Histone H4R3 methylation catalyzed by SKB1/PRMT5 is required for maintaining shoot apical meristem

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Yue, Minghui ^a,b   Li, Qiuling ^a   Zhang, Ya ^a   Zhao, Yan ^a   Zhang, Zhaoliang ^a,b   Bao, Shilai ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H4; HISTONE H4R3; PLANT RNA; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN PRMT5; PROTEIN SKB1; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; CORYNE PROTEIN, ARABIDOPSIS; HISTONE; PRMT5 PROTEIN, ARABIDOPSIS; PROTEIN SERINE THREONINE KINASE;

APICAL MERISTEM; ARABIDOPSIS; ARTICLE; CATALYSIS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CLV3 GENE; CONTROLLED STUDY; CRN GENE; DOWN REGULATION; FEEDBACK SYSTEM; GENE EXPRESSION; GENE INTERACTION; GENE LOCUS; GENE MUTATION; GENETIC TRANSCRIPTION; HISTONE METHYLATION; MUTANT; NONHUMAN; PLANT GENE; PLANT GROWTH; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEEDLING; SHOOT APICAL MERISTEM; UPREGULATION; WUS GENE; BIOSYNTHESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; METHYLATION; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HISTONES; MERISTEM; METHYLATION; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SEEDLING;

EID: 84892612604     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083258     Document Type: Article

References (55)

1. Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5: 110-115. doi:10.1016/S1360-1385(00)01569-7. PubMed: 10707076.
2. Lenhard M, Laux T (1999) Shoot meristem formation and maintenance. Curr Opin Plant Biol 2: 44-50. doi:10.1016/S1369-5266(99)80009-0. PubMed: 10047572.
3. Fletcher JC (2002) Shoot and floral meristem maintenance in Arabidopsis. Annu Rev Plant Biol 53: 45-66. doi:10.1146/annurev.arplant.53.092701.143332. PubMed: 12221985.
4. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G et al. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815. doi:10.1016/S0092-8674(00)81703-1. PubMed: 9865698.
5. Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87-96. PubMed: 8565856.
6. Yadav RK, Perales M, Gruel J, Girke T, Jönsson H et al. (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25: 2025-2030. doi:10.1101/gad.17258511. PubMed: 21979915.
7. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911-1914. doi:10.1126/science.283.5409.1911. PubMed: 10082464.
8. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5: 578-580. doi:10.1038/nchembio.182. PubMed: 19525968.
9. Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121: 2057-2067.
10. Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G et al. (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635-644. doi:10.1016/S0092-8674(00)80700-X. PubMed: 10761929.
11. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617-619. doi:10.1126/science.289.5479.617. PubMed: 10915624.
12. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575-585. doi:10.1016/S0092-8674(00)80239-1. PubMed: 9160749.
13. Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11: 1925-1934. doi: 10.2307/3871087. PubMed: 10521522.
14. Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11: 393-406. doi:10.2307/3870868. PubMed: 10072399.
15. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294. doi:10.1126/science. 1150083. PubMed: 18202283.
16. Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20: 934-946. doi:10.1105/tpc.107.057547. PubMed: 18381924.
17. Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63: 889-900. doi:10.1111/j.1365-313X.2010.04295.x. PubMed: 20626648.
18. Bleckmann A, Weidtkamp-Peters S, Seidel CAM, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152: 166-176. doi:10.1104/pp. 109.149930. PubMed: 19933383.
19. Zhu Y, Wang Y, Li R, Song X, Wang Q et al. (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J 61: 223-233. PubMed: 19843317.
20. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S et al. (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137: 3911-3920. doi: 10.1242/dev.048199. PubMed: 20978082.
21. Betsuyaku S, Takahashi F, Kinoshita A, Miwa H, Shinozaki K et al. (2011) Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol 52: 14-29. doi:10.1093/pcp/pcq157. PubMed: 20965998.
22. Ahmad A, Cao X (2012) Plant PRMTs broaden the scope of arginine methylation. J Genet Genomics 39: 195-208. doi:10.1016/j.jgg.2012.04.001. PubMed: 22624881.
23. Bedford MT, Richard S (2005) Arginine methylation an emerging regulator of protein function. Mol Cell 18: 263-272. doi:10.1016/j.molcel.2005.04.003. PubMed: 15866169.
24. Bedford MT, Clarke SG (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13. doi:10.1016/j.molcel.2008.12.013. PubMed: 19150423.
25. Pahlich S, Zakaryan RP, Gehring H (2006) Protein arginine methylation: Cellular functions and methods of analysis. Biochim Biophys Acta 1764: 1890-1903. doi:10.1016/j.bbapap.2006.08.008. PubMed: 17010682.
26. Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61: 395-420. doi:10.1146/annurev.arplant.043008.091939. PubMed: 20192747.
27. Pal S, Yun R, Datta A, Lacomis L, Erdjument-Bromage H et al. (2003) mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol Cell Biol 23: 7475-7487. doi:10.1128/MCB.23.21.7475-7487.2003. PubMed: 14559996.
28. Kwak YT, Guo J, Prajapati S, Park KJ, Surabhi RM et al. (2003) Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties. Mol Cell 11: 1055-1066. doi: 10.1016/S1097-2765(03)00101-1. PubMed: 12718890.
29. Chari A, Golas MM, Klingenhäger M, Neuenkirchen N, Sander B et al. (2008) An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs. Cell 135: 497-509. doi:10.1016/j.cell.2008.09.020. PubMed: 18984161.
30. Zhou Z, Sun X, Zou Z, Sun L, Zhang T et al. (2010) PRMT5 regulates Golgi apparatus structure through methylation of the golgin GM130. Cell Res 20: 1023-1033. doi:10.1038/cr.2010.56. PubMed: 20421892.
31. Guo S, Bao S (2010) srGAP2 arginine methylation regulates cell migration and cell spreading through promoting dimerization. J Biol Chem 285: 35133-35141. doi:10.1074/jbc.M110.153429. PubMed: 20810653.
32. Deng X, Gu L, Liu C, Lu T, Lu F et al. (2010) Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing. Proc Natl Acad Sci U S A 107: 19114-19119. doi: 10.1073/pnas. 1009669107. PubMed: 20956294.
33. Wang X, Zhang Y, Ma Q, Zhang Z, Xue Y et al. (2007) SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. EMBO J 26: 1934-1941. doi:10.1038/sj.emboj.7601647. PubMed: 17363895.
34. Zhang Z, Zhang S, Zhang Y, Wang X, Li D et al. (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23: 396-411. doi:10.1105/tpc.110. 081356. PubMed: 21258002.
35. Pei Y, Niu L, Lu F, Liu C, Zhai J et al. (2007) Mutations in the Type II protein arginine methyltransferase AtPRMT5 result in pleiotropic developmental defects in Arabidopsis. Plant Physiol 144: 1913-1923. doi:10.1104/pp.107.099531. PubMed: 17573539.
36. Sanchez SE, Petrillo E, Beckwith EJ, Zhang X, Rugnone ML et al. (2010) A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468: 112-118. doi:10.1038/nature09470. PubMed: 20962777.
37. Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8: 394-401. doi:10.1016/S1360-1385(03) 00164-X. PubMed: 12927973.
38. Clark SE (2001) Cell signalling at the shoot meristem. Nat Rev Mol Cell Biol 2: 276-284. doi:10.1038/35067079. PubMed: 11283725.
39. He Y, Amasino RM (2005) Role of chromatin modification in floweringtime control. Trends Plant Sci 10: 30-35. doi:10.1016/j.tplants.2004.11.003. PubMed: 15642521.
40. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30: 349-359. doi:10.1046/j.1365-313X.2002.01289.x. PubMed: 12000682.
41. Bäurle I, Laux T (2005) Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17: 2271-2280. doi:10.1105/tpc.105.032623. PubMed: 15980263.
42. Liu X, Kim YJ, Müller R, Yumul RE, Liu C et al. (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb group proteins. Plant Cell 23: 3654-3670. doi:10.1105/tpc.111.091538. PubMed: 22028461.
43. Li W, Liu H, Cheng ZJ, Su YH, Han HN et al. (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7: e1002243. doi:10.1371/journal.pgen.1002243. PubMed: 21876682.
44. Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823-831.
45. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10: 967-979. doi:10.1046/j.1365-313X.1996.10060967.x. PubMed: 9011081.
46. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M et al. (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967-971. doi:10.1038/35050091. PubMed: 11140682.
47. Tsiantis M, Hay A (2003) Comparative plant development: the time of the leaf? Nat Rev Genet 4: 169-180. doi:10.1038/nrg1002. PubMed: 12610522.
48. Gilbreth M, Yang P, Wang D, Frost J, Polverino A, et al. (1996) The highly conserved skb1 gene encodes a protein that interacts with Shk1, a fission yeast Ste20/PAK homolog. Proc Nat lAcad Sci USA 93: 13802-13807.
49. Gilbreth M, Yang P, Bartholomeusz G, Pimental RA, Kansra S et al. (1998) Negative regulation of mitosis in fission yeast by the shk1 interacting protein skb1 and its human homolog, Skb1Hs. Proc Natl Acad Sci U S A 95: 14781-14786. doi:10.1073/pnas.95.25.14781. PubMed: 9843966.
50. Karkhanis V, Hu YJ, Baiocchi RA, Imbalzano AN, Sif S (2011) Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem Sci 36: 633-641. doi:10.1016/j.tibs.2011.09.001. PubMed: 21975038.
51. Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814. doi:10.1016/S0092-8674(01)00390-7. PubMed: 11440722.
52. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119: 397-418. PubMed: 8287795.
53. Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H et al. (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol 49: 1752-1759. doi:10.1093/pcp/pcn148. PubMed: 18854335.
54. Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131: 3445-3455. doi:10.1242/dev.01182. PubMed: 15226260.
55. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV et al. (2004) Chromatin techniques for plant cells. Plant J 39: 776-789. doi:10.1111/j.1365- 313X.2004.02169.x. PubMed: 15315638.