Gibberellic acid signaling is required for ambient temperature-mediated induction of flowering in Arabidopsis thaliana

Plant Journal

Volumn 84, Issue 5, 2015, Pages 949-962

  Galvão, Vinicius Costa ^a,b   Collani, Silvio ^a   Horrer, Daniel ^a,d   Schmid, Markus ^a,c  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UMEÅ UNIVERSITY   (Sweden)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

ambient temperature; Arabidopsis thaliana; ARP6; FLM; flowering; FT; gibberellin; H2A.Z; PIF; SVP

Indexed keywords

BIOCHEMISTRY; GENES; PLANTS (BOTANY);

ARABIDOPSIS THALIANA; ARP6; FLM; FLOWERING; FT; GIBBERELLIN; H2A.Z; PIF; SVP;

TEMPERATURE;

ACTIN BINDING PROTEIN; ARABIDOPSIS PROTEIN; ARP6 PROTEIN, ARABIDOPSIS; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; FT PROTEIN, ARABIDOPSIS; GIBBERELLIC ACID; GIBBERELLIN; HISTONE; NUCLEOSOME; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHYTOHORMONE; PIF3 PROTEIN, ARABIDOPSIS; PIF4 PROTEIN, ARABIDOPSIS; PIF5 PROTEIN, ARABIDOPSIS; TSF PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOSOME; PHOTOPERIODICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TEMPERATURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FLOWERS; GIBBERELLINS; HISTONES; MICROFILAMENT PROTEINS; NUCLEOSOMES; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHOTOPERIOD; PLANT GROWTH REGULATORS; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 84955210509     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13051     Document Type: Article

References (52)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K., and, Araki, T., (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science, 309, 1052-1056.
2. An, H., Roussot, C., Suarez-Lopez, P., et al. (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development, 131, 3615-3626.
3. Andres, F., Porri, A., Torti, S., Mateos, J., Romera-Branchat, M., Garcia-Martinez, J.L., Fornara, F., Gregis, V., Kater, M.M., and, Coupland, G., (2014) SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc. Natl Acad. Sci. USA, 111, E2760-E2769.
4. Balasubramanian, S., Sureshkumar, S., Lempe, J., and, Weigel, D., (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, e106.
5. Bouche, F., Detry, N., and, Perilleux, C., (2015) Heat can erase epigenetic marks of vernalization in Arabidopsis. Plant Signal. Behav. 10, e990799.
6. Capovilla, G., Schmid, M., and, Posé, D., (2015) Control of flowering by ambient temperature. J. Exp. Bot. 66, 59-69.
7. Claeys, H., De Bodt, S., and, Inze, D., (2014) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci. 19, 231-239.
8. Coleman-Derr, D., and, Zilberman, D., (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet. 8, e1002988.
9. Corbesier, L., Vincent, C., Jang, S.H., et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316, 1030-1033.
10. Deal, R.B., Kandasamy, M.K., McKinney, E.C., and, Meagher, R.B., (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell, 17, 2633-2646.
11. Deal, R.B., Topp, C.N., McKinney, E.C., and, Meagher, R.B., (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell, 19, 74-83.
12. Feng, S., Martinez, C., Gusmaroli, G., et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature, 451, 475-479.
13. Fujimori, T., Yamashino, T., Kato, T., and, Mizuno, T., (2004) Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 45, 1078-1086.
14. Galvão, V.C., and, Schmid, M., (2014) Regulation of flowering by endogenous signals. In Molecular Genetics of Floral Transition and Flower Development (, Fornara, F., ed.) London, UK: Elsevier, pp. 63-102.
15. Galvão, V.C., Horrer, D., Kuttner, F., and, Schmid, M., (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development, 139, 4072-4082.
16. Hauvermale, A.L., Ariizumi, T., and, Steber, C.M., (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol. 160, 83-92.
17. Kawamoto, N., Sasabe, M., Endo, M., Machida, Y., and, Araki, T., (2015) Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation. Sci. Rep. 5, 8341.
18. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and, Choi, G., (2003) Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell, 15, 2399-2407.
19. Kim, J.J., Lee, J.H., Kim, W., Jung, H.S., Huijser, P., and, Ahn, J.H., (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol. 159, 461-478.
20. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and, Franklin, K.A., (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408-413.
21. Krzywinski, M., and, Altman, N., (2014) Visualizing samples with box plots. Nat. Methods, 11, 119-120.
22. Kumar, S.V., and, Wigge, P.A., (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell, 140, 136-147.
23. Kumar, S.V., Lucyshyn, D., Jaeger, K.E., Alos, E., Alvey, E., Harberd, N.P., and, Wigge, P.A., (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature, 484, 242-245.
24. Lee, S., Cheng, H., King, K.E., Wang, W., He, Y., Hussain, A., Lo, J., Harberd, N.P., and, Peng, J., (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev. 16, 646-658.
25. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S., and, Ahn, J.H., (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397-402.
26. Lee, J.H., Ryu, H.S., Chung, K.S., Posé, D., Kim, S., Schmid, M., and, Ahn, J.H., (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science, 342, 628-632.
27. Leivar, P., and, Monte, E., (2014) PIFs: systems integrators in plant development. Plant Cell, 26, 56-78.
28. Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E., and, Quail, P.H., (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18, 1815-1823.
29. Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L., and, Quail, P.H., (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell, 21, 3535-3553.
30. Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C., and, Fankhauser, C., (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312-323.
31. Martin-Trillo, M., Lazaro, A., Poethig, R.S., Gomez-Mena, C., Pineiro, M.A., Martinez-Zapater, J.M., and, Jarillo, J.A., (2006) EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development, 133, 1241-1252.
32. Mathieu, J., Warthmann, N., Kuttner, F., and, Schmid, M., (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol. 17, 1055-1060.
33. Nusinow, D.A., Helfer, A., Hamilton, E.E., King, J.J., Imaizumi, T., Schultz, T.F., Farre, E.M., and, Kay, S.A., (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature, 475, 398-402.
34. Perilleux, C., Pieltain, A., Jacquemin, G., et al. (2013) A root chicory MADS-box sequence and the Arabidopsis flowering repressor FLC share common features that suggest conserved function in vernalization and de-vernalization responses. Plant J. 75, 390-402.
35. Porri, A., Torti, S., Romera-Branchat, M., and, Coupland, G., (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development, 139, 2198-2209.
36. Posé, D., Verhage, L., Ott, F., Yant, L., Mathieu, J., Angenent, G.C., Immink, R.G., and, Schmid, M., (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature, 503, 414-417.
37. Riboni, M., Galbiati, M., Tonelli, C., and, Conti, L., (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiol. 162, 1706-1719.
38. Richter, R., Bastakis, E., and, Schwechheimer, C., (2013) Cross-repressive interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the control of greening, cold tolerance, and flowering time in Arabidopsis. Plant Physiol. 162, 1992-2004.
39. Romera-Branchat, M., Andres, F., and, Coupland, G., (2014) Flowering responses to seasonal cues: what's new? Curr. Opin. Plant Biol. 21, 120-127.
40. Sakuraba, Y., Jeong, J., Kang, M.Y., Kim, J., Paek, N.C., and, Choi, G., (2014) Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat. Commun. 5, 4636.
41. Scortecci, K.C., Michaels, S.D., and, Amasino, R.M., (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 26, 229-236.
42. Silverstone, A.L., Mak, P.Y., Martinez, E.C., and, Sun, T.P., (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics, 146, 1087-1099.
43. Song, Y.H., Shim, J.S., Kinmonth-Schultz, H.A., and, Imaizumi, T., (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu. Rev. Plant Biol. 66, 441-464.
44. Srikanth, A., and, Schmid, M., (2011) Regulation of flowering time: all roads lead to Rome. Cell. Mol. Life Sci. 68, 2013-2037.
45. Taoka, K., Ohki, I., Tsuji, H., et al. (2011) 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature, 476, 332-335.
46. Thines, B.C., Youn, Y., Duarte, M.I., and, Harmon, F.G., (2014) The time of day effects of warm temperature on flowering time involve PIF4 and PIF5. J. Exp. Bot. 65, 1141-1151.
47. Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U., and, Weigel, D., (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309, 1056-1059.
48. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M., and, Araki, T., (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175-1189.
49. Yamaguchi, N., Winter, C.M., Wu, M.F., Kanno, Y., Yamaguchi, A., Seo, M., and, Wagner, D., (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science, 344, 638-641.
50. Yoo, S.K., Chung, K.S., Kim, J., Lee, J.H., Hong, S.M., Yoo, S.J., Yoo, S.Y., Lee, J.S., and, Ahn, J.H., (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139, 770-778.
51. Yu, S., Galvão, V.C., Zhang, Y.C., Horrer, D., Zhang, T.Q., Hao, Y.H., Feng, Y.Q., Wang, S., Schmid, M., and, Wang, J.W., (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell, 24, 3320-3332.
52. Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and, Quail, P.H., (2013) A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9, e1003244.