Gene activation cascade triggered by a single photoperiodic cycle inducing flowering in Sinapis alba

[en] Molecular genetic analyses in Arabidopsis disclosed a genetic pathway whereby flowering is induced by the photoperiod. This cascade is examined here within the time course of floral transition in the long-day (LD) plant Sinapis alba induced by a single photoperiodic cycle. In addition to previously available sequences, the cloning of CONSTANS (SaCO) and FLOWERING LOCUS T (SaFT) homologues allowed expression analyses to be performed to follow the flowering process step by step. A diurnal rhythm in SaCO expression in the leaves was observed and transcripts of SaFT were detected when light was given in phase with SaCO kinetics only. This occurred when day length was extended or when a short day was shifted towards a ‘photophile phase’. The steady-state level of SaFT transcripts in the various physiological situations examined was found to correlate like a rheostat with floral induction strength. Kinetics of SaFT activation were also consistent with previous estimations of translocation of florigen out of leaves, which could actually occur after the inductive cycle. In response to one 22-h LD, initiation of floral meristems by the shoot apical meristem (SAM) started about 2 days after activation of SaFT and was marked by expression of APETALA1 (SaAP1). Meanwhile, LEAFY (SaLFY) was first up-regulated in leaf primordia and in the SAM. FRUITFULL (SaFUL) was later activated in the whole SAM but excluded from floral meristems. These patterns are integrated with previous observations concerning upregulation of SUPPRESSOR OF OVEREXPRESSION OF CO1 (SaSOC1) to provide a temporal and spatial map of floral transition in Sinapis.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

D'Aloia, Maria ; Université de Liège - ULiège > Département des sciences de la vie > Physiologie végétale

Tamseddak, Karim

Bonhomme, Delphine ; Université de Liège - ULiège > Doct. sc. (bioch., biol. mol.&cell., bioinf.&mod.-Bologne)

Bonhomme, Françoise

Bernier, Georges ; Université de Liège - ULiège > Services généraux (Faculté des sciences) > Relations académiques et scientifiques (Sciences)

Périlleux, Claire ; Université de Liège - ULiège > Département des sciences de la vie > Physiologie végétale

Language :

English

Title :

Gene activation cascade triggered by a single photoperiodic cycle inducing flowering in Sinapis alba

Publication date :

2009

Journal title :

Plant Journal

ISSN :

0960-7412

eISSN :

1365-313X

Publisher :

Wiley

Volume :

Pages :

962-973

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture
F.R.S.-FNRS - Fonds de la Recherche Scientifique
Interuniversity Attraction Poles Programme, Belgian State, Belgian Science Policy, P5/13 and P6/33

Available on ORBi :

since 26 November 2009

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Bibliography

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.
Ahn, J. H., Miller, D., Winter, V. J., Banfield, M. J., Lee, J. H., Yoo, S. Y., Henz, S. R., Brady, R. L. Weigel, D. (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25, 605 614.
An, H., Roussot, C., Suárez-López, P. et al. (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development, 131, 3615 3626.
Angerer, L. M., Cox, K. H. Angerer, R. C. (1987) Demonstration of tissue-specific gene-expression by in situ hybridization. In Methods in Enzymology, Vol. 152 Berger, S. L. Kimmel, A. R., eds). Orlando : Academic Press, pp. 649 661.
Bernier, G 1969) Sinapis alba L. In The Induction of Flowering. Some Case Histories Evans, L. T., ed Melbourne, Australia : MacMillan, pp. 305 327.
Bernier, G 1989) Events of the floral transition of meristems. In Plant Reproduction: From Floral Induction to Pollination Lord, E. Bernier, G., eds). Rockville : Amer. Soc. Plant Physiol., pp. 42 50.
Bernier, G. (1997) Growth changes in the shoot apex of Sinapis alba during transition to flowering. J. Exp. Bot. 48, 1071 1077.
Bernier, G. Bonhomme, F. (2001) Expression of genes controlling the flowering process: in which organ or tissue is it essential? Flowering Newsl. 32, 38 42.
Bernier, G., Bodson, M., Kinet, J. M., Jacqmard, A. Havelange, A. (1974) The nature of the floral stimulus in mustard. In Plant Growth Substances 1973. Tokyo : Hirokawa Publ., pp. 980 986.
Bernier, G., Kinet, J. M. Sachs, R. M. (1981) The Physiology of Flowering, Vol. I. Boca Raton, Florida : CRC Press.
Bernier, G., Havelange, A., Houssa, C., Petitjean, A. Lejeune, P. (1993) Physiological signals that induce flowering. Plant Cell, 5, 1147 1155.
Blázquez, M. A., Soowal, L. N., Lee, I. Weigel, D. (1997) LEAFY expression and flower initiation in Arabidopsis. Development, 124, 3835 3844.
Blázquez, M. A., Ferrándiz, C., Madueño, F. Parcy, F. (2006) How floral meristems are built. Plant Mol. Biol. 60, 855 870.
Bonhomme, F., Sommer, H., Bernier, G. Jacqmard, A. (1997) Characterization of SaMADS D from Sinapis alba suggests a dual function of the gene: in inflorescence development and floral organogenesis. Plant Mol. Biol. 34, 573 582.
Bonhomme, F., Kurz, B., Melzer, S., Bernier, G. Jacqmard, A. (2000) Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J. 24, 103 111.
Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K. Melzer, S. (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591 599.
Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R. Coen, E. (1997) Inflorescence commitment and architecture in Arabidopsis. Science, 275, 80 83.
Bünning, E. (1936) Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber. Dtsch. Bot. Ges. 54, 590 607.
Busch, A. Gleissberg, S. (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta, 217, 841 848.
Carmona, M. J., Cubas, P. Martínez-Zapater, J. M. (2002) VFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiol. 130, 68 77.
Castillejo, C. Pelaz, S. (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr. Biol. 18, 1338 1343.
Chardon, F. Damerval, C. (2005) Phylogenomic analysis of the PEBP gene family in cereals. J. Mol. Evol. 61, 579 590.
Corbesier, L., Vincent, C., Jang, S. et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316, 1030 1033.
D'Aloia, M., Tocquin, P. Périlleux, C. (2008) Vernalization- induced repression of FLOWERING LOCUS C stimulates flowering in Sinapis alba and enhances plant responsiveness to photoperiod. New Phytol. 178, 755 765.
Ferrándiz, C., Gu, Q., Martienssen, R. Yanofsky, M. F. (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development, 127, 725 734.
Fletcher, J. C. (2002) Shoot and floral meristem maintenance in Arabidopsis. Annu. Rev. Plant Biol. 53, 45 66.
de Folter, S., Immink, R. G. H., Kieffer, M. et al. (2005) Comprehensive interaction map of the Arabidopsis MADS-box transcription factors. Plant Cell, 17, 1424 1433.
Giakountis, A. Coupland, G. (2008) Phloem transport of flowering signals. Curr. Opin. Plant Biol. 11, 687 694.
Griffiths, S., Dunford, R. P., Coupland, G. Laurie, D. A. (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 131, 1855 1867.
Gu, Q., Ferrándiz, C., Yanofsky, M. F. Martienssen, R. (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development, 125, 1509 1517.
Hajdukiewicz, P., Svab, Z. Maliga, P. (1994) The small, versatile pPZP family of Agrobacterium binary vector for plant transformation. Plant Mol. Biol. 25, 989 994.
Hanzawa, Y., Money, T. Bradley, D. (2005) A single amino acid converts a repressor to an activator of flowering. Proc. Natl Acad. Sci. USA, 102, 7748 7753.
Hempel, F. D., Weigel, D., Mandel, M. A., Ditta, G., Zambryski, P. C., Feldman, L. J. Yanofsky, M. F. (1997) Floral determination and expression of floral regulatory genes in Arabidopsis. Development, 124, 3845 3853.
Hofer, J., Turner, L., Hellens, R., Ambrose, M., Matthews, P., Michael, A. Ellis, N. (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7, 581 587.
Jaeger, K. E. Wigge, P. A. (2007) FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17, 1050 1054.
Kardailsky, I., Shukla, V. K., Ahn, J. H., Dagenais, N., Christensen, S. K., Nguyen, J. T., Chory, J., Harrison, M. J. Weigel, D. (1999) Activation tagging of the floral inducer FT. Science, 286, 1962 1965.
Kinet, J. M. (1972) Sinapis alba, a plant requiring a single long day or a single short day for flowering. Nature, 236, 406 407.
King, R. W., Hisamatsu, T., Goldschmidt, E. E. Blundell, C. (2008) The nature of floral signals in Arabidopsis. I. Photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T (FT). J. Exp. Bot. 59, 3811 3820.
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.
Koncz, C. Schell, J. (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383 396.
Koornneef, M., Hanhart, C. J. van der Veen, J. H. (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57 66.
Lee, H., Suh, S. S., Park, E., Cho, E., Ahn, J. H., Kim, S. G., Lee, J. S., Kwon, Y. M. Lee, I. (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366 2376.
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.
Lejeune, P., Kinet, J. M. Bernier, G. (1988) Cytokinin fluxes during floral induction in the long day plant Sinapis alba L. Plant Physiol. 86, 1095 1098.
Liljegren, S.J., Gustafson-Brown, C., Pinyopich, A., Ditta, G.S. Yanofsky, M.F. (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1, specify meristem fate. Plant Cell, 11, 1007 1018.
Liu, C., Zhou, J., Bracha-Drori, K., Yalovsky, S., Ito, T. Yu, H. (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development, 134, 1901 1910.
Liu, C., Chen, H., Er, H. L., Soo, H. M., Kumar, P. P., Han, J. H., Liou, Y. C. Yu, H. (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development, 135, 1481 1491.
Logemann, E., Birkenbihl, R. P., Ülker, B. Somssich, I. E. (2006) An improved method for preparing Agrobacterium cells that simplifies the Arabidopsis transformation protocol. Plant Methods, 2, 16.
Lysak, M. A. Lexer, C. (2006) Towards the era of comparative evolutionary genomics in Brassicaceae. Plant. Syst. Evol. 259, 175 198.
Mandel, M. A. Yanofsky, M. F. (1995) The Arabidopsis AGL8 MADS-box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell, 7, 1763 1771.
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.
Melzer, S., Kampmann, G., Chandler, J. Apel, K. (1999) FPF1 modulates the competence to flowering in Arabidopsis. Plant J. 18, 395 405.
Melzer, S., Lens, F., Gennen, J., Vanneste, S., Rohde, A. Beeckman, T. (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat. Genet. 40, 1489 1492.
Menzel, G., Apel, K. Melzer, S. (1995) Isolation and analysis of SaMADS C, the APETALA1 cDNA homolog from mustard. Plant Physiol. 108, 853 854.
Menzel, G., Apel, K. Melzer, S. (1996) Identification of two MADS-box genes that are expressed in the apical meristem of the long-day plant Sinapis alba in transition to flowering. Plant J. 9, 399 408.
Michaels, S. D., Himelblau, E., Kim, S. Y., Schomburg, F. M. Amasino, R. M. (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149 156.
Murray, M. G. Thompson, W. F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321 4326.
Paltiel, J., Amin, R., Gover, A., Ori, N. Samach, A. (2006) Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta, 224, 1255 1268.
Parcy, F. (2005) Flowering: a time for integration. Int. J. Dev. Biol. 49, 585 593.
Pouteau, S., Tooke, F. Battey, N. (1998) Quantitative control of inflorescence formation in Impatiens balsamina. Plant Physiol. 118, 1191 1201.
Rao, N.N., Prasad, K., Kumar, P.R. Vijayraghavan, U. (2008) Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture. Proc. Natl Acad. Sci. USA, 105, 3646 3651.
Ratcliffe, O.J., Bradley, D.J. Coen, E.S. (1999) Seperation of shoot and floral identity in Arabidopsis. Development, 126, 1109 1120.
Robson, F., Costa, M. M. R., Hepworth, S. R., Vizir, I., Piñeiro, M., Reeves, P. H., Putterill, J. Coupland, G. (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J. 28, 619 631.
Ruonala, R., Rinne, P. L. H., Kangasjärvi, J. van der Schoot, C. (2008) CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell, 20, 59 74.
Salathia, N., Davis, S. J., Lynn, J. R., Michaels, S. D., Amasino, R. M. Millar, A. J. (2006) FLOWERING LOCUS C -dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways. BMC Plant Biol. 6, 10.
Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, M. F. Coupland, G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613 1616.
Schmid, M., Uhlenhaut, N. H., Godard, F., Demar, M., Bressan, R., Weigel, D. Lohmann, J. U. (2003) Dissection of floral induction pathways using global expression analysis. Development, 130, 6001 6012.
Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Kröber, S., Amasino, R. A. 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.
Sessions, A., Yanofsky, M. F. Weigel, D. (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science, 289, 779 781.
Shavorskaya, O. Lagercrantz, U. (2006) Sequence divergence at the putative flowering time locus COL1 in Brassicaceae. Mol. Phylogenet. Evol. 39, 846 854.
Simon, R.S., Igeño, M.I. Coupland, G. (1996) Activation of floral meristem identity genes in Arabidopsis. Nature, 384, 59 62.
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.
Teper-Bamnolker, P. Samach, A. (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell, 17, 2661 2675.
Thomas, B. Vince-Prue, D. (1997) Photoperiodism in Plants. San Diego : Acad. Press.
Thouet, J., Quinet, M., Ormenese, S., Kinet, J. M. Périlleux, C. (2008) Revisiting the involvement of SELF-PRUNING in the sympodial growth of tomato. Plant Physiol. 148, 61 64.
Turck, F., Fornara, F. Coupland, G. (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573 594.
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.
Wigge, P. A., Kim, M. C., Jaeger, K. E., Busch, W., Schmid, M., Lohmann, J. U. Weigel, D. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309, 1056 1059.
Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. Araki, T. (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175 1189.
Yoo, S. K., Chung, K. S., Kim, J., Lee, J. H., Hong, S. M., Yoo, S. J., Yoo, S. Y., Lee, J. S. 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.