VvFT and VvMADS8, the grapevine homologues of the floral integrators FT and SOC1, have unique expression patterns in grapevine and hasten flowering in Arabidopsis
Lekha Sreekantan A and Mark R. Thomas A BA CSIRO Plant Industry, PO Box 350, Glen Osmond, SA 5064, Australia and Cooperative Research Centre for Viticulture, PO Box 145, Glen Osmond, SA 5064, Australia.
B Corresponding author. Email: Mark.R.Thomas@csiro.au
Functional Plant Biology 33(12) 1129-1139 https://doi.org/10.1071/FP06144
Submitted: 8 June 2006 Accepted: 11 September 2006 Published: 1 December 2006
Abstract
The Vitis vinifera L. flowering genes VvFT and VvMADS8 from the grapevine cultivar Cabernet Sauvignon have been isolated. Sequence analyses showed that VvFT and VvMADS8 were highly homologous to the floral integrators, FLOWERING LOCUS T (FT) and SUPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), respectively, from Arabidopsis. The expression pattern studied through real-time PCR revealed that expression of VvFT was quite low in axillary buds and high in developing inflorescence and berries. VvMADS8 was highly expressed in the axillary buds at the time when inflorescence primordia were being initiated in these buds suggesting that VvMADS8 is a gene involved in the early stages of inflorescence development. In tendrils, considered to be modified inflorescences, VvMADS8 was weakly expressed but high expression of VvFT in these organs showed that expression was irrespective of the flowering process. Through in situ hybridisation, strong expression of VvFT was detected in stamens and the ovary and ovule suggesting additional roles for VvFT in fruit and seed development. Strong expression of VvMADS8 was detected on the inflorescence primordium within the axillary bud. Overexpression of VvFT and VvMADS8 in Arabidopsis hastened flowering showing that both these genes function as promoters of flowering when ectopically expressed in a heterologous plant.
Acknowledgments
This work was supported in part by the Commonwealth Cooperative Research Centre Program, and specifically the Cooperative Research Centre for Viticulture (CRCV) and the Grape and Wine Research and Development Cooperation (GWRDC). We thank Don Mackenzie for technical assistance.
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
An HL,
Roussot C,
Suarez-Lopez P,
Corbesler L, Vincent C , et al.
(2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131, 3615–3626.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bechtold N,
Ellis J, Pelletier G
(1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Comptes Rendus de l’Acadamie des Sciences de Paris — Life Science 316, 1194–1199.
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. The Plant Journal 24, 591–599.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boss PK, Thomas MR
(2000) Tendrils, inflorescences and fruitfulness: a molecular perspective. Australian Journal of Grape and Wine Research 6, 168–174.
Boss PK, Thomas MR
(2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416, 847–850.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boss PK,
Vivier M,
Matsumoto S,
Dry IB, Thomas MR
(2001) A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Molecular Biology 45, 541–553.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boss PK,
Buckeridge EJ,
Poole A, Thomas MR
(2003) New insights into grapevine flowering. Functional Plant Biology 30, 593–606.
| Crossref | GoogleScholarGoogle Scholar |
Boss PK,
Sreekantan L, Thomas MR
(2006) A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Functional Plant Biology 33, 31–41.
| Crossref | GoogleScholarGoogle Scholar |
Buttrose MS
(1974) Climatic factors and fruitfulness in grapevines. Horticultural Abstracts 44, 319–326.
Calonje M,
Cubas P,
Martinez-Zapater JM, Carmona MJ
(2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiology 135, 1491–1501.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Carmona MJ,
Cubas P, Martinez-Zapater JM
(2002) VFL, the grapevine FLORICAULA / LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiology 130, 68–77.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clough SJ, Bent AF
(1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Colasanti J, Sundaresan V
(2000) ‘Florigen’ enters the molecular age: long-distance signals that cause plants to flower. Trends in Biochemical Sciences 25, 236–240.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Coombe BG
(1967) Effects of growth retardants on Vitis vinifera L. Vitis 6, 278–287.
Coombe BG
(1995) Adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1, 100–110.
Corbesier L, Coupland G
(2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant, Cell & Environment 28, 54–66.
| Crossref | GoogleScholarGoogle Scholar |
Cseke LJ,
Zheng J, Podila GK
(2003) Characterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development. Gene 318, 55–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Drews GN,
Bowman JL, Meyerowitz EM
(1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA-2 product. Cell 65, 991–1002.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Endo T,
Shimada T,
Fujii H,
Kobayashi Y,
Araki T, Omura M
(2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Research 14, 703–712.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gleave AP
(1992) A versatile binary vector system with a T-DNA organizational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20, 1203–1207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huang T,
Böhlenius H,
Eriksson S,
Parcy F, Nilsson O
(2005) The mRNA of the Arabidopsis gene FT moves from leaf to shoot apex and induces flowering. Science 309, 1694–1696.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kojima S,
Takahashi Y,
Kobayashi Y,
Monna L,
Sasaki T,
Araki T, Yano M
(2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant & Cell Physiology 43, 1096–1105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koornneef M,
Hanhart CJ, van der Veen JH
(1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular & General Genetics 229, 57–66.
Lazo GR,
Stein PA, Ludwig RA
(1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Bio/Technology 9, 963–967.
| Crossref | GoogleScholarGoogle Scholar |
Martin-Trillo M, Martinez-Zapater JM
(2002) Growing up fast: manipulating the generation time of trees. Current Opinion in Biotechnology 13, 151–155.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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. The Plant Journal 9, 399–408.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mullins MG
(1968) Regulation of inflorescence growth in cuttings of the grapevine (Vitis vinifera L.). Journal of Experimental Botany 19, 532–543.
Parenicova L,
de Folter S,
Kieffer M,
Horner DS, Favalli C , et al.
(2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. The Plant Cell 15, 1538–1551.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ratcliffe OJ,
Amaya I,
Vincent CA,
Rothstein S,
Carpenter R,
Coen ES, Bradley DJ
(1998) A common mechanism controls the life cycle and architecture of plants. Development 125, 1609–1615.
| PubMed |
Rezaian MA, Krake LR
(1987) Nucleic acid extraction and virus detection in grapevine. Journal of Virological Methods 17, 277–285.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Simpson G, Dean C
(2002) Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Srinivasan C, Mullins MG
(1980) Effects of temperature and growth regulators on formation of anlagen, tendrils and inflorescences in Vitis vinifera L. Annals of Botany 45, 439–446.
Svensson M,
Lundh D,
Bergman P, Mandal A
(2005) Characterisation of a T-DNA-tagged gene of Arabidopsis thaliana that regulates gibberellin metabolism and flowering time. Functional Plant Biology 32, 923–932.
| Crossref | GoogleScholarGoogle Scholar |
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. The Plant Cell 15, 2856–2865.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ueki S, Citovsky V
(2001) RNA commutes to work: regulation of plant gene expression by systemically transported RNA molecules. BioEssays 23, 1087–1090.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Utsunomiya N,
Sugiura A, Tomana T
(1978) Effect of CCC and pinching on inflorescence induction and development on lateral shoots in grapevine. Journal of the Japanese Society of Horticultural Science 47, 151–157.
Watson JM, Brill EM
(2004) Eucalyptus grandis has at least two functional SOC1-like floral activator genes. Functional Plant Biology 31, 225–234.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Physiology 46, 1175–1189.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yanovsky MJ, Kay SA
(2003) Living by the calendar: how plants know when to flower. Nature Reviews. Molecular Cell Biology 4, 265–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Physiology 139, 770–778.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zeevaart JAD
(1976) Physiology of flower formation. Annual Review of Plant Physiology 27, 321–348.
| Crossref | GoogleScholarGoogle Scholar |
