The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 represses flowering and promotes vegetative growth

Plant Cell

Volumn 25, Issue 9, 2013, Pages 3296-3310

  Mouhu, Katriina ^a   Kurokura, Takeshi ^a,c   Koskela, Elli A ^a   Albert, Victor A ^b   Elomaa, Paula ^a   Hytönen, Timo ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY AT BUFFALO   (United States)

^c UTSUNOMIYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ELAGATIS; FRAGARIA; FRAGARIA VESCA; FRAGARIA X ANANASSA;

GIBBERELLIN; MADS DOMAIN PROTEIN; PHYTOHORMONE; VEGETABLE PROTEIN;

BIOLOGICAL MODEL; DNA SEQUENCE; FLOWER; FRAGARIA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHOTOPERIODICITY; PHYLOGENY; PHYSIOLOGY; PLANT; RADIATION RESPONSE; SEASON; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

BASE SEQUENCE; FLOWERS; FRAGARIA; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GIBBERELLINS; MADS DOMAIN PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PHOTOPERIOD; PHYLOGENY; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; SEASONS; SEEDLING; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION;

EID: 84886494510     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115055     Document Type: Article

References (89)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K., and Araki, T. (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
2. Albani, M.C., Battey, N.H., and Wilkinson, M.J. (2004). The development of ISSR-derived SCAR markers around the SEASONAL FLOWERING LOCUS (SFL) in Fragaria vesca. Theor. Appl. Genet. 109: 571-579.
3. An, H., Roussot, C., Suárez-López, P., Corbesier, L., Vincent, C., Piñeiro, M., Hepworth, S., Mouradov, A., Justin, S., Turnbull, C., and Coupland, G. (2004). CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615-3626.
4. Appleford, N.E.J., Evans, D.J., Lenton, J.R., Gaskin, P., Croker, S.J., Devos, K.M., Phillips, A.L., and Hedden, P. (2006). Function and transcript analysis of gibberellin-biosynthetic enzymes in wheat. Planta 223: 568-582.
5. Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H., and Nilsson, O. (2006). CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
6. Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R., and Coen, E. (1997). Inflorescence commitment and architecture in Arabidopsis. Science 275: 80-83.
7. Brown, T., and Wareing, P.F. (1965). Genetical control of everbearing habit and 3 other characters in varieties of Fragaria vesca. Euphytica 14: 97-112.
8. Cheon, K., Nakatsuka, A., Tasaki, K., and Kobayashi, N. (2012). Seasonal changes in the expression pattern of flowering-related genes in evergreen azalea 'Oomurasaki' (Rhododendron × pulchrum). Sci. Hortic. (Amsterdam) 134: 176-184.
9. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C., and Coupland, G. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033.
10. D'Aloia, M., Tamseddak, K., Bonhomme, D., Bonhomme, F., Bernier, G., and Périlleux, C. (2009). Gene activation cascade triggered by a single photoperiodic cycle inducing flowering in Sinapis alba. Plant J. 59: 962-973.
11. de Folter, S., Immink, R.G.H., Kieffer, M., Parenicová, L., Henz, S.R., Weigel, D., Busscher, M., Kooiker, M., Colombo, L., Kater, M.M., Davies, B., and Angenent, G.C. (2005). Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17: 1424-1433.
12. Deng, W., Ying, H., Helliwell, C.A., Taylor, J.M., Peacock, W.J., and Dennis, E.S. (2011). FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 6680-6685.
13. Dorca-Fornell, C., Gregis, V., Grandi, V., Coupland, G., Colombo, L., and Kater, M.M. (2011). The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. Plant J. 67: 1006-1017.
14. Edgar, R.C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797.
15. Evans, J.R., Evans, R.R., Regusci, C.L., and Rademacher, W. (1999). Mode of action, metabolism, and uptake of BAS 125W, prohexadione-calcium. HortScience 34: 1200-1201.
16. Ferrario, S., Busscher, J., Franken, J., Gerats, T., Vandenbussche, M., Angenent, G.C., and Immink, R.G.H. (2004). Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. Plant Cell 16: 1490-1505.
17. Guttridge, C.G., and Thompson, P.A. (1964). Effect of gibberellins on growth and flowering of Fragaria and Duchesnea. J. Exp. Bot. 15: 631-646.
18. Hanano, S., and Goto, K. (2011). Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell 23: 3172-3184.
19. Harberd, N.P., Belfield, E., and Yasumura, Y. (2009). The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: How an "inhibitor of an inhibitor" enables flexible response to fluctuating environments. Plant Cell 21: 1328-1339.
20. Hayama, R., Yokoi, S., Tamaki, S., Yano, M., and Shimamoto, K. (2003). Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422: 719-722.
21. Hecht, V., Foucher, F., Ferrándiz, C., Macknight, R., Navarro, C., Morin, J., Vardy, M.E., Ellis, N., Beltrán, J.P., Rameau, C., and Weller, J.L. (2005). Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137: 1420-1434.
22. Hecht, V., Laurie, R.E., Vander Schoor, J.K., Ridge, S., Knowles, C.L., Liew, L.C., Sussmilch, F.C., Murfet, I.C., Macknight, R.C., and Weller, J.L. (2011). The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23: 147-161.
23. Hedden, P., and Thomas, S.G. (2012). Gibberellin biosynthesis and its regulation. Biochem. J. 444: 11-25.
24. Heide, O.M. (1977). Photoperiod and temperature interactions in growth and flowering of strawberry. Physiol. Plant. 40: 21-26.
25. Heide, O.M., and Sønsteby, A. (2007). Interactions of temperature and photoperiod in the control of flowering of latitudinal and altitudinal populations of wild strawberry (Fragaria vesca). Physiol. Plant. 130: 280-286.
26. Hsu, C.Y., et al. (2011). FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc. Natl. Acad. Sci. USA 108: 10756-10761.
27. Hytönen, T., and Elomaa, P. (2011). Genetic and environmental regulation of flowering and runnering in strawberries. Genes Genomes Genomics 5: 56-64.
28. Hytönen, T., Elomaa, P., Moritz, T., and Junttila, O. (2009). Gibberellin mediates daylength-controlled differentiation of vegetative meristems in strawberry (Fragaria x ananassa Duch). BMC Plant Biol. 9: 18.
29. Hytönen, T., Palonen, P., Mouhu, K., and Junttila, O. (2004). Crown branching and cropping potential in strawberry (Fragaria x ananassa Duch.) can be enhanced by day-length treatments. J. Hortic. Sci. Biotechnol. 79: 466-471.
30. Immink, R.G.H., Posé, D., Ferrario, S., Ott, F., Kaufmann, K., Valentim, F.L., de Folter, S., van der Wal, F., van Dijk, A.D.J., Schmid, M., and Angenent, G.C. (2012). Characterization of SOC1's central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol. 160: 433-449.
31. Iwata, H., Gaston, A., Remay, A., Thouroude, T., Jeauffre, J., Kawamura, K., Oyant, L.H.-S., Araki, T., Denoyes, B., and Foucher, F. (2012). The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J. 69: 116-125.
32. Jaeger, K.E., Pullen, N., Lamzin, S., Morris, R.J., and Wigge, P.A. (2013). Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis. Plant Cell 25: 820-833.
33. Jahn, O.L., and Dana, M.N. (1970). Crown and inflorescence development in the strawberry, Fragaria ananassa. Am. J. Bot. 57: 607-612.
34. Jung, J.H., Ju, Y., Seo, P.J., Lee, J.H., and Park, C.M. (2012). The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J. 69: 577-588.
35. Kang, C., Darwish, O., Geretz, A., Shahan, R., Alkharouf, N., and Liu, Z. (2013). Genome-scale transcriptomic insights into earlystage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25: 1960-1978.
36. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
37. Kaufmann, K., Wellmer, F., Muiño, J.M., Ferrier, T., Wuest, S.E., Kumar, V., Serrano-Mislata, A., Madueño, F., Krajewski, P., Meyerowitz, E.M., Angenent, G.C., and Riechmann, J.L. (2010). Orchestration of floral initiation by APETALA1. Science 328: 85-89.
38. Kim, D.-H., Doyle, M.R., Sung, S., and Amasino, R.M. (2009). Vernalization: Winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25: 277-299.
39. Konsin, M., Voipio, I., and Palonen, P. (2001). Influence of photoperiod and duration of short-day treatment on vegetative growth and flowering of strawberry (Fragaria X ananassa duch). J. Hortic. Sci. Biotechnol. 76: 77-82.
40. Koskela, E.A., Mouhu, K., Albani, M.C., Kurokura, T., Rantanen, M., Sargent, D.J., Battey, N.H., Coupland, G., Elomaa, P., and Hytönen, T. (2012). Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol. 159: 1043-1054.
41. Kurokura, T., Inaba, Y., and Sugiyama, N. (2006). Histone H4 gene expression and morphological changes on shoot apices of strawberry (Fragaria × ananassa Duch.) during floral induction. Sci. Hortic. (Amsterdam) 110: 192-197.
42. Lee, H., Suh, S.S., Park, E., Cho, E., Ahn, J.H., Kim, S.G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14: 2366-2376.
43. Lee, J., Oh, M., Park, H., and Lee, I. (2008). SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J. 55: 832-843.
44. Lee, S., Kim, J., Han, J.J., Han, M.J., and An, G. (2004). Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J. 38: 754-764.
45. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E., and Yu, H. (2008). A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell 15: 110-120.
46. Liljegren, S.J., Gustafson-Brown, C., Pinyopich, A., Ditta, G.S., and Yanofsky, M.F. (1999). Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11: 1007-1018.
47. Liu, C., Chen, H., Er, H.L., Soo, H.M., Kumar, P.P., Han, J.H., Liou, Y.C., and Yu, H. (2008). Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135: 1481-1491.
48. Liu, C., Teo, Z.W.N., Bi, Y., Song, S., Xi, W., Yang, X., Yin, Z., and Yu, H. (2013). A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev. Cell 24: 612-622.
49. Lyons, E., and Freeling, M. (2008). How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53: 661-673.
50. Menzel, G., Apel, K., and 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. Plant J. 9: 399-408.
51. Middleton, A.M., Úbeda-Tomás, S., Griffiths, J., Holman, T., Hedden, P., Thomas, S.G., Phillips, A.L., Holdsworth, M.J., Bennett, M.J., King, J.R., and Owen, M.R. (2012). Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proc. Natl. Acad. Sci. USA 109: 7571-7576.
52. Monte, D., and Somerville, S. (2002). Pine tree method for isolation of plant RNA. In DNA Microarrays: A Molecular Cloning Manual, D. Bowtell and J. Sambrook, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 124-126.
53. Moon, J., Lee, H., Kim, M., and Lee, I. (2005). Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol. 46: 292-299.
54. Moon, J., Suh, S.S., Lee, H., Choi, K.R., Hong, C.B., Paek, N.C., Kim, S.G., and Lee, I. (2003). The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J. 35: 613-623.
55. Mouhu, K., Hytönen, T., Folta, K., Rantanen, M., Paulin, L., Auvinen, P., and Elomaa, P. (2009). Identification of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol. 9: 122.
56. Mutasa-Göttgens, E., and Hedden, P. (2009). Gibberellin as a factor in floral regulatory networks. J. Exp. Bot. 60: 1979-1989.
57. Nakamura, T., Song, I.-J., Fukuda, T., Yokoyama, J., Maki, M., Ochiai, T., Kameya, T., and Kanno, A. (2005). Characterization of TrcMADS1 gene of Trillium camtschatcense (Trilliaceae) reveals functional evolution of the SOC1/TM3-like gene family. J. Plant Res. 118: 229-234.
58. Oosumi, T., Gruszewski, H.A., Blischak, L.A., Baxter, A.J., Wadl, P.A., Shuman, J.L., Veilleux, R.E., and Shulaev, V. (2006). Highefficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223: 1219-1230.
59. Osnato, M., Castillejo, C., Matías-Hernández, L., and Pelaz, S. (2012). TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat. Commun. 3: 808.
60. Peng, J., Carol, P., Richards, D.E., King, K.E., Cowling, R.J., Murphy, G.P., and Harberd, N.P. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11: 3194-3205.
61. Pin, P.A., and Nilsson, O. (2012). The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ. 35: 1742-1755.
62. Potter, D., Eriksson, T., Evans, R.C., Oh, S., Smedmark, J.E.E., Morgan, D.R., Kerr, M., Robertson, K.R., Arsenault, M., Dickinson, T.A., and Campbell, C.S. (2007). Phylogeny and classification of Rosaceae. Plant Syst. Evol. 266: 5-43.
63. Randoux, M., Jeauffre, J., Thouroude, T., Vasseur, F., Hamama, L., Juchaux, M., Sakr, S., and Foucher, F. (2012). Gibberellins regulate the transcription of the continuous flowering regulator, RoKSN, a rose TFL1 homologue. J. Exp. Bot. 63: 6543-6554.
64. Ratcliffe, O.J., Bradley, D.J., and Coen, E.S. (1999). Separation of shoot and floral identity in Arabidopsis. Development 126: 1109-1120.
65. Riechmann, J.L., and Meyerowitz, E.M. (1997). MADS domain proteins in plant development. Biol. Chem. 378: 1079-1101.
66. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616.
67. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Kröber, S., Amasino, R.A., and Coupland, G. (2006). The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20: 898-912.
68. Seo, E., Lee, H., Jeon, J., Park, H., Kim, J., Noh, Y.-S., and Lee, I. (2009). Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21: 3185-3197.
69. Shulaev, V., et al. (2011). The genome of woodland strawberry (Fragaria vesca). Nat. Genet. 43: 109-116.
70. Simpson, G.G. (2004). The autonomous pathway: Epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol. 7: 570-574.
71. Stamatakis, A., Hoover, P., and Rougemont, J.A. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 57: 758-771.
72. Suárez-López, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and Coupland, G. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120.
73. Sønsteby, A., and Heide, O. (2008). Long-day rather than autonomous control of flowering in the diploid everbearing strawberry Fragaria vesca ssp. semperflorens. J. Hortic. Sci. Biotechnol. 83: 360-366.
74. Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S., and Shimamoto, K. (2007). Hd3a protein is a mobile flowering signal in rice. Science 316: 1033-1036.
75. Tao, Z., Shen, L., Liu, C., Liu, L., Yan, Y., and Yu, H. (2012). Genomewide identification of SOC1 and SVP targets during the floral transition in Arabidopsis. Plant J. 70: 549-561.
76. Taoka, K., et al. (2011). 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476: 332-335.
77. Torti, S., Fornara, F., Vincent, C., Andrés, F., Nordström, K., Göbel, U., Knoll, D., Schoof, H., and Coupland, G. (2012). Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24: 444-462.
78. Trainin, T., Bar-Ya'akov, I., and Holland, D. (2013). ParSOC1, a MADS-box gene closely related to Arabidopsis AGL20/SOC1, is expressed in apricot leaves in a diurnal manner and is linked with chilling requirements for dormancy break. Tree Genet. Genomes 9: 753-766.
79. Tsuji, H., Taoka, K., and Shimamoto, K. (2011). Regulation of flowering in rice: Two florigen genes, a complex gene network, and natural variation. Curr. Opin. Plant Biol. 14: 45-52.
80. Turck, F., Fornara, F., and Coupland, G. (2008). Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59: 573-594.
81. Turnbull, C. (2011). Long-distance regulation of flowering time. J. Exp. Bot. 62: 4399-4413.
82. Vandenbussche, M., Theissen, G., Van de Peer, Y., and Gerats, T. (2003). Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res. 31: 4401-4409.
83. van Dijk, A.D.J., Morabito, G., Fiers, M., van Ham, R.C.H.J., Angenent, G.C., and Immink, R.G.H. (2010). Sequence motifs in MADS transcription factors responsible for specificity and diversification of protein-protein interaction. PLoS Comput. Biol. 6: e1001017.
84. Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., Alonso-Blanco, C., Coupland, G., and Albani, M.C. (2009). PEP1 regulates perennial flowering in Arabis alpina. Nature 459: 423-427.
85. Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U., and Weigel, D. (2005). Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
86. Wiseman, N.J., and Turnbull, C.G.N. (1999). Effects of photoperiod and paclobutrazol on growth dynamics of petioles in strawberry (Fragaria × ananassa). Aust. J. Plant Physiol. 26: 353-358.
87. Yoo, S.K., Chung, K.S., Kim, J., Lee, J.H., Hong, S.M., Yoo, S.J., Yoo, S.Y., Lee, J.S., and Ahn, J.H. (2005). CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139: 770-778.
88. Zhang, X.R., Henriques, R., Lin, S.S., Niu, Q.W., and Chua, N.H. (2006). Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1: 641-646.
89. Zhou, C.-M., Zhang, T.-Q., Wang, X., Yu, S., Lian, H., Tang, H., Feng, Z.-Y., Zozomova-Lihová, J., and Wang, J.-W. (2013). Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340: 1097-1100.