Abstract
Annual plants complete their life cycle in one year and initiate flowering only once, whereas perennials live for many years and flower repeatedly. How perennials undergo repeated cycles of vegetative growth and flowering that are synchronized to the changing seasons has not been extensively studied1. Flowering is best understood in annual Arabidopsis thaliana2,3, but many closely related species, such as Arabis alpina4,5, are perennials. We identified the A. alpina mutant perpetual flowering 1 (pep1), and showed that PEP1 contributes to three perennial traits. It limits the duration of flowering, facilitating a return to vegetative development, prevents some branches from undergoing the floral transition allowing polycarpic growth habit, and confers a flowering response to winter temperatures that restricts flowering to spring. Here we show that PEP1 is the orthologue of the A. thaliana gene FLOWERING LOCUS C (FLC). The FLC transcription factor inhibits flowering until A. thaliana is exposed to winter temperatures6,7, which trigger chromatin modifications that stably repress FLC transcription8,9,10,11. In contrast, PEP1 is only transiently repressed by low temperatures, causing repeated seasonal cycles of repression and activation of PEP1 transcription that allow it to carry out functions characteristic of the cyclical life history of perennials. The patterns of chromatin modifications at FLC and PEP1 differ correlating with their distinct expression patterns. Thus we describe a critical mechanism by which flowering regulation differs between related perennial and annual species, and propose that differences in chromatin regulation contribute to this variation.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Battey, N. H. & Tooke, F. Molecular control and variation in the floral transition. Curr. Opin. Plant Biol. 5, 62–68 (2002)
Turck, F., Fornara, F. & Coupland, G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573–594 (2008)
Baurle, I. & Dean, C. The timing of developmental transitions in plants. Cell 125, 655–664 (2006)
Ansell, S. W., Grundmann, M., Russell, S. J., Schneider, H. & Vogel, J. C. Genetic discontinuity, breeding-system change and population history of Arabis alpina in the Italian Peninsula and adjacent Alps. Mol. Ecol. 17, 2245–2257 (2008)
Koch, M. A. et al. Three times out of Asia Minor: the phylogeography of Arabis alpina L. (Brassicaceae). Mol. Ecol. 15, 825–839 (2006)
Michaels, S. D. & Amasino, R. M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949–956 (1999)
Sheldon, C. C. et al. The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445–458 (1999)
Bastow, R. et al. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167 (2004)
Sung, S. & Amasino, R. M. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164 (2004)
Gendall, A. R., Levy, Y. Y., Wilson, A. & Dean, C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis . Cell 107, 525–535 (2001)
Finnegan, E. J. & Dennis, E. S. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978–1983 (2007)
Battey, N. H. Aspects of seasonality. J. Exp. Bot. 51, 1769–1780 (2000)
Bohlenius, H. et al. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040–1043 (2006)
Foster, T., Johnston, R. & Seleznyova, A. A morphological and quantitative characterization of early floral development in apple (Malus × domestica Borkh.). Ann. Bot. (Lond.) 92, 199–206 (2003)
Diomaiuto, J. Periodic flowering or continual flowering as a function of temperature in a perennial species: the Ravenelle wallflower (Cheiranthus cheiri L.). Phytomorphology 38, 163–171 (1988)
Hay, A. & Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta . Nature Genet. 38, 942–947 (2006)
Hanikenne, M. et al. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4 . Nature 453, 391–395 (2008)
Schranz, M. E. et al. Characterization and effects of the replicated flowering time gene FLC in Brassica rapa . Genetics 162, 1457–1468 (2002)
D’Aloia, M., Tocquin, P. & Perilleux, C. Vernalization-induced repression of FLOWERING LOCUS C stimulates flowering in Sinapis alba and enhances plant responsiveness to photoperiod. New Phytol. 178, 755–765 (2008)
Schubert, D. et al. Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638–4649 (2006)
Sung, S., Schmitz, R. J. & Amasino, R. M. A. PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis . Genes Dev. 20, 3244–3248 (2006)
Greb, T. et al. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC . Curr. Biol. 17, 73–78 (2007)
Shindo, C., Lister, C., Crevillen, P., Nordborg, M. & Dean, C. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev. 20, 3079–3083 (2006)
Thomas, H., Thomas, H. M. & Ougham, H. Annuality, perenniality and cell death. J. Exp. Bot. 51, 1781–1788 (2000)
Bena, G., Lejeune, B., Prosperi, J.-M. & Olivieri, I. Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Proc. R. Soc. Lond. B 265, 1141–1151 (1998)
Beilstein, M. A., Al-Shehbaz, I. A. & Kellogg, E. A. Brassicaceae phylogeny and trichome evolution. Am. J. Bot. 93, 607–619 (2006)
Yan, L. et al. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–1644 (2004)
Prud’homme, B., Gompel, N. & Carroll, S. B. Emerging principles of regulatory evolution. Proc. Natl Acad. Sci. USA 104, 8605–8612 (2007)
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . Plant J. 16, 735–743 (1998)
Searle, I. et al. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis . Genes Dev. 20, 898–912 (2006)
Sanger, F., Nicklen, S. & Coulson, A. R. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA 74, 5463–5467 (1977)
Ewing, B., Hillier, L., Wendl, M. C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175–185 (1998)
Ewing, B. & Green, P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8, 186–194 (1998)
Gordon, D., Abajian, C. & Green, P. Consed: A graphical tool for sequence finishing. Genome Res. 8, 195–202 (1998)
Lukashin, A. V. & Borodovsky, M. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26, 1107–1115 (1998)
Salamov, A. A. & Solovyev, V. V. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10, 516–522 (2000)
Gremme, G., Brendel, V., Sparks, M. E. & Kurtz, S. Engineering a software tool for gene structure prediction in higher organisms. Inf. Softw. Technol. 47, 965–978 (2005)
Lewis, S. E. et al. Apollo: a sequence annotation editor. Genome Biol. 3, research0082 (2002)
Apweiler, R. et al. InterPro—an integrated documentation resource for protein families, domains and functional sites. Bioinformatics 16, 1145–1150 (2000)
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882 (1997)
Huson, D. H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73 (1998)
Acknowledgements
The authors would like to thank P. Sharma for growing plants and R. Bruggmann for running the gene prediction pipeline. The laboratories of H.S. and G.C. are partly funded by a core grant from the Max Planck Society.
Author information
Authors and Affiliations
Corresponding authors
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-8 with Legends, Supplementary Tables 1-2 and Supplementary References. (PDF 5319 kb)
Rights and permissions
About this article
Cite this article
Wang, R., Farrona, S., Vincent, C. et al. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423–427 (2009). https://doi.org/10.1038/nature07988
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature07988
This article is cited by
-
Phylogenomics of the genus Glycine sheds light on polyploid evolution and life-strategy transition
Nature Plants (2022)
-
Morphological, phenological, and transcriptional analyses provide insight into the diverse flowering traits of a mutant of the relic woody plant Liriodendron chinense
Horticulture Research (2021)
-
Exploring Flowering Genes in Isabgol (Plantago ovata Forsk.) Through Transcriptome Analysis
Plant Molecular Biology Reporter (2021)
-
Influence of Climate Change on Flowering Time
Journal of Plant Biology (2021)
-
Wolfberry genomes and the evolution of Lycium (Solanaceae)
Communications Biology (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.