PHDs govern plant development

Plant Signaling and Behavior

Volumn 10, Issue 7, 2015, Pages

  Mouriz, Alfonso ^a   López González, Leticia ^a   Jarillo, Jose A ^a   Piñeiro, Manuel ^a  

^a UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

Arabidopsis; Chromatin remodeling; Flowering time; Germination; Meiosis; Plant homeodomain; Root development

Indexed keywords

HOMEODOMAIN PROTEIN; NUCLEOSOME;

CHEMISTRY; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; MERISTEM; METABOLISM; NUCLEOSOME; PLANT DEVELOPMENT;

FLOWERS; HOMEODOMAIN PROTEINS; MEIOSIS; MERISTEM; NUCLEOSOMES; PLANT DEVELOPMENT;

EID: 84955575740     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/15592324.2014.993253     Document Type: Article

References (63)

1. Jarillo JA, Pineiro M, Cubas P, Martinez-Zapater JM. Chromatin remodeling in plant development. Int J Dev Biol 2009; 53: 1581-96; PMID: 19247973; http://dx.doi.org/10.1387/ijdb.072460jj
2. He G, Elling AA, Deng XW. The epigenome and plant development. Annu Rev Plant Biol 2011; 62: 411-35; PMID: 21438682; http://dx.doi.org/10.1146/annurevarplant-042110-103806
3. He Y. Chromatin regulation of flowering. Trends Plant Sci 2012; 17: 556-62; PMID: 22658650; http://dx.doi.org/10.1016/j.tplants.2012.05.001
4. Jarillo JA, Piñeiro M. Timing is everything in plant development. The central role of floral repressors. Plant Sci 2011; 181: 364-78; PMID: 21889042; http://dx.doi.org/10.1016/j.plantsci.2011.06.011
5. Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Ann Rev Biochem 2011; 80: 473-99; PMID: 21529160; http://dx.doi.org/10.1146/annurev-biochem-061809-175347
6. Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM. Structure and ligand of a histone acetyltransferase bromodomain. Nature 1999; 399: 491-6; PMID: 10365964; http://dx.doi.org/10.1038/20974
7. Sanchez R, Zhou M-M. The PHD finger: a versatile epigenome reader. Trends Biochem Sci 2011; 36: 364-72; PMID: 21514168
8. Schindler U, Beckmann H, Cashmore AR. HAT3.1, a novel Arabidopsis homeodomain protein containing a conserved cysteine-rich region. Plant J 1993; 4: 137-50; PMID: 8106082; http://dx.doi.org/10.1046/j.1365-313X.1993.04010137.x
9. Li Y, Li H. Many keys to push: diversifying the ‘readership’ of plant homeodomain fingers. Acta Biochim Biophys Sin (Shanghai) 2012; 44: 28-39; PMID: 22194011; http://dx.doi.org/10.1093/abbs/gmr117
10. Musselman CA, Kutateladze TG. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res 2011; 39: 9061-71; PMID: 21813457; http://dx.doi.org/10.1093/nar/gkr613
11. Becker PB. Gene regulation: a finger on the mark. Nature 2006; 442: 31-2; PMID: 16823438; http://dx.doi.org/10.1038/442031a
12. Mellor J. It takes a PHD to read the histone code. Cell 2006; 126: 22-4; PMID: 16839870; http://dx.doi.org/10.1016/j.cell.2006.06.028
13. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006; 442: 86-90; PMID: 16728976
14. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Peña P, Lan F, Kaadige MR, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 2006; 442: 96-9; PMID: 16728974; http://dx.doi.org/10.1038/nature05140
15. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R, Kutateladze TG. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006; 442: 100-3; PMID: 16728977
16. Li H, Ilin S, Wang W, Duncan EM, Wysocka J, Allis CD, Patel DJ. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 2006; 442: 91-5; PMID: 16728978; http://dx.doi.org/10.1038/nature05020
17. Lopez-Gonzalez L, Mouriz A, Narro-Diego L, Bustos R, Martinez-Zapater JM, Jarillo JA, Piñeiro M. Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHDcontaining proteins. Plant Cell 2014; 26: 3922-38; PMID: 25281686; http://dx.doi.org/10.1105/tpc.114.130781
18. Wang CJ, Tseng CC. Recent advances in understanding of meiosis initiation and the apomictic pathway in plants. Front Plant Sci 2014; 5: 497; PMID: 25295051
19. Sebastian J, Ravi M, Andreuzza S, Panoli AP, Marimuthu MP, Siddiqi I. The plant adherin AtSCC2 is required for embryogenesis and sister-chromatid cohesion during meiosis in Arabidopsis. Plant J 2009; 59: 1-13; PMID: 19228337; http://dx.doi.org/10.1111/j.1365-313X.2009.03845.x
20. Reddy TV, Kaur J, Agashe B, Sundaresan V, Siddiqi I. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development 2003; 130: 5975-87; PMID: 14573517; http://dx.doi.org/10.1242/dev.00827
21. Yang X, Makaroff CA, Ma H. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 2003; 15: 1281-95; PMID: 12782723; http://dx.doi.org/10.1105/tpc.010447
22. Borg M, Twell D. Life after meiosis: patterning the angiosperm male gametophyte. Biochem Soc Trans 2010; 38: 577-82; PMID: 20298224; http://dx.doi.org/10.1042/BST0380577
23. Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ. The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 2001; 28: 27-39; PMID: 11696184; http://dx.doi.org/10.1046/j.1365-313X.2001.01125.x
24. Ito T, Shinozaki K. The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHDfinger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 2002; 43: 1285-92; PMID: 12461128; http://dx.doi.org/10.1093/pcp/pcf154
25. Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K. Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 2007; 19: 3549-62; PMID: 18032630; http://dx.doi.org/10.1105/tpc.107.054536
26. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D. Persistent tapetal cell1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 2011; 156: 615-30; PMID: 21515697; http://dx.doi.org/10.1104/pp.111.175760
27. Fernandez Gomez J, Wilson ZA. A barley PHD finger transcription factor that confers male sterility by affecting tapetal development. Plant Biotechnol J 2014; 12: 765-77; PMID: 24684666; http://dx.doi.org/10.1111/pbi.12181
28. Thorstensen T, Grini PE, Mercy IS, Alm V, Erdal S, Aasland R, Aalen RB. The Arabidopsis SET-domain protein ASHR3 is involved in stamen development and interacts with the bHLH transcription factor ABORTED MICROSPORES (AMS). Plant Mol Biol 2008; 66: 47-59; PMID: 17978851; http://dx.doi.org/10.1007/s11103-007-9251-y
29. Bennett T, Scheres B. Root development-two meristems for the price of one? Curr Top Dev Biol 2010; 91: 67-102; PMID: 20705179; http://dx.doi.org/10.1016/S0070-2153(10)91003-X
30. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010; 464: 913-6; PMID: 20220754; http://dx.doi.org/10.1038/nature08836
31. Thomas CL, Schmidt D, Bayer EM, Dreos R, Maule AJ. Arabidopsis plant homeodomain finger proteins operate downstream of auxin accumulation in specifying the vasculature and primary root meristem. Plant J 2009; 59: 426-36; PMID: 19392692; http://dx.doi.org/10.1111/j.1365-313X.2009.03874.x
32. Saiga S, Moller B, Watanabe-Taneda A, Abe M, Weijers D, Komeda Y. Control of embryonic meristem initiation in Arabidopsis by PHD-finger protein complexes. Development 2012; 139: 1391-8; PMID: 22378640; http://dx.doi.org/10.1242/dev.074492
33. Ogas J, Kaufmann S, Henderson J, Somerville C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 1999; 96: 13839-44; PMID: 10570159; http://dx.doi.org/10.1073/pnas.96.24.13839
34. Zhang H, Rider SD Jr, Henderson JT, Fountain M, Chuang K, Kandachar V, Simons A, Edenberg HJ, Romero-Severson J, Muir WM, et al. The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J Biol Chem 2008; 283: 22637-48; PMID: 18539592; http://dx.doi.org/10.1074/jbc.M802129200
35. Aichinger E, Villar CB, Di Mambro R, Sabatini S, Kohler C. The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 2011; 23: 1047-60; PMID: 21441433; http://dx.doi.org/10.1105/tpc.111.083352
36. Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J. The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 2012; 159: 418-32; PMID: 22452853; http://dx.doi.org/10.1104/pp.112.194878
37. Chandrika NN, Sundaravelpandian K, Yu SM, Schmidt W. ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol 2013; 198: 709-20; PMID: 23432399; http://dx.doi.org/10.1111/nph.12194
38. Lee WY, Lee D, Chung WI, Kwon CS. Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 2009; 58: 511-24; PMID: 19154204; http://dx.doi.org/10.1111/j.1365-313X.2009.03795.x
39. Kirik V, Simon M, Huelskamp M, Schiefelbein J. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 2004; 268: 506-13; PMID: 15063185; http://dx.doi.org/10.1016/j.ydbio.2003.12.037
40. Chandrika NN, Sundaravelpandian K, Schmidt W. A PHD in histone language: on the role of histone methylation in plant responses to phosphate deficiency. Plant Signal Behav 2013; 8: e24381; PMID: 23531693; http://dx.doi.org/10.4161/psb.24381
41. Tsukagoshi H, Saijo T, Shibata D, Morikami A, Nakamura K. Analysis of a sugar response mutant of Arabidopsis identified a novel B3 domain protein that functions as an active transcriptional repressor. Plant Physiol 2005; 138: 675-85; PMID: 15894743; http://dx.doi.org/10.1104/pp.104.057752
42. Veerappan V,Wang J, Kang M, Lee J, Tang Y, Jha AK, Shi H, Palanivelu R, Allen RD. A novel HSI2 mutation in Arabidopsis affects the PHD-like domain and leads to derepression of seed-specific gene expression. Planta 2012; 236: 1-17; PMID: 22476218; http://dx.doi.org/10.1007/s00425-012-1630-1
43. Molitor AM, Bu Z, Yu Y, Shen WH. Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 2014; 10: e1004091; PMID: 24465219; http://dx.doi.org/10.1371/journal.pgen.1004091
44. Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of Histone H3 Lysine 27. PLoS Genet 2007; 3: e86; PMID: 17542647; http://dx.doi.org/10.1371/journal. pgen.0030086
45. Michaels SD, Amasino RM. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 1999; 11: 949-56; PMID: 10330478; http://dx.doi.org/10.1105/tpc.11.5.949
46. Kim D-H, Sung S. Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 2013; 25: 454-69; PMID: 23417034; http://dx.doi.org/10.1105/tpc.112.104760
47. Song J, Irwin J, Dean C. Remembering the prolonged cold of winter. Curr Biol 2013; 23: R807-11; PMID: 24028964; http://dx.doi.org/10.1016/j.cub.2013.07.027
48. Sung S, Schmitz RJ, Amasino RM. A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 2006; 20: 3244-8; PMID: 17114575; http://dx.doi.org/10.1101/gad.1493306
49. Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR, Dean C. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 2007; 17: 73-8; PMID: 17174094; http://dx.doi.org/10.1016/j.cub.2006.11.052
50. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 2008; 105: 16831-6; PMID: 18854416; http://dx.doi.org/10.1073/pnas.0808687105
51. Kim D-H, Sung S. The plant homeo domain finger protein, VIN3-LIKE 2, is necessary for photoperiodmediated epigenetic regulation of the floral repressor, MAF5. Proc Natl Acad Sci USA 2010; 107: 17029-34; PMID: 20837520; http://dx.doi.org/10.1073/pnas.1010834107
52. Fu D, Dunbar M, Dubcovsky J. Wheat VIN3-like PHD finger genes are up-regulated by vernalization. Mol Genet Genomics 2007; 277: 301-13; PMID: 17123111; http://dx.doi.org/10.1007/s00438-006-0189-6
53. Koyama K, Hatano H, Nakamura J, Takumi S. Characterization of three VERNALIZATION INSENSITIVE3-like (VIL) homologs in wild wheat, Aegilops tauschii Coss. Hereditas 2012; 149: 62-71; PMID: 22568701; http://dx.doi.org/10.1111/j.1601-5223.2012.02255.x
54. Yang J, Lee S, Hang R, Kim SR, Lee YS, Cao X, Amasino R, An G. OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J 2013; 73: 566-78; PMID: 23083333; http://dx.doi.org/10.1111/tpj.12057
55. Fromm M, Avramova Z. ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes? Curr Opin Plant Biol 2014; 21C: 75-82; PMID: 25047977; http://dx.doi.org/10.1016/j.pbi.2014.07.004
56. Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via Histone 3 Lysine 4 trimethylation. Plant Cell 2008; 20: 580-8; PMID: 18375656; http://dx.doi.org/10.1105/tpc.108.058172
57. Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX, Minobe Y, Yano M. Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J 2011; 66: 603-12; PMID: 21284756; http://dx.doi.org/10.1111/j.1365-313X.2011.04517.x
58. Choi SC, Lee S, Kim SR, Lee YS, Liu C, Cao X, An G. Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3. Plant Physiol 2014; 164: 1326-37; PMID: 24420930; http://dx.doi.org/10.1104/pp.113.228049
59. Fornara F, de Montaigu A, Coupland G. Snapshot: control of flowering in Arabidopsis. Cell 2010; 141: 550-2; PMID: 20434991; http://dx.doi.org/10.1016/j.cell.2010.04.024
60. Gomez-Mena C, Pineiro M, Franco-Zorrilla JM, Salinas J, Coupland G, Martinez-Zapater JM. Early bolting in short days: an Arabidopsis mutation that causes early flowering and partially suppresses the floral phenotype of leafy. Plant Cell 2001; 13: 1011-24; PMID: 11340178; http://dx.doi.org/10.1105/tpc.13.5.1011
61. Piñeiro M, Gomez-Mena C, Schaffer R, Martinez-Zapater JM, Coupland G. Early bolting in short days is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. Plant Cell 2003; 15: 1552-62; PMID: 12837946; http://dx.doi.org/10.1105/tpc.012153
62. Mussig C, Kauschmann A, Clouse SD, Altmann T. The Arabidopsis PHD-finger protein SHL is required for proper development and fertility. Mol Gen Genet 2000; 264: 363-70; PMID: 11129039; http://dx.doi.org/10.1007/s004380000313
63. Mussig C, Altmann T. Changes in gene expression in response to altered SHL transcript levels. Plant Mol Biol 2003; 53: 805-20; PMID: 15082927; http://dx.doi.org/10.1023/B:PLAN.0000023661.65248.4b