery mildew; Golovinomyces cichoracearum E necator (syn Uncinula), 62, 195, 198, 199 E orontii, 93 see also Golovinomyces orontii ethylene (ET), 6, 10, 52, 58–59, 80, 93, 111, 112, 131, 133, 134, 173, 178, 205, 206, 207, 229, 230, 249, 260, 324, 325, 329, 376–377 ETI see also immunity; effector‐triggered immunity ETI receptors, 60–61, 158 see also resistance genes ethylene insensitive (EIN2), 59 ethyl methanesulfonate (EMS), 367–368, 370, 371, 377, 378 Etr1, 376, 377 Eucalyptus spp., 312 Euphorbia pulcherrima, 96 European Food Safety Authorities (EFSA), 172, 187, 296, 299 European Regulations, 296 Eutypa dieback, 197 see also grapevine wood pathogen Eutypa lata, 197 see also grapevine wood pathogen expansin, 200 Exserohilum turcicum, 312 fast neutron, 368, 371 ferredoxin‐like protein (Pflp), 12 ferulic acid esters, 92–93, 98 field trials, 162, 166, 171, 184–187, 227, 278, 287, 291, 300, 301–302, 310, 398 flagellin, 8, 24, 37–38, 109, 132, 135, 247, 257, 258, 322, 324, 390 flavescence doree, 198 flavonoid, 71, 72, 73–75, 75, 76, 83 Flg22, 109 FLS2, 24, 28, 31, 33, 39, 40, 42 see also receptor‐like protein kinases 408 index forward genetics, 365, 366, 376, 381 freezing injury, 198 freezing stress/tolerance, 55, 62, 113, 119 fumonisin, 299, 309 fungicide resistance, 1, 173, 199, 342, 354, 355, 356 Fusarium, xviii, 246, 299, 309, 376 foot rot disease, 352, 356 head blight, 1, 344, 356, 388 Fusarium culmorum, 376, 388 F fujikuroi, 246 F graminearum, 12, 57, 77, 117, 201, 387, 388 F moniliforme, 139 F oxysporum, 55, 57, 62, 99, 135 F.o f sp cubense (Fusarium wilt of banana, Panama disease), 11 F.o f sp lycopersici, 27, 30, 392 F.o f sp radices‐lycopersici, 348 F.o f sp tomato, 392 F proliferatum, 246 F roseum, 99 F solani, 280 F verticillioides, 246, 309 F xylarioides, 222 galactomannan, 222–223 see also mannan gamma irradiation, 371, 378 gene cluster, 26, 35, 79, 80, 81, 172, 393, 395 gene flow, 247, 262 gene‐for‐gene relationship, 385 see also race specificity; ETI gene‐for‐gene resistance, 377 see also resistance (R) genes gene‐stacking, 35, 82–83, 85, 120, 147, 165, 175, 176, 186, 199, 252, 259, 280, 373, 386 genetically modified (GM) crops, xix, 2, 13, 172, 187, 236, 261–263, 277, 278, 285–286, 291, 295–300, 305–309, 312, 388, 400 genome editing, 15, 32, 81–82, 121, 256, 260, 261, 302 see also CRISPR; TALENS genomic selection, genotype, 365, 371, 375, 376 gibberellin, 62, 131, 136, 246, 249, 334, 346, 368 glucosinolate, 71, 77, 80, 81 Glycine max see soybean glycosyltransferase, 79, 94–95 GM crops see genetically modified (GM) crops GM crops and society, 194, 227 GM directive, 342, 350, 366 golden rice, 84 Golovinomyces cichoracearum, 62, 391 see also powdery mildew G orontii, grafting, 193–194, 198, 208–209, 211, 278, 281, 395 see also scion; rootstock grapevine (Vitis vinifera), xviii, 10–12, 59, 62, 73–75, 80, 160–161, 164, 167, 193–211, 310, 311, 355, 356, 376, 395 grapevine leafroll disease, 311 grapevine wood pathogens, 197 see also Eutypa lata; Togninia minima; Phaeomoniella chlamydospora; Botryosphaeria green islands, 40–41, 139, 202, 203 grey leaf spot disease, 312 see also Cercospora zeina grey mould, 356–357, 390 see also Botrytis growth inhibition, 55, 101, 280, 323 haustoria, 3, 4, 6, 28, 174, 195, 196, 198, 219, 221 health benefits, 72, 73, 76, 83, 84, 308, 309, 312 hemibiotrophy, xviii, 3, 4, 5, 6, 7, 8, 10, 12, 40, 53–59, 133–136, 173, 221, 249, 387 hemicellulose, 91, 92, 93, 95, 98 see also xyloglucan; arabinoxylans; mannans Hemileia vastatrix, 1–2, 219–221 see also coffee rust herbicide resistance/tolerance, 73, 82, 187, 221, 227, 228, 233–235, 251, 263, 275, 276, 278, 285–287, 290, 291, 292, 295–297, 301–302, 305, 306, 307, 309, 312, 355 herbivores, 25, 32–33, 71–73, 82, 132–134, 136, 137, 139, 140, 319, 320, 326 herbivore tolerance, 132, 281, 331 see also BT and Cry high‐resolution melt (HRM), 367, 373 histone modification, 63, 111, 330, 393 hormones (phytohormones), xvii, 3, 4, 6, 10, 13, 39, 40, 52, 112–123, 131–147, 161, 173, 202, 248–249, 253, 321, 326, 328, 329, 346 host‐induced gene silencing (HIGS), xx, 15, 16, 201 Hyaloperonospora (syn Peronospora) arabidopsidis, 31, 55, 117, 137, 393 see also downy mildew H parasitica, 28, 93, 379, 391 hydroxycinnamic acid amides (HCAAs), 72, 76, 221 Hymenoscyphus fraxineus, see also ash dieback hypersensitive response (HR), 3, 5, 8, 23, 30, 35, 39, 42, 56, 110, 116, 119, 133, 136, 174, 198, 221, 247, 320, 387, 389, 392, 394, 396 see also programmed cell death (PCD) ICS1, 58–59, 115 immunity, xvii, xviii, xx, 2, 6, 8–9, 23, 25, 27, 30, 31, 33, 37, 38–41, 60, 109–110, 131, 133, 135, 138, 178, 179, 247–250, 312, 322, 330, 334, 367, 375, 379 see also damage‐, effector‐and PAMP‐ triggered immunity auto‐immunity, 393, 396 boosting immunity, 33, 38–41 suppressing immunity, 38–39, 60, 109 see also effectors imprinting, 146, 331 in biological control, 323, 344, 346, 357 individualized TILLING (iTILLING), 376 induced resistance benefits, 224, 331, 332 index 409 induced systemic resistance (ISR), 10, 40, 53, 58, 117, 133, 248, 324–329 insect resistance, 12, 72, 73, 82, 137, 227, 251, 259, 262, 264, 275, 278, 286–287, 290, 291, 292, 295, 298–300, 301–302, 305, 306, 308–309, 312, 328, 331 see also BT and Cry International Service for the Acquisition of Agri‐biotech Applications (ISAAA), xix, 74, 295 intragenesis, 177, 179, 252 see also cisgenesis introgression, xx, 34, 165, 171–172, 179, 194, 224–226, 263, 286 isochorismate pathway, isochorismate syntase (ICS1/SID2), 58, 117, 379 isoflavonoid, 72, 75, 76, 80 ISR see induced systemic resistance JAR1, 59 Jasmonic acid (JA), 6, 7, 10, 52, 57–59, 117, 133, 134, 173, 249, 321, 326, 329 L6, 27, 392, 393 labelling (of GM products), 263, 286, 297, 307 late blight of potatoes, 1, 9, 11, 31, 171–187, 323, 332 see also Phytophthora infestans LI‐COR system, 372, 373 linkage drag, 171, 194 lipids, 141, 174, 329, 394 lipid transfer protein (LTP), 57, 254, 377 lipopolysaccharide, 132, 247, 312, 321, 322, 324 losses caused by pathogens, xvii, 1, 11, 157, 173, 196–198, 202, 218, 219, 221, 224, 278, 281, 289, 296, 298, 387 see also yield Lr34, 378 LysM, 24, 30, 37 see also receptor‐like protein kinases Magnaporthe oryzae (syn M grisea), 27, 30, 62, 73, 135, 139, 245, 257, 323 see also Pyricularia oryzae; rice blast maize streak virus, 310 maize (Zea mays), xvii, xix, 12, 26, 41, 73, 77, 161, 255, 260, 275, 276, 277, 277, 278, 279, 281, 286, 287, 295, 296, 299, 301, 305, 306, 306, 307, 308–310, 312, 348, 362, 367, 369, 370, 390, 394, 396 see also BT‐maize MALDI‐TOF, 367, 373 MAMP‐triggered immunity (MTI), 8, 109 Manduca sexta, 136, 138 mannanase, 222, 223 mannans, 91, 92 marker‐assisted breeding/selection, 2, 200, 202, 212, 224, 227, 230, 262, 265 Melampsora lini, 27, 30, 392 see also flax rust metabolism, 25, 37, 76–85, 132, 139–140, 146–147, 224, 330, 333, 348 Mi (tomato), 394 microbial‐associated molecular patterns (MAMPs), 6, 8, 23–24, 60, 247, 324, 396 microRNA (miRNA), 4, 5, 15, 16, 36–37, 135, 159, 249, 256 miR393, 135 missense, 371, 378 mitogen‐activated protein kinase (MAPK), 6, 109, 110, 133, 134, 140, 141, 174, 178, 221, 248, 255, 329 Mla, 375, 379, 389, 390, 397, 398 Mlo, 3, 375, 379, 399 MNSV, 375, 379 Moko wilt disease, 11 momilactone, 73 monoculture, 1, 35, 386, 400 Monsanto, xix, 287, 289, 305, 306 MTI see PAMP‐triggered immunity (PTI) multiline, 386 mutagen, 366, 367, 367–368, 369–371, 374 mutagenesis, 366, 369, 369–371, 374 mutation, 369–378 mycorrhizal fungi, 138, 248, 325–326, 331 Mycosphaerella fijiensis, 5, 11, 62, 83 see also Black Sigatoka M graminicola (ann Septoria tritici), 387, 388 see also Zymoseptoria tritici; septoria blotch mycotoxins, 1, 12, 299 see also fumonisin; fusarium; trichothecenes; zearalenone natural resistance‐associated macrophage protein (Nramp6), 249 natural selection, 60, 175, 349, 399 necrotrophy, xvii, 3, 4, 5, 6, 7, 8, 10, 12, 16, 57–60, 99, 117, 133–139, 139, 173, 195, 196, 249, 264, 320, 323, 326–327, 387, 391, 395, 399 nematodes, 24–26, 32, 56, 109, 157, 176, 194, 198, 218, 220, 222, 224, 227, 323, 346, 378, 392, 394 Neoscytilidium dimideatum, 195 next generation sequencing (NGS), 35, 368, 373 Nicotiana spp (tobacco), 392 N alata, 57, 62 N attenuata, 137 N benthamiana, 38, 41, 55, 77, 100, 136 N plumbaginifolia, 98 N tabacum, 40, 53, 78, 255, 280 nitric oxide (NO), 135, 136, 248 noble rot see Botrytis non‐expresser of PR genes (NPR1), 6, 10, 12, 40, 58–59, 113–115, 118, 134–137, 248, 379, 393 non‐sense, 371 northern corn leaf blight disease, 312 nucleotide‐binding site‐leucine‐rich repeat proteins (NBS‐LRR), 6, 27, 35–37, 109, 110, 174, 177, 219–220, 225, 236, 256, 266, 380, 388–396 in hybrid necrosis, 394–395 stability, 392–393 410 index oats, 367, 373, 376 oesophageal cancer, 309 Oidium lycopersicum, 93, 392 see also powdery mildew Oryza glaberrima, 245 O nivara, 262 O rufipogon, 262, 395 O sativa, 245 see also rice PAD4, 58, 59, 118 pathogen‐associated molecular patterns (PAMP) see microbial‐associated molecular patterns (MAMPs) PAMP‐triggered immunity (PTI), 8–9, 11, 12, 23, 24, 30, 60, 109–110, 132, 173, 174, 247, 321 see also immunity; MAMP‐triggered immunity (MTI); PTI Panama disease; fusarium wilt of banana papaya, 160, 163, 165–167, 201 papillae, 7, 178–179, 196, 320particle bombardment (biolistics), 13, 228, 233–234, 250–251, 280, 296 Passalora fulva (Cladosporum fulva), 390, 392 pathogen‐associated molecular patterns (PAMPs), 132, 247 pathogen‐derived resistance (PDR), 247, 258 pathogenesis‐related (PR), 249, 254 pathogenesis‐related (PR) proteins, 5, 12, 42, 51–63, 110, 200, 249, 326, 395 pathogenicity factor, 3–5, 6, 99, 351 see also effectors pattern recognition receptors (PRRs), 6, 9, 23–24, 25, 33, 60, 109, 132, 137, 140, 173, 174, 247, 321 pectate lyase (PL), 92, 201 pectin acetylesterases (PAEs), 92, 92 pectin methyl esterases (PMEs) and their inhibitors (PME15), 92, 92, 101, 102, 201, 208, 210 pectinase, 320 see also pectate lyase pectins, 7, 91–96, 98, 102, 200 Pectobacterium, 37, 62, 311 see also Dickeya; Erwinia; soft rot peptide aptamers, 162 Peronspora see also downy mildew; Hyaloperonospora P tabacina 54 pesticides, xvii, 295, 323, 330–332, 334, 342, 354, 356–357 see also agrochemicals Phaeomoniella chlamydospora, 197 see also grapevine wood pathogens phenomics, 16, 146–147, 380 phenotype, 13, 102, 115, 119, 120, 122, 174, 178, 226, 231, 280, 342, 365, 371, 374, 376, 378, 380, 392–394 phenylpropanoid, 71, 74, 75, 76, 80 Phoma lingam, P medicaginis, 76 phylloxera, 193–194 phytoalexin, 3, 5–7, 32, 40, 61, 71–74, 76, 78, 110, 132, 137, 138, 147, 249, 320, 328 phytoanticipins, 7, 8, 71, 73 phytohormones see hormones Phytophthora spp., 376 P cinnamomi, 311 P citrophthora, 300 P infestans, 1, 3, 11, 28, 30, 31, 34, 36, 41, 52, 54, 74, 96, 172, 174, 280, 323, 332 P parasitica, 54, 393 P sojae, 24, 28, 30–31, 40, 377 P tabacina, 54 phytoplasmas, 194–195 phytotoxins, 3, 5, 7, 60, 258, 320, 343 see also toxins Pierce’s disease, 194, 202–211 see also Xylella fastidiosa pineapple (Ananas comosus), 161 pioneer, 276, 301, 305, 306 Piriformospora indica, 325, 346 pit membranes (PMs), 204, 205 plant breeding/breeders, xviii, xx, 8, 10, 11, 14, 60, 147, 172, 179, 193, 235, 282, 292, 305, 333, 354, 380, 385–386, 388, 397–400 plant growth‐promoting rhizobacteria (PGPR), 324–327, 333 Plasmopara viticola, 195–196 see also downy mildew Plectosphaerella cucumerina, 93 ploidy level, 231, 366, 367, 369, 371 polygalacturonase (PG), 92, 92, 99–100, 200, 204, 310–311, 320 polygalacturonase‐inhibiting protein (PGIP), 83, 201, 208–210, 310–311 polyploid, 179, 369, 374 polyprotein, 259 population, mutant, 366, 369, 369–376, 378 population, natural, 24, 34, 36, 173, 175, 177, 186, 193, 199, 220, 225, 253, 263, 299, 344, 375, 379, 386 potato cyst nematode (Globodera rostochiensis), 32 potato R‐genes R3a, 31, 36 potato (Solanum tuberosum), xviii, xix, 1, 3, 4, 11, 62, 76, 98, 99, 161, 171–187, 227, 252, 254, 278–282, 287, 289, 290, 291, 296, 310, 311 Amflora, 296–297 potential for innovation, 400 powdery mildew, 3, 4, 9, 30, 33, 35, 56, 93, 101, 115, 179, 195, 195, 196, 198–200, 322, 332, 355, 356, 375, 378, 379, 387, 389, 390, 392, 397, 398, 399 see also Blumeria; Erysiphe; Golovinomyces; Oidium PR1 (PR‐1), 5, 53–54, 58–59, 111, 112, 118, 134–135, 137, 178, 209, 221, 249 PR2 (PR‐2), 5, 55, 111, 178 see also β‐1,3‐glucanase PR3 (PR‐3), 5, 55, 111, 112, 178 see also chitinase PR4 (PR‐4), 55, 257, 260 PR5 (PR‐5 osmotin), 5, 54–56, 112, 178, 255 PR8 (PR‐8 peroxidase), 224 index 411 PR10 (PR‐10), 55–56, 80, 117, 221 PR12 (PR‐12), 55–57 see also defensin PR17 (PR‐17), 178 Prf, 42, 389–391 primer design, 369, 369, 374 priming induced resistance, 53, 133, 146, 311, 326–334 probenazole, 279, 323, 326, 331 probenazol1 (PBZ1), 56 prochymosin, 279, 281–282 programmed cell death (PCD), 23, 31, 194, 196, 209 see also hypersensitive response promoters, 13–14, 25, 26, 32, 39–40, 42–43, 59, 61, 80–83, 111–121, 143–145, 177, 182–183, 186, 223, 250, 252, 254, 258–260, 330, 393 protein kinase see cysteine‐rich protein kinase (CRK); nitogen‐activated protein kinase (MAPK); pattern recognition receptors (PRR); receptor‐like protein kinases (RLK) PRRs see pattern recognition receptors Pseudomonas, 33, 39 P fluorescens, 324, 348 P putida, 158, 221, 324 P syringae, 3, 9, 54–56, 78, 112, 118, 135, 137, 138, 140, 230, 258 P.s pv garcae, 224 P.s pv glycinea, 28, 376, 377 P.s pv maculicola, 96, 393, 397 P.s pv phaseolicola, 96 P.s pv tabaci, 54 P.s pv tomato (Pst), 28, 31, 32, 55, 62, 112, 289, 389 PTI see immunity; PAMP‐triggered immunity; MTI and PAMP‐triggered immunity Pto, 9, 389–391 Puccinia, see also rust P sorghi, 390, 394 P striiformis, 40, 387, 388 pyramiding see gene stacking Pyricularia oryzae, see also Magnaporthe spp Pythium, 354 P irregular, 135, 136 P ultimum, 30, 349 quantitative trait loci (QTLs), 12, 225, 378 Radish (Raphanus sativus), 57, 354 Ralstonia solanacearum (including Moko disease), 11, 29, 32, 33, 57, 93, 312, 390 Ramularia collo‐cygni, rape (Canola, Brassica napus), xix, 4, 286, 289, 294, 295, 297 Rar1, 6, 389 reactive oxygen species (ROS), 6, 40, 61, 91, 110, 133, 136, 141–143, 143, 144, 174, 178, 196, 248, 320, 328, 348, 394 receptor‐like protein kinases (RLK), 9, 14, 30, 31, 41, 54, 101, 141, 248, 256, 378, 389, 394 see also AHK; BAK1; BR1; CERK1; EFR; FLS2; WAK1 receptor‐like proteins, 6, 389 receptors, xviii, 6, 10, 24–26, 27, 30–32, 37, 40, 61, 92, 132, 134–135, 143, 151, 174, 324 see also pattern recognition receptors resistance, 25, 131, 135, 145, 174, 175, 375–381, 385–400 breeding, 33, 34, 157, 158, 171, 173, 197, 212, 225–227 durable, 385 fitness cost, 199, 333, 385–400 fungicide, 1, 173, 199, 356 induced, 2, 53, 135–137, 140, 158, 220, 247–249, 319–334 partial, 386 transgenic, 10, 11, 37, 42, 54, 61, 74, 78, 80, 83, 103, 111, 112, 118, 119, 120, 121, 124, 143, 146, 162–166, 178, 212, 250–260, 262, 264 viruses, 52, 119, 157–167, 247, 258, 310 resistance (R) genes, 4, 7, 8, 9, 118, 158, 176, 246, 385 see also effector‐triggered immunity autoactivation, 391 epigenetic control, 146, 390, 393 expression, 388–390 synthetic, 387, 399 resource allocation, 118, 140, 333, 349, 387, 391 resveratrol, 72, 73–75, 80, 84 reverse genetics, 365, 366, 377 rhamnogalacturonan, 92, 93, 95, 101 Rhg4, 378 Rhizoctonia solani, 62, 246, 279–280, 349, 377 see also sheath blight Rhodococcus fascians, 40 ribosome‐inactivating proteins, 162 rice blast, 30, 73, 246, 253, 260, 323, 331 see also Magnaporthe oryzae rice (Oryza sativa), 245, 367, 369–371, 373 rice transformation, 250 japonica, 245, 263 indica, 245 RIN4, 9, 28, 32, 391, 394 risk evaluation, 14, 82, 166, 172, 261, 286, 296, 302, 307, 344, 350–351 RLK, 395 see also receptor‐like protein kinases RNA interference (RNAi), 12, 14, 36–37, 120, 159, 258 rootstocks, 141, 167, 193–194, 199, 208–211, 281, 310, 395 Rp1, 390, 394, 396 RPM1, 28, 32, 40, 391, 395, 397 RPP1A, 391 RPP4, 393 RPS1, 31, 371, 377 RPS2, 40, 389, 391, 393 412 index RPS4, 392, 393 RPS5, 392 rust, 3, 9, 24, 377, 378, 387, 395 see also coffee rust; Hemileia; Melampsora; Puccinia; Uromyces Rx, 36, 171–187, 394 RXLR, 31, 34, 36, 174 rye (Secale cereal), 226, 397 sugarcane mosaic virus, 310 superoxide dismutase Cu, Zn (SOD), 12 sweet potato (Ipomoea batatas), 164, 311 see also viruses syngenta, xix, 276, 277, 289, 297, 301, 302, 305, 306, 332 systemic acquired resistance (SAR), 10, 25, 40, 53, 58, 63, 133, 247, 321, 379 systemin, 135–136 safflower (Carthamus tinctorius), 279, 281–282 sakuranetin, 73 salicylic acid (SA), 5, 6, 7, 10, 32, 39, 40, 52, 57, 58, 133, 134, 173, 249, 321, 326, 379 Sanger sequencing, 372 SAR see systemic acquired resistance scion, 193–194, 201, 208–210, 395 Sclerotinia fructigena, 100 S sclerotiorum, 3, 62, 356 scopoletin, 40, 137 Sebacinales, 346 seed treatment, 328, 331, 354, 357 Septoria glycines, 377 septoria tritici blotch, 387, 388 see also Zymoseptoria tritici Sgt1, 389 sharpshooter, glassy‐winged (GWSS), 202, 204, 205, 224 sheath blight, 246 see also Rhizoctonia solani shikimic acid/shikimate pathway, 58 SID2, 379 signalling pathways, 6, 14, 40, 42, 131, 135, 145 siRNAs, 12, 36, 159 smallholder farmers, 307–309 SNC1, 118, 392–393 SNP, 371, 374, 375, 380 social benefits, 84, 261, 285, 289, 308, 309, 312 sodium azide, 370, 371, 378 soft rot, 178 see also Dickeya; Pectobacterium Solanum spp., 171–187 see also potato; tomato source‐sink relation, 146–147 South Africa, 305–313 soybean (Glycine max), xvii, 31, 59, 73, 80, 160, 275–282, 292, 295, 301, 305, 306, 306, 307, 308, 309, 312, 368, 370, 376–378 Spain, 295–302 spontaneous lethal mutants, 391, 394 Sr31 and Sr38 wheat stem rust resistance genes, 176, 326 ssi2, 59 stilbene synthase (StSy), 12, 62, 74–76, 80 stress reaction, 145 stress recovery, 146–147 strigolactones, 5, 7, 135, 138, 147 substantial equivalence, 247, 261 success stories, 162–163 sugar beet (Beta vulgaris), 97 289, 297, 300, 301, 302 sugar cane (Saccharum spp.), 278, 279, 280, 289, 292, 309, 310 tanatin, 258 targeting induced local lesions IN genomes (TILLING), 354, 365–381 technical benefits, 80, 119, 121, 390, 399 terpenoids, 71, 76–77, 81 thaumatin, 55 Thaumatococcus daniellii, 56 thionin, 57, 62, 134, 249, 254 Tir1, 136 tobacco (Nicotiana spp.), 33, 40, 53–56, 62, 78, 80, 97, 100, 102, 117, 137, 143, 164, 223, 227, 249, 300, 302, 310–312, 321, 326, 329, 377, 391, 393–394 Togninia minima, 197 see also grapevine wood pathogens toll/ interleukin‐1 receptor (TIR), 27–29, 110, 135, 388, 391 tomato (Solanum lycopersicum), xx, 5, 12, 28, 30, 33, 36, 38, 42, 62, 74, 80, 84, 98–100, 112, 135, 160, 162–163, 200, 209, 227, 285, 323, 326, 328, 332, 353, 367, 368, 377, 389, 392, 394 Torenia hybrida, 76 toxins, ToxA, trade‐offs, 326, 333, 387, 396 between responses to different pathogens, 390–391, 396–397 with plant development, 391 transcription activator‐like (TAL), 32, 42, 43, 260 transcription activator‐like effector nuclease (TALENS), 15, 35, 37, 43, 81, 120, 121, 261 see also CRISPR; gene editing transcription factors, 6, 10, 29, 31, 40, 109–124, 248 AP2/ERF, 59, 111–113, 119 bZIP, 113–114 HaHB4, 281 MYB, 109, 116–117 NAC, 13, 111, 117 WRKY, 111, 114–115, 119, 123 transgenerational priming, 146, 330 Trichoderma spp., 325, 342, 346, 348, 349, 351–354, 357 T asperellum, 349 T atroviride, 352 T hamatum, 352 T harzianum, 11, 12, 62, 343, 348, 354 T longibrachiatum, 352 T parareesei, 348 T virens, 354 index 413 trichothecenes, 299 tyloses, 7, 205, 207–208 Vitis spp., 199 Vitis vinifera (see also grapevine), 11 volatile organic compounds (VOCs), 10, 320, 324 Uromyces vignae, 220 Verticillium albo‐atrum, 100 V dahlia, 62 victorin, viral small RNAs (vsRNAs), 258 virus‐induced gene silencing (VIGS), 146, 201, 378 virus resistance, 16, 157–167, 258, 259, 262, 278, 280, 310–311, 367, 368, 375, 377, 379 viruses‐transgenic resistance, 310, 311 viruses, 3, 11, 13, 34, 36, 52, 58, 82, 157–167, 198, 224, 245, 246, 387, 392, 394 bean golden mosaic virus (BGMV), 160, 163 beet necrotic yellow vein virus (BNYVV), 301 citrus psorosis virus (CPsV), 280–281 citrus tristeza virus (CTV), 164, 279 cucumber mosaic virus (CMV), 160, 162 grapevine fanleaf virus (GFLV), 160, 198–199 melon necrotic spot virus (MNSV), 375, 379 papaya ringspot virus (PRSV), 160, 163, 166 potato leafroll virus (PLRV), 278–279, 290 potato virus X (PVX), 11, 26, 34, 377, 394 potato virus Y (PVY), xiv, 11, 54, 162, 278, 279, 282, 289, 290 rice hoja blanca virus (RHBV), 246 rice stripe virus (RSV), 246 rice tungro virus (RTV), 246 sweet potato chlorotic stunt virus (SPCSV), 164 sweet potato feathery mottle virus (SPFMV), 164 tobacco etch virus (TEV), 377 watermelon mosaic virus (WMV), 160, 162 wheat streak mosaic virus (WSMV), 161, 164 zucchini yellow mosaic virus (ZYMV), 160, 162 WAK1, 93 see also receptor‐like protein kinases weedy rice, 262 wheat (Triticum aestivum), 26, 33, 35, 57, 62, 113, 117, 161, 164, 176, 223, 226, 250, 255, 278, 279, 281, 287, 288, 289, 292, 302, 367, 369, 370, 372–374, 377–378, 380–381 wine biotechnology, 310 wounding, 55, 57, 111, 134, 136, 262, 329, 396 WRKY see transcription factors Xa21, 253, 255, 256, 262 Xanthomonas spp., 3, 15, 32, 33, 39, 260 X axonopodis pv citri, 281 X campestris, 56, 390 X.c pv musacearum, 11, 12 X.c pv vesicatoria, 29, 55, 56 X oryzae, 82, 246, 257, 258, 260 see also bacterial blight of rice Xylella fastidiosa, 194, 198, 202–211 see also Pierce’s disease xyloglucan (XyGs), 91, 92, 93–94, 98, 101, 201, 204 xyloglucanase (EGase gene (engXCA), 201, 204, 207, 208 yield, 1, 15, 41, 54, 85, 118, 387, 397, 399 yield losses see losses caused by pathogens; yield penalties ; yield costs Yr36, 377 Zea mays, 254–256 see also maize zearalenone, 299, 352 zigzag model, 8, 24, 34 Zymoseptoria tritici, 3, 387, 388 see also septoria blotch WILEY END USER LICENSE AGREEMENT Go to www.wiley.com/go/eula to access Wiley’s ebook EULA