A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species
Paul K. Boss A B , Lekha Sreekantan A and Mark R. Thomas AA Cooperative Research Centre for Viticulture, CSIRO Plant Industry, Horticulture Unit, PO Box 350, Glen Osmond, SA 5064, Australia.
B Corresponding author. Email: paul.boss@csiro.au
Functional Plant Biology 33(1) 31-41 https://doi.org/10.1071/FP05191
Submitted: 2 August 2005 Accepted: 14 September 2005 Published: 3 January 2006
Abstract
Grapevines (Vitis vinifera L.) have unusual plant architecture in that the shoot apical meristem produces both vegetative structures and primordia that are capable of forming inflorescences at regular intervals. These primordia are termed ‘uncommitted’ and differentiate into inflorescences or tendrils depending on the environment in which they are produced. To investigate the molecular relationship between tendrils and inflorescences and vine architecture, we cloned a TFL1 homologue from grapevine (VvTFL1). VvTFL1 is expressed in shoot apices early in latent bud development and in buds soon after bud burst. The grapevine homologue of LEAFY, VFL, is expressed at the same stages as VvTFL1 as well as in the later stages of inflorescence development. Neither VvTFL1 nor VFL were detected in tendrils. VvTFL1 was overexpressed in tobacco and Arabidopsis to confirm that it was functionally similar to TFL1 and not the close homologue FT. Flowering was delayed significantly in tobacco and Arabidopsis transformants overexpressing VvTFL1. However, an unexpected phenotype was observed in some of the transgenic Arabidopsis lines where the floral meristem became indeterminate and a new inflorescence would emerge from within the developing silique. Our findings suggest that VvTFL1 is a repressor of floral development. The nucleotide sequence reported in this paper has been submitted to GenBank under the accession number AF378127 (VvTFL1).
Keywords: Arabidopsis, flowering, grapevine, LEAFY, TERMINAL FLOWER 1, tobacco.
Acknowledgments
This work was supported in part by grants from the Grape and Wine Research and Development Corporation, the Dried Fruits Research and Development Council and the Cooperative Research Centre for Viticulture. The authors thank Di and John Harvey for allowing us to sample material from their vineyard, Don MacKenzie and Coralie Reich for excellent technical assistance and Stuart McClure for help with the SEM.
Amaya I,
Ratcliffe OJ, Bradley DJ
(1999) Expression of CENTRORADIALIS (CEN) and CEN-like genes in tobacco reveals a conserved mechanism controlling phase change in diverse species. The Plant Cell 11, 1405–1417.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Araki T
(2001) Transition from vegetative to reproductive phase. Current Opinion in Plant Biology 4, 63–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Blazquez MA,
Soowal LN,
Lee I, Weigel D
(1997) LEAFY expression and flower initiation in Arabidopsis. Development 124, 3835–3844.
| 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,
Davies C, Robinson SP
(1996) Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation. Plant Physiology 111, 1059–1066.
| 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 |
Bradley D,
Carpenter R,
Copsey L,
Vincent C,
Rothstein S, Coen E
(1996) Control of inflorescence architecture in Antirrhinum. Nature 379, 791–797.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bradley D,
Ratcliffe O,
Vincent C,
Carpenter R, Coen E
(1997) Inflorescence commitment and architecture in Arabidopsis. Science 275, 80–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Carmona MJ,
Cubas P, Martínez-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 |
Coombe BG
(1995) Adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1, 100–110.
Drews GN,
Bowman JL, Meyerowitz EM
(1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ferrandiz C,
Gu Q,
Martienssen R, Yanofsky MF
(2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734.
| PubMed |
Frohman MA,
Dush MK, Martin GR
(1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences USA 85, 8998–9002.
Gleave AP
(1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20, 1203–1207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hanzawa Y,
Money T, Bradley D
(2005) A single amino acid converts a repressor to an activator of flowering. Proceedings of the National Academy of Sciences USA 102, 7748–7753.
| Crossref | GoogleScholarGoogle Scholar |
Horsch RB,
Fry JT,
Hoffmann NI,
Eicholtz D,
Rogers SG, Fraley RT
(1985) A simple and general method for transforming genes into plants. Science 227, 1229–1231.
Jackson, DP (1991). In situ hybridisation in plants. In ‘Molecular plant pathology: a practical approach. I’. pp. 163–169. (Oxford University Press: Oxford)
Jensen CS,
Salchert K, Nielsen KJK
(2001) A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiology 125, 1517–1528.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Joly D,
Perrin M,
Gertz C,
Kronenberger J,
Demangeat G, Masson JE
(2004) Expression analysis of flowering genes from seedling-stage to vineyard life of grapevine cv. Riesling. Plant Science 166, 1427–1436.
| Crossref | GoogleScholarGoogle Scholar |
Kardailsky I,
Shukla VK,
Ahn J,
Dagenais N,
Christensen SK,
Nguyen JT,
Chory J,
Harrison MJ,
Weigel D, Ahn JH
(1999) Activation tagging of the floral inducer FT. Science 286, 1962–1965.
| 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 |
Marchuk D,
Drumm M,
Saulino A, Collins FS
(1991) Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Research 19, 1154.
| PubMed |
Morrison JC
(1991) Bud development in Vitis vinifera L. Botanical Gazette 152, 304–315.
| Crossref | GoogleScholarGoogle Scholar |
Murashige T, Skoog F
(1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
Ohshima S,
Murata M,
Sakamoto W,
Ogura Y, Motoyoshi F
(1997) Cloning and molecular analysis of the Arabidopsis gene Terminal Flower1. Molecular and General Genetics 254, 186–194.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pnueli L,
Carmelgoren L,
Hareven D,
Gutfinger T,
Alvarez J,
Ganal M,
Zamir D, Lifschitz E
(1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125, 1979–1989.
| PubMed |
Pratt C
(1971) Reproductive anatomy in cultivated grapes: a review. American Journal of Enology and Viticulture 22, 92–109.
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 |
Ratcliffe OJ,
Bradley DJ, Coen ES
(1999) Separation of shoot and floral identity in Arabidopsis. Development 126, 1109–1120.
| PubMed |
Srinivasan C, Mullins MG
(1981) Physiology of flowering in the grapevine: a review. American Journal of Enology and Viticulture 32, 47–63.
Tucker SC, Hoefert LL
(1968) Ontogeny of the tendril in Vitis vinifera. American Journal of Botany 55, 1110–1119.
