A sensor kinase controls turgor-driven plant infection by the rice blast fungus

Ryder, Lauren S.; Dagdas, Yasin; Kershaw, Michael J.; Venkataraman, Chandrasekhar; Madzvamuse, Anotida; Xia, Yan; Cruz-Mireles, Neftaly; Soanes, Darren M.; Osés-Ruiz, Míriam; Styles, Vanessa; Sklenář, Jan; Menke, Frank L.H.; Talbot, Nicholas J.

doi:10.1038/s41586-019-1637-x

Cited by 111 publications

(132 citation statements)

References 45 publications

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“…Magnaporthe oryzae (synonym of Pyricularia oryzae) is a filamentous fungal plant pathogen, best known for causing rice (Oryza sativa) and wheat (Triticum aestivum) blast diseases that threaten world food security [23][24][25][26][27]. The initial stages of M. oryzae infection, including spore germination, appressorium development and leaf penetration are well understood, but many details of growth and development inside the plant remain unknown [28][29][30][31]. A central paradigm of plant-microbe interaction is the use of secreted proteins and chemicals by an invading organism to suppress host immunity, blunt the immune response and change host physiology to facilitate infection [32,33].…”

Section: Introductionmentioning

confidence: 99%

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

2021

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Transcriptional dynamic in response to environmental and developmental cues are fundamental to biology, yet many mechanistic aspects are poorly understood. One such example is fungal plant pathogens, which use secreted proteins and small molecules, termed effectors, to suppress host immunity and promote colonization. Effectors are highly expressed in planta but remain transcriptionally repressed ex planta, but our mechanistic understanding of these transcriptional dynamics remains limited. We tested the hypothesis that repressive histone modification at H3-Lys27 underlies transcriptional silencing ex planta, and that exchange for an active chemical modification contributes to transcription of in planta induced genes. Using genetics, chromatin immunoprecipitation and sequencing and RNA-sequencing, we determined that H3K27me3 provides significant local transcriptional repression. We detail how regions that lose H3K27me3 gain H3K27ac, and these changes are associated with increased transcription. Importantly, we observed that many in planta induced genes were marked by H3K27me3 during axenic growth, and detail how altered H3K27 modification influences transcription. ChIP-qPCR during in planta growth suggests that H3K27 modifications are generally stable, but can undergo dynamics at specific genomic locations. Our results support the hypothesis that dynamic histone modifications at H3K27 contributes to fungal genome regulation and specifically contributes to regulation of genes important during host infection.

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Section: Introductionmentioning

confidence: 99%

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

2021

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“…The Sln1 gene enables the appressorium to sense turgor threshold and thereby facilitates host penetration. The sln1 mutant does not organise septins and polarity determinants for leaf infection (Ryder et al , 2019). The M. oryzae mst12 mutant cannot invade rice leaves because it fails to form penetration pegs on plant epidermal cells although its appressoria can develop normal turgor pressure and ultrastructure (Park et al , 2004).…”

Section: Introductionmentioning

confidence: 99%

Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves

Wang

Chern

et al. 2020

New Phytologist

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Broad-spectrum resistance is highly preferred in crop breeding programmes. Previously, we have reported the identification of the broad-spectrum resistance-Digu 1 (bsr-d1) allele from rice Digu. The bsr-d1 allele prevents activation of Bsr-d1 expression by Magnaporthe oryzae infection and degradation of H 2 O 2 by peroxidases, leading to resistance to M. oryzae. However, it remains unknown whether defence pathways other than H 2 O 2 burst and peroxidases contribute to the bsr-d1-mediated immunity.Blast resistance was determined in rice leaves by spray and punch inoculations. Target genes of OsMYB30 were identified by one-hybrid assays in yeast and electrophoretic mobility shift assay. Lignin content was measured by phloroglucinol-HCl staining, and acetyl bromide and thioacidolysis methods.Here, we report the involvement of the OsMYB30 gene in bsr-d1-mediated blast resistance. Expression of OsMYB30 was induced during M. oryzae infection or when Bsr-d1 was knocked out or downregulated, as occurs in bsr-d1 plants upon infection. We further found that OsMYB30 bound to and activated the promoters of 4-coumarate:coenzyme A ligase genes (Os4CL3 and Os4CL5) resulting in accumulation of lignin subunits G and S. This action led to obvious thickening of sclerenchyma cells near the epidermis, inhibiting M. oryzae penetration at the early stage of infection.Our study revealed novel components required for bsr-d1-mediated resistance and penetration-dependent immunity, and advanced our understanding of broad-spectrum disease resistance.

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“…1a). This dome-shaped, darkly melanized cell directs a high internal turgor onto a needle-like penetration peg [14][15][16] , which emerges from a 2-500 nm pore at the appressorial base to puncture the plant's outer defensive barriers, the cuticle and epidermal cell wall. Despite major advances in our understanding of the cellular processes preceding 11,12,[16][17][18][19] and following 20,21 plant cell entry, the (bio)chemical reactions occurring at this nanoscale plant-fungus interface and their role in host penetration remain poorly understood.…”

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confidence: 99%

Unravelling the role of alcohol copper radical oxidases in fungal plant pathogens

Bissaro

Kodama

Hage

et al. 2021

Preprint

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Copper radical oxidases (CRO) form a class of enzymes with a longstanding history encompassing diverse substrate specificities. While the biological function of most CROs remains unknown, we observed that CROs active on aliphatic alcohols are found only in fungal plant pathogens. Here, we unveil the role of these CROs and the identity of their natural redox partner, a haem-iron peroxidase. Combining multiscale approaches, we report that Colletotrichum and Magnaporthe appressoria (specialized cells that puncture the plant cuticles) co-secrete this pair of metalloenzymes early during penetration. We show in vivo that mutant appressoria lacking either or both enzymes have impaired penetration ability and pathogenicity. We reveal in vitro a finely-tuned enzyme interplay is responsible for the oxidation of plant cuticular long-chain alcohols into aldehyde products, suggested to act as key molecular signals in the fungal infection machinery. Our results open new avenues to design oxidase-specific inhibitors as anti-penetrants for crop protection.

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A sensor kinase controls turgor-driven plant infection by the rice blast fungus

Cited by 111 publications

References 45 publications

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves

Unravelling the role of alcohol copper radical oxidases in fungal plant pathogens

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