A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering

Genetics

Volumn 188, Issue 2, 2011, Pages 395-407

  Watanabe, Satoshi ^a   Xia, Zhengjun ^a,b   Hideshima, Rumiko ^c   Tsubokura, Yasutaka ^a   Sato, Shusei ^d   Yamanaka, Naoki ^e   Takahashi, Ryoji ^f   Anai, Toyoaki ^c   Tabata, Satoshi ^d   Kitamura, Keisuke ^g   Harada, Kyuya ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b NORTHEAST INSTITUTE OF GEOGRAPHY AND AGRICULTURAL ECOLOGY   (China)

^c SAGA UNIVERSITY   (Japan)

^d KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^e JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

^f NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

^g HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GIGANTEA PROTEIN; GMFT2A PROTEIN; GMGLA PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ALLELE; ARTICLE; CONTROLLED STUDY; EXON; FLOWERING; GENE EXPRESSION; GENE ISOLATION; GENE MAPPING; GENETIC LINE; GENOTYPE; HETEROZYGOSITY; JAPAN; LATITUDE; MOLECULAR CLONING; NEAR ISOGENIC LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT DEVELOPMENT; PRIORITY JOURNAL; PROGENY; QUANTITATIVE TRAIT LOCUS; RECOMBINANT INBRED STRAIN; RESIDUAL HETEROZYGOUS LINE; SOYBEAN; STOP CODON;

ACCLIMATIZATION; ALTITUDE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CLONING, MOLECULAR; DNA, PLANT; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HETEROZYGOTE; LOD SCORE; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SOYBEAN PROTEINS; SOYBEANS; TIME FACTORS;

GLYCINE MAX;

EID: 79958225100     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.125062     Document Type: Article

References (90)

1. Abe, J., D. Xu, A. Miyano, K. Komatsu, A. Kanazawa et al., 2003 Photoperiod-insensitive Japanese soybean landraces differ at two maturity loci. Crop Sci. 43: 1300-1304.
2. Abe, M., Y. Kobayashi, S. Yamamoto, Y. Daimon, A. Yamaguchi et al., 2005 FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
3. Adams, K. L., and J. F. Wendel, 2005 Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8: 135-141.
4. Araki, T., and Y. Komeda, 1993 Analysis of the role of the lateflowering locus, GI, in the flowering of Arabidopsis thaliana. Plant J. 3: 231-239.
5. Bernard, R. L., 1971 Two major genes for time of flowering and maturity in soybeans. Crop Sci. 11: 242-244.
6. Bonato, E. R., and N. A. Vello, 1999 E6, a dominant gene conditioning early flowering and maturity in soybeans. Genet. Mol. Biol. 22: 229-232.
7. Buzzell, R. I., 1971 Inheritance of a soybean flowering response to fluorescent-daylength conditions. Can. J. Genet. Cytol. 13: 703-707.
8. Buzzell, R. I., and H. D. Voldeng, 1980 Inheritance of insensitivity to long day length. Soybean Genet. Newsl. 7: 26-29.
9. Cao, S., M. Ye and S. Jiang, 2005 Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep. 24: 683-690.
10. Cao, S., S. Jiang and R. Zhang, 2006 The role of GIGANTEA gene in mediating the oxidative stress response and in Arabidopsis. Plant Growth Regul. 48: 261-270.
11. Carmona, M. J., M. Calonje and J. M. Martinez-Zapater 2007 The FT/TFL1 gene family in grapevine. Plant Mol. Biol. 63: 637-650.
12. Cober, E. R., and H. D. Voldeng, 2001 A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Sci. 41: 698-701.
13. Cober, E. R., J. W. Tanner and H. D. Voldeng, 1996 Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Sci. 36: 606-610.
14. Cober, E. R., S. J. Molnar, M. Charette and H. D. Voldeng, 2010 A new locus for early maturity in soybean. Crop Sci. 50: 524-527.
15. Cregan, P. B., T. Jarvik, A. L. Bush, R. C. Shoemaker, K. G. Lark et al., 1999 An integrated genetic linkage map of the soybean genome. Crop Sci. 39: 1464-1490.
16. Doi, K., T. Izawa, T. Fuse, U. Yamanouchi, T. Kubo et al., 2004 Ehd1, a B-type response regulator in rice, confers shortday promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18: 926-936.
17. Dubcovsky, J., and J. Dvorak, 2007 Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316: 1862-1866.
18. Dunford, R. P., S. Griffiths, V. Christodoulou and D. A. Laurie, 2005 Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor. Appl. Genet. 110: 925-931.
19. Ehrenreich, I. M., Y. Hanzawa, L. Chou, J. L. Roe, P. X. Kover et al., 2009 Candidate gene association mapping of Arabidopsis flowering time. Genetics 183: 325-335.
20. Eimert, K., S.-M. Wang, W. Lue and J. Chen, 1995 Monogenic recessive mutation causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7: 1703-1712.
21. Fehr, W. R., C. E. Caviness, D. T. Burmood and J. S. Pennington, 1971 Stage of development descriptions for soybeans, Glycine Max (L.) Merrill. Crop Sci. 11: 929-931.
22. Fowler, S., K. Lee, H. Onouchi, A. Samach, K. Richardson et al., 1999 GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18: 4679-4688.
23. Hayama, R., S. Yokoi, S. Tamaki, M. Yano and K. Shimamoto, 2003 Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422: 719-722.
24. Hayashi, M., A. Miyahara, S. Sato, T. Kato, M. Yoshikawa et al., 2001 Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res. 8: 301-310.
25. Hecht, V., F. Foucher, C. Ferrandiz, R. MacKnight, C. Navarro et al., 2005 Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137: 1420-1434.
26. Hecht, V., C. L. Knowles, J. K. Vander Schoor, L. C. Liew, S. E. Jones 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.
27. Hong, S. Y., S. Lee, P. J. Seo, M. S. Yang and C. M. Park, 2010 Identification and molecular characterization of a Brachypodium distachyon GIGANTEA gene: functional conservation in monocot and dicot plants. Plant Mol. Biol. 72: 485-497.
28. Huq, E., J. M. Tepperman and P. H. Quail, 2000 GIGANTEA is a nuclear protein involved in phytochrome siwgnaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97: 9789-9794.
29. Imaizumi, T., H. G. Tran, T. E. Swartz, W. R. Briggs and S. A. Kay, 2003 FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426: 302-306.
30. Imaizumi, T., T. F. Schultz, F. G. Harmon, L. A. Ho and S. A. Kay, 2005 FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297.
31. Jaillon, O., J. M. Aury, B. Noel, A. Policriti, C. Clepet et al., 2007 The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
32. Jung, C., and A. E. Muller, 2009 Flowering time control and applications in plant breeding. Trends Plant Sci. 14: 563-573.
33. Jung, J. H., Y. H. Seo, P. J. Seo, J. L. Reyes, J. Yun et al., 2007 The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19: 2736-2748.
34. Kanazawa, A., B. Liu, F. Kong, S. Arase and J. Abe, 2009 Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J. Mol. Evol. 69: 164-175.
35. Kojima, S., Y. Takahashi, Y. Kobayashi, L. Monna, T. Sasaki 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.
36. Kong, F., B. Liu, Z. Xia, S. Sato, B. M. Kim 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.
37. Koornneef, M., C. Alonso-Blanco, H. Blankestijn-de Vries, C. J. Hanhart and A. J. Peeters, 1998 Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148: 885-892.
38. Kover, P. X., W. Valdar, J. Trakalo, N. Scarcelli, I.M. Ehrenreich et al., 2009 A multiparent advanced generation inter-cross to finemap quantitative traits in Arabidopsis thaliana. PLoS Genet. 5: e1000551.
39. Kumar, S., M. Nei, J. Dudley and K. Tamura, 2008 MEGA: a biologistcentric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 9: 299-306.
40. Kurepa, J., J. Smalle, M. V. Montagu and D. Inze, 1998 Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering gigantea is tolerant to paraquat. Plant J. 14: 759-764.
41. Lifschitz, E., T. Eviatar, A. Rozman, A. Shalit, A. Goldshmidt et al., 2006 The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA 103: 6398-6403.
42. Lin, M. K., H. Belanger, Y. J. Lee, E. Varkonyi-Gasic, K. Taoka et al., 2007 FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19: 1488-1506.
43. Liu, B., A. Kanazawa, H. Matsumura, R. Takahashi, K. Harada et al., 2008 Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180: 995-1007.
44. Liu, L. J., Y. C. Zhang, Q. H. Li, Y. Sang, J. Mao et al., 2008 COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20: 292-306.
45. Martin-Tryon, E. L., J.A. Kreps and S. L. Harmer, 2007 GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol. 143: 473-486.
46. McBlain, B. A., and R. L. Bernard, 1987 A new gene affecting the time of flowering and maturity in soybean. J. Hered. 78: 160-162.
47. McBlain, B. A., R. L. Bernard, C. R. Cremeens and J. F. Korczak, 1987 A procedure to identify genes affecting maturity using soybean isoline testers. Crop Sci. 27: 1127-1132.
48. McCallum, C. M., L. Comai, E. A. Greene and S. Heinkoff, 2000 Targeting induced local lesions in genomes (TILLING) for plant functional genomics. Plant Physiol. 123: 436-442.
49. Meksem, K., T. W. Doubler, K. Chancharoenchai, N. Nijti S. J. Chang et al. 1999 Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor. Appl. Genet. 99: 1131-1142.
50. Mizoguchi, T., L. Wright, S. Fujiwara, F. Cremer, K. Lee et al., 2005 Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17: 2255-2270.
51. Molnar, S. J., S. Rai, M. Charette and E. R. Cober, 2003 Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome 46: 1024-1036.
52. Murray, M. G., and W. F. Thompson, 1980 Rapid isolation of highmolecular-weight plant DNA. Nucleic Acids Res. 8: 4321-4325.
53. Nelson, D. C., J. Lasswell, L. E. Rogg, M. A. Cohen and B. Bartel, 2000 FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101: 331-340.
54. Nemoto, Y., M. Kisaka, T. Fuse, M. Yano and Y. Ogihara, 2003 Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J. 36: 82-93.
55. Njiti, V. N., T. W. Doubler, R. J. Suttner, L. E. Gray, P. T. Gibson et al., 1998 Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycine in near-isogenic lines. Crop Sci. 38: 472-477.
56. Ohyanagi, H., T. Tanaka, H. Sakai, Y. Shigemoto, K. Yamaguchi et al., 2006 The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information. Nucleic Acids Res. 34: D741-D744.
57. Oliverio, K. A., M. Crepy, E. L. Martin-Tryon, R. Milich, S.L. Harmer et al., 2007 GIGANTEA regulates phytochrome A-mediated photomorphogenesis independently of its role in the circadian clock. Plant Physiol. 144: 495-502.
58. Paltiel, P., R. Amin, A. Gover, N. Ori and A. Samach, 2006 Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta 224: 1255-1268.
59. Redei, G. P., 1962 Supervital mutants of Arabidopsis. Genetics 47:443-460.
60. Rozen, S., and H. J. Skaletsky, 2000 Primer3 on the WWW for general users and for biologist programmers, pp. 365-386 in Bioinformatics Methods and Protocols: Methods in Molecular Biology, edited by S. Krawetz. and S Misener. Humana Press, Totowa, NJ.
61. Saidon, G., W. D. Beversdorf and H. D. Voldeng, 1989 Adjusting of the soybean phenology using the E4 loci. Crop Sci. 29: 1361-1365.
62. Samach, A., H. Onouchi, S. E. Gold, G. S. Ditta, Z. Schwarz-Sommer et al., 2000 Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616.
63. Sato, S., T. Kaneko, Y. Nakamura, E. Asamizu, T. Kato et al., 2001 Structural analysis of a Lotus japonicus genome. I. Sequence features and mapping of fifty-six TAC clones which cover the 5.4 mb regions of the genome. DNA Res. 8: 311-318.
64. Sawa, M., D. A. Nusinow, S. A. Kay and T. Imaizumi, 2007 FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318: 261-265.
65. Schlueter, J. A., P. Dixon, C. Granger, D. Grant, L. Clark et al., 2004 Mining EST databases to resolve evolutionary events in major crop species. Genome 47: 868-876.
66. Schmutz, J., S. B. Cannon, J. Schlueter, J. Ma, T. Mitros et al., 2010 Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
67. Serikawa, M., K. Miwa, T. Kondo and T. Oyama, 2008 Functional conservation of clock-related genes in flowering plants: overexpression and RNA interference analyses of the circadian rhythm in the monocotyledon Lemna gibba. Plant Physiol. 146: 1952-1963.
68. Shoemaker, R. C., K. Polzin, J. Labate, J. Specht, E. C. Brummer et al., 1996 Genome duplication in soybean (Glycine subgenus soja). Genetics 144: 329-338.
69. Suarez-Lopez, P., K. Wheatley, F. Robson, H. Onouchi, F. Valverde et al., 2001 CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120.
70. Tasma, I. M., and R. C. Shoemaker, 2003 Mapping flowering time gene homologs in soybean and their association with maturity (E) loci. Crop Sci. 43: 319-328.
71. Taylor, A., A. J. Massiah and B. Thomas, 2010 Conservation of Arabidopsis thaliana photoperiodic flowering time genes in onion (Allium cepa L.). Plant Cell Physiol. 51: 1638-1647.
72. Thakare, D., S. Kumudini and R. D. Dinkins, 2010 Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231: 951-963.
73. Triwitayakorn, K., V. N. Njiti, M. J. Iqbal, S. Yaegashi, C. Town et al., 2005 Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome 48: 125-138.
74. Tsubokura, Y., R. Onda, S. Sato, Z. Xia, M. Hayashi et al., 2008 Characterization of soybean genome based on synteny analysis with Lotus japonicus. Breed. Sci. 58: 157-167.
75. Tsuchiya, T., N. Kameya and I. Nakamura, 2009 Straight walk: a modified method of ligation-mediated genome walking for plant species with large genomes. Anal. Biochem. 388: 158-160.
76. Tuinstra, M. R., G. Ejeta and P. B. Goldsbrough, 1997 Heterogeneous inbred family (HIF) analysis: a method for developing nearisogenic lines that differ at quantitative traits loci. Theor. Appl. Genet. 95: 1005-1011.
77. Valverde, F., A. Mouradov, W. Soppe, D. Ravenscroft, A. Samach et al., 2004 Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003-1006.
78. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee et al., 1995 AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407-4414.
79. Watanabe, S., T. Tadjuddin, N. Yamanaka, M. Hayashi and K. Harada, 2004 Analysis of QTLs for reproductive development and seed quality traits in soybean using recombinant inbred lines. Breed. Sci. 54: 399-407.
80. Watanabe, S., R. Hideshima, Z. Xia, Y. Tsubokura, S. Sato et al., 2009 Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182: 1251-1262.
81. Xia, Z., H. Sato, S. Watanabe, S. Kawasaki and K. Harada, 2005 Construction and characterization of a BAC library of soybean. Euphytica 141: 129-137.
82. Xue, W., Y. Xing, X. Weng, Y. Zhao, W. Tang et al., 2008 Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40: 761-767.
83. Yamanaka, N., Y. Nagamura, Y. Tsubokura, K. Yamamoto, R. Takahashi et al., 2000 Quantitative trait locus analysis of flowering time in soybean using a RFLP linkage map. Breed. Sci. 50: 109-115.
84. Yamanaka, N., S. Ninomiya, M. Hoshi, Y. Tsubokura, M. Yano et al., 2001 An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. DNA Res. 8: 61-72.
85. Yamanaka, N., S. Watanabe, K. Toda, M. Hayashi, H. Fuchigami et al., 2004 Fine mapping of FT1 locus for soybean flowering time, using a residual heterozygous line derived from a recombinant inbred line. Theor. Appl. Genet. 110: 634-639.
86. Yan, L., D. Fu, C. Li, A. Blechl, G. Tranquilli et al., 2006 The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. USA 103: 19581-19586.
87. Yang, B., X. Wen, N. S. Kodali, C. A. Oleykowski, C. G. Miller et al., 2000 Purification, cloning, and characterization of the CEL I nuclease. Biochemistry 39: 3533-3541.
88. Yano, M., Y. Katayose, M. Ashikari, U. Yamanouchi, L. Monna 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.
89. Yanovsky, M. J., and S. A. Kay, 2002 Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308-312.
90. Zhao, X. Y., M. S. Liu, J. R. Li, C. M. Guan and X. S. Zhang, 2005 The wheat TaGI1, involved in photoperiodic flowering, encodes an Arabidopsis GI ortholog. Plant Mol. Biol. 58: 53-64.