Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 32, 2012, Pages

  Xia, Zhengjun ^a,b   Watanabe, Satoshi ^b   Yamada, Tetsuya ^c   Tsubokura, Yasutaka ^b   Nakashima, Hiroko ^d   Zhai, Hong ^a   Anai, Toyoaki ^d   Sato, Shusei ^e   Yamazaki, Toshimasa ^b   Lü, Shixiang ^a   Wu, Hongyan ^a   Tabata, Satoshi ^e   Harada, Kyuya ^b  

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

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d SAGA UNIVERSITY   (Japan)

^e KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Photoperiodic insensibility; Photoperiodism; Quantitative trait locus

Indexed keywords

GLYCOPROTEIN E1; MESYLIC ACID ETHYL ESTER;

ALLELE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FLOWERING; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; INTRON; MOLECULAR CLONING; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOPERIODICITY; PRIORITY JOURNAL; SOYBEAN; STOP CODON; TRANSCRIPTION REGULATION; TRANSGENIC PLANT;

BASE SEQUENCE; BLOTTING, SOUTHERN; CHROMOSOME MAPPING; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CLONING, MOLECULAR; CLUSTER ANALYSIS; DNA PRIMERS; ETHYL METHANESULFONATE; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC LOCI; GENETIC VARIATION; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOTOPERIOD; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SOYBEANS;

GLYCINE MAX;

EID: 84864393863     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1117982109     Document Type: Article

References (78)

1. Jung C, Müller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563-573.
2. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001-1013.
3. Garner WW, Allard HA (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res 18:553-606.
4. Samach A, et al. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613-1616. (Pubitemid 30387421)
5. Robson F, et al. (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619-631. (Pubitemid 34107863)
6. Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091-3097.
7. Tsuji H, Taoka K, 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.
8. Corbesier L, et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030-1033. (Pubitemid 46799490)
9. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050-1054. (Pubitemid 46899530)
10. Mathieu J,Warthmann N, Küttner F, SchmidM (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055-1060. (Pubitemid 46899531)
11. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033-1036. (Pubitemid 46799491)
12. Notaguchi M, et al. (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol 49:1645-1658.
13. Ben-Naim O, et al. (2006) The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J 46:462-476.
14. Hayama R, Agashe B, Luley E, King R, Coupland G (2007) A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988-3000. (Pubitemid 350276707)
15. Liu JY, Yu JP, McIntosh L, Kende H, Zeevaart JAD (2001) Isolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering. Plant Physiol 125:1821-1830. (Pubitemid 32375765)
16. Lifschitz E, 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.
17. Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol 135:677-684. (Pubitemid 38819013)
18. Owen FV (1927) Inheritance studies in soybeans. II. Glabrousness, color of pubescence, time of maturity, and linkage relations. Genetics 12:519-529.
19. Bernard RL (1971) Two major genes for time of flowering and maturity in soybeans. Crop Sci 11:242-244.
20. Abe J, et al. (2003) Photoperiod-insensitive Japanese soybean landraces differ at two maturity loci. Crop Sci 43:1300-1304. (Pubitemid 36774858)
21. Buzzell RI (1971) Inheritance of a soybean flowering response to fluorescent-daylength conditions. Can J Genet Cytol 13:703-707.
22. Buzzell RI, Voldeng HD (1980) Inheritance of insensitivity to long day length. Soybean Genet Newsl 7:26-29.
23. McBlain BA, Bernard RL, Cremeens CR, Korczak JF (1987) A procedure to identify genes affecting maturity using soybean isoline testers. Crop Sci 27:1127-1132.
24. Saindon G, Beversdorf WD, Voldeng HD (1989) Adjustment of the soybean phenology using the E4 locus. Crop Sci 29:1361-1365.
25. Bonato ER, Vello NA (1999) E6 a dominant gene conditioning early flowering and maturity in soybeans. Genet Mol Biol 22:229-232. (Pubitemid 29368816)
26. Cober ER, Voldeng HD (2001) A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Sci 41:698-701. (Pubitemid 32595937)
27. Cober ER, Molnar SJ, Charette M, Voldeng HD (2010) A new locus for early maturity in soybean. Crop Sci 50:524-527.
28. Ray JD, Hinson K, Mankono EB, Malo FM (1995) Genetic control of a long-juvenile trait in soybean. Crop Sci 35:1001-1006.
29. Cober ER, Tanner JW, Voldeng HD (1996a) Genetic control of photoperiod response in early-maturing near-isogenic soybean lines. Crop Sci 36:601-605.
30. Cober ER, Tanner JW, Voldeng HD (1996b) Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Sci 36:606-610. (Pubitemid 26324182)
31. Watanabe S, et al. (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251-1262.
32. Liu B, et al. (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180:995-1007.
33. Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11-24.
34. Watanabe S, 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.
35. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci USA 97:9789-9794. (Pubitemid 30650854)
36. Tasma IM, Shoemaker RC (2003) Mapping flowering time gene homologs in soybean and their association with maturity (E) loci. Crop Sci 43:319-328. (Pubitemid 36108223)
37. Hecht V, et al. (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420-1434. (Pubitemid 43119339)
38. Kong FJ, et al. (2010) Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodicflowering in soybean. Plant Physiol 154:1220-1231.
39. Thakare D, Kumudini S, Dinkins RD (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231:951-963.
40. Thakare D, Kumudini S, Dinkins RD (2011) The alleles at the E1 locus impact the expression pattern of two soybean FT-like genes shown to induce flowering in Arabidopsis. Planta 234:933-943.
41. Yamanaka N, et al. (2005) Fine mapping of the FT1 locus for soybean flowering time using a residual heterozygous line derived from a recombinant inbred line. Theor Appl Genet 110:634-639. (Pubitemid 40383380)
42. Schmutz J, et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178-183.
43. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929-931.
44. Sakata K, et al. (2002) RiceGAAS: An automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98-102. (Pubitemid 34679515)
45. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78-94. (Pubitemid 27192680)
46. Lukashin AV, Borodovsky M (1998) GeneMark.hmm: New solutions for gene finding. Nucleic Acids Res 26:1107-1115. (Pubitemid 28291669)
47. Liu BH, Abe J (2010) QTL mapping for photoperiod insensitivity of a Japanese soybean landrace Sakamotowase. J Hered 101:251-256.
48. McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeting induced local lesions IN genomes (TILLING) for plant functional genomics. Plant Physiol 123:439-442. (Pubitemid 30411129)
49. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: A unified platform for automated protein structure and function prediction. Nat Protoc 5:725-738.
50. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat Protoc 4:363-371.
51. Yamasaki K, et al. (2004) Solution structure of the B3 DNA binding domain of the Arabidopsis cold-responsive transcription factor RAV1. Plant Cell 16:3448-3459. (Pubitemid 41096018)
52. Swaminathan K, Peterson K, Jack T (2008) The plant B3 superfamily. Trends Plant Sci 13:647-655.
53. Robbins J, Dilworth SM, Laskey RA, Dingwall C (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:615-623. (Pubitemid 121002977)
54. Raikhel N (1992) Nuclear targeting in plants. Plant Physiol 100:1627-1632.
55. Wong CE, Singh MB, Bhalla PL (2009) Molecular processes underlying the floral transition in the soybean shoot apical meristem. Plant J 57:832-845.
56. Libault M, et al. (2010) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 63:86-99.
57. Liu H, et al. (2009) Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). J Plant Physiol 166:278-289.
58. Sato H, Yamada T, Kita Y, Ishimoto M, Kitamura K (2007) Production of transgenic plants and their early seed set in Japanese soybean variety, Kariyutaka. Plant Biotechnol 24:533-536.
59. Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2007) Ectopic expression of OsLFL1 in rice represses Ehdl by binding on its promoter. Biochem Biophys Commun 360:251-256. (Pubitemid 46990351)
60. Castillejo C, Pelaz S (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr Biol 18:1338-1343.
61. Mochida K, et al. (2009) In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Res 16:353-369.
62. Mochida K, et al. (2010) LegumeTFDB: An integrative database of Glycine max, Lotus japonicus and Medicago truncatula transcription factors. Bioinformatics 26:290-291.
63. Abel S, Theologis A (1995) A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum). Plant J 8:87-96.
64. Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585-596. (Pubitemid 41225470)
65. Gonzales MD, et al. (2005) The Legume Information System (LIS): An integrated information resource for comparative legume biology. Nucleic Acids Res 33(database issue):D660-D665.
66. Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA 106:4555-4560.
67. Ebana K, et al. (2011) Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor Appl Genet 122:1199-1210.
68. Funatsuki H, Kawaguchi K, Matsuba S, Sato Y, Ishimoto M (2005) Mapping of QTL associated with chilling tolerance during reproductive growth in soybean. Theor Appl Genet 111:851-861. (Pubitemid 41473382)
69. Lin C (2000) Photoreceptors and regulation of flowering time. Plant Physiol 123:39-50.
70. Weller JL, Beauchamp N, Kerckhoffs LH, Platten JD, Reid JB (2001) Interaction of phytochromes A and B in the control of de-etiolation and flowering in pea. Plant J 26:283-294. (Pubitemid 32623534)
71. Takano M, et al. (2005) Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17:3311-3325.
72. Zhang Q, et al. (2008) Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc Natl Acad Sci USA 105:21028-21033.
73. Xia Z, Sato H, Watanabe S, Kawasaki S, Harada K (2005) Construction and characterization of a BAC library of soybean. Euphytica 141:129-137. (Pubitemid 40564413)
74. Song QJ, et al. (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122-128. (Pubitemid 38908557)
75. Xia Z, et al. (2007) An integrated high-density linkage map of soybean with RFLP, SSR, STS, and AFLP markers using A single F2 population. DNA Res 14:257-269.
76. Li HJ, et al. (2011) POD1 regulates pollen tube guidance in response to micropylar female signaling and acts in early embryo patterning in Arabidopsis. Plant Cell 23:3288-3302.
77. Sheen J (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 127:1466-1475.
78. Xie ZM, et al. (2009) Soybean Trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic Arabidopsis. PLoS ONE 4:e6898.