Plant Relationships: Fungal-Plant Interactions

Series Preface
	The Mycota Series-2022
Volume Preface to the Third Edition
Contents
Editors and Contributors
Part I: Pathogenic Fungus-Plant Interactions
	1: Modulation of Host Immunity and Development by Ustilago maydis
		1.1 Ustilago maydis, the Causal Agent of Maize Smut Disease
			1.1.1 The Process of Infection
			1.1.2 Ustilago maydis Inside the Plant
			1.1.3 The Molecular Basis of Biotrophy
			1.1.4 The Infection Cycle Ends with Spore Formation
		1.2 Evolution, Structure, and Features of U. maydis Effectors
			1.2.1 The Clustered Occurrence of the Effectome
			1.2.2 Inter- and Intraspecific Effectome Differences
			1.2.3 Effectome Evolution
			1.2.4 Effectors and Their Impact on Pathogen Fitness
			1.2.5 The Effector Interactome
		1.3 Transcriptional Regulation of the U. maydis Effectome
			1.3.1 Early Regulators of Biotrophy
			1.3.2 Late Regulators of Biotrophy
			1.3.3 Post-Transcriptional Regulation of the Effectome and Its Transcriptional Feedback
			1.3.4 Spatial Regulation of the Effectome
			1.3.5 Host Accession Specific Effector Regulation
		1.4 The Molecular Functions of U. maydis Effectors
			1.4.1 Antimicrobial Effectors and Niche Protection
			1.4.2 Antimicrobial Secondary Metabolites of U. maydis
			1.4.3 Indirect Niche Protection by U. maydis?
			1.4.4 Intraspecific Competition of U. maydis
		1.5 Extracellular Plant Immunity Modulation by U. maydis
			1.5.1 The Apoplastic Battleground
			1.5.2 Interference with Pathogenesis-Related Plant Proteins
			1.5.3 Fungal Cell-Wall Associated Effectors
			1.5.4 Protease Inhibition as a Key Virulence Mechanism
		1.6 U. maydis Effectors with Intracellular Virulence Functions
			1.6.1 Salicylic Acid Signaling Manipulation by U. maydis
			1.6.2 Secondary Metabolism Manipulation
			1.6.3 Tumorigenic Effectors
			1.6.4 Functional Clusters of Effectors
			1.6.5 Maize Lipoxygenase 3, Susceptibility Factor and Effector Target
			1.6.6 Exploiting Growth Versus Defense Antagonism
			1.6.7 A Possible Translocation Machinery for Intracellular Effectors
		1.7 U. maydis as a Model System in the Post-Genomic Era
		References
	2: RNA Dialogues in Fungal-Plant Relationships
		2.1 Introduction
			2.1.1 Fungal-Plant Communication
			2.1.2 Regulatory Small RNAs and RNAi
			2.1.3 Fungal Extracellular RNAs
		2.2 Cross-Kingdom RNAi in Fungal-Plant Relationships
		2.3 RNA Translocation in Fungi and Plants
			2.3.1 Transport of mRNAs
			2.3.2 Fungal EVs and Their Function in RNA Transport
		2.4 RNAi-Based Applications for Antifungal Disease Control in Plants
			2.4.1 Host-Induced Gene Silencing in Fungal-Plant Interactions
			2.4.2 Spray-Induced Gene Silencing in Fungal-Plant Interactions
		2.5 Conclusions
			2.5.1 Fungal sRNA Effectors
			2.5.2 RNA Transport
		References
	3: The Role of Tox Effector Proteins in the Parastagonospora Nodorum-Wheat Interaction
		3.1 Introduction
		3.2 The Main Characters, Tox Genes and Their Partners
		3.3 Evolution and Diversity of Tox Genes in Globally Distributed Populations of P. nodorum
		3.4 Mechanistic Insights from Detailed Studies of Effector Proteins
			3.4.1 Target Wheat Immune Proteins
		3.5 Crystal Structures Provide Insights into Conserved Effector Folds and Processing
		3.6 Overall Conclusions and Outlook
		References
Part II: Mutualistic Fungus-Plant Interactions
	4: Genomes of Arbuscular Mycorrhizal Fungi
		4.1 Introduction
		4.2 Organization of the Genome
		4.3 Regulation of the Genome(s)
		4.4 Transmission of the Genome
		4.5 Perspectives on Adaptation and Evolution
		References
	5: Diversity of Seed Endophytes: Causes and Implications
		5.1 Introduction
		5.2 Taxonomy of Fungal Seed Endophytes and Host Plants
			5.2.1 Epichloë, Periglandula, and Relatives (Order Hypocreales)
			5.2.2 Alternaria and Relatives (Order Pleosporales)
			5.2.3 Morning Glory Endophytes of Order Chaetothyriales
		5.3 Seed-Endophyte-Host Interactions
			5.3.1 Host Compatibility
			5.3.2 Host Specificity
			5.3.3 Host Protection Against Herbivory
			5.3.4 Host Protection Against Abiotic Stresses
		5.4 Anti-herbivore Alkaloids
			5.4.1 Ergot Alkaloids, Including Ergovaline
			5.4.2 Indole-Diterpene Alkaloids, Including Lolitrems
			5.4.3 Pyrrolizidine Alkaloids, Including Lolines
			5.4.4 Pyrrolopyrazine Alkaloids, Including Peramine
			5.4.5 Indolizidine Alkaloids Including Swainsonine
		5.5 Evolutionary Relationships, Hybridization, Polyploidy, and Horizontal Gene Transfers
			5.5.1 Haploid Epichloë Species
			5.5.2 Polyploid Epichloë Species
			5.5.3 Hyphal Fusion and Karyogamy
			5.5.4 Horizontal Gene Transfer or Not?
		5.6 Relationship Between Epichloë Symbiosis and Host Plant Interaction with Herbivores
		5.7 Epichloë Control on Host Plant-Associated Symbiotic Microorganisms
			5.7.1 Endophyte-Mediated Host Interaction with AMF
			5.7.2 Endophyte-Mediated Host Protection Against Pathogens
			5.7.3 Epichloë Effects on the Plant Association with Non-systemic Fungal Endophytes
			5.7.4 Epichloë Effects on the Rhizosphere
		5.8 Endophyte Effects on Plant Population Dynamics
		5.9 Epichloë Effects on Communities and Ecosystem Processes
		5.10 Applications
			5.10.1 Natural Strains in Forage Grasses
			5.10.2 Genetically Altered Strains
			5.10.3 Symbiotically Modified Cereals
		References
	6: Lichens and Their Allies Past and Present
		6.1 Introduction
		6.2 Lichen-Forming Fungi (LFF)
			6.2.1 Gains and Losses of Lichenization
			6.2.2 Species Concepts and Phylogenies
			6.2.3 Species Pairs and Cryptic Species
			6.2.4 Morphodemes and Morphotype Pairs (= Photosymbiodemes)
			6.2.5 Non-lichen Mutualistic Fungal Interactions with Cyanobacteria and Unicellular Green Algae
			6.2.6 Mycophycobioses
			6.2.7 Secondary Metabolites
		6.3 Lichen Photobionts
			6.3.1 Diversity and Specificity
			6.3.2 Tripartite Lichens
			6.3.3 Cyanotrophy
		6.4 Peculiarities of Lichen Symbiosis
			6.4.1 A. Symbiotic vs. Free-Living LFF
			6.4.2 Morphogenetic Capacity of the Mycobiont
			6.4.3 The Mycobiont-Photobiont-Interface
			6.4.4 Water Relations and Gas Exchange
			6.4.5 Heavy Metal and Radionuclides
		6.5 The Microbiome of Lichen Thalli
			6.5.1 The Bacteriome: Bacterial Epi- and Endobionts of Lichen Thalli
			6.5.2 Lichenicolous Fungi
			6.5.3 Lichenicolous Lichens
			6.5.4 Endolichenic Fungi (ELF)
			6.5.5 The Virome of Lichens
		6.6 Fossil Lichens and Their Microbiome
			6.6.1 Fossil vs. Extant Lichens
			6.6.2 Palaeozoic Fossils
			6.6.3 Mesozoic Fossils
			6.6.4 Cenozoic Fossils
			6.6.5 The Microbiome of Fossil Lichens
		6.7 Lichen-Animal Relations
			6.7.1 The Micro- and Mesofauna of Lichen Thalli
			6.7.2 Lichenivory: Invertebrates
			6.7.3 Lichenivory: Vertebrates
			6.7.4 Endozoochory
			6.7.5 Epizoochory
		6.8 Lichenomimesis
			6.8.1 Lichenomimesis in Animals
			6.8.2 Lichenomimesis in Members of the Araceae (Flowering Plants)
		6.9 Conclusions and Outlook
		References
	7: Lichen Fungal Secondary Metabolites: Progress in the Genomic Era Toward Ecological Roles in the Interaction
		7.1 Introduction
		7.2 Lichen Mycobionts Produce a Unique Diversity of Bioactive Secondary Metabolites
			7.2.1 Lichen Secondary Metabolites Have Been Used for Their Biological Activities
			7.2.2 Biological Functions of Lichen Secondary Metabolites
			7.2.3 How Lichen Mycobionts Produce Secondary Metabolites
		7.3 The Genomes of Lichenized Fungi Have Revealed a Unique Potential for Polyketide Production
			7.3.1 A Decade of Mycobiont Genome Sequencing
			7.3.2 An Abundance of Polyketide Biosynthetic Pathways
			7.3.3 Linking Biosynthetic Gene Clusters to Known Lichen Compounds
		7.4 Heterologous Expression as a Strategy to Elucidate Lichen Biosynthetic Pathways
			7.4.1 Successful Expression of Lichen Polyketide Synthases in Saccharomyces cerevisiae
			7.4.2 Successful Expression of a Lichen Gene Cluster in Ascochyta rabiei
			7.4.3 Difficulties in Heterologously Expressing Lichen Polyketide Synthases in Aspergillus oryzae
			7.4.4 Indirect Studies Using Orthologous Pathways Provide Information About Potential Lichen Compounds
		7.5 Toward Understanding the Role of Mycobiont Secondary Metabolites in Lichen Ecosystems
			7.5.1 In vitro Reconstitution of Lichen Ecosystems
			7.5.2 Spatial Distribution of Mycobiont Secondary Metabolites
			7.5.3 Genetic Manipulation of Mycobionts
		7.6 Conclusion
		References
Part III: Sensing and Signalling in Fungus-Plant Interactions
	8: Regulation of Plant Infection Processes by MAP Kinase Pathways in Ascomycetous Pathogens
		8.1 Introduction
		8.2 The Pmk1/Kss1 Invasive Growth (IG) Pathway
			8.2.1 Regulation of Appressorium Formation by the PMK1 Pathway in M. oryzae
			8.2.2 Regulating the Formation of Various Infection Structures in Fungal Pathogens
			8.2.3 Invasive Growth After Penetration
			8.2.4 Sexual Reproduction
		8.3 The Cell Wall Integrity (CWI) MAPK Pathway
			8.3.1 Penetration and Infectious Growth
			8.3.2 Cell Wall Integrity and Hyphal Growth
			8.3.3 Hyphal Fusion and Parasexual Reproduction
		8.4 The High-Osmolarity Glycerol (HOG) Pathway
			8.4.1 Species-Specific Roles in Pathogenesis
			8.4.2 Osmoregulation and Survival
			8.4.3 Oxidative Stress
		8.5 Concluding Remarks
		References
	9: Role of pH in the Control of Fungal MAPK Signalling and Pathogenicity
		9.1 Ambient pH Sensing and Adaptation in Fungi
			9.1.1 Sensing and Adaptation to Alkaline Ambient pH: the Pal/Rim Pathway
			9.1.2 Sensing and Adaptation to Acid Ambient pH
			9.1.3 Modulation of Ambient pH and Its Role in Plant Pathogenicity
		9.2 Role of Cytosolic pH in Fungal Signalling and Pathogenicity
			9.2.1 Cytosolic pH Homeostasis
			9.2.2 Role of pHc in Signalling and Cell Growth
			9.2.3 Cytosolic pH As a Regulator of Fungal Pathogenicity
		9.3 Conclusions
		References
	10: Role of Volatile Organic Compounds in Establishment of the Trichoderma-Plant Interaction
		10.1 Trichoderma: Multifaceted Plant Symbionts
		10.2 Volatile Organic Compound Profiling of Trichoderma
		10.3 Trichoderma Genes for Volatile Organic Compound Emission
		10.4 Plant Responses to Trichoderma Volatile Organic Compounds
			10.4.1 Growth and Morphogenesis
			10.4.2 Reinforcement of Immunity
			10.4.3 Metabolic Reprogramming
			10.4.4 Genetic Responses
		10.5 Concluding Remarks
		References
Part IV: Regulation of Fungal Gene Expression and Development
	11: Epigenetic Regulation of Fungal Genes Involved in Plant Colonization
		11.1 Introduction
		11.2 Current Knowledge on Fungal Chromatin Organization and Key Elements Involved in Chromatin Remodeling
			11.2.1 Historical Overview of Chromosome Organization
			11.2.2 Key Players Ensuring the Equilibrium Between Heterochromatin and Euchromatin
		11.3 Contribution of Omics Data to Our Understanding of the Genomic, Epigenomic, and Transcriptomic Context of Fungal Genes In...
			11.3.1 Fungal Genomes Are as Puzzling as the Fungal Kingdom
			11.3.2 Organization of the Epigenomic Landscape in Plant-Interacting Fungi
			11.3.3 Complex Expression Patterns of Genes Involved in Host Interactions
			11.3.4 Lessons from Combined Analysis of Genomic, Transcriptomic, and Epigenomic Data
		11.4 Chromatin-based Regulation of Effector Gene Expression Combined or not to the Action of Specific Transcription Factors
			11.4.1 Effect of a Change in Genomic Context on the Expression of Effector Genes
			11.4.2 Role of Proteins Involved in Chromatin Remodeling on the Control of Effector Gene Expression
			11.4.3 First Evidence of Dual Control for the Expression of Effector Genes by Specific Transcription Factors and Chromatin Rem...
		11.5 Future Challenges Concerning the Chromatin-Based Control of Plant-Associated Genes
		References
	12: Toward Understanding the Role of Chromatin in Secondary Metabolite Gene Regulation in the Rice Pathogen Fusarium fujikuroi
		12.1 Introduction
		12.2 Secondary Metabolism in F. fujikuroi: The Road So Far
			12.2.1 Gene Architecture and Cluster Organization
			12.2.2 Distinct SM Profiles Determine the Pathotype in F. fujikuroi
		12.3 Regulation of SM Gene Expression in F. fujikuroi
			12.3.1 Chromatin Structure: A Natural Obstacle for Transcription
			12.3.2 Prominent Histone Marks: Of ``Writers, Readers and Erasers´´
				12.3.2.1 Histone Acetylation and Its Role for SM Gene Regulation in F. fujikuroi
				12.3.2.2 Histone Methylation and Its Role in SM Gene Regulation in F. fujikuroi
					12.3.2.2.1 H3K4 Methylation
					12.3.2.2.2 H3K36 Methylation
					12.3.2.2.3 H3K9 Methylation
					12.3.2.2.4 H3K27 Methylation
					12.3.2.2.5 H4K20 Methylation
		12.4 Concluding Remarks and Perspectives
		References
	13: The Rice Blast Fungus Magnaporthe oryzae Uses a Turgor-Dependent, Septin-Mediated Mechanism to Invade Rice
		13.1 Introduction
			13.1.1 Rice Blast Disease
		13.2 Life Cycle of M. oryzae
		13.3 Cell Signalling and Fungal Pathogenicity in M. oryzae
		13.4 Pmk1 MAPK Signalling Pathway
		13.5 How Is Turgor Sensed Within the Appressorium
		13.6 Melanin Biosynthesis and Regulation
		13.7 Turgor Sensing
		13.8 Septin-Dependent Plant Infection
		13.9 Conclusions
		References
	14: Role of Light in the Life Cycle of Botrytis cinerea
		14.1 Adaptations to the Plant Host
			14.1.1 Penetration Structures
			14.1.2 Virulence Determinants
		14.2 Adaptations to Light
			14.2.1 Genetic Make-up: Photoperception
			14.2.2 Gene Expression: Photoregulation
			14.2.3 Reproduction: Photomorphogenesis and Phototropism
			14.2.4 Metabolism: Photoprotection
			14.2.5 Enzyme Systems: Photodamage Repair
			14.2.6 Circadian Clock: Photoentrainment
		14.3 Conclusion: Botrytis Exploits the Host for Nutrition and Sun Protection
		References
Part V: Genomes and Evolution
	15: Species of Zymoseptoria (Dothideomycetes) as a Model System to Study Plant Pathogen Genome Evolution
		15.1 Introduction
		15.2 Genome Architecture in Zymoseptoria Species
			15.2.1 ``Gold Standard´´ Reference Genome
			15.2.2 Transposable Element Content
			15.2.3 Accessory Chromosomes
		15.3 Adaptive Evolution Within and Between Zymoseptoria Species
			15.3.1 Signatures of Selection in Z. tritici Genomes
			15.3.2 Signatures of Selection Between Species of Zymoseptoria
		15.4 Genetic Variation Between Zymoseptoria Species
			15.4.1 Recurrent Hybridization Shapes Genetic Variation in Zymoseptoria Genomes
		15.5 Concluding Remarks
		References
	16: Accessory Chromosomes of the Fusarium oxysporum Species Complex and Their Contribution to Host Niche Adaptation
		16.1 Fusarium oxysporum: A Species Complex Occupying Diverse Ecological Niches
		16.2 Accessory Chromosomes: Contributors of Host-Specific Pathogenicity Among the FOSC
		16.3 Determinants of Host-Specific Pathogenicity
			16.3.1 An Expanded Kinase Family Enhances Environmental Sensing
			16.3.2 Crosstalk Coordinates the Functions of Core and Accessory Chromosomes
			16.3.3 Effectors Disarm Host Defense
			16.3.4 Convergent Points Highlight Adaptation to Both Abiotic and Biotic Stresses
		16.4 Mechanisms of Niche Adaptation: Genome Evolution and Maintenance
		16.5 Conclusion and Perspective
			16.5.1 Improving the Quality of AC Assemblies
			16.5.2 Exploring the Origin of ACs
			16.5.3 Effective Regulation of ACs
			16.5.4 Novel Therapeutic and Management Strategies
		References
Part VI: Global Pandemics and Food Security
	17: Global Landscape of Rust Epidemics by Puccinia Species: Current and Future Perspectives
		17.1 An Introduction to Rust Fungi and the Puccinia Species
		17.2 Important Crops and Ecosystems Affected by Puccinia Species
			17.2.1 Wheat
			17.2.2 Barley
			17.2.3 Oat
			17.2.4 Sugarcane
			17.2.5 Maize
			17.2.6 Sorghum
		17.3 The Life Cycle of Puccina Species and Its Role in Disease Epidemics
		17.4 Important Epidemics Caused by Puccinia Species
			17.4.1 Wheat Rusts
				17.4.1.1 Stem Rust
				17.4.1.2 Stripe Rust
				17.4.1.3 Leaf Rust
			17.4.2 Barley Rusts
				17.4.2.1 Stem Rust
				17.4.2.2 Stripe Rust
				17.4.2.3 Leaf Rust
			17.4.3 Oat Rusts
			17.4.4 Corn Rusts
			17.4.5 Sorghum Rust
			17.4.6 Sugarcane Rusts
			17.4.7 Myrtle Rust
		17.5 Molecular Basis of Rust Virulence
		17.6 Genomic Resources to Study Virulence Evolution
			17.6.1 Evolution of Rust Genome Assembly Approaches
		17.7 Conclusions and Perspectives
		References
	18: Magnaporthe oryzae and Its Pathotypes: A Potential Plant Pandemic Threat to Global Food Security
		18.1 Introduction
		18.2 History of Blast Disease Outbreaks
		18.3 Pathotype Delineation Among M. oryzae Isolates
		18.4 Biology of the Pathogen
			18.4.1 Sexual Reproduction
			18.4.2 Asexual Reproduction
			18.4.3 Disease Cycles
		18.5 Blast of Major Cereals: Wheat and Rice
		18.6 Molecular Cross-talks between Host and Magnaporthe oryzae
		18.7 Host Species Specificity
			18.7.1 Effectoromics of M. oryzae
		18.8 Management Strategies
			18.8.1 Restricting Movement of Seeds from Diseased Areas to Disease-free Areas
			18.8.2 Early Detection and Disease Forecasting
			18.8.3 Cultural and Sanitary Practices
			18.8.4 Chemical Control
			18.8.5 Development of Fungicide Resistance in M. oryzae
			18.8.6 Breeding for Blast-resistant Varieties
				18.8.6.1 Mutation Breeding
				18.8.6.2 Genome Editing Using CRISPR-Cas Technology for Developing Blast Resistance
			18.8.7 Biological Control
			18.8.8 Integrated Management
		18.9 Conclusions and Future Prospects
			18.9.1 Population Structure and Evolution of M. oryzae Pathotypes
			18.9.2 Management of Blast Disease
		References