Isolation and functional analysis of CONSTANS-LIKE genes suggests that a central role for CONSTANS in flowering time control is not evolutionarily conserved in Medicago truncatula

Frontiers in Plant Science

Volumn 5, Issue , 2014, Pages

  Wong, Albert C S ^a   Hecht, Valérie F G ^a   Picard, Kelsey ^b   Diwadkar, Payal ^b   Laurie, Rebecca E ^b   Wen, Jiangqi ^c   Mysore, Kirankumar ^c   Macknight, Richard C ^b   Weller, James L ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c PLANT BIOLOGY DIVISION   (United States)

Author keywords

CONSTANS; Flowering; Legume; Medicago; Photoperiod

Indexed keywords

EID: 84907381499     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00486     Document Type: Article

References (62)

1. Adrian, J., Farrona, S., Reimer, J. J., Albani, M. C., Coupland, G., and Turck, F. (2010). cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22, 1425–1440. doi: 10.1105/tpc.110.074682
2. Andres, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639. doi: 10.1038/n rg3291
3. Ballerini, E.S., and Kramer, E.M. (2011). In the light of evolution: a reevaluation of conservation in the CO-FT regulon and its role in photoperiodic regulation of flowering time. Front. Plant Sci. 2:81. doi: 10.3389/fpls.2011. 00081
4. Ben-Naim, O., Eshed, R., Parnis, A., Teper-Bamnolker, P., Shalit, A., Coupland, G., et al. (2006). The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J. 46, 462–476. doi: 10.1111/j.1365-313X.2006.02706.x
5. Brambilla, V., and Fornara, F. (2013). Molecular control of flowering in response to day length in rice. J. Integr. Plant Biol. 55, 410–418. doi: 10.1111/jipb.12033
6. Campoli, C., Drosse, B., Searle, I., Coupland, G., and Von Korff, M. (2012). Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J. 69, 868–880. doi: 10.1111/j.1365-313X.2011.04839.x
7. Cao, S., Kumimoto, R.W., Gnesutta, N., Calogero, A.M., Mantovani, R., and Holt, B.F. 3rd (2014). A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26, 1009–1017. doi: 10.1105/tpc.113.120352
8. Cheng, X.-F., and Wang, Z.-Y. (2005). Overexpression of COL9, a CONSTANS LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J. 43, 758–768. doi: 10.1111/j.1365-313X.2005.02491.x
9. Chia, T. Y., Muller, A., Jung, C., and Mutasa-Gottgens, E. S. (2008). Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus. J. Exp. Bot. 59, 2735–2748. doi: 10.1093/jxb/ern129
10. Datta, S., Hettiarachchi, G.H., Deng, X.W., and Holm, M. (2006). Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. Plant Cell 18, 70–84. doi: 10.1105/tpc.105.038182
11. Fan, C., Hu, R., Zhang, X., Wang, X., Zhang, W., Zhang, Q., et al. (2014). Conserved CO-FT regulons contribute to the photoperiod flowering control in soybean. BMC Plant Biol. 14:9. doi: 10.1186/1471-222 9-14-9
12. Fornara, F., Panigrahi, K. C., Gissot, L., Sauerbrunn, N., Ruhl, M., Jarillo, J. A., et al. (2009). Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17, 75–86. doi: 10.1016/j.devcel.2009.06.015
13. Gonzalez-Schain, N.D., Diaz-Mendoza, M., Zurczak, M., and Suarez-Lopez, P. (2012). Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J. 70, 678–690. doi: 10.1111/j.1365-313X.2012.04909.x
14. Griffiths, S., Dunford, R. P., Coupland, G., and Laurie, D. A. (2003). The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 131, 1855–1867. doi: 10.1104/pp.102.016188
15. Hassidim, M., Harir, Y., Yakir, E., Kron, I., and Green, R.M. (2009). Over-expression of CONSTANS-LIKE 5 can induce flowering in shortday grown Arabidopsis. Planta 230, 481–491. doi: 10.1007/s00425-0090958-7
16. Hecht, V., Foucher, F., Ferrandiz, C., Macknight, R., Navarro, C., Morin, J., et al. (2005). Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137, 1420–1434. doi: 10.1104/pp.104.0 57018
17. Hecht, V., Knowles, C. L., Vander Schoor, J. K., Liew, L. C., Jones, S. E., Lambert, M. J. M., et al. (2007). Pea LATE BLOOMER1 is a GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologs. Plant Physiol. 144, 648–661. doi: 10.1104/pp.107.096818
18. Hecht, V., Laurie, R. E., Vander Schoor, J. K., Ridge, S., Knowles, C. L., Liew, L. C., et al. (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. doi: 10.1105/tpc.110.0 81042
19. Hellens, R. P., Allan, A. C., Friel, E. N., Bolitho, K., Grafton, K., Templeton, M. D., et al. (2005). Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13. doi: 10.1186/1746-4811-1-13
20. Hsu, C. Y., Adams, J. P., No, K., Liang, H., Meilan, R., Pechanova, O., et al. (2012). Overexpression of CONSTANS homologs CO1 and CO2 fails to alter normal reproductive onset and fall bud set in woody perennial poplar. PLoS ONE 7:e45448. doi: 10.1371/journal.pone.0045448
21. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R., and Kay, S. A. (2003). FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302–306. doi: 10.1038/nature02090
22. Izawa, T., Oikawa, T., Sugiyama, N., Tanisaka, T., Yano, M., and Shimamoto, K. (2002). Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering in rice. Genes Dev. 16, 2006–2020. doi: 10.1101/gad.999202
23. Jang, S., Marchal, V., Panigrahi, K. C., Wenkel, S., Soppe, W., Deng, X. W., et al. (2008). Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J. 27, 1277–1288. doi: 10.1038/emboj.2008.68
24. Jung, J.-H., Seo, Y.-H., Seo, P. J., Reyes, J. L., Yun, J., Chua, N.-H., et al. (2007). The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736–2748. doi: 10.1105/tpc.107.054528
25. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195. doi: 10.1016/S1360-1385(02)02251-3
26. Kim, J.J., Lee, J.H., Kim, W., Jung, H.S., Huijser, P., and Ahn, J.H. (2012). The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol. 159, 461–478. doi: 10.1104/pp.111.192369
27. Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., et al. (2002). Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096–1105. doi: 10.1093/pcp/pcf156
28. Kong, F., Liu, B., Xia, Z., Sato, S., Kim, B.M., Watanabe, S., et al. (2010). Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 154, 1220–1231. doi: 10.1104/pp.110.160796
29. Koornneef, M., Hanhart, C. J., and Van Der Veen, J. H. (1991). A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57–66. doi: 10.1007/BF00264213
30. Kumar, S. V., Lucyshyn, D., Jaeger, K. E., Alos, E., Alvey, E., Harberd, N. P., et al. (2012). Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245. doi: 10.1038/nature 10928
31. Laurie, R.E., Diwadkar, P., Jaudal, M., Zhang, L., Hecht, V., Wen, J., et al. (2011). The Medicago FLOWERING LOCUS T homolog, MtFTa1, is a key regulator of flowering time. Plant Physiol. 156, 2207–2224. doi: 10.1104/pp.111. 180182
32. Ledger, S., Strayer, C., Ashton, F., Kay, S.A., and Putterill, J. (2001). Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J. 26, 15–22. doi: 10.1046/j.1365-313x.2001.01003.x
33. Lee, Y. S., Jeong, D. H., Lee, D. Y., Yi, J., Ryu, C. H., Kim, S. L., et al. (2010). OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J. 63, 18–30. doi: 10.1111/j.1365-313X.2010.04226.x
34. Liew, L. C., Hecht, V., Laurie, R. E., Knowles, C. L., Vander Schoor, J. K., Macknight, R. C., et al. (2009). DIE NEUTRALIS and LATE BLOOMER 1 contribute to regulation of the pea circadian clock. Plant Cell 21, 3198–3211. doi: 10.1105/tpc.109.067223
35. Liew, L. C., Hecht, V., Sussmilch, F. C., and Weller, J. L. (2014). The pea photoperiod response gene STERILE NODES is an ortholog of LUX ARRHYTHMO. Plant Physiol. 165, 648–657. doi: 10.1104/pp.114.237008
36. Liu, B., Kanazawa, A., Matsumura, H., Takahashi, R., Harada, K., and Abe, J. 2008. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180, 995–1007. doi: 10.1534/genet-ics.108.092742
37. Liu, H., Yu, X., Li, K., Klejnot, J., Yang, H., Lisiero, D., et al. 2008. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535–1539. doi: 10.1126/science.1163927
38. Martinez-Trujillo, M., Limones-Briones, V., Cabrera-Ponce, J.L., and Herrera Estrella, L. (2004). Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol. Biol. Rep. 22, 22–30. doi: 10.1007/BF02773350
39. Navarro, C., Abelenda, J. A., Cruz-Oro, E., Cuellar, C. A., Tamaki, S., Silva, J., et al. (2011). Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478, 119–122. doi: 10.1038/nature10431
40. Onouchi, H., Igeno, M.I., Perilleux, C., Graves, K., and Coupland, G. (2000). Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12, 885–900. doi: 10.1105/tpc.12.6.885
41. Putterill, J., Robson, F., Lee, K., Simon, R., and Coupland, G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847–857. doi: 10.1016/0092-8674(95)90288-0
42. Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, M. F., et al. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613–1616. doi: 10.1126/sci-ence.288.5471.1613
43. Song, Y.H., Ito, S., and Imaizumi, T. (2013). Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci. 18, 575–583. doi: 10.1016/j.tplants.2013.05.003
44. Song, Y. H., Smith, R. W., To, B. J., Millar, A. J., and Imaizumi, T. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336, 1045–1049. doi: 10.1126/science.1219644
45. Strayer, C., Oyama, T., Schultz, T.F., Raman, R., and Al, E. (2000). Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771. doi: 10.1126/science.289.5480.768
46. 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. doi: 10.1038/35074138
47. Sun, H., Jia, Z., Cao, D., Jiang, B., Wu, C., Hou, W., et al. (2011). GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PLoS ONE 6:e29238. doi: 10.1371/journal.pone.0029238
48. Tadege, M., Wen, J., He, J., Tu, H., Kwak, Y., Eschstruth, A., et al. (2008). Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 54, 335–347. doi: 10.1111/j.1365-313X.2008.03418.x
49. Thomas, B., and Vince-Prue, D. (1997). Photoperiodism in Plants. London: Academic Press.
50. Tiwari, S. B., Shen, Y., Chang, H. C., Hou, Y., Harris, A., Ma, S. F., et al. (2010). The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57–66. doi: 10.1111/j.1469-8137.2010.03251.x
51. Tsuji, H., Taoka, K., and Shimamoto, K. (2013). Florigen in rice: complex gene network for florigen transcription, florigen activation complex, and multiple functions. Curr. Opin. Plant Biol. 16, 228–235. doi: 10.1016/j.pbi.2013.01.005
52. Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coupland, G. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003–1006. doi: 10.1126/science.1091761
53. Watanabe, S., Hideshima, R., Xia, Z., Tsubokura, Y., Sato, S., Nakamoto, Y., et al. (2009). Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182, 1251–1262. doi: 10.1534/genetics.108.098772
54. Watanabe, S., Xia, Z., Hideshima, R., Tsubokura, Y., Sato, S., Yamanaka, N., et al. (2011). A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics 188, 395–407. doi: 10.1534/genetics.110.125062
55. Weller, J. L., Batge, S. L., Smith, J. J., Kerckhoffs, L. H. J., Sineshchekov, V. A., Murfet, I. C., et al. (2004). A dominant mutation in the pea PHYA gene confers enhanced responses to light and impairs the light-dependent degradation of phytochrome A. Plant Physiol. 135, 2186–2195. doi: 10.1104/pp.103.036103
56. Weller, J. L., Hecht, V., Vander Schoor, J. K., Davidson, S. E., and Ross, J. J. (2009). Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY5 Pathway. Plant Cell 21, 800–813. doi: 10.1105/tpc.108.063628
57. Weller, J. L., Liew, L. C., Hecht, V. F., Rajandran, V., Laurie, R. E., Ridge, S., et al. (2012). A conserved molecular basis for photoperiod adaptation in two temperate legumes. Proc. Natl. Acad. Sci. U.S.A. 109, 21158–21163. doi: 10.1073/pnas.1207943110
58. Wu, F., Price, B.W., Haider, W., Seufferheld, G., Nelson, R., and Hanzawa, Y. (2014). Functional and evolutionary characterization of the CONSTANS gene family in short-day photoperiodic flowering in soybean. PLoS ONE 9:e85754. doi: 10.1371/journal.pone.0085754
59. Xia, Z., Watanabe, S., Yamada, T., Tsubokura, Y., Nakashima, H., Zhai, H., et al. (2012). Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc. Natl. Acad. Sci. U.S.A. 109, E2155–E2164. doi: 10.1073/pnas.1117982109
60. Yamashino, T., Yamawaki, S., Hagui, E., Ueoka-Nakanishi, H., Nakamichi, N., Ito, S., et al. (2013). Clock-controlled and FLOWERING LOCUS T (FT)-dependent photoperiodic pathway in Lotus japonicus I: verification of the flowering-associated function of an FT homolog. Biosci. Biotechnol. Biochem. 77, 747–753. doi: 10.1271/bbb.120871
61. Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., et al. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473–2484. doi: 10.1105/tpc.12.12.2473
62. Zhai, H., Lu, S., Liang, S., Wu, H., Zhang, X., Liu, B., et al. (2014). GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS ONE 9:e89030. doi: 10.1371/jour-nal.pone.0089030