Cargando…

The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae

As the causal agent of the blast disease, Magnaporthe oryzae is one of the most destructive fungal pathogens of rice. Histone acetylation/deacetylation is important for remodeling of chromatin superstructure and thus altering gene expression. In this study, two genes encoding histone deacetylases, n...

Descripción completa

Detalles Bibliográficos
Autores principales: Lin, Chaoxiang, Cao, Xue, Qu, Ziwei, Zhang, Shulin, Naqvi, Naweed I., Deng, Yi Zhen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8265625/
https://www.ncbi.nlm.nih.gov/pubmed/34190584
http://dx.doi.org/10.1128/mSphere.00118-21
_version_ 1783719774471061504
author Lin, Chaoxiang
Cao, Xue
Qu, Ziwei
Zhang, Shulin
Naqvi, Naweed I.
Deng, Yi Zhen
author_facet Lin, Chaoxiang
Cao, Xue
Qu, Ziwei
Zhang, Shulin
Naqvi, Naweed I.
Deng, Yi Zhen
author_sort Lin, Chaoxiang
collection PubMed
description As the causal agent of the blast disease, Magnaporthe oryzae is one of the most destructive fungal pathogens of rice. Histone acetylation/deacetylation is important for remodeling of chromatin superstructure and thus altering gene expression. In this study, two genes encoding histone deacetylases, namely, MoRPD3 and MoHST4, were identified and functionally characterized in M. oryzae. MoHst4 was required for proper mycelial growth and pathogenicity, whereas overproduction of MoRpd3 led to loss of pathogenicity, likely due to a block in conidial cell death and restricted invasive growth within the host plants. Green fluorescent protein (GFP)-MoRpd3 localized to the nucleus and cytoplasm in vegetative hyphae and developing conidia. By comparative transcriptomics analysis, we identified potential target genes epigenetically regulated by histone deacetylases (HDACs) containing MoRpd3 or MoHst4, which may contribute to conidia formation and/or conidial cell death, which is a prerequisite for successful appressorium-mediated host invasion. Taken together, our results suggest that histone deacetylases MoRpd3 and MoHst4 differentially regulate mycelial growth, asexual development, and pathogenesis in M. oryzae. IMPORTANCE HDACs (histone deacetylases) regulate various aspects of growth, development, and pathogenesis in plant-pathogenic fungi. Most members of HDAC classes I to III have been functionally characterized, except for orthologous Rpd3 and Hst4, in the rice blast fungus Magnaporthe oryzae. In this study, we assessed the function of MoRpd3 and MoHst4 by reverse genetics and found that they differentially regulate M. oryzae vegetative growth, asexual development, and infection. Particularly, MoRpd3 negatively regulates M. oryzae pathogenicity, likely through suppression of conidial cell death, which we recently reported as being critical for appressorium maturation and functioning. Overall, this study broadens our understanding of fungal pathobiology and its critical regulation by histone modification(s) during cell death and in planta differentiation.
format Online
Article
Text
id pubmed-8265625
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-82656252021-07-23 The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae Lin, Chaoxiang Cao, Xue Qu, Ziwei Zhang, Shulin Naqvi, Naweed I. Deng, Yi Zhen mSphere Research Article As the causal agent of the blast disease, Magnaporthe oryzae is one of the most destructive fungal pathogens of rice. Histone acetylation/deacetylation is important for remodeling of chromatin superstructure and thus altering gene expression. In this study, two genes encoding histone deacetylases, namely, MoRPD3 and MoHST4, were identified and functionally characterized in M. oryzae. MoHst4 was required for proper mycelial growth and pathogenicity, whereas overproduction of MoRpd3 led to loss of pathogenicity, likely due to a block in conidial cell death and restricted invasive growth within the host plants. Green fluorescent protein (GFP)-MoRpd3 localized to the nucleus and cytoplasm in vegetative hyphae and developing conidia. By comparative transcriptomics analysis, we identified potential target genes epigenetically regulated by histone deacetylases (HDACs) containing MoRpd3 or MoHst4, which may contribute to conidia formation and/or conidial cell death, which is a prerequisite for successful appressorium-mediated host invasion. Taken together, our results suggest that histone deacetylases MoRpd3 and MoHst4 differentially regulate mycelial growth, asexual development, and pathogenesis in M. oryzae. IMPORTANCE HDACs (histone deacetylases) regulate various aspects of growth, development, and pathogenesis in plant-pathogenic fungi. Most members of HDAC classes I to III have been functionally characterized, except for orthologous Rpd3 and Hst4, in the rice blast fungus Magnaporthe oryzae. In this study, we assessed the function of MoRpd3 and MoHst4 by reverse genetics and found that they differentially regulate M. oryzae vegetative growth, asexual development, and infection. Particularly, MoRpd3 negatively regulates M. oryzae pathogenicity, likely through suppression of conidial cell death, which we recently reported as being critical for appressorium maturation and functioning. Overall, this study broadens our understanding of fungal pathobiology and its critical regulation by histone modification(s) during cell death and in planta differentiation. American Society for Microbiology 2021-06-30 /pmc/articles/PMC8265625/ /pubmed/34190584 http://dx.doi.org/10.1128/mSphere.00118-21 Text en Copyright © 2021 Lin et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Lin, Chaoxiang
Cao, Xue
Qu, Ziwei
Zhang, Shulin
Naqvi, Naweed I.
Deng, Yi Zhen
The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title_full The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title_fullStr The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title_full_unstemmed The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title_short The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae
title_sort histone deacetylases morpd3 and mohst4 regulate growth, conidiation, and pathogenicity in the rice blast fungus magnaporthe oryzae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8265625/
https://www.ncbi.nlm.nih.gov/pubmed/34190584
http://dx.doi.org/10.1128/mSphere.00118-21
work_keys_str_mv AT linchaoxiang thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT caoxue thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT quziwei thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT zhangshulin thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT naqvinaweedi thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT dengyizhen thehistonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT linchaoxiang histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT caoxue histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT quziwei histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT zhangshulin histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT naqvinaweedi histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae
AT dengyizhen histonedeacetylasesmorpd3andmohst4regulategrowthconidiationandpathogenicityinthericeblastfungusmagnaportheoryzae