
Polycomb Repressive Complex 2-Mediated H3K27 Trimethylation Is Required for Pathogenicity in Magnaporthe oryzae
#These authors contributed equally to this work
Received date: 2021-08-20
Accepted date: 2021-11-23
Online published: 2022-04-07
Polycomb repressive complex 2 (PRC2) contributes to catalyze the methylation of histone H3 at lysine 27 and plays vital roles in transcriptional silencing and growth development in various organisms. In Magnaporthe oryzae, histone H3K27 is found to associate with altered transcription of in planta induced genes. However, it is still unknown whether and how H3K27me3 modification is involved in pathogenicity to rice and stress response. In this study, we found that core subunits of PRC2, Kmt6-Suz12-Eed, were required for fungal pathogenicity to rice in M. oryzae. Kmt6-Suz12-Eed localized in the nuclei and was necessary for the establishment of H3K27me3 modification. With ChIP-seq analysis, 9.0% of genome regions enriched with H3K27me3 occupancy, which corresponded to 1033 genes in M. oryzae. Furthermore, deletion of Kmt6, Suz12 or Eed altered genome-wide transcriptional expression, while the de-repression genes in the ∆kmt6 strain were highly associated with H3K27me3 occupancy. Notably, plenty of genes which encode effectors and secreted enzymes, secondary metabolite synthesis genes, and cell wall stress-responsive genes were directly occupied with H3K27me3 modification and de-repression in the ∆kmt6 strain. These results elaborately explained how PRC2 was required for pathogenicity, which is closely related to effector modulated host immunity and host environment adaption.
Wu Zhongling, Qiu Jiehua, Shi Huanbin, Lin Chuyu, Yue Jiangnan, Liu Zhiquan, Xie Wei, Naweed I. Naqvi, Kou Yanjun, Tao Zeng . Polycomb Repressive Complex 2-Mediated H3K27 Trimethylation Is Required for Pathogenicity in Magnaporthe oryzae[J]. Rice Science, 2022 , 29(4) : 363 -374 . DOI: 10.1016/j.rsci.2021.11.006
| [1] | Blackledge N P, Rose N R, Klose R J. 2015. Targeting Polycomb systems to regulate gene expression: Modifications to a complex story. Nat Rev Mol Cell Biol, 16: 643-649. |
| [2] | Cavalli G, Heard E. 2019. Advances in epigenetics link genetics to the environment and disease. Nature, 571: 489-499. |
| [3] | Chadha S, Sharma M. 2014. Transposable elements as stress adaptive capacitors induce genomic instability in fungal pathogen Magnaporthe oryzae. PLoS One, 9: e94415. |
| [4] | Chujo T, Scott B. 2014. Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte- plant symbiosis. Mol Microbiol, 92: 413-434. |
| [5] | Connolly L R, Smith K M, Freitag M. 2013. The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet, 9: e1003916. |
| [6] | Ding S L, Liu W D, Iliuk A, Ribot C, Vallet J, Tao A, Wang Y, Lebrun M H, Xu J R. 2010. The Tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell, 22: 2495-2508. |
| [7] | Dong Y H, Li Y, Zhao M M, Jing M F, Liu X Y, Liu M X, Guo X X, Zhang X, Chen Y, Liu Y F, Liu Y H, Ye W W, Zhang H F, Wang Y C, Zheng X B, Wang P, Zhang Z G. 2015. Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity- related genes, revealing gene gain and lose dynamics in genome evolution. PLoS Pathog, 11: e1004801. |
| [8] | Dong Y H, Li Y, Qi Z Q, Zheng X B, Zhang Z G. 2016. Genome plasticity in filamentous plant pathogens contributes to the emergence of novel effectors and their cellular processes in the host. Curr Genet, 62: 47-51. |
| [9] | Dumesic P A, Homer C M, Moresco J J, Pack L R, Shanle E K, Coyle S M, Strahl B D, Fujimori D G, Yates III J R, Madhani H D. 2015. Product binding enforces the genomic specificity of a yeast Polycomb repressive complex. Cell, 160: 204-218. |
| [10] | Feng W Z, Yin Z Y, Wu H W, Liu P, Liu X Y, Liu M X, Yu R, Gao C Y, Zhang H F, Zheng X B, Wang P, Zhang Z G. 2021. Balancing of the mitotic exit network and cell wall integrity signaling governs the development and pathogenicity in Magnaporthe oryzae. PLoS Pathog, 17: e1009080. |
| [11] | Fouché S, Plissonneau C, Croll D. 2018. The birth and death of effectors in rapidly evolving filamentous pathogen genomes. Curr Opin Microbiol, 46: 34-42. |
| [12] | Galazka J M, Freitag M. 2014. Variability of chromosome structure in pathogenic fungi: Of ‘ends and odds’. Curr Opin Microbiol, 20: 19-26. |
| [13] | He M, Xu Y P, Chen J H, Luo Y, Lv Y, Su J, Kershaw M J, Li W T, Wang J, Yin J J, Zhu X B, Liu X H, Chern M, Ma B T, Wang J C, Qin P, Chen W L, Wang Y P, Wang W M, Ren Z L, Wu X J, Li P, Li S G, Peng Y L, Lin F C, Talbot N J, Chen X W. 2018. MoSnt2-dependent deacetylation of histone H3 mediates MoTor- dependent autophagy and plant infection by the rice blast fungus Magnaporthe oryzae. Autophagy, 14: 1543-1561. |
| [14] | 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. Proc Natl Acad Sci USA, 110: 6027-6032. |
| [15] | Kassis J A, Brown J L. 2013. Polycomb group response elements in Drosophila and vertebrates. Adv Genet, 81: 83-118. |
| [16] | Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, Minami E. 2012. Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS One, 7: e49423. |
| [17] | Khang C H, Berruyer R, Giraldo M C, Kankanala P, Park S Y, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell, 22: 1388-1403. |
| [18] | Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S L. 2013. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol, 14: R36. |
| [19] | Kou Y J, Tan Y H, Ramanujam R, Naqvi N I. 2017. Structure- function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast. New Phytol, 214: 330-342. |
| [20] | Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods, 9: 357-359. |
| [21] | Langmead B, Trapnell C, Pop M, Salzberg S L. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol, 10: R25. |
| [22] | Lanzuolo C, Orlando V. 2012. Memories from the polycomb group proteins. Annu Rev Genet, 46: 561-589. |
| [23] | Lee J, Lee J J, Jeon J. 2019. A histone deacetylase, MoHOS2 regulates asexual development and virulence in the rice blast fungus. J Microbiol, 57: 1115-1125. |
| [24] | Li Z C, Fu X, Wang Y Z, Liu R Y, He Y H. 2018. Polycomb- mediated gene silencing by the BAH-EMF1 complex in plants. Nat Genet, 50: 1254-1261. |
| [25] | Margueron R, Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature, 469: 343-349. |
| [26] | Mathioni S M, Patel N, Riddick B, Sweigard J A, Czymmek K J, Caplan J L, Kunjeti S G, Kunjeti S, Raman V, Hillman B I, Kobayashi D Y, Donofrio N M. 2013. Transcriptomics of the rice blast fungus Magnaporthe oryzae in response to the bacterial antagonist Lysobacter enzymogenes reveals candidate fungal defense response genes. PLoS One, 8: e76487. |
| [27] | 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. Plant Cell, 21: 1273-1290. |
| [28] | Netea M G, Joosten L A B, Latz E, Mills K H G, Natoli G, Stunnenberg H G, O'Neill L A, Xavier R J. 2016. Trained immunity: A program of innate immune memory in health and disease. Science, 352: aaf1098. |
| [29] | Oh Y, Donofrio N, Pan H Q, Coughlan S, Brown D E, Meng S W, Mitchell T, Dean R A. 2008. Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol, 9: R85. |
| [30] | 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 Genet, 11: e1005385. |
| [31] | Qian B, Liu X Y, Ye Z Y, Zhou Q K, Liu P, Yin Z Y, Wang W H, Zheng X B, Zhang H F, Zhang Z G. 2021. Phosphatase- associated protein MoTip41 interacts with the phosphatase MoPpe1 to mediate crosstalk between TOR and cell wall integrity signalling during infection by the rice blast fungus Magnaporthe oryzae. Environ Microbiol, 23: 791-809. |
| [32] | Ridenour J B, Möller M, Freitag M. 2020. Polycomb repression without bristles: Facultative heterochromatin and genome stability in fungi. Genes, 11(6): 638. |
| [33] | Robinson J T, Thorvaldsdóttir H, Winckler W, Guttman M, Lander E S, Getz G, Mesirov J P. 2011. Integrative genomics viewer. Nat Biotechnol, 29: 24-26. |
| [34] | 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. Annu Rev Phytopathol, 56: 21-40. |
| [35] | Schuettengruber B, Bourbon H M, di Croce L, Cavalli G. 2017. Genome regulation by polycomb and trithorax: 70 years and counting. Cell, 171: 34-57. |
| [36] | Sharpee W, Oh Y, Yi M, Franck W, Eyre A, Okagaki L H, Valent B, Dean R A. 2017. Identification and characterization of suppressors of plant cell death (SPD) effectors from Magnaporthe oryzae. Mol Plant Pathol, 18: 850-863. |
| [37] | Tao Z, Shen L S, Gu X F, Wang Y Z, Yu H, He Y H. 2017. Embryonic epigenetic reprogramming by a pioneer transcription factor in plants. Nature, 551: 124-128. |
| [38] | Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol, 28: 511-515. |
| [39] | Villalba F, Collemare J, Landraud P, Lambou K, Brozek V, Cirer B, Morin D, Bruel C, Beffa R, Lebrun M H. 2008. Improved gene targeting in Magnaporthe grisea by inactivation of MgKU80 required for non-homologous end joining. Fungal Genet Biol, 45: 68-75. |
| [40] | 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 Res, 48: 1790-1799. |
| [41] | Wiles E T, Selker E U. 2017. H3K27 methylation: A promiscuous repressive chromatin mark. Curr Opin Genet Dev, 43: 31-37. |
| [42] | Wiles E T, McNaught K J, Kaur G, Selker J M L, Ormsby T, Aravind L, Selker E U. 2020. Evolutionarily ancient BAH-PHD protein mediates Polycomb silencing. Proc Natl Acad Sci USA, 117: 11614-11623. |
| [43] | Xiao J, Jin R, Yu X, Shen M, Wagner J D, Pai A, Song C, Zhuang M, Klasfeld S, He C S, Santos A M, Helliwell C, Pruneda-Paz J L, Kay S A, Lin X W, Cui S J, Garcia M F, Clarenz O, Goodrich J, Zhang X Y, Austin R S, Bonasio R, Wagner D. 2017. Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis. Nat Genet, 49: 1546-1552. |
| [44] | Yang Z L, Qian S M, Scheid R N, Lu L, Chen X S, Liu R, Du X, Lv X C, Boersma M D, Scalf M, Smith L M, Denu J M, Du J M, Zhong X H. 2018. EBS is a bivalent histone reader that regulates floral phase transition in Arabidopsis. Nat Genet, 50: 1247-1253. |
| [45] | Zhang S L, Liang M L, Naqvi N I, Lin C X, Qian W Q, Zhang L H, Deng Y Z. 2017. Phototrophy and starvation-based induction of autophagy upon removal of Gcn5-catalyzed acetylation of Atg7 in Magnaporthe oryzae. Autophagy, 13: 1318-1330. |
| [46] | 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 Genet, 17: e1009376. |
| [47] | Zhang Y, Liu T, Meyer C A, Eeckhoute J, Johnson D S, Bernstein B E, Nusbaum C, Myers R M, Brown M, Li W, Liu X S. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol, 9: R137. |
/
| 〈 |
|
〉 |