Conserved CO-FT regulons contribute to the photoperiod flowering control in soybean

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Fan, Chengming ^a,b   Hu, Ruibo ^c   Zhang, Xiaomei ^a   Wang, Xu ^a   Zhang, Wenjing ^a   Zhang, Qingzhe ^a   Ma, Jinhua ^a   Fu, Yong Fu ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^c QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

Author keywords

CONSTANS; FLOWERING LOCUS T; Functional divergence; Ortholog; Paralog; Soybean

Indexed keywords

ARABIDOPSIS; GLYCINE MAX; MAGNOLIOPHYTA;

VEGETABLE PROTEIN;

ARTICLE; CIRCADIAN RHYTHM; FLOWER; GENE DUPLICATION; GENETICS; METABOLISM; PHOTOPERIODICITY; PHYLOGENY; PHYSIOLOGY; SOYBEAN;

CIRCADIAN RHYTHM; FLOWERS; GENE DUPLICATION; PHOTOPERIOD; PHYLOGENY; PLANT PROTEINS; SOYBEANS;

EID: 84892166764     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-9     Document Type: Article

References (82)

1. Reeves PH, Coupland G. Response of plant development to environment: control of flowering by daylength and temperature. Curr Opin Plant Biol 2000, 3(1):37-42. 10.1016/S1369-5266(99)00041-2, 10679453.
2. Valverde F. CONSTANS and the evolutionary origin of photoperiodic timing of flowering. J Exper Botany 2011, 62(8):2453-2463.
3. Turck F, Fornara F, Coupland G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Ann Rev Plant Biol 2008, 59:573-594.
4. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 2001, 410(6832):1116-1120. 10.1038/35074138, 11323677.
5. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 2004, 303(5660):1003-1006. 10.1126/science.1091761, 14963328.
6. Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. The EMBO journal 2008, 27(8):1277-1288. 10.1038/emboj.2008.68, 2291449, 18388858.
7. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes & Dev 2002, 16(15):2006-2020. 10.1101/gad.999202, 186415, 12154129.
8. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 2003, 422(6933):719-722. 10.1038/nature01549, 12700762.
9. Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 2006, 312(5776):1040-1043. 10.1126/science.1126038, 16675663.
10. Greenup A, Peacock WJ, Dennis ES, Trevaskis B. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot (Lond) 2009, 103(8):1165-1172.
11. Nemoto Y, Kisaka M, Fuse T, Yano M, Ogihara Y. Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J 2003, 36(1):82-93. 10.1046/j.1365-313X.2003.01859.x, 12974813.
12. Martin J, Storgaard M, Andersen CH, Nielsen KK. Photoperiodic regulation of flowering in perennial ryegrass involving a CONSTANS -like homolog. Plant Mol Biol 2004, 56(2):159-169. 10.1007/s11103-004-2647-z, 15604735.
13. Lagercrantz U, Axelsson T. Rapid evolution of the family of CONSTANS LIKE genes in plants. Mol Biol Evol 2000, 17(10):1499-1507. 10.1093/oxfordjournals.molbev.a026249, 11018156.
14. Putterill J, Robson F, Lee K, Simon R, Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 1995, 80(6):847-857. 10.1016/0092-8674(95)90288-0, 7697715.
15. Griffiths S, Dunford RP, Coupland G, Laurie DA. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 2003, 131(4):1855-1867. 10.1104/pp.102.016188, 166942, 12692345.
16. Serrano G, Herrera-Palau R, Romero JM, Serrano A, Coupland G, Valverde F. Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr Biol 2009, 19(5):359-368. 10.1016/j.cub.2009.01.044, 19230666.
17. Klug A, Schwabe JW. Protein motifs 5. Zinc fingers. FASEB J 1995, 9(8):597-604.
18. Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, Wu SH. The Arabidopsis B-box zinc finger family. Plant Cell 2009, 21(11):3416-3420. 10.1105/tpc.109.069088, 2798317, 19920209.
19. Robert LS, Robson F, Sharpe A, Lydiate D, Coupland G. Conserved structure and function of the Arabidopsis flowering time gene CONSTANS in Brassica napus. Plant Mol Biol 1998, 37(5):763-772. 10.1023/A:1006064514311, 9678571.
20. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 2000, 12(12):2473-2484. 102231, 11148291.
21. Liu J, Yu J, McIntosh L, Kende H, Zeevaart JA. Isolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering. Plant Physiol 2001, 125(4):1821-1830. 10.1104/pp.125.4.1821, 88838, 11299362.
22. Guo JL, Yang Q, Liang F, Xing YJ, Wang Z. Molecular cloning and expression analysis of a novel CONSTANS-like gene from potato. Biochem Biokhimiia 2007, 72(11):1241-1246.
23. Almada R, Cabrera N, Casaretto JA, Ruiz-Lara S, Gonzalez Villanueva E. VvCO and VvCOL1, two CONSTANS homologous genes, are regulated during flower induction and dormancy in grapevine buds. Plant Cell Reports 2009, 28(8):1193-1203. 10.1007/s00299-009-0720-4, 19495771.
24. Hsu CY, Adams JP, No K, Liang H, Meilan R, Pechanova O, Barakat A, Carlson JE, Page GP, Yuceer C. Overexpression of CONSTANS homologs CO1 and CO2 fails to alter normal reproductive onset and fall bud set in woody perennial poplar. PloS one 2012, 7(9):e45448. 10.1371/journal.pone.0045448, 3446887, 23029015.
25. Chia TY, Muller A, Jung C, Mutasa-Gottgens ES. Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus. J Exper Botany 2008, 59(10):2735-2748.
26. Granovsky AE, Rosner MR. Raf kinase inhibitory protein: a signal transduction modulator and metastasis suppressor. Cell Res 2008, 18(4):452-457. 10.1038/cr.2008.43, 18379591.
27. Chardon F, Damerval C. Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 2005, 61(5):579-590. 10.1007/s00239-004-0179-4, 16170456.
28. Hedman H, Kallman T, Lagercrantz U. Early evolution of the MFT-like gene family in plants. Plant Mol Biol 2009, 70(4):359-369. 10.1007/s11103-009-9478-x, 19288213.
29. Xi W, Liu C, Hou X, Yu H. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 2010, 22(6):1733-1748. 10.1105/tpc.109.073072, 2910974, 20551347.
30. Karlgren A, Gyllenstrand N, Kallman T, Sundstrom JF, Moore D, Lascoux M, Lagercrantz U. Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 2011, 156(4):1967-1977. 10.1104/pp.111.176206, 3149940, 21642442.
31. Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, et al. A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 2011, 23(9):3215-3229. 10.1105/tpc.111.088492, 3203438, 21896881.
32. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E. Control of inflorescence architecture in Antirrhinum. Nature 1996, 379(6568):791-797. 10.1038/379791a0, 8587601.
33. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E. Inflorescence commitment and architecture in Arabidopsis. Science 1997, 275(5296):80-83. 10.1126/science.275.5296.80, 8974397.
34. Pin PA, Nilsson O. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, Cell Environ 2012, 35(10):1742-1755. 10.1111/j.1365-3040.2012.02558.x, 22697796.
35. Wigge PA. FT, a mobile developmental signal in plants. Curr Biol 2011, 21(9):R374-R378. 10.1016/j.cub.2011.03.038, 21549960.
36. Amasino R. Seasonal and developmental timing of flowering. Plant J 2010, 61(6):1001-1013. 10.1111/j.1365-313X.2010.04148.x, 20409274.
37. Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 2006, 25(3):605-614. 10.1038/sj.emboj.7600950, 1383534, 16424903.
38. Hanzawa Y, Money T, Bradley D. A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 2005, 102(21):7748-7753. 10.1073/pnas.0500932102, 1140427, 15894619.
39. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Sci 2010, 330(6009):1397-1400.
40. Flagel LE, Wendel JF. Gene duplication and evolutionary novelty in plants. New Phytolog 2009, 183(3):557-564.
41. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463(7278):178-183. 10.1038/nature08670, 20075913.
42. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA. The fate of duplicated genes in a polyploid plant genome. Plant J 2013, 73(1):143-153.
43. Fan C, Wang X, Hu R, Wang Y, Xiao C, Jiang Y, Zhang X, Zheng C, Fu YF. The pattern of Phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biol 2013, 13:48. 10.1186/1471-2229-13-48, 3621523, 23510338.
44. Shimizu M, Ichikawa K, Aoki S. Photoperiod-regulated expression of the PpCOL1 gene encoding a homolog of CO/COL proteins in the moss Physcomitrella patens. Biochem Biophys Res Commun 2004, 324(4):1296-1301. 10.1016/j.bbrc.2004.09.194, 15504355.
45. Holefors A, Opseth L, Ree Rosnes AK, Ripel L, Snipen L, Fossdal CG, Olsen JE. Identification of PaCOL1 and PaCOL2, two CONSTANS-like genes showing decreased transcript levels preceding short day induced growth cessation in Norway spruce. Plant Physiol Biochem 2009, 47(2):105-115. 10.1016/j.plaphy.2008.11.003, 19097801.
46. Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE. Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc Natl Acad Sci USA 2011, 108(50):20236-20241. 10.1073/pnas.1116325108, 3250134, 22128331.
47. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D. Activation tagging of the floral inducer FT. Science 1999, 286(5446):1962-1965. 10.1126/science.286.5446.1962, 10583961.
48. Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 2006, 103(16):6398-6403. 10.1073/pnas.0601620103, 1458889, 16606827.
49. Itoh H, Nonoue Y, Yano M, Izawa T. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nature Gen 2010, 42(7):635-638.
50. Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, et al. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 2011, 108(26):10756-10761. 10.1073/pnas.1104713108, 3127867, 21653885.
51. Lazakis CM, Coneva V, Colasanti J. ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J Exper Botany 2011, 62(14):4833-4842.
52. Meng X, Muszynski MG, Danilevskaya ON. The FT-like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize. Plant Cell 2011, 23(3):942-960. 10.1105/tpc.110.081406, 3082274, 21441432.
53. Oda A, Narumi T, Li T, Kando T, Higuchi Y, Sumitomo K, Fukai S, Hisamatsu T. CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums. J Exper Botany 2012, 63(3):1461-1477.
54. Xu F, Rong X, Huang X, Cheng S. Recent advances of flowering locus T gene in higher plants. Int J Mol Sci 2012, 13(3):3773-3781. 3317742, 22489182.
55. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. A pair of related genes with antagonistic roles in mediating flowering signals. Science 1999, 286(5446):1960-1962. 10.1126/science.286.5446.1960, 10583960.
56. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T. TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 2005, 46(8):1175-1189. 10.1093/pcp/pci151, 15951566.
57. Ballerini ES, Kramer EM. In the light of evolution: a re-evaluation of conservation in the CO-FT regulon and its role in photoperiodic regulation of flowering time. Frontiers Plant Sci 2011, 2:81.
58. Jung CH, Wong CE, Singh MB, Bhalla PL. Comparative genomic analysis of soybean flowering genes. PloS one 2012, 7(6):e38250. 10.1371/journal.pone.0038250, 3367986, 22679494.
59. Kong F, Liu B, Xia Z, Sato S, Kim BM, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, et al. Two co-ordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol 2010, 154(3):1220-1231. 10.1104/pp.110.160796, 2971601, 20864544.
60. Sun H, Jia Z, Cao D, Jiang B, Wu C, Hou W, Liu Y, Fei Z, Zhao D, Han T. GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PloS one 2011, 6(12):e29238. 10.1371/journal.pone.0029238, 3237611, 22195028.
61. D'Aloia M, Bonhomme D, Bouche F, Tamseddak K, Ormenese S, Torti S, Coupland G, Perilleux C. Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 2011, 65(6):972-979. 10.1111/j.1365-313X.2011.04482.x, 21205031.
62. Jang S, Torti S, Coupland G. Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 2009, 60(4):614-625. 10.1111/j.1365-313X.2009.03986.x, 19656342.
63. Yoo SJ, Hong SM, Jung HS, Ahn JH. The cotyledons produce sufficient FT protein to induce flowering: evidence from cotyledon micro grafting in Arabidopsis. Plant Cell Physiol 2013, 54(1):119-128. 10.1093/pcp/pcs158, 23204014.
64. Liu H, Wang H, Gao P, Xü J, Xü T, Wang J, Wang B, Lin C, Fu Y-F. Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). J Plant Physiol 2009, 166(3):278-289. 10.1016/j.jplph.2008.06.003, 18707796.
65. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 2002, 43(10):1096-1105. 10.1093/pcp/pcf156, 12407188.
66. Yamashino T, Yamawaki S, Hagui E, Ueoka-Nakanishi H, Nakamichi N, Ito S, Mizuno T. 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 2013, 77(4):747-753.
67. Ledger S, Strayer C, Ashton F, Kay SA, Putterill J. Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 2001, 26(1):15-22. 10.1046/j.1365-313x.2001.01003.x, 11359606.
68. Datta S, Hettiarachchi GH, Deng XW, Holm M. Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. Plant Cell 2006, 18(1):70-84. 10.1105/tpc.105.038182, 1323485, 16339850.
69. Hassidim M, Harir Y, Yakir E, Kron I, Green RM. Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta 2009, 230(3):481-491. 10.1007/s00425-009-0958-7, 19504268.
70. Cheng XF, Wang ZY. Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 2005, 43(5):758-768. 10.1111/j.1365-313X.2005.02491.x, 16115071.
71. Hayama R, Agashe B, Luley E, King R, Coupland G. A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 2007, 19(10):2988-3000. 10.1105/tpc.107.052480, 2174708, 17965272.
72. Purwestri YA, Ogaki Y, Tamaki S, Tsuji H, Shimamoto K. The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant Ccell Physiol 2009, 50(3):429-438.
73. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 2007, 316(5827):1030-1033. 10.1126/science.1141752, 17446353.
74. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39(Web Server issue):W29-W37. 3125773, 21593126.
75. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
76. Severin AJ, Cannon SB, Graham MM, Grant D, Shoemaker RC. Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. Plant Cell 2011, 23(9):3129-3136. 10.1105/tpc.111.089573, 3203428, 21917551.
77. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 2012, 40(7):e49. 10.1093/nar/gkr1293, 3326336, 22217600.
78. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19(9):1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.
79. Chen QJ, Zhou HM, Chen J, Wang XC. Using a modified TA cloning method to create entry clones. Anal Biochem 2006, 358(1):120-125. 10.1016/j.ab.2006.08.015, 16970900.
80. Hu R, Fan C, Li H, Zhang Q, Fu Y-F. Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Mol Biol 2009, 10(1):93. 10.1186/1471-2199-10-93, 2761916, 19785741.
81. Zhang X, Henriques R, Lin SS, Niu QW, Chua NH. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature protocols 2006, 1(2):641-646. 10.1038/nprot.2006.97, 17406292.
82. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998, 16(6):735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.