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The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors

The rice blast fungus Magnaporthe oryzae causes a devastating disease that threatens global rice (Oryza sativa) production. Despite intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high-resolution transcriptional profiling study of...

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Autores principales: Yan, Xia, Tang, Bozeng, Ryder, Lauren S, MacLean, Dan, Were, Vincent M, Eseola, Alice Bisola, Cruz-Mireles, Neftaly, Ma, Weibin, Foster, Andrew J, Osés-Ruiz, Miriam, Talbot, Nicholas J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10118281/
https://www.ncbi.nlm.nih.gov/pubmed/36808541
http://dx.doi.org/10.1093/plcell/koad036
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author Yan, Xia
Tang, Bozeng
Ryder, Lauren S
MacLean, Dan
Were, Vincent M
Eseola, Alice Bisola
Cruz-Mireles, Neftaly
Ma, Weibin
Foster, Andrew J
Osés-Ruiz, Miriam
Talbot, Nicholas J
author_facet Yan, Xia
Tang, Bozeng
Ryder, Lauren S
MacLean, Dan
Were, Vincent M
Eseola, Alice Bisola
Cruz-Mireles, Neftaly
Ma, Weibin
Foster, Andrew J
Osés-Ruiz, Miriam
Talbot, Nicholas J
author_sort Yan, Xia
collection PubMed
description The rice blast fungus Magnaporthe oryzae causes a devastating disease that threatens global rice (Oryza sativa) production. Despite intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high-resolution transcriptional profiling study of the entire plant-associated development of the blast fungus. Our analysis revealed major temporal changes in fungal gene expression during plant infection. Pathogen gene expression could be classified into 10 modules of temporally co-expressed genes, providing evidence for the induction of pronounced shifts in primary and secondary metabolism, cell signaling, and transcriptional regulation. A set of 863 genes encoding secreted proteins are differentially expressed at specific stages of infection, and 546 genes named MEP (Magnaportheeffector protein) genes were predicted to encode effectors. Computational prediction of structurally related MEPs, including the MAX effector family, revealed their temporal co-regulation in the same co-expression modules. We characterized 32 MEP genes and demonstrate that Mep effectors are predominantly targeted to the cytoplasm of rice cells via the biotrophic interfacial complex and use a common unconventional secretory pathway. Taken together, our study reveals major changes in gene expression associated with blast disease and identifies a diverse repertoire of effectors critical for successful infection.
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spelling pubmed-101182812023-04-21 The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors Yan, Xia Tang, Bozeng Ryder, Lauren S MacLean, Dan Were, Vincent M Eseola, Alice Bisola Cruz-Mireles, Neftaly Ma, Weibin Foster, Andrew J Osés-Ruiz, Miriam Talbot, Nicholas J Plant Cell Large-Scale Biology The rice blast fungus Magnaporthe oryzae causes a devastating disease that threatens global rice (Oryza sativa) production. Despite intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high-resolution transcriptional profiling study of the entire plant-associated development of the blast fungus. Our analysis revealed major temporal changes in fungal gene expression during plant infection. Pathogen gene expression could be classified into 10 modules of temporally co-expressed genes, providing evidence for the induction of pronounced shifts in primary and secondary metabolism, cell signaling, and transcriptional regulation. A set of 863 genes encoding secreted proteins are differentially expressed at specific stages of infection, and 546 genes named MEP (Magnaportheeffector protein) genes were predicted to encode effectors. Computational prediction of structurally related MEPs, including the MAX effector family, revealed their temporal co-regulation in the same co-expression modules. We characterized 32 MEP genes and demonstrate that Mep effectors are predominantly targeted to the cytoplasm of rice cells via the biotrophic interfacial complex and use a common unconventional secretory pathway. Taken together, our study reveals major changes in gene expression associated with blast disease and identifies a diverse repertoire of effectors critical for successful infection. Oxford University Press 2023-02-18 /pmc/articles/PMC10118281/ /pubmed/36808541 http://dx.doi.org/10.1093/plcell/koad036 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Large-Scale Biology
Yan, Xia
Tang, Bozeng
Ryder, Lauren S
MacLean, Dan
Were, Vincent M
Eseola, Alice Bisola
Cruz-Mireles, Neftaly
Ma, Weibin
Foster, Andrew J
Osés-Ruiz, Miriam
Talbot, Nicholas J
The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title_full The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title_fullStr The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title_full_unstemmed The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title_short The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
title_sort transcriptional landscape of plant infection by the rice blast fungus magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors
topic Large-Scale Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10118281/
https://www.ncbi.nlm.nih.gov/pubmed/36808541
http://dx.doi.org/10.1093/plcell/koad036
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