WEREWOLF, a regulator of root hair pattern formation, controls flowering time through the regulation of FT mRNA stability

Plant Physiology

Volumn 156, Issue 4, 2011, Pages 1867-1877

  Seo, Eunjoo ^a   Yu, Jihyeon ^a   Ryu, Kook Hui ^b   Lee, Myeong Min ^b   Lee, Ilha ^a  

^a Seoul National University   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79961186676     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.176685     Document Type: Article

References (74)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056
2. Ausín I, Alonso-Blanco C, Jarillo JA, Ruiz-García L, Martínez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36: 162-166
3. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125: 655-664
4. Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 12: 96-102
5. Bernhardt C, Lee MM, Gonzalez A, Zhang F, Lloyd A, Schiefelbein J (2003) The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130: 6431-6439
6. Bernhardt C, Zhao MZ, Gonzalez A, Lloyd A, Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132: 291-298
7. Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404: 889-892
8. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell (Suppl) 16: S18-S31
9. Castillejo C, Pelaz S (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr Biol 18: 1338-1343
10. Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423: 881-885
11. Choi K, Park C, Lee J, Oh M, Noh B, Lee I (2007) Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134: 1931-1941
12. Corbesier L, Vincent C, Jang SH, Fornara F, Fan QZ, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033
13. Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120: 2465-2474
14. Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A (2005) Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. Plant Cell 17: 1941-1952
15. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18: 4679-4688
16. Gutierrez RA, Ewing RM, Cherry JM, Green PJ (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch-and specific clock-controlled genes. Proc Natl Acad Sci USA 99: 11513-11518
17. Helliwell CA, Wood CC, Robertson M, Peacock WJ, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46: 183-192
18. Hempel FD, Weigel D, Mandel MA, Ditta G, Zambryski PC, Feldman LJ, Yanofsky MF (1997) Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124: 3845-3853
19. Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J 21: 4327-4337
20. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17: 1050-1054
21. Jiang D, Wang Y, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3: e3404
22. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286: 1962-1965
23. Kellogg EA (2001) Root hairs, trichomes and the evolution of duplicate genes. Trends Plant Sci 6: 550-552
24. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286: 1960-1962
25. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229: 57-66
26. Koshino-Kimura Y, Wada T, Tachibana T, Tsugeki R, Ishiguro S, Okada K (2005) Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol 46: 817-826
27. Kwak SH, Schiefelbein J (2007) The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Dev Biol 302: 118-131
28. Kwak SH, Shen R, Schiefelbein J (2005) Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307: 1111-1113
29. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366-2376
30. Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6: 75-83
31. Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao HY, Lee I, Deng XW (2007a) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731-749
32. Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J 55: 832-843
33. Lee JH, Hong SM, Yoo SJ, Park OK, Lee JS, Ahn JH (2006) Integration of floral inductive signals by FLOWERING LOCUS T and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1. Physiol Plant 126: 475-483
34. Lee JH, Park SH, Lee JS, Ahn JH (2007b) A conserved role of SHORT VEGETATIVE PHASE (SVP) in controlling flowering time of Brassica plants. Biochim Biophys Acta 1769: 455-461
35. Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99: 473-483
36. Lee MM, Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14: 611-618
37. Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15: 110-120
38. Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW (1996) The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122: 1253-1260
39. Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8: 1505-1517
40. Mathieu J, Warthmann N, Küttner F, Schmid M(2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17: 1055-1060
41. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956
42. Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46: 292-299
43. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35: 613-623
44. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell (Suppl) 14: S111-S130
45. Oda A, Fujiwara S, Kamada H, Coupland G, Mizoguchi T (2004) Antisense suppression of the Arabidopsis PIF3 gene does not affect circadian rhythms but causes early flowering and increases FT expression. FEBS Lett 557: 259-264
46. Oh M, Lee I (2007) Historical perspective on breakthroughs in flowering field. J Plant Biol 50: 249-256
47. Ohashi Y, Oka A, Ruberti I, Morelli G, Aoyama T (2002) Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant J 29: 359-369
48. Onouchi H, Igeño MI, Périlleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12: 885-900
49. Paciorek T, Sauer M, Balla J, Wiśniewska J, Friml J (2006) Immunocytochemical technique for protein localization in sections of plant tissues. Nat Protoc 1: 104-107
50. Page T, Macknight R, Yang CH, Dean C (1999) Genetic interactions of the Arabidopsis flowering time gene FCA, with genes regulating floral initiation. Plant J 17: 231-239
51. Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156: 1349-1362
52. Piñeiro M, Gómez-Mena C, Schaffer R, Martínez-Zapater JM, Coupland G (2003) EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. Plant Cell 15: 1552-1562
53. Ruiz-García L, Madueño F, Wilkinson M, Haughn G, Salinas J, Martínez-Zapater JM (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9: 1921-1934
54. Ryu KH, Kang YH, Park YH, Hwang I, Schiefelbein J, Lee MM(2005) The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development 132: 4765-4775
55. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
56. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jürgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21: 5036-5046
57. Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6: 74-78
58. Searle I, He YH, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20: 898-912
59. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296: 285-289
60. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456
61. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120
62. Takada S, Goto K (2003) TERMINAL FLOWER2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 15: 2856-2865
63. Teper-Bamnolker P, Samach A (2005) The flowering integrator FTregulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17: 2661-2675
64. Tiwari SB, Shen Y, Chang HC, Hou YL, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, et al (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187: 57-66
65. Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32: 255-262
66. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003-1006
67. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129: 5409-5419
68. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113-1116
69. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11: 1337-1350
70. Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377: 495-500
71. Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18: 2971-2984
72. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059
73. Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol 139: 770-778
74. Zhang F, Gonzalez A, Zhao MZ, Payne CT, Lloyd A (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130: 4859-4869