Plants have evolved annual and perennial life forms as alternative strategies to adapt reproduction and survival to environmental constraints. In isolated situations, such as islands, woody perennials have evolved repeatedly from annual ancestors1. Although the molecular basis of the rapid evolution of insular woodiness is unknown, the molecular difference between perennials and annuals might be rather small, and a change between these life strategies might not require major genetic innovations2,3. Developmental regulators can strongly affect evolutionary variation4 and genes involved in meristem transitions are good candidates for a switch in growth habit. We found that the MADS box proteins SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FRUITFULL (FUL) not only control flowering time, but also affect determinacy of all meristems. In addition, downregulation of both proteins established phenotypes common to the lifestyle of perennial plants, suggesting their involvement in the prevention of secondary growth and longevity in annual life forms.
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Carlquist, S. Island Biology (Columbia University Press, New York, 1974).
Thomas, H., Thomas, H.M. & Ougham, H. Annuality, perenniality and cell death. J. Exp. Bot. 51, 1781–1788 (2000).
Battey, N. & Tooke, F. Molecular control and variation in the floral transition. Curr. Opin. Plant Biol. 5, 62–68 (2002).
Cronk, Q.C.B. Plant evolution and development in a post-genomic context. Nat. Rev. Genet. 2, 607–619 (2001).
Corbesier, L. et al. FT protein movement contributes to long-distance signalling in floral induction of Arabidopsis . Science 316, 1030–1033 (2007).
Wigge, P.A. et al. Integration of spatial and temporal information during floral induction in Arabidopsis . Science 309, 1056–1059 (2005).
Borner, R. et al. A MADS domain gene involved in the transition to flowering in Arabidopsis . Plant J. 24, 591–599 (2000).
Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis . Science 288, 1613–1616 (2000).
Lee, H. et al. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis . Genes Dev. 14, 2366–2376 (2000).
Schmid, M. et al. Dissection of floral induction pathways using global expression analysis. Development 130, 6001–6012 (2003).
Hempel, F.D. et al. Floral determination and expression of floral regulatory genes in Arabidopsis . Development 124, 3845–3853 (1997).
Ferrandiz, C., Gu, Q., Martienssen, R. & Yanofsky, M. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734 (2000).
de Folter, S. et al. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17, 1424–1433 (2005).
Tooke, F. & Ordlidge, M. Chiurugwi, T. & Battey, N. Mechanisms and function of flower and inflorescence reversion. J. Exp. Bot. 56, 2587–2599 (2005).
Long, J. & Barton, M.K. Initiation of axillary and floral meristems in Arabidopsis . Dev. Biol. 218, 341–353 (2000).
Demura, T. & Fukuda, H. Transcriptional regulation in wood formation. Trends Plant Sci. 12, 64–70 (2007).
Sibout, R., Plantegenet, S. & Hardtke, C.S. Flowering as a condition for xylem expansion in Arabidopsis hypocotyls and root. Curr. Biol. 18, 458–463 (2008).
Schönrock, N. et al. Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev. 20, 1667–1678 (2006).
Kardailsky, I. et al. Activation tagging of the floral inducer FT. Science 286, 1962–1965 (1999).
Kobayashi, Y. et al. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962 (1999).
Teper-Bamnolker, P. & Samach, A. The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17, 2661–2675 (2005).
Yoo, S.K. et al. CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis . Plant Physiol. 139, 770–778 (2005).
Lifschitz, E. et al. The tomato FT orthologs triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA 103, 6398–6403 (2006).
Poduska, B. Humphrey, T. Redweik, A. & Grbic, V. The synergistic activation of FLOWERING LOCUS C by FRIGIDA and a new flowering gene AERIAL ROSETTE 1 underlies a novel morphology in Arabidopsis . Genetics 163, 1457–1465 (2003).
Wang, Q. et al. HUA2 caused natural variation in shoot morphology of A. thaliana . Curr. Biol. 17, 1513–1519 (2007).
Groover, A.T. What genes make a tree a tree? Trends Plant Sci. 10, 210–214 (2005).
Kim, S.-C., Crawford, D.J., Francisco-Ortega, J. & Santos-Guerra, A. A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proc. Natl. Acad. Sci. USA 93, 7743–7748 (1996).
Böhle, U.-R., Hilger, H.H. & Martin, W.F. Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc. Natl. Acad. Sci. USA 93, 11740–11745 (1996).
We appreciate the continuous support of K. Apel, D. Inzé and E. Smets. We thank J. Chandler and M. De Cock for critical reading of the manuscript. S.V. is indebted to the Institute for the Promotion of Innovation through Science and Technology in Flanders for a predoctoral fellowship. F.L. and A.R. are postdoctoral fellows of the Research Foundation-Flanders (FWO). Seeds of 35S:FT plants were provided by P. Wigge (John Innes Centre), seeds of the soc1-1 allele were provided by G. Coupland (Max Planck Institute for Plant Breeding Research) and seeds of soc1-2 in Col and Ler backgrounds by I. Lee (University of Seoul).
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Melzer, S., Lens, F., Gennen, J. et al. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 40, 1489–1492 (2008). https://doi.org/10.1038/ng.253
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