Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements

The fine-tuned expression dynamics of the effector genes are pivotal for the transition from vegetative growth to host colonization of pathogenic filamentous fungi. However, mechanisms underlying the dynamic regulation of these genes remain largely unknown. Here, through comparative transcriptome an...

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Main Authors: Jia-hui XIE, Wei TANG, Guo-dong LU, Yong-he HONG, Zhen-hui ZHONG, Zong-hua WANG, Hua-kun ZHENG
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:Journal of Integrative Agriculture
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2095311923000114
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author Jia-hui XIE
Wei TANG
Guo-dong LU
Yong-he HONG
Zhen-hui ZHONG
Zong-hua WANG
Hua-kun ZHENG
author_facet Jia-hui XIE
Wei TANG
Guo-dong LU
Yong-he HONG
Zhen-hui ZHONG
Zong-hua WANG
Hua-kun ZHENG
author_sort Jia-hui XIE
collection DOAJ
description The fine-tuned expression dynamics of the effector genes are pivotal for the transition from vegetative growth to host colonization of pathogenic filamentous fungi. However, mechanisms underlying the dynamic regulation of these genes remain largely unknown. Here, through comparative transcriptome and chromatin immunoprecipitation sequencing (ChIP-seq) analyses of the methyltransferase PoKmt6 in rice blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae), we found that PoKmt6-mediated H3K27me3 deposition was enriched mainly at fast-evolving regions and contributed to the silencing of a subset of secreted proteins (SP) and transposable element (TE) families during the vegetative growth of P. oryzae. Intriguingly, we observed that a group of SP genes, which were depleted of H3K27me3 modification, could also be silenced via the H3K27me3-mediated repression of the nearby TEs. In conclusion, our results indicate that H3K27me3 modification mediated by PoKmt6 regulates the expression of some SP genes in fast-evolving regions through the suppression of nearby TEs.
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spelling doaj.art-93cbff5078f34f808f59d58ef09a25092023-10-13T13:53:11ZengElsevierJournal of Integrative Agriculture2095-31192023-10-01221030593068Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elementsJia-hui XIE0Wei TANG1Guo-dong LU2Yong-he HONG3Zhen-hui ZHONG4Zong-hua WANG5Hua-kun ZHENG6State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; National Engineering Research Center of JUNCAO Technology, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; Correspondence HONG Yong-heState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; Correspondence ZHONG Zhen-huiState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; Fuzhou Institute of Oceanography, Minjiang University, Fuzhou 350108, P.R.China; Correspondence WANG Zong-huaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; Fujian Universities Key Laboratory for Plant Microbe Interaction, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; National Engineering Research Center of JUNCAO Technology, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China; Correspondence ZHENG Hua-kunThe fine-tuned expression dynamics of the effector genes are pivotal for the transition from vegetative growth to host colonization of pathogenic filamentous fungi. However, mechanisms underlying the dynamic regulation of these genes remain largely unknown. Here, through comparative transcriptome and chromatin immunoprecipitation sequencing (ChIP-seq) analyses of the methyltransferase PoKmt6 in rice blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae), we found that PoKmt6-mediated H3K27me3 deposition was enriched mainly at fast-evolving regions and contributed to the silencing of a subset of secreted proteins (SP) and transposable element (TE) families during the vegetative growth of P. oryzae. Intriguingly, we observed that a group of SP genes, which were depleted of H3K27me3 modification, could also be silenced via the H3K27me3-mediated repression of the nearby TEs. In conclusion, our results indicate that H3K27me3 modification mediated by PoKmt6 regulates the expression of some SP genes in fast-evolving regions through the suppression of nearby TEs.http://www.sciencedirect.com/science/article/pii/S2095311923000114secreted proteintransposable elementsfast-evolving regionsH3K27me3
spellingShingle Jia-hui XIE
Wei TANG
Guo-dong LU
Yong-he HONG
Zhen-hui ZHONG
Zong-hua WANG
Hua-kun ZHENG
Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
Journal of Integrative Agriculture
secreted protein
transposable elements
fast-evolving regions
H3K27me3
title Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
title_full Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
title_fullStr Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
title_full_unstemmed Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
title_short Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements
title_sort histone h3k27me3 methylation regulates the expression of secreted proteins distributed at fast evolving regions through transcriptional repression of transposable elements
topic secreted protein
transposable elements
fast-evolving regions
H3K27me3
url http://www.sciencedirect.com/science/article/pii/S2095311923000114
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