BREVIPEDICELLUS Interacts with the SWI2/SNF2 Chromatin Remodeling ATPase BRAHMA to Regulate and Expression in Control of Inflorescence Architecture
BP is a class-I KNOX transcription factor that controls normal inflorescence architecture development by repressing the expression of two KNOX genes, KNAT2 and KNAT6. In this study, we showed that Arabidopsis BP directly interacts with the SWI2/SNF2 chromatin remodeling ATPase BRM. brm and bp mutants displayed similar inflorescence architecture defects, with clustered inflorescences, horizontally orientated pedicels, and short pedicels and internodes. Furthermore, BP and BRM co-target to KNAT2 and KNAT6 genes and repress their expression. This work reveals a new regulatory mechanism that BP associates with BRM in control of inflorescence architecture development.
Vyšlo v časopise:
BREVIPEDICELLUS Interacts with the SWI2/SNF2 Chromatin Remodeling ATPase BRAHMA to Regulate and Expression in Control of Inflorescence Architecture. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005125
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005125
Souhrn
BP is a class-I KNOX transcription factor that controls normal inflorescence architecture development by repressing the expression of two KNOX genes, KNAT2 and KNAT6. In this study, we showed that Arabidopsis BP directly interacts with the SWI2/SNF2 chromatin remodeling ATPase BRM. brm and bp mutants displayed similar inflorescence architecture defects, with clustered inflorescences, horizontally orientated pedicels, and short pedicels and internodes. Furthermore, BP and BRM co-target to KNAT2 and KNAT6 genes and repress their expression. This work reveals a new regulatory mechanism that BP associates with BRM in control of inflorescence architecture development.
Zdroje
1. Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14: 547–558. 11910003
2. Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, et al. (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci U S A 99: 4730–4735. 11917137
3. Bhatt AM, Etchells JP, Canales C, Lagodienko A, Dickinson H (2004) VAAMANA—a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene 328: 103–111. 15019989
4. Hamant O, Pautot V (2010) Plant development: a TALE story. C R Biol 333: 371–381. doi: 10.1016/j.crvi.2010.01.015 20371112
5. Rutjens B, Bao D, van Eck-Stouten E, Brand M, Smeekens S, et al. (2009) Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J 58: 641–654. doi: 10.1111/j.1365-313X.2009.03809.x 19175771
6. Smith HM, Hake S (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15: 1717–1727. 12897247
7. Byrne ME, Groover AT, Fontana JR, Martienssen RA (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 130: 3941–3950. 12874117
8. Hake S, Smith HM, Holtan H, Magnani E, Mele G, et al. (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20: 125–151. 15473837
9. Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69. 8538741
10. Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957–1965. 11934861
11. Kanrar S, Onguka O, Smith HM (2006) Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta 224: 1163–1173. 16741748
12. Ragni L, Belles-Boix E, Gunl M, Pautot V (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell 20: 888–900. doi: 10.1105/tpc.108.058230 18390591
13. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407–412. 17522673
14. Yu CW, Liu X, Luo M, Chen C, Lin X, et al. (2011) HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol 156: 173–184. doi: 10.1104/pp.111.174417 21398257
15. Liu X, Yu CW, Duan J, Luo M, Wang K, et al. (2012) HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol 158: 119–129. doi: 10.1104/pp.111.184275 21994348
16. Yuan L, Liu X, Luo M, Yang S, Wu K (2013) Involvement of histone modifications in plant abiotic stress responses. J Integr Plant Biol 55: 892–901. doi: 10.1111/jipb.12060 24034164
17. Cairns BR (2005) Chromatin remodeling complexes: strength in diversity, precision through specialization. Current opinion in genetics & development 15: 185–190.
18. Ho L, Crabtree GR (2010) Chromatin remodelling during development. Nature 463: 474–484. doi: 10.1038/nature08911 20110991
19. Kwon CS, Hibara K, Pfluger J, Bezhani S, Metha H, et al. (2006) A role for chromatin remodeling in regulation of CUC gene expression in the Arabidopsis cotyledon boundary. Development 133: 3223–3230. 16854978
20. Han SK, Sang Y, Rodrigues A, Wu MF, Rodriguez PL, et al. (2012) The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24: 4892–4906. doi: 10.1105/tpc.112.105114 23209114
21. Wu MF, Sang Y, Bezhani S, Yamaguchi N, Han SK, et al. (2012) SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. Proc Natl Acad Sci U S A 109: 3576–3581. doi: 10.1073/pnas.1113409109 22323601
22. Zhu Y, Rowley MJ, Bohmdorfer G, Wierzbicki AT (2013) A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Molecular cell 49: 298–309. doi: 10.1016/j.molcel.2012.11.011 23246435
23. Farrona S, Hurtado L, Bowman JL, Reyes JC (2004) The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering. Development 131: 4965–4975. 15371304
24. Farrona S, Hurtado L, March-Diaz R, Schmitz RJ, Florencio FJ, et al. (2011) Brahma is required for proper expression of the floral repressor FLC in Arabidopsis. PLoS One 6: e17997. doi: 10.1371/journal.pone.0017997 21445315
25. Hurtado L, Farrona S, Reyes JC (2006) The putative SWI/SNF complex subunit BRAHMA activates flower homeotic genes in Arabidopsis thaliana. Plant Mol Biol 62: 291–304. 16845477
26. Efroni I, Han SK, Kim HJ, Wu MF, Steiner E, et al. (2013) Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev Cell 24: 438–445. doi: 10.1016/j.devcel.2013.01.019 23449474
27. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428–438. 15469500
28. Farrona S, Hurtado L, Reyes JC (2007) A nucleosome interaction module is required for normal function of Arabidopsis thaliana BRAHMA. J Mol Biol 373: 240–250. 17825834
29. Tang X, Hou A, Babu M, Nguyen V, Hurtado L, et al. (2008) The Arabidopsis BRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves. Plant Physiol 147: 1143–1157. doi: 10.1104/pp.108.121996 18508955
30. Smith HM, Boschke I, Hake S (2002) Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci U S A 99: 9579–9584. 12093897
31. Viola IL, Gonzalez DH (2006) Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins. Biol Chem 387: 31–40. 16497162
32. Bolduc N, Hake S (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21: 1647–1658. doi: 10.1105/tpc.109.068221 19567707
33. Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, et al. (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109: 1560–1565. doi: 10.1073/pnas.1112871109 22238427
34. Belles-Boix E, Hamant O, Witiak SM, Morin H, Traas J, et al. (2006) KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell 18: 1900–1907. 16798887
35. Kwon CS, Chen C, Wagner D (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev 19: 992–1003. 15833920
36. Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, et al. (1996) Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 10: 2117–2130. 8804307
37. Battaglioli E, Andres ME, Rose DW, Chenoweth JG, Rosenfeld MG, et al. (2002) REST repression of neuronal genes requires components of the hSWI.SNF complex. J Biol Chem 277: 41038–41045. 12192000
38. Harikrishnan KN, Chow MZ, Baker EK, Pal S, Bassal S, et al. (2005) Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nature genetics 37: 254–264. 15696166
39. Tie F, Banerjee R, Conrad PA, Scacheri PC, Harte PJ (2012) Histone demethylase UTX and chromatin remodeler BRM bind directly to CBP and modulate acetylation of histone H3 lysine 27. Molecular and cellular biology 32: 2323–2334. doi: 10.1128/MCB.06392-11 22493065
40. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, et al. (2010) Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer cell 18: 316–328. doi: 10.1016/j.ccr.2010.09.006 20951942
41. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nature reviews Genetics 8: 9–22. 17173055
42. Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nature reviews Molecular cell biology 10: 697–708. doi: 10.1038/nrm2763 19738629
43. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343–349. doi: 10.1038/nature09784 21248841
44. Gutierrez L, Oktaba K, Scheuermann JC, Gambetta MC, Ly-Hartig N, et al. (2012) The role of the histone H2A ubiquitinase Sce in Polycomb repression. Development 139: 117–127. doi: 10.1242/dev.074450 22096074
45. Lodha M, Marco CF, Timmermans MC (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev 27: 596–601. doi: 10.1101/gad.211425.112 23468429
46. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, et al. (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15: 1560–1565. 16139211
47. Archacki R, Buszewicz D, Sarnowski TJ, Sarnowska E, Rolicka AT, et al. (2013) BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in arabidopsis. PLoS One 8: e58588. doi: 10.1371/journal.pone.0058588 23536800
48. Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO reports 3: 224–229. 11882541
49. Yu X, 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 U S A 105: 7618–7623. doi: 10.1073/pnas.0802254105 18467490
50. Liu X, Chen CY, Wang KC, Luo M, Tai R, et al. (2013) PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 25: 1258–1273. doi: 10.1105/tpc.113.109710 23548744
51. Luo M, Yu CW, Chen FF, Zhao L, Tian G, et al. (2012) Histone deacetylase HDA6 is functionally associated with AS1 in repression of KNOX genes in arabidopsis. PLoS genetics 8: e1003114. doi: 10.1371/journal.pgen.1003114 23271976
52. Zhou Y, Tan B, Luo M, Li Y, Liu C, et al. (2013) HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings. Plant Cell 25: 134–148. doi: 10.1105/tpc.112.096313 23362207
53. Liu X, Yang S, Zhao M, Luo M, Yu CW, et al. (2014) Transcriptional repression by histone deacetylases in plants. Mol Plant 7: 764–772. doi: 10.1093/mp/ssu033 24658416
54. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079
55. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609
56. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature protocols 2: 1565–1572. 17585298
57. Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nature methods 2: 213–218. 16163802
58. Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360–1367. 12194816
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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