Expansion and functional divergence of Jumonji C-containing histone demethylases: Significance of duplications in ancestral angiosperms and vertebrates

Plant Physiology

Volumn 168, Issue 4, 2015, Pages 1321-1337

  Qian, Shengzhan ^a   Wang, Yingxiang ^a   Ma, Hong ^a,b   Zhang, Liangsheng ^c  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c TONGJI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; EUKARYOTA; FUNGI; MAGNOLIOPHYTA; MAMMALIA; VERTEBRATA;

CHROMATIN; HISTONE; HISTONE DEMETHYLASE;

AMINO ACID SEQUENCE; ANGIOSPERM; ANIMAL; CHROMATIN; ENZYMOLOGY; EVOLUTION; GENE DUPLICATION; GENETICS; METABOLISM; METHYLATION; PHYLOGENY; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SYNTENY; VERTEBRATE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANGIOSPERMS; ANIMALS; BIOLOGICAL EVOLUTION; CHROMATIN; GENE DUPLICATION; HISTONES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; METHYLATION; PHYLOGENY; SEQUENCE ALIGNMENT; SYNTENY; VERTEBRATES;

EID: 84939133178     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00520     Document Type: Article

References (84)

1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105
2. Ahmad A, Cao X (2012) Plant PRMTs broaden the scope of arginine methylation. J Genet Genomics 39: 195-208
3. Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, et al (2007) New nomenclature for chromatin-modifying enzymes. Cell 131: 633-636
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
5. Amborella Genome Project (2013) The Amborella genome and the evolution of flowering plants. Science 342: 1241089
6. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36
7. Barker MS, Vogel H, Schranz ME (2009) Paleopolyploidy in the Brassicales: analyses of the Cleome transcriptome elucidate the history of genome duplications in Arabidopsis and other Brassicales. Genome Biol Evol 1: 391-399
8. Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T, Kremitzki C, Brown LG, Rozen S, Warren WC, Wilson RK, et al (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466: 612-616
9. Byvoet P, Shepherd GR, Hardin JM, Noland BJ (1972) The distribution and turnover of labeled methyl groups in histone fractions of cultured mammalian cells. Arch Biochem Biophys 148: 558-567
10. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043
11. Catchen JM, Conery JS, Postlethwait JH (2009) Automated identification of conserved synteny after whole-genome duplication. Genome Res 19: 1497-1505
12. Chen X, Hu Y, Zhou DX (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim Biophys Acta 1809: 421-426
13. Cho JN, Ryu JY, Jeong YM, Park J, Song JJ, Amasino RM, Noh B, Noh YS (2012) Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 22: 736-748
14. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grützner F, Kaessmann H (2014) Origins and functional evolution of Y chromosomes across mammals. Nature 508: 488-493
15. Crevillén P, Yang H, Cui X, Greeff C, Trick M, Qiu Q, Cao X, Dean C (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515: 587-590
16. Day RC, Herridge RP, Ambrose BA, Macknight RC (2008) Transcriptome analysis of proliferating Arabidopsis endosperm reveals biological implications for the control of syncytial division, cytokinin signaling, and gene expression regulation. Plant Physiol 148: 1964-1984
17. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314
18. Deleris A, Greenberg MV, Ausin I, Law RW, Moissiard G, Schubert D, Jacobsen SE (2010) Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep 11: 950-955
19. Dong X, Weng Z (2013) The correlation between histone modifications and gene expression. Epigenomics 5: 113-116
20. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14: 755-763
21. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
22. Fan D, Dai Y, Wang X, Wang Z, He H, Yang H, Cao Y, Deng XW, Ma L (2012) IBM1, a JmjC domain-containing histone demethylase, is involved in the regulation of RNA-directed DNA methylation through the epigenetic control of RDR2 and DCL3 expression in Arabidopsis. Nucleic Acids Res 40: 8905-8916
23. Feng B, Lu D, Ma X, Peng Y, Sun Y, Ning G, Ma H (2012) Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J 72: 612-624
24. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330: 622-627
25. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al (2014) Pfam: the protein families database. Nucleic Acids Res 42: D222-D230
26. Gan ES, Xu YF, Wong JY, Goh JG, Sun B, Wee WY, Huang JB, Ito T (2014) Jumonji demethylases moderate precocious flowering at elevated temperature via regulation of FLC in Arabidopsis. Nat Commun 5: 5098
27. Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313: 903-919
28. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: W695-W699
29. Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16: 1664-1674
30. Gu X (2006) A simple statistical method for estimating type-II (clusterspecific) functional divergence of protein sequences. Mol Biol Evol 23: 1937-1945
31. Gu X, Zou Y, Su Z, Huang W, Zhou Z, Arendsee Z, Zeng Y (2013) An update of DIVERGE software for functional divergence analysis of protein family. Mol Biol Evol 30: 1713-1719
32. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704
33. Henikoff S, Shilatifard A (2011) Histone modification: cause or cog? Trends Genet 27: 389-396
34. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315
35. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467
36. Jeong JH, Song HR, Ko JH, Jeong YM, Kwon YE, Seol JH, Amasino RM, Noh B, Noh YS (2009) Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS ONE 4: e8033
37. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100
38. Jones MA, Covington MF, DiTacchio L, Vollmers C, Panda S, Harmer SL (2010) Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc Natl Acad Sci USA 107: 21623-21628
39. Jones MA, Harmer S (2011) JMJD5 functions in concert with TOC1 in the Arabidopsis circadian system. Plant Signal Behav 6: 445-448
40. Kasahara M (2007) The 2R hypothesis: an update. Curr Opin Immunol 19: 547-552
41. Kavi HH, Birchler JA (2009) Interaction of RNA polymerase II and the small RNA machinery affects heterochromatic silencing in Drosophila. Epigenetics Chromatin 2: 15
42. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727
43. Ko JH, Mitina I, Tamada Y, Hyun Y, Choi Y, Amasino RM, Noh B, Noh YS (2010) Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J 29: 3208-3215
44. Kooistra SM, Helin K (2012) Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol 13: 297-311
45. Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286: 964-967
46. Lei L, Zhou SL, Ma H, Zhang LS (2012) Expansion and diversification of the SET domain gene family following whole-genome duplications in Populus trichocarpa. BMC Evol Biol 12: 51
47. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40: D302-D305
48. Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61: 395-420
49. Lu F, Cui X, Zhang S, Jenuwein T, Cao X (2011a) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43: 715-719
50. Lu F, Cui X, Zhang S, Liu C, Cao X (2010) JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20: 387-390
51. Lu F, Li G, Cui X, Liu C, Wang XJ, Cao X (2008) Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol 50: 886-896
52. Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, Siu JP, Tobin EM (2011b) The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol 155: 906-915
53. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260
54. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102: 5454-5459
55. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229
56. Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6: 838-849
57. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, et al (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49: 1135-1149
58. Noh B, Lee SH, Kim HJ, Yi G, Shin EA, Lee M, Jung KJ, Doyle MR, Amasino RM, Noh YS (2004) Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 16: 2601-2613
59. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132: 603-614
60. Panopoulou G, Hennig S, Groth D, Krause A, Poustka AJ, Herwig R, Vingron M, Lehrach H (2003) New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. Genome Res 13: 1056-1066
61. Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101: 9903-9908
62. Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650
63. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574
64. Sani E, Herzyk P, Perrella G, Colot V, Amtmann A (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14: R59
65. Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319: 462-465
66. Shen Y, Conde e Silva N, Audonnet L, Servet C, Wei W, Zhou DX (2014) Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis. Front Plant Sci 5: 290
67. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953
68. Shi Y, Whetstine JR (2007) Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 25: 1-14
69. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690
70. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
71. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739
72. Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320: 486-488
73. Tang H, Bowers JE, Wang X, Paterson AH (2010) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA 107: 472-477
74. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816
75. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191
76. Yan Y, Shen L, Chen Y, Bao S, Thong Z, Yu H (2014) A MYB-domain protein EFM mediates flowering responses to environmental cues in Arabidopsis. Dev Cell 30: 437-448
77. Yang H, Han Z, Cao Y, Fan D, Li H, Mo H, Feng Y, Liu L,Wang Z, Yue Y, et al (2012a) A companion cell-dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression. PLoS Genet 8: e1002664
78. Yang H, Mo H, Fan D, Cao Y, Cui S, Ma L (2012b) Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant Cell Rep 31: 1297-1308
79. Yang W, Jiang D, Jiang J, He Y (2010) A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant J 62: 663-673
80. Yu X, Li L, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105: 7618-7623
81. Zhang L, Ma H (2012) Complex evolutionary history and diverse domain organization of SET proteins suggest divergent regulatory interactions. New Phytol 195: 248-263
82. Zhang L, Wang L, Yang Y, Cui J, Chang F, Wang Y, Ma H (2015) Analysis of Arabidopsis floral transcriptome: detection of new florally expressed genes and expansion of Brassicaceae-specific gene families. Front Plant Sci 5: 802
83. Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133: 3085-3095
84. Zhou X, Ma H (2008) Evolutionary history of histone demethylase families: distinct evolutionary patterns suggest functional divergence. BMC Evol Biol 8: 294