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PEP1 regulates perennial flowering in Arabis alpina

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Wang, Renhou, Farrona, Sara, Vincent, Coral, Joecker, Anika, Schoof, Heiko, Turck, Franziska, Alonso-Blanco, Carlos, Coupland, George, Albani, Maria C.·2009·Nature

DOI 10.1038/nature07988

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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 studied. Flowering is best understood in annual Arabidopsis thaliana, but many closely related species, such as Arabis alpina, 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 temperatures, which trigger chromatin modifications that stably repress FLC transcription. 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.

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Sanger, F., Nicklen, S., & Coulson, A. R. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.12.5463 · Cited by 68,572
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 38,685
Floral dip: a simplified method for Agrobacterium ‐mediated transformation of Arabidopsis thaliana
Clough, S. J., & Bent, A. F. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00343.x · Cited by 22,014
Base-Calling of Automated Sequencer Traces Using Phred. I. Accuracy AssessmentPreprint
Ewing, B., Hillier, L., Wendl, M. C., & Green, P. (1998) · Genome Research · doi:10.1101/gr.8.3.175 · Cited by 6,993
Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities
Ewing, B., & Green, P. (1998) · Genome Research · doi:10.1101/gr.8.3.186 · Cited by 5,439
Consed: a graphical tool for sequence finishing.Preprint
Gordon, D., Abajian, C., & Green, P. (1998) · Genome Research · doi:10.1101/gr.8.3.195 · Cited by 3,706
FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering
Michaels, S. D., & Amasino, R. M. (1999) · The Plant Cell · doi:10.1105/tpc.11.5.949 · Cited by 2,010
SplitsTree: analyzing and visualizing evolutionary data
Huson, D. (1998) · Bioinform. · doi:10.1093/bioinformatics/14.1.68 · Cited by 1,615
GeneMark.hmm: new solutions for gene finding
Lukashin, A. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.4.1107 · Cited by 1,536
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Yan, L., Loukoianov, A., Blechl, A. E., Tranquilli, G. E., Ramakrishna, W., SanMiguel, P. J., Bennetzen, J. L., Echenique, V. C., & Dubcovsky, J. (2004) · Science · doi:10.1126/science.1094305 · Cited by 1,161

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Andrés, F., & Coupland, G. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3291 · Cited by 1,538
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Forrest, J. R. K., & Miller‐Rushing, A. J. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0145 · Cited by 768
Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies
Smaczniak, C., Immink, R. G. H., Angenent, G. C., & Kaufmann, K. (2012) · Development · doi:10.1242/dev.074674 · Cited by 570
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Koornneef, M., & Meinke, D. W. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04086.x · Cited by 490
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Edwards, J. A., Santos‐Medellín, C., Liechty, Z., Nguyen, B., Lurie, E., Eason, S., Phillips, G. C., & Sundaresan, V. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2003862 · Cited by 488
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Jin, S., Nasim, Z., Susila, H., & Ahn, J. H. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.05.007 · Cited by 142
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Lundgren, M. R., & Marais, D. L. D. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.003 · Cited by 141
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Self-citation
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König, P., Tautenhahn, S., Cornelissen, J. H. C., Kattge, J., Bönisch, G., & Römermann, C. (2017) · Global Ecology and Biogeography · doi:10.1111/geb.12696 · Cited by 134
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Thermal energy dissipation and xanthophyll cycles beyond the Arabidopsis model
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Song, J., Irwin, J. A., & Dean, C. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.027 · Cited by 109
Patterns of phenotypic plasticity and local adaptation in the wide elevation range of the alpine plant Arabis alpina
de Villemereuil, P., Mouterde, M., Gaggiotti, O., & Till-Bottraud, I. (2018) · Journal of Ecology · doi:10.1111/1365-2745.12955 · Cited by 90
Flowering Locus C’s Lessons: Conserved Chromatin Switches Underpinning Developmental Timing and Adaptation
Hepworth, J., & Dean, C. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.00496 · Cited by 111
Transcriptome variation along bud development in grapevine (Vitis viniferaL.)
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Cao, Y., Li, Y.-L., Fan, Y.-F., Li, Z., Yoshida, K., Wang, J., Ma, X.-K., Wang, N., Mitsuda, N., Kotake, T., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02152-8 · Cited by 112
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McGarry, R. C., & Ayre, B. G. (2012) · Plant Science · doi:10.1016/j.plantsci.2012.03.002 · Cited by 104
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Zhuang, Y., Wang, X., Li, X., Hu, J., Fan, L., Landis, J. B., Cannon, S. B., Grimwood, J., Schmutz, J., Jackson, S. A., et al. (2022) · Nature Plants · doi:10.1038/s41477-022-01102-4 · Cited by 94
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Chapman, E. A., Thomsen, H. C., Tulloch, S., Correia, P. M. P., Luo, G., Najafi, J., DeHaan, L. R., Crews, T. E., Olsson, L., Lundquist, P., et al. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.898769 · Cited by 100
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Koenig, D., & Weigel, D. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3883 · Cited by 94
A regulatory circuit conferring varied flowering response to cold in annual and perennial plants
Hyun, Y., Vincent, C. A., Tilmes, V., Bergonzi, S., Kiefer, C., Richter, R., Martínez-Gallegos, R., Severing, E. I., & Coupland, G. (2019) · Science · doi:10.1126/science.aau8197 · Cited by 94
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Gaston, A., Perrotte, J., Lerceteau-Köhler, E., Rousseau‐Gueutin, M., Petit, A., Hernould, M., Rothan, C., & Denoyes-Rothan, B. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert047 · Cited by 95
Identification of flowering genes in strawberry, a perennial SD plant
Mouhu, K., Hytönen, T., Folta, K. M., Rantanen, M., Paulin, L. G., Auvinen, P., & Elomaa, P. (2009) · BMC Plant Biology · doi:10.1186/1471-2229-9-122 · Cited by 86
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Fischbeck, A., Leucht, K., Frey-Wagner, I. M., Bentz, S., Pesch, T., Kellermeier, S., Krebs, M., Fried, M., Rogler, G., Hausmann, M., et al. (2010) · Gut · doi:10.1136/gut.2009.201988 · Cited by 86
Nitrate acts at the Arabidopsis thaliana shoot apical meristem to regulate flowering time
Olas, J. J., Dingenen, J. V., Abel, C., Działo, M., Feil, R., Krapp, A., Schlereth, A., & Wahl, V. (2019) · New Phytologist · doi:10.1111/nph.15812 · Cited by 87
Gene regulatory networks controlled by FLOWERING LOCUS C that confer variation in seasonal flowering and life history
Madrid, E., Chandler, J., & Coupland, G. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa216 · Cited by 87
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Adrian, J., Torti, S., & Turck, F. (2009) · Molecular Plant · doi:10.1093/mp/ssp031 · Cited by 87
Self-citation
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Self-citation
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Castaings, L., Bergonzi, S., Albani, M. C., Kemi, U., Savolainen, O., & Coupland, G. (2014) · Nature Communications · doi:10.1038/ncomms5457 · Cited by 81
Self-citation
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Brunner, A. M., Evans, L. M., Hsu, C.-Y., & Sheng, X. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00732 · Cited by 79
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Koch, М. A., Kiefer, M., German, D. A., Al-Shehbaz, I. A., Franzke, A., Mummenhoff, K., & Schmickl, R. (2012) · Taxon · doi:10.1002/tax.615007 · Cited by 79
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Authors: Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., Alonso-Blanco, C., Coupland, G., & Albani, M. C.
Affiliations: Max Planck Institute for Plant Breeding Research (DE)
Corresponding author: Coupland, George
Albani, Maria C.
ORCID: Farrona, Sara
Vincent, Coral
Schoof, Heiko
Turck, Franziska
Coupland, George
Albani, Maria C.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2009-04-15
Volume: 459
Issue: 7245
Pages: 423-427
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature07988
OpenAlex: W2158386692
Cited by: 376
References: 41
Citations by year: 2026: 18 · 2025: 15 · 2024: 14 · 2023: 14 · 2022: 16 · 2021: 22 · 2020: 28 · 2019: 29 · 2018: 24 · 2017: 21 · 2016: 21 · 2015: 20 · 2014: 20 · 2013: 31 · 2012: 23
FWCI: 33.12
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Max Planck Digital Library (submittedVersion, other-oa)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders: Max-Planck-Gesellschaft
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Life Sciences › Agricultural and Biological Sciences › Plant Science › Flowering Plant Growth and Cultivation
Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords: Pep-1, Arabis alpina, FLOWERING LOCUS C, floral repressor, flowering duration, floral induction, polycarpy, vernalization, histone modifications, chromatin modification, spring flowering, Arabidopsis thaliana
MeSH terms: Chromatin, Histones, Methylation, Molecular Sequence Data, Mutation, Periodicity, Plant Proteins, Genes, Plant, Arabidopsis, Gene Expression Regulation, Plant, MADS Domain Proteins, Arabidopsis Proteins, Arabis, Flowers

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PEP1 regulates perennial flowering in Arabis alpina

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