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Journal of Integrative Agriculture  2023, Vol. 22 Issue (10): 3059-3068    DOI: 10.1016/j.jia.2023.01.011
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Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements

XIE Jia-hui1, TANG Wei1, LU Guo-dong1, 4, HONG Yong-he1#, ZHONG Zhen-hui1#, WANG Zong-hua1, 3#, ZHENG Hua-kun1, 2, 4#

1 State 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
2 Fujian Universities Key Laboratory for Plant Microbe Interaction, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China
3 Fuzhou Institute of Oceanography, Minjiang University, Fuzhou 350108, P.R.China
4 National Engineering Research Center of JUNCAO Technology, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China
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摘要  效应因子表达的精准调控对病原菌从营养阶段到定殖于植物体内的转变至关重要。但是,我们对这些基因的动态调节机制的了解仍有限。本研究通过比较转录组学和染色质免疫沉淀测序方式对稻瘟病菌中甲基化转移酶PoKMT6进行功能分析,发现PoKmt6介导的H3K27me3主要富集在快速进化区,并且这种修饰导致部分分泌蛋白(SP)编码基因和转座子(TE)在菌丝体阶段被沉默。有趣的是,我们发现部分SP基因本身不受H3K27me3修饰,但其附近TEH3K27me3修饰可以间接沉默这些基因的表达。综上所述,我们的结果表明,在快速进化区,PoKmt6介导的H3K27me3通过抑制附近TE的表达来调节部分SP基因表达。

Abstract  

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 Poryzae.  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.

Keywords:  secreted protein       transposable elements       fast-evolving regions      H3K27me3  
Received: 23 October 2022   Accepted: 28 November 2022
CLC Number: 
 
Fund: This work was supported by the grants from the National Natural Science Foundation of China (U1805232, 31770156, and 32172365) and the China Postdoctoral Science Foundation (2021M690637).
About author:  XIE Jia-hui, E-mail: bbxjh1994@163.com; #Correspondence ZHENG Hua-kun, E-mail: huakunzheng@163.com; WANG Zong-hua, E-mail: zonghuaw@163.com; ZHONG Zhen-hui, E-mail: zhenhuizhong@gmail.com; HONG Yong-he, E-mail: 13615047326@163.com

Cite this article: 

XIE Jia-hui, TANG Wei, LU Guo-dong, HONG Yong-he, ZHONG Zhen-hui, WANG Zong-hua, ZHENG Hua-kun. 2023. Histone H3K27me3 methylation regulates the expression of secreted proteins distributed at fast-evolving regions through transcriptional repression of transposable elements. Journal of Integrative Agriculture, 22(10): 3059-3068.

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