Phylogenetic profiling resolves early emergence of PRC2 and illuminates its functional core

. 2022 Jul ; 5 (7) : . [epub] 20220419

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35440471

Polycomb repressive complex 2 (PRC2) is involved in maintaining transcriptionally silent chromatin states through methylating lysine 27 of histone H3 by the catalytic subunit enhancer of zeste [E(z)]. Here, we report the diversity of PRC2 core subunit proteins in different eukaryotic supergroups with emphasis on the early-diverged lineages and explore the molecular evolution of PRC2 subunits by phylogenetics. For the first time, we identify the putative ortholog of E(z) in Discoba, a lineage hypothetically proximal to the eukaryotic root, strongly supporting emergence of PRC2 before the diversification of eukaryotes. Analyzing 283 species, we robustly detect a common presence of E(z) and ESC, indicating a conserved functional core. Full-length Su(z)12 orthologs were identified in some lineages and species only, indicating, nonexclusively, high divergence of VEFS-Box-containing Su(z)12-like proteins, functional convergence of sequence-unrelated proteins, or Su(z)12 dispensability. Our results trace E(z) evolution within the SET-domain protein family, proposing a substrate specificity shift during E(z) evolution based on SET-domain and H3 histone interaction prediction.

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Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, et al. (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66: 4–119. 10.1111/jeu.12691 Accessed February 18, 2022. PubMed DOI PMC

Alvarez-Venegas R (2014) Bacterial SET domain proteins and their role in eukaryotic chromatin modification. Front Genet 5: 65. 10.3389/fgene.2014.00065Accessed January 21, 2021. PubMed DOI PMC

Alvarez-Venegas R, Sadder M, Tikhonov A, Avramova Z (2007) Origin of the bacterial SET domain genes: Vertical or horizontal? Mol Biol Evol 24: 482–497. 10.1093/molbev/msl184Accessed January 21, 2021. PubMed DOI

Aravind L, Iyer LM (2003) Provenance of SET-domain histone methyltransferases through duplication of a simple structural unit. Cell Cycle 2: 369–376. 10.4161/cc.2.4.419 PubMed DOI

Baile F, Merini W, Hidalgo I, Calonje M (2021) EAR domain-containing transcription factors trigger PRC2-mediated chromatin marking in Arabidopsis. Plant Cell 33: 2701–2715. 10.1093/plcell/koab139Accessed December 15, 2021. PubMed DOI PMC

Bauer M, Trupke J, Ringrose L (2016) The quest for mammalian polycomb response elements: Are we there yet? Chromosoma 125: 471–496. 10.1007/s00412-015-0539-4Accessed June 22, 2021. PubMed DOI PMC

Bender LB, Cao R, Zhang Y, Strome S (2004) The MES-2/MES-3/MES-6 complex and regulation of histone H3 methylation in C. elegans. Curr Biol 14: 1639–1643. 10.1016/j.cub.2004.08.062 PubMed DOI

Berke L, Snel B (2014) The histone modification H3K27me3 is retained after gene duplication and correlates with conserved noncoding sequences in Arabidopsis. Genome Biol Evol 6: 572–579. 10.1093/gbe/evu040Accessed Februry 9, 2022. PubMed DOI PMC

Bieluszewski T, Xiao J, Yang Y, Wagner D (2021) PRC2 activity, recruitment, and silencing: A comparative perspective. Trends Plant Sci 26: 1186–1198. 10.1016/j.tplants.2021.06.006Accessed February 18, 2022. PubMed DOI

Burki F, Roger AJ, Brown MW, Simpson AGB (2020) The new tree of eukaryotes. Trends Ecol Evol 35: 43–55. 10.1016/j.tree.2019.08.008Accessed May 26, 2021. PubMed DOI

Calonje M (2014) PRC1 marks the difference in plant PcG repression. Mol Plant 7: 459–471. 10.1093/mp/sst150 PubMed DOI

Carvalho S, Raposo AC, Martins FB, Grosso AR, Sridhara SC, Rino J, Carmo-Fonseca M, De Almeida SF (2013) Histone methyltransferase SETD2 coordinates FACT recruitment with nucleosome dynamics during transcription. Nucleic Acids Res 41: 2881–2893. 10.1093/nar/gks1472Accessed March 16, 2021. PubMed DOI PMC

Chammas P, Mocavini I, Di Croce L (2020) Engaging chromatin: PRC2 structure meets function. Br J Cancer 122: 315–328. 10.1038/s41416-019-0615-2 Accessed June 22, 2021. PubMed DOI PMC

Chen DH, Huang Y, Ruan Y, Shen WH (2016) The evolutionary landscape of PRC1 core components in green lineage. Planta 243: 825–846. 10.1007/s00425-015-2451-9Accessed February 9, 2022. PubMed DOI

Cheng X, Collins RE, Zhang X (2005) Structural and sequence motifs of protein (histone) methylation enzymes. Annu Rev Biophys Biomol Struct 34: 267–294. 10.1146/annurev.biophys.34.040204.144452Accessed March 25, 2021. PubMed DOI PMC

Déléris A, Berger F, Duharcourt S (2021) Role of Polycomb in the control of transposable elements. Trends Genet 37: 882–889. 10.1016/j.tig.2021.06.003Accessed August 30, 2021. PubMed DOI

Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: Protein lysine methyltransferases. Genome Biol 6: 227. 10.1186/gb-2005-6-8-227 PubMed DOI PMC

Dumesic PA, Homer CM, Moresco JJ, Pack LR, Shanle EK, Coyle SM, Strahl BD, Fujimori DG, Yates JR, Madhani HD (2015) Product binding enforces the genomic specificity of a yeast Polycomb repressive complex. Cell 160: 204–218. 10.1016/j.cell.2014.11.039 PubMed DOI PMC

Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol 15: 711–723. 10.1038/nrmicro.2017.133Accessed March 16, 2021. PubMed DOI

Figueroa RI, Bravo I, Fraga S, Garcés E, Llaveria G (2009) The life history and cell cycle of Kryptoperidinium foliaceum, A dinoflagellate with two eukaryotic nuclei. Protist 160: 285–300. 10.1016/j.protis.2008.12.003 PubMed DOI

Frapporti A, Miró Pina C, Arnaiz O, Holoch D, Kawaguchi T, Humbert A, Eleftheriou E, Lombard B, Loew D, Sperling L, et al. (2019) The Polycomb protein Ezl1 mediates H3K9 and H3K27 methylation to repress transposable elements in Paramecium. Nat Commun 10: 2710–2715. 10.1038/s41467-019-10648-5 PubMed DOI PMC

Gahan JM, Rentzsch F, Schnitzler CE (2020) The genetic basis for PRC1 complex diversity emerged early in animal evolution. Proc Natl Acad Sci U S A 117: 22880–22889. 10.1073/pnas.2005136117Accessed February 9, 2022. PubMed DOI PMC

Hennig L, Bouveret R, Gruissem W (2005) MSI1-like proteins: An escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15: 295–302. 10.1016/j.tcb.2005.04.004 PubMed DOI

Herz HM, Garruss A, Shilatifard A (2013) SET for life: Biochemical activities and biological functions of SET domain-containing proteins. Trends Biochem Sci 38: 621–639. 10.1016/j.tibs.2013.09.004Accessed March 23, 2020. PubMed DOI PMC

Huang Y, Chen DH, Liu BY, Shen WH, Ruan Y (2017) Conservation and diversification of polycomb repressive complex 2 (PRC2) proteins in the green lineage. Brief Funct Genomics 16: 106–119. 10.1093/bfgp/elw007 PubMed DOI

Jacob Y, Feng S, LeBlanc CA, Bernatavichute YV, Stroud H, Cokus S, Johnson LM, Pellegrini M, Jacobsen SE, Michaels SD (2009) ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol 16: 763–768. 10.1038/nsmb.1611Accessed March 15, 2021. PubMed DOI PMC

Jamieson K, Rountree MR, Lewis ZA, Stajich JE, Selker EU (2013) Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Natl Acad Sci U S A 110: 6027–6032. 10.1073/pnas.1303750110 PubMed DOI PMC

Jiao L, Liu X (2016) Structural analysis of an active fungal PRC2. Nucleus 7: 284–291. 10.1080/19491034.2016.1183849Accessed December 14, 2021. PubMed DOI PMC

Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, Armbrust EV, Archibald JM, Bharti AK, Bell CJ, et al. (2014) The marine microbial eukaryote transcriptome sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol 12: e1001889. 10.1371/journal.pbio.1001889 PubMed DOI PMC

Ketel CS, Andersen EF, Vargas ML, Suh J, Strome S, Simon JA (2005) Subunit contributions to histone methyltransferase activities of fly and worm polycomb group complexes. Mol Cell Biol 25: 6857–6868. 10.1128/mcb.25.16.6857-6868.2005 PubMed DOI PMC

Köhler C, Villar CBR (2008) Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18: 236–243. 10.1016/j.tcb.2008.02.005Accessed October 31, 2020. PubMed DOI

Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A, Wren J (2019) RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. 10.1093/bioinformatics/btz305 PubMed DOI PMC

Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA, Graham SW, Grosse I, Li Z, Melkonian M, Mirarab S, et al. (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574: 679–685. 10.1038/s41586-019-1693-2 PubMed DOI PMC

Leger MM, Kolisko M, Kamikawa R, Stairs CW, Kume K, Čepička I, Silberman JD, Andersson JO, Xu F, Yabuki A, et al. (2017) Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes. Nat Ecol Evol 1: 0092. 10.1038/s41559-017-0092Accessed April 1, 2021. PubMed DOI PMC

Lewis ZA (2017) Polycomb group systems in fungi: New models for understanding polycomb repressive complex 2. Trends Genet 33: 220–231. 10.1016/j.tig.2017.01.006Accessed February 18, 2022. PubMed DOI

Lhuillier-Akakpo M, Frapporti A, Denby Wilkes C, Matelot M, Vervoort M, Sperling L, Duharcourt S (2014) Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements. PLoS Genet 10: e1004665. 10.1371/journal.pgen.1004665Accessed December 28, 2021. PubMed DOI PMC

Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung MS, Ercan S, Ikegami K, Jensen M, Kolasinska-Zwierz P, et al. (2011) Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 21: 227–236. 10.1101/gr.115519.110Accessed June 22, 2021. PubMed DOI PMC

Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, Allis CD (2007) RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21: 1530–1545. 10.1101/gad.1544207Accessed January 4, 2022. PubMed DOI PMC

Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343–349. 10.1038/nature09784Accessed June 22, 2021. PubMed DOI PMC

Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250. 10.1126/science.1143609 PubMed DOI PMC

Mikulski P, Komarynets O, Fachinelli F, Weber APM, Schubert D (2017) Characterization of the polycomb-group mark H3K27me3 in unicellular algae. Front Plant Sci 8: 607. 10.3389/fpls.2017.00607 PubMed DOI PMC

Mozgova I, Köhler C, Hennig L (2015) Keeping the gate closed: Functions of the polycomb repressive complex PRC2 in development. Plant J 83: 121–132. 10.1111/tpj.12828Accessed May 8, 2021. PubMed DOI

Müller J, Verrijzer P (2009) Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev 19: 150–158. 10.1016/j.gde.2009.03.001 PubMed DOI

O’Donnell S, Chaux F, Fischer G (2020) Highly contiguous nanopore genome assembly of Chlamydomonas reinhardtii CC-1690. Microbiol Resour Announc 9: e00726-20. 10.1128/MRA.00726-20 PubMed DOI PMC

Pina CM, Kawaguchi T, Charmant O, Michaud A, Cohen I, Humbert A, Jaszczyszyn Y, Del Maestro L, Holoch D, Ait-Si-Ali S, et al. (2021) Paramecium polycomb repressive complex 2 physically interacts with the small RNA binding PIWI protein to repress transposable elements. BioRxiv 10.1101/2021.08.12.456067Accessed December 15, 2021 Preprint posted Posted August 12, 2021. PubMed DOI

Piunti A, Shilatifard A (2021) The roles of Polycomb repressive complexes in mammalian development and cancer. Nat Rev Mol Cell Biol 22: 326–345. 10.1038/s41580-021-00341-1Accessed May 24, 2021. PubMed DOI

Rai AN, Vargas ML, Wang L, Andersen EF, Miller EL, Simon JA (2013) Elements of the polycomb repressor SU(Z)12 needed for histone H3-K27 methylation, the interface with E(Z), and in vivo function. Mol Cell Biol 33: 4844–4856. 10.1128/MCB.00307-13Accessed February 9, 2022. PubMed DOI PMC

Ridenour JB, Möller M, Freitag M (2020) Polycomb repression without bristles: Facultative heterochromatin and genome stability in fungi. Genes (Basel) 11: 638. 10.3390/genes11060638Accessed February 18, 2022. PubMed DOI PMC

Schuettengruber B, Bourbon HM, Di Croce L, Cavalli G (2017) Genome regulation by polycomb and trithorax: 70 years and counting. Cell 171: 34–57. 10.1016/j.cell.2017.08.002Accessed May 24, 2021. PubMed DOI

Seppey M, Manni M, Zdobnov EM (2019) BUSCO: Assessing genome assembly and annotation completeness. Methods Mol Biol 1962: 227–245. 10.1007/978-1-4939-9173-0_14 PubMed DOI

Shaver S, Casas-Mollano JA, Cerny RL, Cerutti H (2010) Origin of the polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics 5: 301–312. 10.4161/epi.5.4.11608Accessed March 19, 2020. PubMed DOI

Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, et al. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754–759. 10.1126/science.282.5389.754Accessed January 25, 2021. PubMed DOI

Suganuma T, Pattenden SG, Workman JL (2008) Diverse functions of WD40 repeat proteins in histone recognition. Genes Dev 22: 1265–1268. 10.1101/gad.1676208Accessed October 27, 2020. PubMed DOI PMC

Tikhonenkov DV, Strassert JFH, Janouškovec J, Mylnikov AP, Aleoshin VV, Burki F, Keeling PJ (2020) Predatory colponemids are the sister group to all other alveolates. Mol Phylogenet Evol 149: 106839. 10.1016/j.ympev.2020.106839 PubMed DOI

Tracy C, Warren JS, Szulik M, Wang L, Garcia J, Makaju A, Russell K, Miller M, Franklin S (2018) The smyd family of methyltransferases: Role in cardiac and skeletal muscle physiology and pathology. Curr Opin Physiol 1: 140–152. 10.1016/j.cophys.2017.10.001Accessed March 16, 2021. PubMed DOI PMC

Vervoort M, Meulemeester D, Béhague J, Kerner P (2016) Evolution of prdm genes in animals: Insights from comparative genomics. Mol Biol Evol 33: 679–696. 10.1093/molbev/msv260Accessed July 24, 2020. PubMed DOI PMC

Vijayanathan M, Trejo-Arellano MG, Mozgová I (2022) Polycomb repressive complex 2 in eukaryotes-an evolutionary perspective. Epigenomes 6: 3. 10.3390/epigenomes6010003Accessed February 9, 2022. PubMed DOI PMC

Wiles ET, Selker EU (2017) H3K27 methylation: A promiscuous repressive chromatin mark. Curr Opin Genet Dev 43: 31–37. 10.1016/j.gde.2016.11.001 PubMed DOI PMC

Xu J, Zhao X, Mao F, Basrur V, Ueberheide B, Chait BT, Allis CD, Taverna SD, Gao S, Wang W, et al. (2021) NAR breakthrough article A polycomb repressive complex is required for RNAi-mediated heterochromatin formation and dynamic distribution of nuclear bodies. Nucleic Acids Res 49: 5407–5425. 10.1093/nar/gkaa1262Accessed December 14, 2021. PubMed DOI PMC

Yeates TO (2002) Structures of SET domain proteins: Protein lysine methyltransferases make their mark. Cell 111: 5–7. 10.1016/s0092-8674(02)01010-3 PubMed DOI

Zhang L, Ma H (2012) Complex evolutionary history and diverse domain organization of SET proteins suggest divergent regulatory interactions. New Phytol 195: 248–263. 10.1111/j.1469-8137.2012.04143.xAccessed March 21, 2020. PubMed DOI

Zhao X, Deton Cabanillas AF, Veluchamy A, Bowler C, Vieira FRJ, Tirichine L (2020) Probing the diversity of polycomb and Trithorax proteins in cultured and environmentally sampled microalgae. Front Mar Sci 7: 1–17. 10.3389/fmars.2020.00189 PubMed DOI

Zhao X, Rastogi A, Deton Cabanillas AF, Ait Mohamed O, Cantrel C, Lombard B, Murik O, Genovesio A, Bowler C, Bouyer D, et al. (2021) Genome wide natural variation of H3K27me3 selectively marks genes predicted to be important for cell differentiation in Phaeodactylum tricornutum. New Phytol 229: 3208–3220. 10.1111/nph.17129Accessed May 24, 2021. PubMed DOI

Zhou H, Liu Y, Liang Y, Zhou D, Li S, Lin S, Dong H, Huang L (2020) The function of histone lysine methylation related SET domain group proteins in plants. Protein Sci 29: 1120–1137. 10.1002/pro.3849Accessed March 21, 2020. PubMed DOI PMC

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