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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-hui5#, WANG Zonghua1, 3#, ZHENG Hua-kun1, 2, 4#

1State 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

2Fujian Universities Key Laboratory for Plant Microbe Interaction, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, P.R.China

3Fuzhou Institute of Oceanography, Minjiang University, Fuzhou 350108, P.R.China

4National Engineering Research Center of JUNCAO Technology, College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, P.R.China

5Current address: Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA 90095, USA

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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 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.
Keywords:  secreted protein       transposable elements       fast-evolving regions      H3K27me3  
Online: 24 January 2023  
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This work was supported by grants from the Natural Science Foundations of China to Zonghua Wang (U1805232 and 31770156) and Huakun Zheng (32172365), China Postdoctoral Science Foundation (2021M690637) to Yonghe Hong.

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 Zonghua, 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, Doi:10.1016/j.jia.2023.01.011

 ADDIN EN.REFLIST Castanera R, Lopez-Varas L, Borgognone A, LaButti K, Lapidus A, Schmutz J, Grimwood J, Perez G, Pisabarro A G,Grigoriev I V. 2016. Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genetics, 12, e1006108.

Chen S B, Songkumarn P, Venu R, Gowda M, Bellizzi M, Hu J N, Liu W D, Ebbole D, Meyers B,Mitchell T. 2013. Identification and characterization of in planta–expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice. Molecular

Plant-Microbe Interactions, 26, 191-202.

Cho Y, Ohm R A, Grigoriev I V,Srivastava A. 2013. Fungal‐specific transcription factor AbPf2 activates pathogenicity in Alternaria brassicicola. The Plant Journal, 75, 498-514.

Chujo T,Scott B. 2014. Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte–plant symbiosis. Molecular Microbiology, 92, 413-434.

Connolly L R, Smith K M,Freitag M. 2013. The Fusarium graminearum histone H3K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genetics, 9, e1003916.

Croll D,McDonald B A. 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathogens, 8, e1002608.

Dallery J-F, Lapalu N, Zampounis A, Pigné S, Luyten I, Amselem J, Wittenberg A H, Zhou S, de Queiroz M V,Robin G P. 2017. Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters. BMC Genomics, 18, 1-22.

Dean R, Van Kan J A, Pretorius Z A, Hammond‐Kosack K E, Di Pietro A, Spanu P D, Rudd J J, Dickman M, Kahmann R,Ellis J. 2012. The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13, 414-430.

Dean R A, Talbot N J, Ebbole D J, Farman M L, Mitchell T K, Orbach M J, Thon M, Kulkarni R, Xu J-R,Pan H. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature, 434, 980-986.

Déléris A, Berger F,Duharcourt S. 2021. Role of Polycomb in the control of transposable elements. Trends in Genetics, 37, 882-889.

Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie A R,Feussner I. 2011. Metabolic priming by a secreted fungal effector. Nature, 478, 395-398.

Dong S M, Raffaele S,Kamoun S. 2015. The two-speed genomes of filamentous pathogens: waltz with plants. Current Opinion in Genetics Development, 35, 57-65.

Fouché S, Badet T, Oggenfuss U, Plissonneau C, Francisco C S,Croll D. 2020. Stress-driven transposable element de-repression dynamics and virulence evolution in a fungal pathogen. Molecular Biology Evolution, 37, 221-239.

Freitag M. 2017. Histone methylation by SET domain proteins in fungi. Annual Review of Microbiology, 71, 413-439.

Gacek A,Strauss J. 2012. The chromatin code of fungal secondary metabolite gene clusters. Applied Microbiology Biotechnology, 95, 1389-1404.

Giraldo M C, Dagdas Y F, Gupta Y K, Mentlak T A, Yi M, Martinez-Rocha A L, Saitoh H, Terauchi R, Talbot N J,Valent B. 2013. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nature Communications, 4, 1-12.

Giraldo M C,Valent B. 2013. Filamentous plant pathogen effectors in action. 11, 800-814.

Gómez-Rubio V. 2017. ggplot2-elegant graphics for data analysis. Journal of Statistical Software, 77, 1-3.

Guo X R, Zhong D B, Xie W, He Y H, Zheng Y Q, Lin Y, Chen Z J, Han Y J, Tian D G,Liu W D. 2019. Functional identification of novel cell death-inducing effector proteins from Magnaporthe oryzae. Rice, 12, 1-12.

Honda S,Selker E U. 2008. Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora crassa. Molecular Cellular Biology, 28, 6044-6055.

Hosaka A,Kakutani T. 2018. Transposable elements, genome evolution and transgenerational epigenetic variation. Current Opinion in Genetics Development, 49, 43-48.

Islam M T, Croll D, Gladieux P, Soanes D M, Persoons A, Bhattacharjee P, Hossain M, Gupta D R, Rahman M,Mahboob M G. 2016. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology, 14, 1-11.

Jamieson K, Rountree M R, Lewis Z A, Stajich J E,Selker E U. 2013. Regional control of histone H3 lysine 27 methylation in Neurospora. Proceedings of the National Academy of Sciences, 110, 6027-6032.

Kasuga T,Gijzen M. 2013. Epigenetics and the evolution of virulence. Trends in Microbiology, 21, 575-582.

Kershaw M J,Talbot N J. 2009. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proceedings of the National Academy of Sciences, 106, 15967-15972.

Latorre S M, Reyes-Avila C S, Malmgren A, Win J, Kamoun S,Burbano H A. 2020. Differential loss of effector genes in three recently expanded pandemic clonal lineages of the rice blast fungus. BMC Biology, 18, 1-15.

Li B,Dewey C N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 1-16.

Li Y, Han Y J, Qu M Y, Chen J, Chen X F, Geng X Q, Wang Z H,Chen S B. 2020. Apoplastic cell death-inducing proteins of filamentous plant pathogens: roles in plant-pathogen interactions. Frontiers in Genetics, 11, 661.

Lin C Y, Wu Z L, Shi H B, Yu J W, Xu M T, Lin F C, Kou Y J,Tao Z. 2022. The additional PRC2 subunit and Sin3 histone deacetylase complex are required for the normal distribution of H3K27me3 occupancy and transcriptional silencing in Magnaporthe oryzae. New Phytologist, 236, 576-589

Meile L, Peter J, Puccetti G, Alassimone J, McDonald B A,Sánchez-Vallet A. 2020. Chromatin dynamics contribute to the spatiotemporal expression pattern of virulence genes in a fungal plant pathogen. MBio, 11, e02343-02320.

Meng S, Liu Z Q, Shi H B, Wu Z L, Qiu J H, Wen H, Lin F C, Tao Z, Luo C X,Kou Y J. 2021. UvKmt6-mediated H3K27 trimethylation is required for development, pathogenicity, and stress response in Ustilaginoidea virens. Virulence, 12, 2972-2988.

Mirzadi Gohari A, Mehrabi R, Robert O, Ince I A, Boeren S, Schuster M, Steinberg G, De Wit P J,Kema G H. 2014. Molecular characterization and functional analyses of ZtWor1, a transcriptional regulator of the fungal wheat pathogen Zymoseptoria tritici. Molecular Plant Pathology, 15, 394-405.

Mosquera G, Giraldo M C, Khang C H, Coughlan S,Valent B. 2009. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. The Plant Cell, 21, 1273-1290.

Nishimura T, Mochizuki S, Ishii-Minami N, Fujisawa Y, Kawahara Y, Yoshida Y, Okada K, Ando S, Matsumura H,Terauchi R. 2016. Magnaporthe oryzae glycine-rich secretion protein, Rbf1 critically participates in pathogenicity through the focal formation of the biotrophic interfacial complex. PLoS Pathogens, 12, e1005921.

Ökmen B, Collemare J, Griffiths S, van der Burgt A, Cox R,de Wit P J. 2014. Functional analysis of the conserved transcriptional regulator CfWor1 in Cladosporium fulvum reveals diverse roles in the virulence of plant pathogenic fungi. Molecular Microbiology, 92, 10-27.

Pham K T M, Inoue Y, Vu B V, Nguyen H H, Nakayashiki T, Ikeda K-i,Nakayashiki H. 2015. MoSET1 (histone H3K4 methyltransferase in Magnaporthe oryzae) regulates global gene expression during infection-related morphogenesis. PLoS Genetics, 11, e1005385.

Rebollo R, Romanish M T,Mager D L. 2012. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annual Review of Genetics, 46, 21-42.

Robinson M D, McCarthy D J,Smyth G K. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.

Rodriguez‐Moreno L, Ebert M K, Bolton M D,Thomma B P. 2018. Tools of the crook‐infection strategies of fungal plant pathogens. The Plant Journal, 93, 664-674.

Rovenich H, Boshoven J C,Thomma B P. 2014. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Current Opinion in Plant Biology, 20, 96-103.

Rybak K, See P T, Phan H T, Syme R A, Moffat C S, Oliver R P,Tan K C. 2017. A functionally conserved Zn2Cys6 binuclear cluster transcription factor class regulates necrotrophic effector gene expression and host‐specific virulence of two major Pleosporales fungal pathogens of wheat. Molecular Plant Pathology, 18, 420-434.

Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H, Yoshino K, Yoshida K,Matsumura H. 2012. Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PloS Pathogens, 8, e1002711.

Sánchez-Vallet A, Fouché S, Fudal I, Hartmann F E, Soyer J L, Tellier A,Croll D. 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annual Review of Phytopathology, 56, 21-40.

Santhanam P,Thomma B P. 2013. Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Molecular Plant-Microbe Interactions, 26, 249-256.

Schmidt S M,Panstruga R. 2011. Pathogenomics of fungal plant parasites: what have we learnt about pathogenesis? Current Opinion in Plant Biology, 14, 392-399.

Seidl M F,Thomma B P. 2017. Transposable elements direct the coevolution between plants and microbes. Trends in Genetics, 33, 842-851.

Slotkin R K,Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8, 272-285.

Soyer J L, El Ghalid M, Glaser N, Ollivier B, Linglin J, Grandaubert J, Balesdent M-H, Connolly L R, Freitag M,Rouxel T. 2014. Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genetics, 10, e1004227.

Studt L, Janevska S, Arndt B, Boedi S, Sulyok M, Humpf H-U, Tudzynski B,Strauss J. 2017. Lack of the COMPASS component Ccl1 reduces H3K4 trimethylation levels and affects transcription of secondary metabolite genes in two plant–pathogenic Fusarium species. Frontiers in Microbiology, 7, 2144.

Studt L, Rösler S M, Burkhardt I, Arndt B, Freitag M, Humpf H U, Dickschat J S,Tudzynski B. 2016. Knock‐down of the methyltransferase Kmt6 relieves H3K27me3 and results in induction of cryptic and otherwise silent secondary metabolite gene clusters in Fusarium fujikuroi. Environmental Microbiology, 18, 4037-4054.

Wang L Y, Chen H, Li J J, Shu H D, Zhang X X, Wang Y C, Tyler B M,Dong S M. 2020. Effector gene silencing mediated by histone methylation underpins host adaptation in an oomycete plant pathogen. Nucleic Acids Research, 48, 1790-1799.

Wu C X, Lin Y H, Zheng H W, Abubakar Y S, Peng M H, Li J J, Yu Z, Wang Z H, Naqvi N I,Li G P. 2021. The retromer CSC subcomplex is recruited by MoYpt7 and sequentially sorted by MoVps17 for effective conidiation and pathogenicity of the rice blast fungus. Molecular Plant Pathology, 22, 284-298.

Wu Z L, Qiu J H, Shi H B, Lin C Y, Yue J-N, Liu Z Q, Xie W, Kou Y J,Tao Z. 2021. Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression of effectors and regulate pathogenicity in Magnaporthe oryzae. bioRxiv.

Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y, Chuma I, Takano Y,Win J. 2009. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. The Plant Cell, 21(5), 1573-1591.

Zhang W, Huang J,Cook D E. 2021. Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae. PLoS Genetics, 17, e1009376.

Zhong Z H, Chen M L, Lin L Y, Chen R Q, Liu D, Norvienyeku J, Zheng H K,Wang Z H. 2020. Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae. Msystems, 5, e00346-00320.

Zhong Z H, Lin L Y, Chen M L, Lin L L, Chen X F, Lin Y H, Chen X, Wang Z H, Norvienyeku J,Zheng H K. 2019. Expression divergence as an evolutionary alternative mechanism adopted by two rice subspecies against rice blast infection. Rice, 12, 1-10.

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