UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>

Epigenetic modification is important for cellular functions. Trimethylation of histone H3 lysine 4 (H3K4me3), which associates with transcriptional activation, is one of the important epigenetic modifications. In this study, the biological functions of UvKmt2-mediated H3K4me3 modification were chara...

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Main Authors: Shuai Meng, Huanbin Shi, Chuyu Lin, Zhongling Wu, Fucheng Lin, Zeng Tao, Yanjun Kou
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/6/553
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author Shuai Meng
Huanbin Shi
Chuyu Lin
Zhongling Wu
Fucheng Lin
Zeng Tao
Yanjun Kou
author_facet Shuai Meng
Huanbin Shi
Chuyu Lin
Zhongling Wu
Fucheng Lin
Zeng Tao
Yanjun Kou
author_sort Shuai Meng
collection DOAJ
description Epigenetic modification is important for cellular functions. Trimethylation of histone H3 lysine 4 (H3K4me3), which associates with transcriptional activation, is one of the important epigenetic modifications. In this study, the biological functions of UvKmt2-mediated H3K4me3 modification were characterized in <i>Ustilaginoidea virens</i>, which is the causal agent of the false smut disease, one of the most destructive diseases in rice. Phenotypic analyses of the Δ<i>Uvkmt2</i> mutant revealed that <i>UvKMT2</i> is necessary for growth, conidiation, secondary spore formation, and virulence in <i>U. virens</i>. Immunoblotting and chromatin immunoprecipitation assay followed by sequencing (ChIP-seq) showed that <i>UvKMT2</i> is required for the establishment of H3K4me3, which covers 1729 genes of the genome in <i>U. virens</i>. Further RNA-seq analysis demonstrated that UvKmt2-mediated H3K4me3 acts as an important role in transcriptional activation. In particular, H3K4me3 modification involves in the transcriptional regulation of conidiation-related and pathogenic genes, including two important mitogen-activated protein kinases <i>UvHOG1</i> and <i>UvPMK1</i>. The down-regulation of <i>UvHOG1</i> and <i>UvPMK1</i> genes may be one of the main reasons for the reduced pathogenicity and stresses adaptability of the ∆<i>Uvkmt2</i> mutant. Overall, H3K4me3, established by histone methyltransferase <i>UvKMT2</i>, contributes to fungal development, secondary spore formation, virulence, and various stress responses through transcriptional regulation in <i>U. virens</i>.
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spelling doaj.art-2e315958f2984a3ca08a80f6bb124b732023-11-23T17:23:59ZengMDPI AGJournal of Fungi2309-608X2022-05-018655310.3390/jof8060553UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>Shuai Meng0Huanbin Shi1Chuyu Lin2Zhongling Wu3Fucheng Lin4Zeng Tao5Yanjun Kou6State Key Lab of Rice Biology, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Lab of Rice Biology, China National Rice Research Institute, Hangzhou 311400, ChinaState Key Lab of Rice Biology, Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, ChinaState Key Lab of Rice Biology, Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, ChinaState Key Lab of Rice Biology, Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, ChinaState Key Lab of Rice Biology, Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, ChinaState Key Lab of Rice Biology, China National Rice Research Institute, Hangzhou 311400, ChinaEpigenetic modification is important for cellular functions. Trimethylation of histone H3 lysine 4 (H3K4me3), which associates with transcriptional activation, is one of the important epigenetic modifications. In this study, the biological functions of UvKmt2-mediated H3K4me3 modification were characterized in <i>Ustilaginoidea virens</i>, which is the causal agent of the false smut disease, one of the most destructive diseases in rice. Phenotypic analyses of the Δ<i>Uvkmt2</i> mutant revealed that <i>UvKMT2</i> is necessary for growth, conidiation, secondary spore formation, and virulence in <i>U. virens</i>. Immunoblotting and chromatin immunoprecipitation assay followed by sequencing (ChIP-seq) showed that <i>UvKMT2</i> is required for the establishment of H3K4me3, which covers 1729 genes of the genome in <i>U. virens</i>. Further RNA-seq analysis demonstrated that UvKmt2-mediated H3K4me3 acts as an important role in transcriptional activation. In particular, H3K4me3 modification involves in the transcriptional regulation of conidiation-related and pathogenic genes, including two important mitogen-activated protein kinases <i>UvHOG1</i> and <i>UvPMK1</i>. The down-regulation of <i>UvHOG1</i> and <i>UvPMK1</i> genes may be one of the main reasons for the reduced pathogenicity and stresses adaptability of the ∆<i>Uvkmt2</i> mutant. Overall, H3K4me3, established by histone methyltransferase <i>UvKMT2</i>, contributes to fungal development, secondary spore formation, virulence, and various stress responses through transcriptional regulation in <i>U. virens</i>.https://www.mdpi.com/2309-608X/8/6/553<i>false smut</i>conidiationvirulenceKmt2H3K4me3rice
spellingShingle Shuai Meng
Huanbin Shi
Chuyu Lin
Zhongling Wu
Fucheng Lin
Zeng Tao
Yanjun Kou
UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
Journal of Fungi
<i>false smut</i>
conidiation
virulence
Kmt2
H3K4me3
rice
title UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
title_full UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
title_fullStr UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
title_full_unstemmed UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
title_short UvKmt2-Mediated H3K4 Trimethylation Is Required for Pathogenicity and Stress Response in <i>Ustilaginoidea virens</i>
title_sort uvkmt2 mediated h3k4 trimethylation is required for pathogenicity and stress response in i ustilaginoidea virens i
topic <i>false smut</i>
conidiation
virulence
Kmt2
H3K4me3
rice
url https://www.mdpi.com/2309-608X/8/6/553
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