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Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum
Histone acetylation, balanced by histone acetyltransferase (HAT) and histone deacetylase (HDAC) complexes, affects dynamic transitions of chromatin structure to regulate transcriptional accessibility. However, little is known about the interplay between HAT and HDAC complexes in Fusarium graminearum...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660929/ https://www.ncbi.nlm.nih.gov/pubmed/33137093 http://dx.doi.org/10.1371/journal.pgen.1009185 |
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author | Jiang, Hang Xia, Aliang Ye, Meng Ren, Jingyi Li, Dongao Liu, Huiquan Wang, Qinhu Lu, Ping Wu, Chunlan Xu, Jin-Rong Jiang, Cong |
author_facet | Jiang, Hang Xia, Aliang Ye, Meng Ren, Jingyi Li, Dongao Liu, Huiquan Wang, Qinhu Lu, Ping Wu, Chunlan Xu, Jin-Rong Jiang, Cong |
author_sort | Jiang, Hang |
collection | PubMed |
description | Histone acetylation, balanced by histone acetyltransferase (HAT) and histone deacetylase (HDAC) complexes, affects dynamic transitions of chromatin structure to regulate transcriptional accessibility. However, little is known about the interplay between HAT and HDAC complexes in Fusarium graminearum, a causal agent of Fusarium Head Blight (FHB) that uniquely contains chromosomal regions enriched for house-keeping or infection-related genes. In this study, we identified the ortholog of the human inhibitor of growth (ING1) gene in F. graminearum (FNG1) and found that it specifically interacts with the FgEsa1 HAT of the NuA4 complex. Deletion of FNG1 led to severe growth defects and blocked conidiation, sexual reproduction, DON production, and plant infection. The fng1 mutant was normal in H3 acetylation but significantly reduced in H4 acetylation. A total of 34 spontaneous suppressors of fng1 with faster growth rate were isolated. Most of them were still defective in sexual reproduction and plant infection. Thirty two of them had mutations in orthologs of yeast RPD3, SIN3, and SDS3, three key components of the yeast Rpd3L HDAC complex. Four mutations in these three genes were verified to suppress the defects of fng1 mutant in growth and H4 acetylation. The rest two suppressor strains had a frameshift or nonsense mutation in a glutamine-rich hypothetical protein that may be a novel component of the FgRpd3 HDAC complex in filamentous fungi. FgRpd3, like Fng1, localized in euchromatin. Deletion of FgRPD3 resulted in severe growth defects and elevated H4 acetylation. In contract, the Fgsds3 deletion mutant had only a minor reduction in growth rate but FgSIN3 appeared to be an essential gene. RNA-seq analysis revealed that 48.1% and 54.2% of the genes with altered expression levels in the fng1 mutant were recovered to normal expression levels in two suppressor strains with mutations in FgRPD3 and FgSDS3, respectively. Taken together, our data showed that Fng1 is important for H4 acetylation as a component of the NuA4 complex and functionally related to the FgRpd3 HDAC complex for transcriptional regulation of genes important for growth, conidiation, sexual reproduction, and plant infection in F. graminearum. |
format | Online Article Text |
id | pubmed-7660929 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-76609292020-11-18 Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum Jiang, Hang Xia, Aliang Ye, Meng Ren, Jingyi Li, Dongao Liu, Huiquan Wang, Qinhu Lu, Ping Wu, Chunlan Xu, Jin-Rong Jiang, Cong PLoS Genet Research Article Histone acetylation, balanced by histone acetyltransferase (HAT) and histone deacetylase (HDAC) complexes, affects dynamic transitions of chromatin structure to regulate transcriptional accessibility. However, little is known about the interplay between HAT and HDAC complexes in Fusarium graminearum, a causal agent of Fusarium Head Blight (FHB) that uniquely contains chromosomal regions enriched for house-keeping or infection-related genes. In this study, we identified the ortholog of the human inhibitor of growth (ING1) gene in F. graminearum (FNG1) and found that it specifically interacts with the FgEsa1 HAT of the NuA4 complex. Deletion of FNG1 led to severe growth defects and blocked conidiation, sexual reproduction, DON production, and plant infection. The fng1 mutant was normal in H3 acetylation but significantly reduced in H4 acetylation. A total of 34 spontaneous suppressors of fng1 with faster growth rate were isolated. Most of them were still defective in sexual reproduction and plant infection. Thirty two of them had mutations in orthologs of yeast RPD3, SIN3, and SDS3, three key components of the yeast Rpd3L HDAC complex. Four mutations in these three genes were verified to suppress the defects of fng1 mutant in growth and H4 acetylation. The rest two suppressor strains had a frameshift or nonsense mutation in a glutamine-rich hypothetical protein that may be a novel component of the FgRpd3 HDAC complex in filamentous fungi. FgRpd3, like Fng1, localized in euchromatin. Deletion of FgRPD3 resulted in severe growth defects and elevated H4 acetylation. In contract, the Fgsds3 deletion mutant had only a minor reduction in growth rate but FgSIN3 appeared to be an essential gene. RNA-seq analysis revealed that 48.1% and 54.2% of the genes with altered expression levels in the fng1 mutant were recovered to normal expression levels in two suppressor strains with mutations in FgRPD3 and FgSDS3, respectively. Taken together, our data showed that Fng1 is important for H4 acetylation as a component of the NuA4 complex and functionally related to the FgRpd3 HDAC complex for transcriptional regulation of genes important for growth, conidiation, sexual reproduction, and plant infection in F. graminearum. Public Library of Science 2020-11-02 /pmc/articles/PMC7660929/ /pubmed/33137093 http://dx.doi.org/10.1371/journal.pgen.1009185 Text en © 2020 Jiang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Jiang, Hang Xia, Aliang Ye, Meng Ren, Jingyi Li, Dongao Liu, Huiquan Wang, Qinhu Lu, Ping Wu, Chunlan Xu, Jin-Rong Jiang, Cong Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title | Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title_full | Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title_fullStr | Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title_full_unstemmed | Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title_short | Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum |
title_sort | opposing functions of fng1 and the rpd3 hdac complex in h4 acetylation in fusarium graminearum |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660929/ https://www.ncbi.nlm.nih.gov/pubmed/33137093 http://dx.doi.org/10.1371/journal.pgen.1009185 |
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