Contents · Part 1 Fungal diseases of cereals 1 Diseases affecting wheat and barley: rusts 3 R. F....

© Burleigh Dodds Science Publishing Limited, 2019. All rights reserved.

ContentsSeries list x

Acknowledgements xv

Introduction xvi

Part 1 Fungal diseases of cereals

1 Diseases affecting wheat and barley: rusts 3R. F. Park, University of Sydney, Australia

1 Introduction 32 The incidence and impact of wheat rust diseases 43 The incidence and impact of barley rust diseases 64 Rust resistance genes 85 Rust pathogen biology 106 Integrated methods of rust control 117 Durable resistance 118 Future trends in research 149 Where to look for further information 14

10 Acknowledgements 1511 References 15

2 Fusarium diseases: biology and management perspectives 23Edward C. Rojas, Hans J. L. Jørgensen, Birgit Jensen and David B. Collinge, University of Copenhagen, Denmark

1 Introduction 232 Fusarium epidemiology and distribution 243 Disease cycle and infection 254 Host–pathogen interaction 275 Genetic resistance 286 Mycotoxins 297 Yield and quality losses 318 Disease management 319 Future trends 34

10 Conclusion 3511 Acknowledgements 3612 Where to look for further information 3613 References 37

3 Diseases affecting wheat: Septoria tritici blotch 47S. B. Goodwin, USDA-ARS, USA

1 Introduction 472 Use of fungicides for controlling STB 493 Breeding for increased resistance to STB 534 Understanding the molecular basis of the host–pathogen interaction 58

vi Contents


5 Conclusion and future trends 606 Where to look for further information 617 References 62

4 Diseases affecting wheat and barley: powdery mildew 69Javier Sánchez-Martín, Salim Bourras and Beat Keller, University of Zürich, Switzerland

1 Introduction 692 The biology of the powdery mildew disease 703 Agricultural management strategies to control mildews 724 Race-specific resistance: new approaches for fast gene

isolation in wheat and barley 745 Quantitative disease resistance: identification of partially acting

resistance genes and first insights into their molecular mechanism 786 Recent insights into the molecular basis of race-specific resistance

against Blumeria graminis 807 Case study: identification, functional characterisation and

applications of the Pm3 wheat powdery mildew resistance genes in wheat breeding 81

8 Future directions 839 Where to look for further information 84

10 References 85

5 Diseases affecting wheat: tan spot 95C. S. Moffat, Curtin University, Australia; and F. M. Santana, Embrapa Trigo, Brazil

1 Introduction 952 Disease management considerations 973 The host–pathogen interaction 1004 The genetics of host resistance 1015 Case study: ToxA-assisted breeding for tan spot resistance in Australia 1026 Conclusion and future trends 1037 Where to look for further information 1048 References 104

6 Diseases affecting wheat: Septoria nodorum blotch 109A. K. Ruud and M. Lillemo, Norwegian University of Life Sciences, Norway

1 Introduction 1092 Parastagonospora nodorum – the causal agent

of Septoria nodorum blotch 1123 Disease management 1144 The genetics of resistance 1155 Genetic mapping of resistance and use of markers in breeding 1216 A case study on SNB resistance in Norwegian wheat 1277 Conclusion and future trends 1338 Where to look for further information 1349 References 134


Contents vii

7 A lesser-known pathogen of wheat: Bipolaris sorokiniana 145E. Hill and P. Solomon, The Australian National University, Australia

1 Introduction 1452 Geographic distribution of disease 1463 How does B. sorokiniana cause disease in wheat? 1474 Pathogenic variability 1475 Disease management 1486 Conclusion and future trends 1507 References 150

8 Diseases affecting wheat: wheat blast 155J. L. N. Maciel, Embrapa Wheat, Brazil

1 Introduction 1552 Symptoms and conditions for wheat blast development 1563 Origin of wheat blast 1564 Reproductive biology of Magnaporthe oryzae 1575 The new causal agent of wheat blast: Pyricularia graminis-tritici 1576 Alternatives for survival of the causal agent 1587 Genetic control 1608 Chemical control 1629 Conclusion and future trends 164

10 References 164

9 Diseases affecting barley: net blotches 171Simon R. Ellwood, Curtin University, Australia; and Hugh Wallwork, South Australian Research and Development Institute, Australia

1 Introduction 1712 Control measures for net blotch 1733 Host–pathogen genetic interactions 1744 Case study: breeding for durable resistance to the net form of net

blotch in South Australia 1765 Summary and future trends in research 1786 Where to look for further information 1787 References 179

10 Diseases affecting barley: scald 183Wolfgang Knogge, Leibniz Institute of Plant Biochemistry, Germany

1 Introduction 1832 History, origins and general characteristics of scald 1843 Haplotypes, virulence variation and recombination 1884 Resistance genetics and mechanisms 1905 Host specificity, effector proteins and agricultural consequences of

fungal biology 1996 Crop protection and management 2027 Conclusion 2048 Where to look for further information 2059 References 205

viii Contents


Part 2 Key challenges in integrated disease management of cereals

11 Challenges and prospects for fungicidal control of wheat diseases 219R. J. Bryson and H-D. Brix, BASF SE, Germany

1 Introduction 2192 Global wheat production 2203 Crop loss, plant health and the value of fungicide applications 2224 Evolution of the pesticide regulatory environment 2245 Status of the global fungicide market 2256 Conclusion and future trends 2317 References 231

12 Occurrence and avoidance of fungicide resistance in cereal diseases 235Lise Nistrup Jørgensen, Aarhus University, Denmark; Richard Peter Oliver, Curtin University, Australia; and Thies Marten Heick, Aarhus University, Denmark

1 Introduction 2352 Key fungicide classes for the control of cereal diseases 2373 Cases of fungicide resistance 2394 Mechanisms of resistance 2395 Elements of anti-resistance strategies 2446 Farmers’ and advisors’ perspectives 2517 Where to look for further information 2528 References 252

13 Trends in exploring wheat and barley germplasm for novel disease resistance traits 261Sambasivam Periyannan, Australian National University, Australia; and Lee Hickey, University of Queensland, Australia

1 Introduction 2612 Advances in phenotyping germplasm for disease resistance 2623 Advances in genomics for discovery of disease resistance loci 2644 Conclusion and future trends 2665 Where to look for further information 2676 References 267

14 Developments in diagnostic techniques for cereal pathogens 271Sadia Iqbal and Michael G. K. Jones, Western Australian State Agricultural Biotechnology Centre - Murdoch University, Australia

1 Introduction 2712 Prevention strategies and pre-symptom identification 2723 Protein-based identification and serological methods 2744 Nucleic-acid-based techniques 2755 Point-of-care diagnostics 2786 Next-generation sequencing for plant diagnostics 2807 Non-invasive imaging techniques 2808 Conclusions 2819 Where to look for further information 282

10 References 283


Contents ix

15 Natural antifungal compounds for the control of diseases in wheat and other cereals 289A. Schouten, Wageningen University, The Netherlands

1 Introduction 2892 Plant defence compounds 2903 Outsourcing defences: recruiting soil microbes 2964 Facilitating the outsourcing of defences 3005 Resistance to microbial antagonism 3026 Conclusions and future trends 3037 Acknowledgements 3058 Where to look for further information 3059 References 306

16 The role of crop rotation, intercropping and tillage practices for foliar disease management of wheat and barley 317T. K. Turkington, Agriculture and Agri-Food Canada, Canada; K. Xi, Alberta Agriculture and Forestry, Canada; and H. R. Kutcher, University of Saskatchewan, Canada

1 Introduction 3172 Increasing temporal diversity: crop rotation 3183 Increasing spatial diversity: intercropping 3224 Increasing genetic diversity: gene deployment 3235 The role of conservation tillage 3246 Conclusions and future trends 3287 Where to look for further information 3298 References 330

Index 339


IntroductionDiseases remain a serious problem in wheat and barley cultivation. It has been estimated that around 20% of global crop production is lost to diseases. Leading fungal diseases affecting wheat and barley include rusts, Septoria blotches, powdery mildew, tan spot, spot blotch, net blotch, scald and Fusarium species. Conventional control using fungicides faces a number of challenges such as increasing regulation and the spread of fungicide resistance. The chapters in this volume sum up the wealth of research addressing this challenge. The volume reviews key recent research on the main fungal diseases, their modes of infection and potential strategies for dealing with them. The volume also looks at key challenges in developing integrated approaches to disease management, from breeding more resistant varieties to improved identification of disease and the use of natural antifungal compounds.

Part 1 Fungal diseases of cereals

The first part of the volume reviews the latest research on understanding the main fungal diseases of cereals. Chapter 1 examines rusts affecting wheat and barley. The chapter explores the incidence and impact of wheat and barley rust diseases. The chapter then examines genes for rust resistance and the pathogen biology of rusts, before going on to consider integrated methods of rust control. Finally, the chapter addresses the challenge of achieving durable resistance to rusts in wheat.

Moving from rusts to another class of fungal diseases, Chapter 2 considers the biology and management of Fusarium diseases. The chapter reviews yield and quality losses caused by Fusarium. It then summarises recent findings on Fusarium-cereal interactions, mode of infection and host-plant responses. The chapter then discusses the way this understanding can be used to improve integrated disease management of Fusarium. As well as assessing what we know about understanding and improving genetic resistance, it also discusses work to identify new fungicide molecules that aim for specific fungal metabolic pathways during infection at an early stage. The chapter also discusses the effectiveness of integrated management techniques such as ways to prevent initial infection, changes to tillage and fertilization practices, the role of rotations, more targeted use of fungicides and the use of biological control agents. Finally, the chapter also reviews what we know about the mycotoxins produced by Fusarium fungi and what can be done to reduce them.

The subject of Chapter 3 is Septoria tritici blotch (STB), a fungal disease affecting wheat. STB is one of the most common and economically-important diseases of wheat worldwide. Fungicides have been the primary means of disease management since the 1980s, but resistance has rendered some compounds ineffective. Qualitative or quantitative resistance genes have now been found on all 21 wheat chromosomes, giving a rich but complex source of genes for plant improvement. Molecular markers are now available for many resistance genes making marker-assisted selection for increased resistance an achievable goal for the future. The first STB resistance gene has now been cloned but the mechanism of resistance remains a mystery. Despite the huge progress made during the past twenty years, STB remains a difficult disease that is likely to require substantial future efforts for its control. Building on the latest research on host-pathogen interactions,


Introduction xvii

the chapter evaluates current methods of disease management, particularly in improving resistance, ongoing challenges and future trends in managing the disease.

Chapter 4 moves on to consider the characteristics and effects of powdery mildew. Powdery mildew pathogens are among the most important cereal disease-causing organisms, and can result in significant losses in yield and reductions in grain quality. They pose a significant challenge for barley and wheat agricultural production systems. The chapter provides an overview of current knowledge on wheat and barley resistance to powdery mildew. The chapter discusses current research on disease biology and epidemiology and how a better understanding of the basic molecular mechanisms of cereal-mildew interactions can be used in disease management. The chapter reviews the efficacy of management techniques. These include altering seeding rates and irrigation to create a more open crop canopy structure and less disease-conducive micro-climate, splitting nitrogen applications, removing volunteer plants, more targeted use of fungicides as well as the potential the use of biopesticides. A particular focus is improving resistance. The chapter reviews new approaches for fast gene isolation in wheat and barley, the identification of resistance genes and research into the molecular mechanisms underlying resistance. The chapter includes a case study on the identification, functional characterization and applications of the Pm3 wheat powdery mildew resistance genes in wheat breeding.

The next fungal disease of wheat to be considered, in Chapter 5, is tan spot. The chapter focuses on disease management, including cultural practices, chemical control, and the impact of the choice of wheat varieties. The chapter presents a detailed case study of the management of tan spot in Brazil, and considers the importance of host-pathogen interactions and the genetics of host resistance. Finally, the chapter includes a case study of ToxA-assisted breeding for tan spot resistance in Australia.

The focus of Chapter 6 is Septoria nodorum blotch. The chapter describes the causal agent of Septoria nodorum blotch, the fungus Parastagonospora nodorum, and outlines methods of disease management. The chapter examines genetic factors that produce resistance to Septoria nodorum blotch, and explains the process of the genetic mapping of resistance and the use of markers in breeding. Finally, the chapter presents a detailed case study on resistance to Septoria nodorum blotch in Norwegian wheat. Moving on to a lesser-known pathogen of wheat, Chapter 7 considers the challenge posed by Bipolaris sorokiniana. The chapter describes the geographic distribution of the disease and describes how Bipolaris sorokiniana causes disease in wheat, focusing on the fungus’s pathogenic variability as well as methods of disease management.

Chapter 8 considers wheat blast, describing the characteristics, origin and survival of this fungus, based on the experience of managing the disease in Brazil (where losses are particularly high). The chapter describes the disease’s origin, disease symptoms and conditions for wheat blast development, and the latest research on its causal agent. Finally, the chapter considers both genetic and chemical control options for wheat blast. The subject of Chapter 9 is net blotches. The chapter addresses the available control measures for net blotch, considering host-pathogen genetic interactions in both the spot and net forms of net blotch. The chapter includes a detailed case study on the subject of breeding for durable resistance to the net form of net blotch in South Australia.

The final chapter of the section, Chapter 10, deals with scald (leaf blotch), which is caused by the hemi¬biotrophic pathogen Rhynchosporium commune. Scald is one of the major diseases of barley worldwide. The chapter reviews the origins, epidemiology and other characteristic features of scald, and considers the agricultural consequences of the

xviii Introduction


pathogen’s biology. The chapter then considers resistance breeding programs, in which more than a dozen major resistance genes as well as quantitative trait loci (QTLs) have been identified, and discusses strategies to minimize the damage caused by the disease, including agricultural practices and combinations of different fungicides.

Part 2 Key challenges in integrated disease management of cereals

The second part of the volume discusses key challenges in integrated disease management of wheat and barley. These challenges include developing new fungicides, the problem of fungicide resistance, breeding disease-resistance varieties, improving disease identification and the use of natural antifungal compounds. The focus of Chapter 11 is the key challenges in developing new fungicides to treat cereal diseases. The chapter considers the current status of global wheat production, the impact of crop loss on food security, and the emergence of the current regulatory environment surrounding pesticides. The chapter then discusses the current status of the global fungicide market, and some of the major issues in its future longevity: the development of resistance to active ingredients, the impact of legislation that may restrict or remove active ingredients from the market, and the rising costs of developing new active ingredients.

Chapter 12 moves on to examine the occurrence of fungicide resistance in cereal diseases and ways to avoid it. The targeted use of fungicides can help minimise the yield losses caused to grain cereals by plant pathogenic fungi. However, the long-term use of fungicide classes based on a single mode of action has imposed consistent selection pressures on certain pathogens. Over time, this has resulted in many cases of fungicide resistance, leading to a reduction or the total loss of field performance of a range of active ingredients. There is a pressing need to develop better anti-resistance management strategies. The chapter briefly reviews the development of resistance in cereal pathogens, before presenting and evaluating a variety of anti-resistance strategies. The chapter includes detailed case studies of how data from field trials have helped to illustrate the effectiveness of different control strategies.

Complementing the previous chapter’s focus on breeding for resistance, Chapter 13 concentrates on improving genetic resources in the breeding of disease-resistant varieties of wheat and other cereals. The chapter highlights recent advances in phenotyping, genotyping and other breeding technologies that have the potential to speed up the discovery and utilization of new sources of disease resistance for wheat and barley. Technologies covered in the chapter include Focused identification of germplasm strategy (FIGS), speed breeding, Genome wide association studies (GWAS) and Genomic selection (GS).

The focus of Chapter 14 is the improvement of diagnostic techniques for disease identification in wheat and other cereal crops. Cereal pests and diseases can significantly reduce potential crop yields. Correct and timely identification in-field is key to their control. The chapter summarises and evaluates some of the many available methods for detection of pests and diseases, ranging from classical methods of plant pathology, such as visual or microscopic recognition, to new DNA sequencing technologies. The chapter discusses how protein-based diagnostics that rely on specificity of antibodies, such as variations on ELISA detection and dipstick or lateral flow devices, have been extended to protein


Introduction xix

profiling by MALDI-TOF mass spectrometry. Nucleic acid-based amplification techniques using various forms of PCR are also now widely implemented, including isothermal amplification and in field pathogen detection. The chapter shows how the molecular diagnostic techniques are being rapidly supplemented with image-based diagnostics, which rely on hyperspectral imaging, applied via satellites or drones for regional or field scale monitoring of disease incidence and progression.

Moving from diagnostic techniques to disease control, Chapter 15 examines the role of natural antifungal compounds in controlling diseases in wheat and other cereals. Secondary metabolites are essential when considering the ecological context in which an organism operates. They have an array of functions, related to signalling and dealing with biotic and abiotic stress situations. For defence against pathogenic fungi, plants can synthesise various metabolites. Wheat, like several other cereals, produces various benzoxazinoids which are also associated with herbicide detoxification and the defence against herbivores and microorganisms. Apart from these benzoxazinoids, wheat seems to produce only a limited number of other metabolites with known antifungal activity when compared to other cereals. Nevertheless, wheat is still capable of successfully defending itself against pathogenic fungi by outsourcing its defences, i.e. through the mobilization of the microbial community. The chapter provides an overview of the way in which these natural antimicrobial compounds contribute to the defence of wheat against fungal pathogens, as well as considering the counter defensive actions undertaken by some of those fungal pathogens.

The volume’s final chapter, Chapter 16, continues the theme of disease management by examining the role of tillage practices, rotations and intercropping in combatting diseases of wheat and other cereals. The great majority of modern agroecosystems comprise rotations of a small number of crop species where each year’s crop is a genetically uniform monoculture. The narrow genetic basis for disease resistance in modern cultivars increases the potential for pathogens to overcome this resistance and attack a large number of plants at a similar state of development. The chapter presents a number of strategies for limiting foliar disease development in wheat and barley. The chapter discusses how crop rotations with non-cereal species can substantially reduce inoculum sources for residue-borne cereal leaf diseases. The chapter then examines other strategies, such as intercropping, gene deployment and conservation tillage. The chapter discusses the effectiveness of each strategy against particular foliar diseases. The chapter concludes that there is potential for residue-borne cereal leaf diseases to be managed under conservation tillage via crop rotation, fungicide application and careful choice of variety.


Index2,4-diacetylphloroglucinol (DAPG) 299, 3022,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one

(DIMBOA) 290, 293, 3022-acetamidophenol (BOA-X) 293–2942-hydroxy-2-1,4-benzoxazin-3-one (HBOA) 2914-HBA. see 4-hydroxybenzoic acid (4-HBA)4-hydroxy-3-methoxycinnamic acid 295–2964-hydroxybenzoic acid (4-HBA) 3045-hydroxytryptamine 2946-amino-5-oxocyclohex-2-ene-1-carboxylic acid

(AOCHC) 2987NSK2 30314 α-demethylase 33, 34, 51, 115, 173, 202,

242, 24718-Terena cultivar BR 161

ABC. see ATP binding cassette (ABC)Abscisic acid 28ACM941 33Adult plant resistance (APR) genes 8, 9–10, 12,

13, 78, 120Aegilops ventricosa 162AFLP analysis 172AgriBio. see Centre for AgriBioscience (AgriBio)Agriculture and Horticulture Development

Board (AHDB) 203, 246Agroecosystems 73, 317, 328AgWest Plant Laboratories 273AHDB. see Agriculture and Horticulture

Development Board (AHDB)Airborne biological agents 272AK toxin 116Allelopathy 289–290All stage resistance (ASR) genes 8, 12, 13Altar C84 6Alternaria alternata 116Aminophenoxazines 293–294AMs. see Arbuscular mycorrhizae (AMs)Antifungal compounds for disease control

description 289–290facilitating outsourcing of defences 300

adaptation of antagonists 301–302outsourcing defences 296–297

2,4-diacetylphloroglucinol (DAPG) 299cyclic lipopeptides (CLPs) 299–300phenazine-1-carboxylic acid (PCA)

298–299pyrrolnitrin 300

plant defence 2904-hydroxy-3-methoxycinnamic acid

295–296benzoxazinoids 291–294serotonins 294–295

resistance to microbial antagonism 302–303

AOCHC. see 6-amino-5-oxocyclohex-2-ene-1-carboxylic acid (AOCHC)

APR. see Adult plant resistance (APR) genesArbuscular mycorrhizae (AMs) 304Area under the disease progress curve

(AUDPC) 145Ascogonium 157Ascomycota 185–186Ascospores 70, 96, 112–113Asexual conidia 25, 26, 71Asexual spores 25, 26, 96ASR. see All stage resistance (ASR) genesAssociation mapping (AM). see Genome-wide

association mapping study (GWAS)Atlas 46 cultivar 190ATP binding cassette (ABC) 52AUDPC. see Area under the disease progress

curve (AUDPC)Australian Cereal Rust Control Program 273Australian Grains Research and Development

Corporation 273Autophagy mechanisms 27Avirulence genes 55Avr1-CO39 avirulence gene 162Avr gene 74AvrPm2 gene 80AvrR-R gene pairs 84Avr-R-Svr interaction 80–81Azoles. see Demethylation inhibitor (DMI)

Bacillus amyloliquefaciens 34Bacillus megaterium 34Barley net blotch (BNB) 250BASF 245Benzoxazinoids

antifungal activities in wheat, maize and rye 293

fungal defences and microbial antagonism 293–294

Bioaerosols. see Airborne biological agentsBioinformatics tools 118‘BIO PCR’ 276Biopesticides 73–74Bipolaris sorokiniana 145, 146, 147–148

cause 147description 145geographic distribution 146–147management 148–150pathogenic variability 147–148

Black Hulless. see rpgBH/rpgS geneBlack rust. see Stem rust, of wheatBlumeria graminis

as causal agent 70–72race-specific resistance against 80–81

BNB. see Barley net blotch (BNB)BOA-X. see 2-acetamidophenol (BOA-X)Bobwhite wheat cultivar 29Brown rust. see Leaf rust, of wheatBulgaria 88 cultivar 55

Index340


CA. see Comparative Assessment (CA)CAN. see Cooperative Assays Network (CAN)Candidate for substitution (CfS) 228Carbendazim 51Carbohydrate-Activated Enzymes

(CAZymes) 27Carboxin 240CAZymes. see Carbohydrate-Activated Enzymes

(CAZymes)CCG. see Cylindrical conidia group (CCG)cDNA-AFLP profiling experiment 60Centre for AgriBioscience (AgriBio) 279Cerall® 34Cereal pathogens, diagnostic techniques for

description 271–272next-generation sequencing 280non-invasive imaging 280

‘Plantix’ 281nucleic-acid-based techniques

fluorescence-based PCR assays 278PCR-based assays 276in situ hybridization (ISH) 278

point-of-carehelicase-dependent amplification

(HDA) 279–280loop-mediated isothermal amplification

(LAMP) 279prevention strategies and pre-symptom

identificationmorphological 273visual 273

protein-based identification and serological methods

based on characteristic proteins 274–275CfS. see Candidate for substitution (CfS)Chasmothecia 70Chlamydospores 25Chlorosis 100, 120Chlorothalonil 49CI10587 genotype 10CIMMYT germplasm 6, 130, 149CLPs. see Cyclic lipopeptides (CLPs)Cochliobolus victoriae 116Common root rot (CRR) 145, 146, 147Comparative Assessment (CA) 228, 249Conidiophores 71Cooperative Assays Network (CAN) 163CPPs. see Crop protection products (CPPs)CRISPR/Cas9 34, 83–84Crop debris management 97Crop monoculture 318Crop protection products (CPPs) 225, 231Crop rotation 98, 114, 328Cross-protection 322CRR. see Common root rot (CRR)‘Cut-off criteria’ 227–228Cyclic lipopeptides (CLPs) 297, 299–300Cylindrical conidia group (CCG) 185, 199

CYP51. see 14 α-demethylaseCytB gene 240Cytochrome b (Cyt-b) gene 164

DAPG. see 2,4-diacetylphloroglucinol (DAPG)DArT. see Diversity Arrays Technology (DArT)Demethylation inhibitor (DMI) 32, 51, 52, 115,

202, 237, 240, 242–243Deoxynivalenol (DON) 27, 29, 30, 31Department of Agriculture and Fisheries 273Department of Agriculture and Food 173Department of Primary Industries, Parks, Water

and Environment 273Department of Primary Industries and Regional

Development 273DHs. see Double haploids (DHs)DIBOA 291, 293DIMBOA. see 2,4-dihydroxy-7-methoxy-1,

4-benzoxazin-3-one (DIMBOA)Directive 91/414/EEC 227Disease-forecasting systems 272‘The disease triangle’ model 72Diversity Arrays Technology (DArT) 57, 265DMI. see Demethylation inhibitor (DMI)DNA marker technologies 12DON. see Deoxynivalenol (DON)Double haploids (DHs) 121DOW AgroSciences 245Drinking Water Directive 1998/83/EC 249

EC. see European Commission (EC)EC 1107/2009 227, 231, 248, 249ECM. see Extracellular matrix (ECM)Effector-triggered immunity (ETI) 118, 119Enzyme-linked immunosorbent assay

(ELISA) 274–275Ergosterol 202ETI. see Effector-triggered immunity (ETI)EU 28. see European Union (EU) 28EU Directive 91/414/EEC 227European Commission (EC) 248European Union (EU) 28 221Extended rotations 318Extracellular matrix (ECM) 147

FAO. see Food and Agriculture Organization (FAO)

FAO-LEX 225Farm Economy: A Cyclopedia of Agriculture

for the Practical Farmer and His Family 329

Farrer, William 12FCR. see Fusarium crown rot (FCR)Ferulic acid. see 4-hydroxy-3-methoxycinnamic

acidFGSC. see Fusarium graminearum species

complex (FGSC)FHB. see Fusarium head blight (FHB)


Index 341

FIGS. see Focused identification of germplasm strategy (FIGS)

FISH. see Fluorescence In Situ Hybridization (FISH)

Flor, H. H. 53Fluorescence In Situ Hybridization (FISH) 278Focused identification of germplasm strategy

(FIGS) 82, 262–263Foliar disease management

conservation tillage 324–327crop rotation 318

limiting cereal leaf diseases 319–321description 317–318genetic diversity 323–324intercropping 322–324

Foliar fungicides 174, 177Food and Agriculture Organization (FAO) 225‘Formae speciales’ 70FRAC. see Fungicide Resistance Action

Committee (FRAC)FRAG. see Fungicide Resistance Action Group

(FRAG)Fungicidal control of wheat diseases

crop loss, plant health and value 222–224description 219–220global fungicide market

developing fungicide active ingredients 228–231

European regulatory environment and its impact 227–228

resistance and its impact 226–227global wheat production 220–221pesticide regulatory environment 224–225

Fungicide Resistance Action Committee (FRAC) 237

Fungicide Resistance Action Group (FRAG) 237Fungicide resistance in cereal diseases

anti-resistance strategiesalternative control measures 250–251field trials 246–247need for disease control agents 248–249regulatory constraints 249–250

cases 239description 235–237Farmers’ and advisors’ perspectives

251–252fungicide classes for control 237–239mechanisms

DMI 242–243due to efflux pump overexpression

243–244enhanced gene expression 243QoI 240SDHI 240target site mutations 239–240

Fungicides 11, 24, 32–33, 61, 73, 98–99, 149–150, 202–204

Fusarium avenaceum 25

Fusarium crown rot (FCR) 23, 25, 26, 27, 28, 31, 32, 33, 34

Fusarium culmorum 25, 33Fusarium diseases

cycle and infection 25–26description 23–24epidemiology and distribution 24–25genetic resistance 28–29host–pathogen interaction 27–28management

agricultural practices 31–32biological control 33–34fungicides 32–33

mycotoxins 29–30yield and quality losses 31

Fusarium graminearum 24–25, 27, 28, 30, 33Fusarium graminearum species complex

(FGSC) 24Fusarium head blight (FHB) 23, 25, 27, 28, 31,

32, 34, 293Fusarium root rot. see Fusarium crown rot (FCR)

G143A Cyt-b gene mutation 164, 173, 203G143A translated protein 52Gaeumannomyces graminis var. tritici 293, 297GBS. see Genotyping-by-sequencing (GBS)Gene deployment 323–324Gene-for-gene relationship/model 53, 74Gene isolation, in wheat and barley 74–78Gene pyramiding 75Genetics 11

diversity 318, 323–324mapping 174

Genome-wide association mapping study (GWAS) 56, 57, 83, 132, 174, 265

Genomic selection (GS) 265–266, 265–266Genotyping-by-sequencing (GBS) 121Germplasm for disease resistance

description 261–262genomics

allele mining 266genome-wide association studies

(GWAS) 265genomic selection (GS) 265–266identification of markers and linkage

maps 266phenotyping

focused identification of germplasm strategy (FIGS) 262–263

high-throughput screening 263–264speed breeding 263

Germplasm screening approach 102Gibberellic acid 28Golden Promise cultivar 199Green bridge 3, 319Grenelle programme 227Growth-stage-specific resistance 78GS. see Genomic selection (GS)

Index342


GWAS. see Genome-wide association mapping study (GWAS)

Hanna X Atlas 201HBOA. see 2-hydroxy-2-1,4-benzoxazin-3-one

(HBOA)HDA. see Helicase-dependent amplification

(HDA)Head scab. see Fusarium head blight (FHB)Helicase-dependent amplification (HDA)

279–280Helminthosporium leaf blight (HLB) 146,

148–149Helminthosporol toxins 147Hexahydrophenazine-1,6-dicarboxylic acid

(HHPDC) 298HIGS. see Host-Induced Gene Silencing (HIGS)HLB. see Helminthosporium leaf blight (HLB)Hordeum spontaneum 262Hordeum vulgare 69, 171, 183, 184, 235,

261, 262Host-Induced Gene Silencing (HIGS) 34Host-specific toxins (HSTs) 116HPMA. see N-(2-hydroxyphenyl) malonamic acid

(HPMA)HSTs. see Host-specific toxins (HSTs)Hybridisation event 70

IAA. see Indole acetic acid (IAA)IK726 33Illumina iSelect 90K wheat SNP chip 131, 132Image recognition technology 281InatreqTM 245Indole acetic acid (IAA) 304Induced systemic resistance (ISR) 303In situ hybridization (ISH) 278Internal transcribed spacer (ITS) 276International Allelopathy Society 289International Centre for Agricultural Research in

the Dry Areas 263International Code of Conduct on Pesticide

Management: Guidelines on Pesticide Legislation 225

International Code of Conduct on the Distribution and Use of Pesticides 225

International Wheat Genome Sequencing Consortium 76

ISH. see In situ hybridization (ISH)ISR. see Induced systemic resistance (ISR)ITS. see Internal transcribed spacer (ITS)

Jasmonate (JA) pathway 28, 29

Kompetitive Allele Specific PCR (KASP) 121

Lactobacillus plantarum 34LAMP. see Loop-mediated isothermal

amplification (LAMP)

Land equivalent ratios (LER) 323Laser desorption/ionization Fourier transform

ion cyclotron resonance mass spectrometric imaging (LDI-FT-ICR-MSI) 305

LDI-FT-ICR-MSI. see Laser desorption/ionization Fourier transform ion cyclotron resonance mass spectrometric imaging (LDI-FT-ICR-MSI)

Leaf blotch. see ScaldLeaf infiltration effector assays 102Leaf rust, of wheat 6Leaf tip necrosis 12LER. see Land equivalent ratios (LER)Leucine-rich repeats (LRRs) 119Loop-mediated isothermal amplification

(LAMP) 279Lr12 gene 9Lr27 and Lr31 genes 9Lr34 and Lr67 genes 80LRRs. see Leucine-rich repeats (LRRs)

Macroconidia 25Magnaporthe grisea 13Magnaporthe oryzae 155, 156–157, 158,

159–161, 163–164Major facilitator superfamily (MFS) 52, 243MALDI-TOF. see Matrix-assisted laser

desorption/ionization-time of flight (MALDI-TOF)

Malonichrome 27Mancozeb 49Marker-assisted selection (MAS) 10, 84, 127Marker-trait associations (MTAs) 126, 132Marsonia/Marssonina secalis 184MAS. see Marker-assisted selection (MAS)Mass spectroscopy 275Matrix-assisted laser desorption/ionization-time

of flight (MALDI-TOF) 274, 275MBC. see Methyl benzimidazole carbamate

(MBC)MDR. see Multidrug resistance (MDR)Methyl benzimidazole carbamate (MBC) 51,

202, 226, 237MFS. see Major facilitator superfamily (MFS)MgMFS1 gene 52, 243MIC. see Minimal inhibitory concentration (MIC)Microconidia 25Mildewcides 239Mildew resistance locus A (Mla) 74Minimal inhibitory concentration (MIC) 299Mixed reproduction system 112–113Mlo gene 78Molisch, H. 289MTAs. see Marker-trait associations (MTAs)Multidrug resistance (MDR) 52, 243Multilines/mixtures strategy 75Mutagenesis 77


Index 343

Mutant Chromosome Sequencing (MutChromSeq) 77

Mutational genomics 77MutChromSeq. see Mutant Chromosome

Sequencing (MutChromSeq)MutRenSeq 77Mycosphaerella graminicola. see Zymoseptoria

triticiMycotoxin 24, 25, 29–30

N-(2-hydroxyphenyl) malonamic acid (HPMA) 293

National Action Plan 249Natural ecosystem 318Naxos wheat cultivar 131NBS. see Nucleotide binding site (NBS)Necrosis 100, 120Necrosis-inducing peptides (NIP) 198, 199Necrotrophic effectors (NEs) 116–120, 127Necrotrophic phase 27Necrotrophs 58NEs. see Necrotrophic effectors (NEs)Net blotches

control measures 173–174description 171–173host–pathogen genetic interactions

net form of net blotch (NFNB) 175–176spot form of net blotch (SFNB) 174–175

resistance to NFNB in South Australia 176–178

Net form of net blotch (NFNB) 171, 173, 174, 175–177

New South Wales Department of Primary Industries 273

Next-generation sequencing (NGS). see Genotyping-by-sequencing (GBS)

NFNB. see Net form of net blotch (NFNB)Nicotiana 83NIP. see Necrosis-inducing peptides (NIP)Nitrogen fertilizer rate 327Nivalenol (NIV) 30NLR. see Nucleotidebinding and leucine-rich

repeat (NLR)Nonribosomal peptide synthetases (NRPS) 299Norwegian wheat, SNB resistance in

effector sensitivities in field resistance 130–131

field testing methodologycorrection for confounding traits 128–130and seedling experiments 130

genetics in germplasm 131genome-wide association mapping study

(GWAS) 132QTL mapping 131

pathogen population 128results 132–133

NPR1 gene 29NRPS. see Nonribosomal peptide synthetases

(NRPS)

Nucleotidebinding and leucine-rich repeat (NLR) 12, 81

Nucleotide binding site (NBS) 119Numa Pompilius (King) 219

PacBio. see Pacific Biosciences (PacBio)Pacific Biosciences (PacBio) 118Padlock probe. see Rolling circle amplification

(RCA)PAMP. see Pathogen-associated molecular

patterns (PAMP)PAMP-triggered immunity (PTI) 118Parastagonospora avenae 110Parastagonospora nodorum 58, 109, 110, 128,

321Partially acting resistance genes and molecular

mechanism 78–80Pathogen-associated molecular patterns

(PAMP) 119Pathogenesis-related (PR) proteins 60Pathogen-specific quantitative-loop-mediated

isothermal amplification (qLAMP) 160PCA. see Phenazine-1-carboxylic acid (PCA);

Principal component analysis (PCA)P. coronata f. sp. hordei 7–8PCR. see Polymerase chain reaction (PCR)Pectin esterase inhibitor (PEI) 199Pectin methyl esterases (PMEs) 199PEI. see Pectin esterase inhibitor (PEI)Pesticide Authorisation Directive

91/414/EEC 248Pesticide load index (PLI) 227Pesticide Safety Precaution Scheme 225PFT. see Pore-forming toxin-like protein (PFT)P. graminis f. sp. tritici 4–5, 10–11Phenazine-1-carboxylic acid (PCA) 297,

298–299, 299PHL. see Prehelminthosporol (PHL)PhzA enzyme 298Pi21 gene 80Pi-CO39 (t) resistance gene 162‘PicoGreen’ assay 278Plant Pest Diagnostic Service 273PLI. see Pesticide load index (PLI)Pm8 rye-derived gene 76PMEs. see Pectin methyl esterases (PMEs)Poaceae 291Polymerase chain reaction (PCR) 101, 121, 272,

275–276based assays 276fluorescence-based 278

Polyversum® 34Pore-forming toxin-like protein (PFT) 29Powdery mildew disease

agricultural management strategies 72–74biology

causal agent 70–72geographical distribution and yield

losses 72

Index344


description 69–70gene discovery 83genome editing 83–84pangenome for wheat and barley 84pathogen-informed strategies 84Pm3 genes in wheat breeding

marker development and characterisation 81–82

molecular improvement based on functional diversity 82–83

transgenic wheat genotypes 83quantitative resistance (QR) 78–80race-specific resistance 74–78

against Blumeria graminis 80–81PR. see Pathogenesis-related (PR) proteinsP. recondita 6PreDicta B 273Prehelminthosporol (PHL) 148Primary Industries and Regions South

Australia 273Principal component analysis (PCA) 293Proquinazid 239Protein mass fingerprinting 275Protein profiling 275Pseudomonas chlororaphis 34Pseudomonas fluorescens 300–301P. striiformis f. sp. hordei 6–7P. striiformis f. sp. tritici 5, 11P. teres f. maculata (PTM) 171–172, 175PTI. see PAMP-triggered immunity (PTI)PTM. see P. teres f. maculata (PTM)Ptr effector 100–101P. triticina 6PTT. see Pyrenophora teres f. teres (PTT)Puccinia graminis 8Putrescine 27Pycnidiospores 112Pyrenophora teres 245, 250Pyrenophora teres f. teres (PTT) 171–172, 175Pyrenophora tritici-repentis 58, 95, 109, 110,

128, 321Pyricularia graminis-tritici 158–159, 160–161,

163–164Pyricularia oryzae. see Magnaporthe oryzaePyrrolnitrin 297Pythium oligandrum 34

Q2-87 strain 301Q8r1-96 strain 301Q21861. see Rpg5/RpgQ geneQFhb1-mediated resistance 29Qfhs.ndsu-3BS 29qLAMP. see Pathogen-specific quantitative-

loop-mediated isothermal amplification (qLAMP)

QoIs. see Quinone-outside inhibitors (QoIs)qPCR molecular techniques 197, 272QR. see Quantitative resistance (QR)

QTLs. see Quantitative trait loci (QTLs)Quantitative resistance (QR) 78–80, 201Quantitative trait loci (QTLs) 10, 28–29, 34, 56,

61, 79–80, 101, 120, 121, 126–127, 129, 131, 132, 173, 196–197, 201

Quinofumelin 239Quinone-outside inhibitors (QoIs) 52, 115, 173,

237, 240, 252Quinoxyfen 239

R. agropyri 185Ramularia collo-cygni 245, 250Ramularia leaf spot (RLS) 250RAPD markers 6, 172RCA. see Rolling circle amplification (RCA)Reactive oxygen species (ROS) 100Recombinant inbred lines (RILs) 121Recombinase Polymerase Amplification

(RPA) 279Regalia® 73Regulation (EC) No 1185/2009 251Renan wheat cultivar 161Resistance gene exome sequence capture

(RenSeq) 77Resistance management strategies 237Restriction fragment length polymorphism

(RFLP) 186, 189Reverse transcription PCR (RT-PCR) 276Revysol® 245RFLP. see Restriction fragment length

polymorphism (RFLP)R. graminicola 184Rhizobia 304Rhynchosporium commune 183, 185, 186,

188–189, 195, 197, 198, 200, 204RIDA®QUICK 275RIDASCREEN® 275RILs. see Recombinant inbred lines (RILs)RLS. see Ramularia leaf spot (RLS)RNA sequencing (RNA-seq) 59, 280Robigalia games 219Robigus (Roman God of Rust) 219Rolling circle amplification (RCA) 279Romulus (King) 219R. orthosporum 185ROS. see Reactive oxygen species (ROS)RPA. see Recombinase Polymerase Amplification

(RPA)Rpg5/RpgQ gene 9rpgBH/rpgS gene 9R. secalis 184–185RT-PCR. see Reverse transcription PCR (RT-PCR)‘Rust Bust’ programme 273Rust diseases

barleycrown 7–8leaf 7stem 8


Index 345

stripe 6–7description 3–4durable resistance 11

control in agriculture 12–13to leaf rust in barley 13

integrated methods of control 11pathogen biology 10–11resistance genes

barley leaf rust 9–10barley stem rust 9barley stripe rust 10wheat leaf rust 8–9wheat stripe rust 9

wheatleaf 6stem 4–5stripe 5

Salicylic acid (SA) pathway 28, 29SAR. see Systemic acquired resistance (SAR)SB. see Spot blotch (SB)Scald

agricultural consequences of fungal biology 200–201

description 183epidemiology 186–188fungicide-based crop protection 202–204haplotypes 188–190history and host specialization 184–186host specificity and effector proteins 199–200integrated crop protection

management 204origin and global migration 186resistance genetics 190, 195–197resistance mechanisms 197–199taxonomy and phylogeny 184–186virulence variation and recombination

188–190SCAR. see Sequence-characterized amplified

region (SCAR)SDHI. see Succinate dehydrogenase inhibitors

(SDHI)Secale cereale 184Seedling blight. see Fusarium crown rot (FCR)Septoria avenae blotch 110Septoria leaf spot complex 326, 327Septoria nodorum blotch (SNB)

description 109–110genetic mapping

association mapping 126genomic prediction and selection 127linkage 121, 126marker-assisted selection and resistance

breeding 126–127molecular markers 121

genetics of resistanceescape mechanisms and environmental

impacts 120

gene-for-gene models 116host-specific toxins (HSTs) 116nature and sensitivity genes 119–120necrotrophic effectors (NEs) 116–119sensitivity gene interactions in P.

nodorum–wheat pathosystem 117–119impacts 110–112management

agricultural practice 114fungicide control 115use of resistant cultivars 115

nomenclature 110Parastagonospora nodorum

life cycle and epidemiology 112–113symptoms 113–114

production of wheat 109resistance in Norwegian wheat

effector sensitivities in field resistance 130–131

field testing methodology 128–130genetics in germplasm 131pathogen population 128

Septoria nodorum leaf and glume blotch (SNB) 109, 126

Septoria tritici. see Zymoseptoria triticiSeptoria tritici blotch (STB) 109, 110, 246,

250, 321description 47–49host–pathogen interaction 58–60resistance to 53–58use of fungicides 49–53

Sequence-characterized amplified region (SCAR) 276

Serological test kits 275Sexual ascospores 25Sexual spores. see AscosporesSFNB. see Spot form of net blotch (SFNB)SIGS. see Spray-Induced Gene Silencing (SIGS)Simple-sequence repeat (SSR) 5, 57, 121Single-nucleotide polymorphisms (SNPs) 56,

121, 265, 266SNB. see Septoria nodorum leaf and glume

blotch (SNB)SNPs. see Single-nucleotide polymorphisms

(SNPs)SnTox1 gene 117, 118, 120, 130–131SnTox2-Snn2 120SnTox3 130–131SnTox3-Snn3 120, 131SnToxA gene 128, 130SnToxA-Tsn1 120Soil microbes 296–297Solid Phase Reversible Immobilization

(SPRI) 276South Australian Research and Development

Institute 273Splashing 25Spontaneous generation, concept of 219

Index346


Spot blotch (SB) 145, 146, 148–149Spot form of net blotch (SFNB) 171, 173,

174–175, 174–175Spray-Induced Gene Silencing (SIGS) 34SPRI. see Solid Phase Reversible Immobilization

(SPRI)Sr31, resistance genes 5SrTmp resistance gene 5SSR. see Simple-sequence repeat (SSR)START. see Steroidogenic acute regulatory

protein-related transfer (START)STB. see Septoria tritici blotch (STB)Stb1 gene 55Stb6 gene 60, 61Stb16q gene 56Stem rust, of wheat 4–5Steroidogenic acute regulatory protein-related

transfer (START) 12Stripe rust, of wheat 5Strobilurins. see Quinone-outside inhibitors

(QoIs)Succinate dehydrogenase inhibitors (SDHI) 52,

203, 225, 237–238, 240, 250Sumai 3 29SvrPm3a1/f1 suppressor allele 81Systemic acquired resistance (SAR) 29

TAFC. see Triacetylfusarinine C (TAFC)TaMLO homologues 79Tan spot 327

description 95–97genetics of host resistance 101–102host–pathogen interaction 100–101management

in Brazil 99–100chemical control 98–99cultural practices 97–98wheat variety choice 99

ToxA-assisted breeding in Australia 102–103TaqMan assays 278Targeting Induced Lesions IN Genomes

(TILLING) 79TASAG ELISA Testing Services 273Tebuconazole 243TEF1-α. see Translational Elongation Factor 1α

(TEF1-α)Thousand kernel weight (TKW) 145Tilletia 220TILLING. see Targeting Induced Lesions IN

Genomes (TILLING)TKTTF pathotype 5TKW. see Thousand kernel weight (TKW)

ToxA 100, 101–102, 117ToxB 100, 101ToxC 100–101Translational Elongation Factor 1α (TEF1-α)

276Triacetylfusarinine C (TAFC) 27Triademinol 243Triazoles. see Demethylation inhibitor (DMI)Trichodiene synthase 5 (Tri5) 27TRI enzymatic genes 27Triticum aestivum 3, 69, 109, 235, 261Triticum durum 3, 109Triticum monococcum 53Triticum turgidum 261Tsn1 host cells 118TTKSK, North American race designation 5Turk cultivar 190, 201Turk X Atlas 201

‘Ug99’ lineage 5Urochloa 158US Department of Agriculture (USDA) 263

Vada, Dutch cultivar 13Vavilov Institute of Plant Genetic Resources 263Victorin toxin 116

Wall-associated kinase (WAK) 119Water Framework Directive 2000/60/EC 249Wheat blast

alternatives for survivalinfection of wheat seeds 159–160infective activity 159saprophytic activity in wheat straw 160

chemical control 162–164description 155–156genetic control

resistance and molecular markers 162origin 156–157Pyricularia graminis-tritici 157–158reproductive biology of Magnaporthe

oryzae 157symptoms and conditions 156

Wheat scab. see Fusarium head blight (FHB)

Yellow rust. see Stripe rust, of wheatYr1–Yr76 genes 9, 10, 11

Zearalenone (ZEA) 30Zymoseptoria tritici 47, 51, 55, 56, 58–60, 109,

128, 224, 226, 243

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Transcript of Contents · Part 1 Fungal diseases of cereals 1 Diseases affecting wheat and barley: rusts 3 R. F....