Skip to main content
SpringerLink
Log in

Not all Is SET for Methylation: Evolution of Eukaryotic Protein Methyltransferases

  • Protocol
  • First Online:
Histone Methyltransferases

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2529))

Abstract

Dynamic posttranslational modifications to canonical histones that constitute the nucleosome (H2A, H2B, H3, and H4) control all aspects of enzymatic transactions with DNA. Histone methylation has been studied heavily for the past 20 years, and our mechanistic understanding of the control and function of individual methylation events on specific histone arginine and lysine residues has been greatly improved over the past decade, driven by excellent new tools and methods. Here, we will summarize what is known about the distribution and some of the functions of protein methyltransferases from all major eukaryotic supergroups. The main conclusion is that protein, and specifically histone, methylation is an ancient process. Many taxa in all supergroups have lost some subfamilies of both protein arginine methyltransferases (PRMT) and the heavily studied SET domain lysine methyltransferases (KMT). Over time, novel subfamilies, especially of SET domain proteins, arose. We use the interactions between H3K27 and H3K36 methylation as one example for the complex circuitry of histone modifications that make up the “histone code,” and we discuss one recent example (Paramecium Ezl1) for how extant enzymes that may resemble more ancient SET domain KMTs are able to modify two lysine residues that have divergent functions in plants, fungi, and animals. Complexity of SET domain KMT function in the well-studied plant and animal lineages arose not only by gene duplication but also acquisition of novel DNA- and histone-binding domains in certain subfamilies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Allis CD (2015) Epigenetics, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  2. Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32:6511–6518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Wu T, Yuan T, Tsai SN, Wang C, Sun SM, Lam HM, Ngai SM (2009) Mass spectrometry analysis of the variants of histone H3 and H4 of soybean and their post-translational modifications. BMC Plant Biol 9:98

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Lu CC, Coradin M, Porter EG, Garcia BA (2021) Accelerating the field of epigenetic histone modification through mass spectrometry-based approaches. Mol Cell Proteomics 20:100006

    Article  CAS  PubMed  Google Scholar 

  5. Sidoli S, Kori Y, Lopes M, Yuan ZF, Kim HJ, Kulej K, Janssen KA, Agosto LM, da Cunha JPC, Andrews AJ, Garcia BA (2019) One minute analysis of 200 histone posttranslational modifications by direct injection mass spectrometry. Genome Res 29:978–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Garcia B (2016) Quantitative proteomics for understanding the histone code. J Biomol Tech 24(supplement):S10

    Google Scholar 

  7. Allshire RC, Madhani HD (2018) Ten principles of heterochromatin formation and function. Nat Rev Mol Cell Bio 19:229–244

    Article  CAS  Google Scholar 

  8. Iyer LM, Anantharaman V, Wolf MY, Aravind L (2008) Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol 38:1–31

    Article  CAS  PubMed  Google Scholar 

  9. Burki F, Roger AJ, Brown MW, Simpson AGB (2020) The new tree of eukaryotes. Trends Ecol Evol 35:43–55

    Article  PubMed  Google Scholar 

  10. Burki F (2014) The eukaryotic tree of life from a global Phylogenomic perspective. CSH Perspect Biol 6:a016147

    Google Scholar 

  11. Leger MM, Kolisko M, Kamikawa R, Stairs CW, Kume K, Cepicka I, Silberman JD, Andersson JO, Xu FF, Yabuki A, Eme L, Zhang QQ, Takishita K, Inagaki Y, Simpson AGB, Hashimoto T, Roger AJ (2017) Organelles that illuminate the origins of trichomonas hydrogenosomes and giardia mitosomes. Nat Ecol Evol 1:0092

    Article  PubMed  PubMed Central  Google Scholar 

  12. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JEJ, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926

    Article  CAS  PubMed  Google Scholar 

  13. Xu FF, Jex A, Svard SG (2020) A chromosome-scale reference genome for Giardia intestinalis WB. Sci Data 7:38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Adam RD (2000) The Giardia lamblia genome. Int J Parasitol 30:475–484

    Article  CAS  PubMed  Google Scholar 

  15. Sodre CL, Chapeaurouge AD, Kalume DE, Lima LD, Perales J, Fernandes O (2009) Proteomic map of Trypanosoma cruzi CL Brener: the reference strain of the genome project. Arch Microbiol 191:177–184

    Article  CAS  PubMed  Google Scholar 

  16. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou LH, Huang YT, Kindlund E, Ktingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarteton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409–415

    Article  CAS  PubMed  Google Scholar 

  17. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DMA, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite plasmodium falciparum. Nature 419:498–511

    Article  CAS  PubMed  Google Scholar 

  18. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bouligand Y, Norris V (2001) Chromosome separation and segregation in dinoflagellates and bacteria may depend on liquid crystalline states. Biochimie 83:187–192

    Article  CAS  PubMed  Google Scholar 

  20. Rizzo PJ (1991) The enigma of the dinoflagellate chromosome. J Protozool 38:246–252

    Article  Google Scholar 

  21. Rizzo PJ (2003) Those amazing dinoflagellate chromosomes. Cell Res 13:215–217

    Article  CAS  PubMed  Google Scholar 

  22. Gonzalez-Pech RA, Stephens TG, Chen YB, Mohamed AR, Cheng YY, Shah S, Dougan KE, Fortuin MDA, Lagorce R, Burt DW, Bhattacharya D, Ragan MA, Chan CX (2021) Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium. BMC Biol 19:73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Preer JR Jr (2000) Epigenetic mechanisms affecting macronuclear development in paramecium and Tetrahymena. J Eukaryot Microbiol 47:515–524

    Article  CAS  PubMed  Google Scholar 

  24. Ruiz F, Vayssie L, Klotz C, Sperling L, Madeddu L (1998) Homology-dependent gene silencing in paramecium. Mol Biol Cell 9:931–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Cummings DJ, Tait A, Goddard JM (1974) Methylated bases in DNA from Paramecium aurelia. Biochim Biophys Acta 374:1–11

    Article  CAS  PubMed  Google Scholar 

  26. Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Segurens B, Daubin V, Anthouard V, Aiach N, Arnaiz O, Billaut A, Beisson J, Blanc I, Bouhouche K, Camara F, Duharcourt S, Guigo R, Gogendeau D, Katinka M, Keller AM, Kissmehl R, Klotz C, Koll F, Le Mouel A, Lepere G, Malinsky S, Nowacki M, Nowak JK, Plattner H, Poulain J, Ruiz F, Serrano V, Zagulski M, Dessen P, Betermier M, Weissenbach J, Scarpelli C, Schachter V, Sperling L, Meyer E, Cohen J, Wincker P (2006) Global trends of whole-genome duplications revealed by the ciliate paramecium tetraurelia. Nature 444:171–178

    Article  CAS  PubMed  Google Scholar 

  27. Agyekum TP, Botwe PK, Arko-Mensah J, Issah I, Acquah AA, Hogarh JN, Dwomoh D, Robins TG, Fobil JN (2021) A systematic review of the effects of temperature on anopheles mosquito development and survival: implications for malaria control in a future warmer climate. Int J Environ Res Public Health 18:7255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Clement R, Dimnet L, Maberly SC, Gontero B (2016) The nature of the CO2-concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytol 209:1417–1427

    Article  CAS  PubMed  Google Scholar 

  29. Duan DL, Wang XL, Yao JT, Liu DY, Hong WG, Hu ZM, Xia YH, Shao ZR, Li QY, Zhang J (2013) Draft genome sequences of Saccharina japonica. Phycologia 52:27–27

    Google Scholar 

  30. Liu T, Wang XM, Wang GL, Jia SG, Liu GM, Shan GL, Chi S, Zhang J, Yu YH, Xue T, Yu J (2019) Evolution of complex thallus alga: genome sequencing of Saccharina japonica. Front Genet 10:378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ye NH, Zhang XW, Miao M, Fan X, Zheng Y, Xu D, Wang JF, Zhou L, Wang DS, Gao Y, Wang YT, Shi WY, Ji PF, Li DM, Guan Z, Shao CW, Zhuang ZM, Gao ZW, Qi J, Zhao FQ (2015) Saccharina genomes provide novel insight into kelp biology. Nat Commun 6:6986

    Article  CAS  PubMed  Google Scholar 

  32. Mao YX, Tyler BM (1996) The Phytophthora sojae genome contains tandem repeat sequences which vary from strain to strain. Fungal Genet Biol 20:43–51

    Article  CAS  PubMed  Google Scholar 

  33. Zhang X, Liu B, Zou F, Shen DY, Yin ZY, Wang RB, He F, Wang YC, Tyler BM, Fan W, Qian WQ, Dou DL (2019) Whole genome re-sequencing reveals natural variation and adaptive evolution of Phytophthora sojae. Front Microbiol 10:2792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie JM, Frickenhaus S, Gonzalez K, Herman EK, Lin YC, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G, Dacks JB, Delwiche CF, Dyhrman ST, Glockner G, John U, Richards T, Worden AZ, Zhang XY, Grigoriev IV, Allen AE, Bidle K, Borodovsky M, Bowler C, Brownlee C, Cock JM, Elias M, Gladyshev VN, Groth M, Guda C, Hadaegh A, Iglesias-Rodriguez MD, Jenkins J, Jones BM, Lawson T, Leese F, Lindquist E, Lobanov A, Lomsadze A, Malik SB, Marsh ME, Mackinder L, Mock T, Mueller-Roeber B, Pagarete A, Parker M, Probert I, Quesneville H, Raines C, Rensing SA, Riano-Pachon DM, Richier S, Rokitta S, Shiraiwa Y, Soanes DM, van der Giezen M, Wahlund TM, Williams B, Wilson W, Wolfe G, Wurch LL, Annotation EH (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213

    Article  CAS  PubMed  Google Scholar 

  35. Westbroek P, Brown CW, Vanbleijswijk J, Brownlee C, Brummer GJ, Conte M, Egge J, Fernandez E, Jordan R, Knappertsbusch M, Stefels J, Veldhuis M, Vanderwal P, Young J (1993) A model system approach to biological climate forcing - the example of Emiliania huxleyi. Glob Planet Chang 8:27–46

    Article  Google Scholar 

  36. Seitz R (2011) Bright water: hydrosols, water conservation and climate change. Clim Chang 105:365–381

    Article  Google Scholar 

  37. Lefebvre SC, Benner I, Stillman JH, Parker AE, Drake MK, Rossignol PE, Okimura KM, Komada T, Carpenter EJ (2012) Nitrogen source and pCO(2) synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle. Glob Chang Biol 18:493–503

    Article  Google Scholar 

  38. Archibald JM, Lane CE (2009) Going, going, not quite gone: Nucleomorphs as a case study in nuclear genome reduction. J Hered 100:582–590

    Article  CAS  PubMed  Google Scholar 

  39. Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF, Kuo A, Rensing SA, Schmutz J, Symeonidi A, Elias M, Eveleigh RJM, Herman EK, Klute MJ, Nakayama T, Obornik M, Reyes-Prieto A, Armbrust EV, Aves SJ, Beiko RG, Coutinho P, Dacks JB, Durnford DG, Fast NM, Green BR, Grisdale CJ, Hempel F, Henrissat B, Hoppner MP, Ishida KI, Kim E, Koreny LK, Kroth PG, Liu Y, Malik SB, Maier UG, McRose D, Mock T, Neilson JAD, Onodera NT, Poole AM, Pritham EJ, Richards TA, Rocap G, Roy SW, Sarai C, Schaack S, Shirato S, Slamovits CH, Spencer DF, Suzuki S, Worden AZ, Zauner S, Barry K, Bell C, Bharti AK, Crow JA, Grimwood J, Kramer R, Lindquist E, Lucas S, Salamov A, McFadden GI, Lane CE, Keeling PJ, Gray MW, Grigoriev IV, Archibald JM (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65

    Article  CAS  PubMed  Google Scholar 

  40. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Babu MM, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tang X, Zhao L, Chen H, Chen YQ, Chen W, Song Y, Ratledge C (2015) Complete genome sequence of a high lipid-producing strain of Mucor circinelloides WJ11 and comparative genome analysis with a low lipid-producing strain CBS 277.49. PLoS One 10:e0137543

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:546–567

    Article  CAS  PubMed  Google Scholar 

  43. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868

    Article  CAS  PubMed  Google Scholar 

  44. Kämper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

    Article  PubMed  CAS  Google Scholar 

  45. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu SQ, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng JS, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PRH, Zhang XM, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Boettger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TCG, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of hydra. Nature 464:592–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Adema CM, Hillier LW, Jones CS, Loker ES, Knight M, Minx P, Oliveira G, Raghavan N, Shedlock A, do Amaral LR, Arican-Goktas HD, Assis JG, Baba EH, Baron OL, Bayne CJ, Bickham-Wright U, Biggar KK, Blouin M, Bonning BC, Botka C, Bridger JM, Buckley KM, Buddenborg SK, Caldeira RL, Carleton J, Carvalho OS, Castillo MG, Chalmers IW, Christensens M, Clifton S, Cosseau C, Coustau C, Cripps RM, Cuesta-Astroz Y, Cummins SF, Di Stephano L, Dinguirard N, Duval D, Emrich S, Feschotte C, Feyereisen R, FitzGerald P, Fronick C, Fulton L, Galinier R, Gava SG, Geusz M, Geyer KK, Giraldo-Calderon GI, Gomes MD, Gordy MA, Gourbal B, Grunau C, Hanington PC, Hoffmann KF, Hughes D, Humphries J, Jackson DJ, Jannotti-Passos LK, Jeremias WD, Jobling S, Kamel B, Kapusta A, Kaur S, Koene JM, Kohn AB, Lawson D, Lawton SP, Liang D, Limpanont Y, Liu SJ, Lockyer AE, Lovato TL, Ludolf F, Magrini V, McManus DP, Medina M, Misra M, Mitta G, Mkoji GM, Montague MJ, Montelongo C, Moroz LL, Munoz-Torres MC, Niazi U, Noble LR, Oliveira FS, Pais FS, Papenfuss AT, Peace R, Pena JJ, Pila EA, Quelais T, Raney BJ, Rast JP, Rollinson D, Rosse IC, Rotgans B, Routledge EJ, Ryan KM, Scholte LLS, Storey KB, Swain M, Tennessen JA, Tomlinson C, Trujillo DL, Volpi EV, Walker AJ, Wang T, Wannaporn I, Warren WC, Wu XJ, Yoshino TP, Yusuf M, Zhang SM, Zhao M, Wilson RK (2017) Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nat Commun 8:15451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YHC, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Miklos GLG, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies A, de Pablos B, Delcher A, Deng ZM, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong FC, Gorrell JH, Gu ZP, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston DA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke ZX, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai ZW, Lasko P, Lei YD, Levitsky AA, Li JY, Li ZY, Liang Y, Lin XY, Liu XJ, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RDC, Scheeler F, Shen H, Shue BC, Siden-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AHH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, Woodage T, Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang GG, Zhao Q, Zheng LS, Zheng XQH, Zhong FN, Zhong WY, Zhou XJ, Zhu SP, Zhu XH, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

    Article  PubMed  Google Scholar 

  48. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XQH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang JH, Miklos GLG, Nelson C, Broder S, Clark AG, Nadeau C, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng ZM, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge WM, Gong FC, Gu ZP, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke ZX, Ketchum KA, Lai ZW, Lei YD, Li ZY, Li JY, Liang Y, Lin XY, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue BX, Sun JT, Wang ZY, Wang AH, Wang X, Wang J, Wei MH, Wides R, Xiao CL, Yan CH, Yao A, Ye J, Zhan M, Zhang WQ, Zhang HY, Zhao Q, Zheng LS, Zhong F, Zhong WY, Zhu SPC, Zhao SY, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An HJ, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigo R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi HY, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Mays AD, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu XJ, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen MY, Wu D, Wu M, Xia A, Zandieh A, Zhu XH (2001) The sequence of the human genome. Science 291:1304–1351

    Article  CAS  PubMed  Google Scholar 

  49. Weiner AKM, Ceron-Romero MA, Yan Y, Katz LA (2020) Phylogenomics of the epigenetic toolkit reveals punctate retention of genes across eukaryotes. Genome Biol Evol 12:2196–2210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hwang JW, Cho Y, Bae GU, Kim SN, Kim YK (2021) Protein arginine methyltransferases: promising targets for cancer therapy. Exp Mol Med 53:788–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Liu CY, Lu FL, Cui X, Cao XF (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420

    Article  CAS  PubMed  Google Scholar 

  52. Zhang X, Zhou L, Cheng XD (2000) Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J 19:3509–3519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang M, Xu JY, Hu H, Ye BC, Tan MJ (2018) Systematic proteomic analysis of protein methylation in prokaryotes and eukaryotes revealed distinct substrate specificity. Proteomics 18:1700300

    Article  CAS  Google Scholar 

  54. Tewary SK, Zheng YG, Ho MC (2019) Protein arginine methyltransferases: insights into the enzyme structure and mechanism at the atomic level. Cell Mol Life Sci 76:2917–2932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kaniskan HU, Martini ML, Jin J (2018) Inhibitors of protein methyltransferases and demethylases. Chem Rev 118:989–1068

    Article  CAS  PubMed  Google Scholar 

  56. Emery-Corbin SJ, Hamey JJ, Ansell BRE, Balan B, Tichkule S, Stroehlein AJ, Cooper C, McInerney BV, Hediyeh-Zadeh S, Vuong D, Crombie A, Lacey E, Davis MJ, Wilkins MR, Bahlo M, Svard SG, Gasser RB, Jex AR (2020) Eukaryote-ConservedMethylarginine is absent in diplomonads and functionally compensated in giardia. Mol Biol Evol 37:3525–3549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Fisk JC, Read LK (2011) Protein arginine methylation in parasitic protozoa. Eukaryot Cell 10:1013–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lott K, Zhu L, Fisk JC, Tomasello DL, Read LK (2014) Functional interplay between protein arginine methyltransferases in Trypanosoma brucei. Microbiol Open 3:595–609

    Article  CAS  Google Scholar 

  59. Hashimoto H, Kafkova L, Raczkowski A, Jordan KD, Read LK, Debler EW (2020) Structural basis of protein arginine methyltransferase activation by a catalytically dead homolog (Prozyme). J Mol Biol 432:410–426

    Article  CAS  PubMed  Google Scholar 

  60. Kafkova L, Debler EW, Fisk JC, Jain K, Clarke SG, Read LK (2017) The major protein arginine methyltransferase in Trypanosoma brucei functions as an enzyme-Prozyme complex. J Biol Chem 292:2089–2100

    Article  CAS  PubMed  Google Scholar 

  61. Campagnaro GD, Nay E, Plevin MJ, Cruz AK, Walrad PB (2021) Arginine methyltransferases as regulators of RNA-binding protein activities in pathogenic Kinetoplastids. Front Mol Biosci 8:692668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fan Q, Miao J, Cui L, Cui LW (2009) Characterization of PRMT1 from plasmodium falciparum. Biochem J 421:107–118

    Article  CAS  PubMed  Google Scholar 

  63. Zeeshan M, Kaur I, Joy J, Saini E, Paul G, Kaushik A, Dabral S, Mohmmed A, Gupta D, Malhotra P (2017) Proteomic identification and analysis of arginine-methylated proteins of plasmodium falciparum at asexual blood stages. J Proteome Res 16:368–383

    Article  CAS  PubMed  Google Scholar 

  64. Ahmad A, Dong YZ, Cao XF (2011) Characterization of the PRMT gene family in Rice reveals conservation of arginine methylation. PLoS One 6:e22664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER, O'Rourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Schmoll M, Dattenbock C, Carreras-Villasenor N, Mendoza-Mendoza A, Tisch D, Aleman MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, Delaye L, Esquivel-Naranjo EU, Frischmann A, Gallardo-Negrete Jde J, Garcia-Esquivel M, Gomez-Rodriguez EY, Greenwood DR, Hernandez-Onate M, Kruszewska JS, Lawry R, Mora-Montes HM, Munoz-Centeno T, Nieto-Jacobo MF, Nogueira Lopez G, Olmedo-Monfil V, Osorio-Concepcion M, Pilsyk S, Pomraning KR, Rodriguez-Iglesias A, Rosales-Saavedra MT, Sanchez-Arreguin JA, Seidl-Seiboth V, Stewart A, Uresti-Rivera EE, Wang CL, Wang TF, Zeilinger S, Casas-Flores S, Herrera-Estrella A (2016) The genomes of three uneven siblings: footprints of the lifestyles of three Trichoderma species. Microbiol Mol Biol Rev 80:205–327

    Article  PubMed  PubMed Central  Google Scholar 

  67. Wang YC, Li C (2012) Evolutionarily conserved protein arginine methyltransferases in non-mammalian animal systems. FEBS J 279:932–945

    Article  CAS  PubMed  Google Scholar 

  68. Jahan S, Xu WN, Ilic A, Davie JR (2017) Protein arginine methyltransferases (PRMTs) and transcriptionally active chromatin domains. Biochem Cell Biol 95:182–182

    Google Scholar 

  69. Jain K, Clarke SG (2019) PRMT7 as a unique member of the protein arginine methyltransferase family: a review. Arch Biochem Biophys 665:36–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE (1998) Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150:613–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. van Leeuwen F, Gafken PR, Gottschling DE (2002) Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109:745–756

    Article  PubMed  Google Scholar 

  72. Kim W, Choi M, Kim JE (2014) The histone methyltransferase Dot1/DOT1L as a critical regulator of the cell cycle. Cell Cycle 13:726–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Allis CD, Berger SL, Cote J, Dent S, Jenuwein T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007) New nomenclature for chromatin-modifying enzymes. Cell 131:633–636

    Article  CAS  PubMed  Google Scholar 

  74. Pontvianne F, Blevins T, Pikaard CS (2010) Arabidopsis histone lysine methyltransferases. Adv Bot Res 53:1–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Min J, Feng Q, Li Z, Zhang Y, Xu RM (2003) Structure of the catalytic domain of human DOT1L, a non-SET domain Nucleosomal histone methyltransferase. Cell 112:711–723

    Article  CAS  PubMed  Google Scholar 

  76. Ng HH, Xu RM, Zhang Y, Struhl K (2002) Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 277:34655–34657

    Article  CAS  PubMed  Google Scholar 

  77. Worden EJ, Wolberger C (2019) Activation and regulation of H2B-ubiquitin-dependent histone methyltransferases. Curr Opin Struc Biol 59:98–106

    Article  CAS  Google Scholar 

  78. Valencia-Sanchez MI, De Ioannes P, Wang M, Truong DM, Lee R, Armache JP, Boeke JD, Armache KJ (2021) Regulation of the Dot1 histone H3K79 methyltransferase by histone H4K16 acetylation. Science 371(363):eabc6663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Cui LW, Fan Q, Cui L, Miao J (2008) Histone lysine methyltransferases and demethylases in plasmodium falciparum. Int J Parasitol 38:1083–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Alvarez-Venegas R (2014) Bacterial SET domain proteins and their role in eukaryotic chromatin modification. Front Genet 5:65

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Freitag M (2017) Histone methylation by SET domain proteins in fungi. Annu Rev Microbiol 71:413–439

    Article  CAS  PubMed  Google Scholar 

  83. Zhou HY, Liu YH, Liang YW, Zhou D, Li SF, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Frapporti A, Pina CM, Arnaiz O, Holoch D, Kawaguchi T, Humbert A, Eleftheriou E, Lombard B, Loew D, Sperling L, Guitot K, Margueron R, Duharcourt S (2019) The Polycomb protein Ezl1 mediates H3K9 and H3K27 methylation to repress transposable elements in paramecium. Nat Commun 10:2710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Chen DH, Qiu HL, Huang Y, Zhang L, Si JP (2020) Genome-wide identification and expression profiling of SET DOMAIN GROUP family in Dendrobium catenatum. BMC Plant Biol 20:40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22:1298–1306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Jacob Y, Stroud H, Leblanc C, Feng S, Zhuo L, Caro E, Hassel C, Gutierrez C, Michaels SD, Jacobsen SE (2010) Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466:987–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326

    Article  CAS  PubMed  Google Scholar 

  91. Kuroda MI, Kang H, De S, Kassis JA (2020) Dynamic competition of Polycomb and Trithorax in transcriptional programming. Annu Rev Biochem 89:235–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, Greenblatt JF, Shilatifard A (2001) COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci U S A 98:12902–12907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Thornton JL, Westfield GH, Takahashi YH, Cook M, Gao X, Woodfin AR, Lee JS, Morgan MA, Jackson J, Smith ER, Couture JF, Skiniotis G, Shilatifard A (2014) Context dependency of Set1/COMPASS-mediated histone H3 Lys4 trimethylation. Genes Dev 28:115–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Eissenberg JC, Shilatifard A (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339:240–249

    Article  CAS  PubMed  Google Scholar 

  95. Sze CC, Cao KX, Collings CK, Marshall SA, Rendleman EJ, Ozark PA, Chen FX, Morgan MA, Wang L, Shilatifard A (2017) Histone H3K4 methylation-dependent and -independent functions of Set1A/COMPASS in embryonic stem cell self-renewal and differentiation. Genes Dev 31:1732–1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A (2008) Molecular regulation of H3K4 Trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol 28:7337–7344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Wang PF, Lin CQ, Smith ER, Guo H, Sanderson BW, Wu M, Gogol M, Alexander T, Seidel C, Wiedemann LM, Ge K, Krumlauf R, Shilatifard A (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 29:6074–6085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Hu DQ, Garruss AS, Gao X, Morgan MA, Cook M, Smith ER, Shilatifard A (2013) The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nat Struc Mol Biol 20:1093–1097

    Article  CAS  Google Scholar 

  99. Strahl BD, Ohba R, Cook RG, Allis CD (1999) Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci U S A 96:14967–14972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 10:1107–1117

    Article  CAS  PubMed  Google Scholar 

  101. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, Greenblatt JF, Shilatifard A (2003) The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11:721–729

    Article  CAS  PubMed  Google Scholar 

  102. Aranda S, Mas G, Di Croce L (2015) Regulation of gene transcription by Polycomb proteins. Science Adv 1:e1500737

    Article  Google Scholar 

  103. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang XM, Lin JC, Liang GN, Jones PA, Tanay A (2008) Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci U S A 105:12979–12984

    Article  PubMed  PubMed Central  Google Scholar 

  104. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 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

    Article  CAS  PubMed  Google Scholar 

  106. Merini W, Calonje M (2015) PRC1 is taking the lead in PcG repression. Plant J 83:110–120

    Article  CAS  PubMed  Google Scholar 

  107. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23:4061–4071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Laugesen A, Hojfeldt JW, Helin K (2019) Molecular mechanisms directing PRC2 recruitment and H3K27 methylation. Mol Cell 74:8–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Kahn TG, Dorafshan E, Schultheis D, Zare A, Stenberg P, Reim I, Pirrotta V, Schwartz YB (2016) Interdependence of PRC1 and PRC2 for recruitment to Polycomb response elements. Nucleic Acids Res 44:10132–10149

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Horard B, Tatout C, Poux S, Pirrotta V (2000) Structure of a polycomb response element and in vitro binding of polycomb group complexes containing GAGA factor. Mol Cell Biol 20:3187–3197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Xiao J, Jin R, Yu X, Shen M, Wagner JD, Pai A, Song C, Zhuang M, Klasfeld S, He C, Santos AM, Helliwell C, Pruneda-Paz JL, Kay SA, Lin X, Cui S, Garcia MF, Clarenz O, Goodrich J, Zhang X, Austin RS, Bonasio R, Wagner D (2017) Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis. Nat Genet 49:1546–1552

    Article  CAS  PubMed  Google Scholar 

  112. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Lewis ZA (2017) Polycomb Group Systems in Fungi: new models for understanding Polycomb repressive complex 2. Trends Genet 33:220–231

    Article  CAS  PubMed  Google Scholar 

  114. Wiles ET, Selker EU (2017) H3K27 methylation: a promiscuous repressive chromatin mark. Curr Opin Genet Dev 43:31–37

    Article  CAS  PubMed  Google Scholar 

  115. Ridenour JB, Möller M, Freitag M (2020) Polycomb repression without bristles: facultative heterochromatin and genome stability in fungi. Genes 11:638

    Article  CAS  PubMed Central  Google Scholar 

  116. Smolle M, Workman JL, Venkatesh S (2013) reSETting chromatin during transcription elongation. Epigenetics 8:10–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Veerappan CS, Avramova Z, Moriyama EN (2008) Evolution of SET domain protein families in the unicellular and multicellular Ascomycota fungi. BMC Evol Biol 8:190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Schmitges FW, Prusty AB, Faty M, Stützer A, Lingaraju GM, Aiwazian J, Sach R, Hess D, Li L, Bunker RD, Wirth U, Bouwmeester T, Bauer A, Ly-Hartig N, Zhao K, Chan H, Gu J, Gut H, Fischle W, Müller J, Thomä N (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42:330–341

    Article  CAS  PubMed  Google Scholar 

  119. Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B (2011) H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem 286:7983–7989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Lu C, Jain SU, Hoelper D, Bechet D, Molden RC, Ran LL, Murphy D, Venneti S, Hameed M, Pawel BR, Wunder JS, Dickson BC, Lundgren SM, Jani KS, De Jay N, Papillon-Cavanagh S, Andrulis IL, Sawyer SL, Grynspan D, Turcotte RE, Nadaf J, Fahiminiyah S, Muir TW, Majewski J, Thompson CB, Chi P, Garcia BA, Allis CD, Jabado N, Lewis PW (2016) Histone H3K36 mutations promote sarcomagenesis through altered histone methylation landscape. Science 352:844–849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Gaydos LJ, Rechtsteiner A, Egelhofer TA, Carroll CR, Strome S (2012) Antagonism between MES-4 and Polycomb repressive complex 2 promotes appropriate gene expression in C. elegans germ cells. Cell Rep 2:1169–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Janevska S, Baumann L, Sieber CMK, Münsterkotter M, Ulrich J, Kämper J, Güldener U, Tudzynski B (2018) Elucidation of the two H3K36me3 histone methyltransferases Set2 and Ash1 in fusarium fujikuroi unravels their different chromosomal targets and a major impact of Ash1 on genome stability. Genetics 208:153–171

    Article  CAS  PubMed  Google Scholar 

  123. Papp B, Muller J (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20:2041–2054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Bicocca VT, Ormsby T, Adhvaryu KK, Honda S, Selker EU (2018) ASH1-catalyzed H3K36 methylation drives gene repression and marks H3K27me2/3-competent chromatin. elife 7:e41497

    Article  PubMed  PubMed Central  Google Scholar 

  125. Möller M, Schotanus K, Soyer JL, Haueisen J, Happ K, Stralucke M, Happel P, Smith KM, Connolly LR, Freitag M, Stukenbrock EH (2019) Destabilization of chromosome structure by histone H3 lysine 27 methylation. PLoS Genet 15:e1008093

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Finogenova K, Bonnet J, Poepsel S, Schafer IB, Finkl K, Schmid K, Litz C, Strauss M, Benda C, Muller J (2020) Structural basis for PRC2 decoding of active histone methylation marks H3K36me2/3. elife 9:e61964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Musselman CA, Avvakumov N, Watanabe R, Abraham CG, Lalonde ME, Hong Z, Allen C, Roy S, Nunez JK, Nickoloff J, Kulesza CA, Yasui A, Cote J, Kutateladze TG (2012) Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat Struct Mol Biol 19:1266–1272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Qin S, Guo Y, Xu C, Bian C, Fu M, Gong S, Min J (2013) Tudor domains of the PRC2 components PHF1 and PHF19 selectively bind to histone H3K36me3. Biochem Biophys Res Commun 430:547–553

    Article  CAS  PubMed  Google Scholar 

  129. Cai L, Rothbart SB, Lu R, Xu B, Chen WY, Tripathy A, Rockowitz S, Zheng D, Patel DJ, Allis CD, Strahl BD, Song J, Wang GG (2013) An H3K36 methylation-engaging Tudor motif of polycomb-like proteins mediates PRC2 complex targeting. Mol Cell 49:571–582

    Article  CAS  PubMed  Google Scholar 

  130. Choi J, Bachmann AL, Tauscher K, Benda C, Fierz B, Muller J (2017) DNA binding by PHF1 prolongs PRC2 residence time on chromatin and thereby promotes H3K27 methylation. Nat Struct Mol Biol 24:1039–1047

    Article  CAS  PubMed  Google Scholar 

  131. Dorafshan E, Kahn TG, Glotov A, Savitsky M, Walther M, Reuter G, Schwartz YB (2019) Ash1 counteracts Polycomb repression independent of histone H3 lysine 36 methylation. EMBO Rep 20:e46762

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Dorafshan E, Kahn TG, Glotov A, Savitsky M, Schwartz YB (2019) Genetic dissection reveals the role of Ash1 domains in counteracting polycomb repression. G3 (Bethesda) 9:3801–3812

    Article  CAS  Google Scholar 

  133. Basenko EY, Sasaki T, Ji L, Prybol CJ, Burckhardt RM, Schmitz RJ, Lewis ZA (2015) Genome-wide redistribution of H3K27me3 is linked to genotoxic stress and defective growth. Proc Natl Acad Sci U S A 112:E6339–E6348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Jamieson K, Wiles ET, McNaught KJ, Sidoli S, Leggett N, Shao Y, Garcia BA, Selker EU (2016) Loss of HP1 causes depletion of H3K27me3 from facultative heterochromatin and gain of H3K27me2 at constitutive heterochromatin. Genome Res 26:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Connolly LR, Smith KM, Freitag M (2013) The fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet 9:e1003916

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  136. Dumesic PA, Homer CM, Moresco JJ, Pack LR, Shanle EK, Coyle SM, Strahl BD, Fujimori DG, Yates JR 3rd, Madhani HD (2015) Product binding enforces the genomic specificity of a yeast polycomb repressive complex. Cell 160:204–218

    Article  CAS  PubMed  Google Scholar 

  137. Montgomery SA, Tanizawa Y, Galik B, Wang N, Ito T, Mochizuki T, Akimcheva S, Bowman JL, Cognat V, Marechal-Drouard L, Ekker H, Hong SF, Kohchi T, Lin SS, Liu LD, Nakamura Y, Valeeva LR, Shakirov EV, Shippen DE, Wei WL, Yagura M, Yamaoka S, Yamato KT, Liu C, Berger F (2020) Chromatin Organization in Early Land Plants Reveals an ancestral association between H3K27me3, transposons, and constitutive heterochromatin. Curr Biol 30:573–588 e577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Ho JWK, June YL, Liu T, Alver BH, Lee S, Ikegami K, Sohn KA, Minoda A, Tolstorukov MY, Appert A, Parker SCJ, Gu TT, Kundaje A, Riddle NC, Bishop E, Egelhofer TA, Hu SS, Alekseyenko AA, Rechtsteiner A, Asker D, Belsky JA, Bowmanm SK, Chens QB, Chen RAJ, Day DS, Dong Y, Dose AC, Duan XK, Epstein CB, Ercan S, Feingold EA, Ferrari F, Garrigues JM, Gehlenborg N, Good PJ, Haseley P, He D, Herrmann M, Hoffman MM, Jeffers TE, Kharchenko PV, Kolasinska-Zwierz P, Kotwaliwale CV, Kumar N, Langley SA, Larschan EN, Latorre I, Libbrecht MW, Lin XQ, Park R, Pazin MJ, Pham HN, Plachetka A, Qin B, Schwartz YB, Shoresh N, Stempor P, Vielle A, Wang CY, Whittle CM, Xue HL, Kingstonm RE, Kim JH, Bernstein BE, Dernburg AF, Pirrotta V, Kuroda MI, Noble WS, Tullius TD, Kellis M, MacAlpine DM, Strome S, Elgin SCR, Liu XS, Lieb JD, Ahringer J, Karpen GH, Park PJ (2014) Comparative analysis of metazoan chromatin organization. Nature 512:449–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Hawkins RD, Hon GC, Lee LK, Ngo Q, Lister R, Pelizzola M, Edsall LE, Kuan S, Luu Y, Klugman S, Antosiewicz-Bourget J, Ye Z, Espinoza C, Agarwahl S, Shen L, Ruotti V, Wang W, Stewart R, Thomson JA, Ecker JR, Ren B (2010) Distinct Epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6:479–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Mozzetta C, Pontis J, Fritsch L, Robin P, Portoso M, Proux C, Margueron R, Ait-Si-Ali S (2014) The histone H3 lysine 9 methyltransferases G9a and GLP regulate polycomb repressive complex 2-mediated gene silencing. Mol Cell 53:277–289

    Article  CAS  PubMed  Google Scholar 

  141. Peters AH, Kubicek S, Mechtler K, O’Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JH, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12:1577–1589

    Article  CAS  PubMed  Google Scholar 

  142. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14:1025–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Veluchamy A, Rastogi A, Lin X, Lombard B, Murik O, Thomas Y, Dingli F, Rivarola M, Ott S, Liu XY, Sun YZ, Rabinowicz PD, McCarthy J, Allen AE, Loew D, Bowler C, Tirichine L (2015) An integrative analysis of post-translational histone modifications in the marine diatom Phaeodactylum tricornutum. Genome Biol 16:102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  144. Qian C, Zhou MM (2006) SET domain protein lysine methyltransferases: structure, specificity and catalysis. Cell Mol Life Sci 63:2755–2763

    Article  CAS  PubMed  Google Scholar 

  145. Xiao B, Jing C, Kelly G, Walker PA, Muskett FW, Frenkiel TA, Martin SR, Sarma K, Reinberg D, Gamblin SJ, Wilson JR (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev 19:1444–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Couture JF, Dirk LMA, Brunzelle JS, Houtz RL, Trievel RC (2008) Structural origins for the product specificity of SET domain protein methyltransferases. Proc Natl Acad Sci U S A 105:20659–20664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Starr TN, Thornton JW (2017) Exploring protein sequence-function landscapes. Nat Biotechnol 35:125–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Anderson DW, McKeown AN, Thornton JW (2015) Intermolecular epistasis shaped the function and evolution of an ancient transcription factor and its DNA binding sites. elife 4:e07864

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We thank the members of the Freitag Lab for discussions. We apologize to our colleagues whose original research is not cited because of space constraints. Accession numbers and sequences of proteins discussed are available upon request. Work in the Freitag lab is supported by grants from the NSF (MCB1818006), the NIH (R01GM132644), and the US-Israel BSF (#2019034).

Author information

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR, USA

    Allyson A. Erlendson & Michael Freitag

Authors
  1. Allyson A. Erlendson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Freitag
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Freitag .

Editor information

Editors and Affiliations

  1. Institute Curie, INSERM U934/CNRS UMR 3215, Paris, France

    Raphaël Margueron

  2. Institute Curie, INSERM U934/CNRS UMR 3215, Paris, France

    Daniel Holoch

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Erlendson, A.A., Freitag, M. (2022). Not all Is SET for Methylation: Evolution of Eukaryotic Protein Methyltransferases. In: Margueron, R., Holoch, D. (eds) Histone Methyltransferases. Methods in Molecular Biology, vol 2529. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2481-4_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2481-4_1

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2480-7

  • Online ISBN: 978-1-0716-2481-4

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation