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Genome Dynamics of a Cereal Killer: Strategies for Controlling Ancient

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Genome Dynamics of a Cereal Killer: Strategies for Controlling Ancient Genome Dynamics of a Cereal Killer: Strategies for Bangladeshi fields with 100% loss. Controlling Ancient and Emerging Crop Diseases Magnaporthe oryzae causes: Ancient disease: rice blast Emerging disease: wheat blast Ministry of Agriculture ordered infected fields burned 2007 Photo: Valent 2009 Photo: von Tiedemann & Duveiller Rice pathotype Wheat pathotype Barbara Valent Dept. of Plant Pathology, Kansas State University Nature 532, 421-422 (2016) Plant Diseases Threaten our Food Wheat blast caused by the fungus Magnaporthe oryzae Potato Late Blight – Phytophthora infestans Banana Fusarium Wilt – F. oxysporum cubense Triticum pathotype Hard to control: One spore can kill the entire wheat head. One useful resistance gene gives partial head blast control. Irish Potato Famine New Race TR4 Favorable environment Wheat Stem Rust – Puccinia graminis tritici Rice Blast – Magnaporthe oryzae oryza overwhelms resistance plus fungicides. Seed-borne fungus with potential huge impact on global grain trade. New Race UG99 Super Hybrid Rice in China Warm rainy weather at heading results in 100% empty heads. Wheat blast Presentation Outline Wheat blast identified in Brazil in 1985; spread to other countries in South America; jumped to Bangladesh in 2016. • M. oryzae is highly evolved for pathogenicity on grasses Effectors: pathogen proteins specifically expressed and secreted in the host Spore Appressorium Biotrophic Interfacial Complex Brazil, 2012 Invasive Hyphae Cytoplasmic Effectors • Evolutionary genomics Bangladesh, 2016 Paritosh Malaker – Genome dynamics with supernumerary mini-chromosomes CIMMYT – Mobile EFFECTOR genes impact blast disease control Wheat blast affected ~15% of total wheat area in Bangladesh in the first year 1 Presentation Outline Effectors are generally small unique proteins only expressed during plant invasion • M. oryzae is highly evolved for pathogenicity on grasses Avirulence (AVR) Effectors trigger resistance Resistance Gene Products: NBS-LRR Resistance Receptors Root Clade Blast Clade Wood Clade Other Fungi AVR Effectors • Evolutionary genomics – Genome dynamics with supernumerary mini-chromosomes – Mobile EFFECTOR genes impact blast disease control Zhang et al., 2018, Sci. Rep. The blast fungus needs to invade living host cells so M. oryzae: a sophisticated cereal killer hypersensitive host-cell death blocks infection Susceptible interaction - rice without resistance gene Pita Conidium with Spore Tip Mucilage Glues the spore to the hydrophobic rice Fungus with Avirulence surface through rain or dew, which are Effector AVR-Pita critical for penetration. Hypersensitive resistance on rice with resistance gene Pita Fungus with Avirulence Effector AVR-Pita 2 μm Micrographs - Rick Howard, DuPont-Pioneer Appressoria generate high pressure to puncture the host Blast Clade diverged ca. 21 million years ago surface and enter the plant Fungal Order Magnaporthales Saprobe on submerged wood Leaf and Seed Head Pathogens Penetration Peg 24 mya • APPRESSORIA to penetrate cuticle • 21 mya Hundreds of small Appressorium 5 μm unique EFFECTOR proteins to hijack plant processes Extremely high turgor pressure (80 times atmospheric pressure) Root Pathogens and powerful adhesives critical for penetration Zhang et al., 2018, Sci. Rep. Rick Howard, DuPont 2 At Least 100 Pathogenicity Genes Characterized: Many Effectors are key to understanding blast disease impact appressorium differentiation and function Effectors: pathogen proteins specifically expressed and secreted in host tissue R R R R R Two opposite roles of effectors depending on host genotypes: (1) promote host susceptibility (2) trigger host immunity / Resistance Video from Nick Talbot, Sainsbury Lab Kershaw et al, Genetics, 2019 At Least 100 Pathogenicity Genes Characterized: Many After penetration: the blast fungus delivers 100’s of impact appressorium differentiation and function ‘cytoplasmic’ effectors inside plant cells Critical for infection: • Hyphal Differentiation • Co-opting Plant Processes Red Rings: Cytoplasmic effectors Green lines: (Extracellular effectors) Repeated in each newly invaded cell. Video from Nick Talbot, Sainsbury Lab Kershaw et al, Genetics, 2019 Blue: Rice Cytoplasm Fungal invasive hyphae are enclosed in a plant-derived Effectors that Accumulate in BICs are Translocated into Extra-Invasive Hyphal Membrane (EIHM) the Rice Cytoplasm Rice Nucleus Merge FM4-64 C.H.Khang Green – Cytoplasmic EYFP FM4-64 channel shows • EXTRACELLULAR EFFECTOR BAS4:GFP (green) is secreted by the Red – FM4-64 EIHM in this black and Yellow – co-localization white inverse image fungus and retained within host-derived EIHM • CYTOPLASMIC EFFECTOR PWL2:mCherry (red) is secreted into the Live Cell Imaging of the fungus invading rice leaf sheath cells BIC and translocated into the rice cell Kankanala et al., Plant Cell 2007 3 How are cytoplasmic effectors secreted into BICS? Summary: Hundreds of Pathogenicity Genes and Effectors Contribute to Disease Extracellular effectors PWL2 Cytoplasmic • Mutation of pathogenicity genes shows an impact on disease effectors BAS1 development – Use of Host Induced Gene Silencing of PTH genes to control disease? Extracellular • Mutation of effector genes in laboratory studies rarely impacts effectors: secreted disease development, suggesting functional redundancy for by conventional, effectors golgi-dependent secretion Cytoplasmic effectors: targeted Therefore, the fungus can lose an individual effector to BICs by a nonconventional gene and still cause disease. secretion system that bypasses the Golgi How do cytoplasmic effectors cross the rice plasma membrane? Presentation Outline • M. oryzae is highly evolved for pathogenicity on grasses Avirulence (AVR) Effectors trigger resistance Resistance Gene Products: NBS-LRR Resistance Receptors PWL2:mRFP BAS4:eGFP Effector Co-localization Studies Co-localization with Inhibition of plant AVR Effectors fluorescent plant endocytosis by VIGS and components (plasma chemicals • Evolutionary genomics By co-opting host membrane) clathrin-mediated – Genome dynamics with supernumerary mini-chromosomes endocytosis – Mobile EFFECTOR genes impact blast disease control Ely Oliveira-Garcia Where do cytoplasmic effectors go and what do they do? Avirulence (AVR) effectors trigger resistance R R R R R R R R Resistance Resistance • 13 AVR genes cloned (11 correspond to identified rice R genes) nucleus • >100 major R genes identified in rice; many more AVR genes Pwl2:mCherry:NLS (red) Red fluorescent cytoplasmic effector remain to be identified Bas4:EGFP (green) PWL2 - black and white inverse image • The rice blast fungus is able to overcome/break individual Many cytoplasmic effectors move through resistance genes within 2 to 3 years of their deployment by host plasmodesmata into neighboring cells mutation/loss of effectors Khang et al., Plant Cell (2010) 4 Recognition of an AVR effector by a corresponding rice Host Jump to Wheat – Loss of an AVR/R Gene Interaction resistance receptor triggers resistance PWT3 “Breakdown” of R genes in the field comes • Lolium strains with the from mutation, mainly deletion, of the PWT3 AVR gene don’t corresponding AVR gene in the pathogen Wide cultivation of infect wheat with the R rwt3 wheat in Brazil Host genotypes gene Rwt3. in the 1980s Rwt3 Wheat rwt3 Wheat Pita_ r/r • This model implies that Population of fungus with PWT3 rwt3 cultivars served as increases Pathogen springboards for the host AVR-Pita_ S Emergence of mutant jump of fungal strains genotypes fungus (Infects the entire with PWT3 in Brazil. wheat population avr/avr Rwt3 Wheat rwt3 Wheat Resistance and avirulence are generally inherited as single dominant genes Yukio Tosa Kobe University Inoue et al., Science, 2017 Telomere-to-telomere genome assembly for Pathogen AVR effector genes are key to M. oryzae biology aggressive wheat blast strain B71 Scaf. 1-5 • M. oryzae is a haploid Ascomycete with ~40 Mb 1 • Determine rice cultivar specificity (e.g. AVR-Pita1) 7 genome with ~13,000 genes • Wheat pathogen B71 has 7 core chromosomes that are highly • Highly mutable AVR genes (frequencies of 10-3, conserved relative to rice pathogens often by gene deletion) responsible for the rapid 6 2 • Scaffolds 1-5 are not anchored ability of the fungus to overcome deployed R to chromosomes 1 – 7 in the rice genes reference genome 5 • Determine host species specificity 3 4 Sanzhen Liu Bolivian strain B71 isolated in 2012 is closely related to the Bangladeshi strains Peng et al, bioRxiv, 2018 M. oryzae, a single species with crop-adapted pathotypes M. oryzae dispensable mini-chromosomes identified in the 1990s S. cerevisiae 1992 chrom. sizes Eleusine pth. (Finger Millet ) 1,640 – • Core chromosomes are >5 Mb 2,500 kb in size Lolium pth. • Many strains contain mini- (Ryegrass) 980 kb chromosomes generally <3 Mb Setaria pth. in size (Foxtail Millet ) • CHEF Gel 240 kb Found in 0, 1, 2 or more copies in different strains Triticum pth. OryzaRice pth. • Mini-chromosomes don’t (Wheat) (Rice) ~7000 segregate normally in meiosis and can be missing in asexual 1985 years ago spores Family tree based on whole genome sequencing (SNPs/Mb uniquely aligned DNA) Gladieux et al. mBio 2018 Southern Blot Orbach et al. Mol. Plant-Microbe Interact., 1996 5 All five B71 scaffolds are from a mini-chromosome Illumina sequencing of eight additional strains Pathogen Strain B71mini Mini 2.0 Mb Name Year isolated Host species Isolation location 1988 T25 1988 Triticum Paraná, Brazil Py5020 2005 Triticum Paraná, Brazil • Mini DNA recovered from gels Py22.1 2007 Triticum
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