Genetic variation in soybean at the maturity locus e4 is involved in adaptation to long days at high latitudes

Agronomy

Volumn 3, Issue 1, 2013, Pages 117-134

  Tsubokura, Yasutaka ^a   Matsumura, Hisakazu ^b   Xu, Meilan ^c   Liu, Baohui ^d   Nakashima, Hiroko ^e   Anai, Toyoaki ^e   Kong, Fanjiang ^d   Yuan, Xiaohui ^d   Kanamori, Hiroyuki ^f   Katayose, Yuichi ^a   Takahashi, Ryoji ^b,g   Harada, Kyuya ^a   Abe, Jun ^c  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

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

^e SAGA UNIVERSITY   (Japan)

^f NATIONAL VETERINARY ASSAY LABORATORY   (Japan)

^g NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

Author keywords

Flowering; Genetic diversity; Photoperiod insensitivity; Phytochrome A; Soybean

Indexed keywords

EID: 84879783798     PISSN: None     EISSN: 20734395     Source Type: Journal    
DOI: 10.3390/agronomy3010117     Document Type: Article

References (47)

1. Ehrenreich, I.M.; Hanzawa, Y.; Chou, L.; Roe, J.L.; Kover, P.X.; Purugganan, M.D. Candidate gene association mapping of Arabidopsis flowering time. Genetics 2009, 183, 325–335.
2. Alonso-Blanco, C.; Aarts, M.G.M.; Bentsink, L.; Keurentjes, J.J.B.; Reymond, M.; Vreugdenhil, D.; Koornneef, M. What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 2009, 21, 1877–1896.
3. Johanson, U.; West, J.; Lister, C.; Michaels, S.; Amashino, R.M.; Dean, C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 2000, 290, 344–347.
4. Gazzani, S.; Gendall, A.R.; Lister, C.; Dean, C. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 2003, 132, 1107–1114.
5. Michaels, S.D.; He, Y.; Scortecci, K.C.; Amasino, R.M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl. Acad. Sci. USA 2003, 100, 10102–10107.
6. Shindo, C.; Aranzana, M.J.; Lister, C.; Baxter, C.;. Nicholls, C.; Nordborg, M.; Dean, C. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol. 2005, 138, 1163–1173.
7. Shindo, C.; Bernasconi, G.; Hardtke, C.S. Natural genetic variation in Arabidopsis: Tools, traits and prospects for evolutionary ecology. Ann. Bot. 2007, 99, 1043–1054.
8. Takahashi, Y.; Teshima, K.M.; Yokoi, S.; Innan, H.; Shimamoto, K. Variation in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc. Natl. Acad. Sci. USA 2009, 106, 4555–4560.
9. Buzzell, R.I. Inheritance of a soybean flowering response to fluorescent-daylength conditions. Can. J. Genet. Cytol. 1971, 13, 703–707.
10. Buzzell, R.I.; Voldeng, H.D. Inheritance of insensitivity to long day length. Soybean Genet. Newsl. 1980, 7, 26–29.
11. Saindon, G.; Voldeng, H.D.; Beversdorf, W.D.; Buzzell, R.I. Genetic control of long daylength response in soybean. Crop Sci. 1989, 29, 1436–1439.
12. Cober, E.R.; Tanner, J.W.; Voldeng, H.D. Genetic control of photoperiod response in early-maturing near-isogenic soybean lines. Crop Sci. 1996, 36, 601–605.
13. Cober, E.R.; Tanner, J.W.; Voldeng, H.D. Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Sci. 1996, 36, 606–610.
14. Cober, E.R.; Voldeng, H.D. A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Sci 2001, 41, 698–701.
15. Cober, E.R.; Voldeng, H.D. Low R:FR light quality delays flowering of E7E7 soybean lines. Crop Sci. 2001, 41, 1823–1826.
16. Watanabe, S.; Harada, K.; Abe, J. Genetic and molecular bases of photoperiod responses of flowering in soybean. Breed Sci. 2012, 61, 531–543.
17. Liu, B.; Kanazawa, A.; Matsumura, H.; Takahashi, R.; Harada, K.; Abe, J. Genetic redundancy in soybean photoresponses associated with duplication of phytochrome A gene. Genetics 2008, 180, 996–1007.
18. Watanabe, S.; Hideshima, R.; Xia, Z.; Tsubokura, Y.; Sato, S.; Nakamoto, Y.; Yamanaka, N.; Takahashi, R.; Ishimoto, M.; Anai, T.; et al. Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 2009, 182, 1251–1262.
19. Xia, Z.; Watanabe, S.; Yamada, T.; Tsubokura, Y.; Nakashima, H.; Zhai, H.; Anai, T.; Sato, S.; Yamazaki, T.; Lü, S.; et al. Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc. Natl. Acad. Sci. USA 2012, 109, E2155–E2164.
20. Abe, J.; Xu, D.H.; Miyano, A.; Komatsu, K.; Kanazawa, A.; Shimamoto, Y. Photoperiod-insensitive Japanese soybean landraces differ at two maturity loci. Crop Sci. 2003, 43, 1300–1304.
21. Liu, B.; Abe, J. QTL mapping for photoperiod-insensitivity of a Japanese soybean landrace Sakamotowase. J. Hered. 2009, 101, 251–256.
22. Kanazawa, A.; Liu, B.; Kong, F.; Arase, S.; Abe, J. Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J. Mol. Evol. 2009, 69, 164–175.
23. Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.; Mitros, T.; Nelson, W.; Hyten, D.L.; Song, Q.; Thelen, J.J.; Cheng, J.; et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178–183.
24. Lam, H.M.; Xu, X.; Liu, X.; Chen, W.; Yang, G.; Wong, F.L.; Li, M.W.; He, W.; Qin, N.; Wang, B.; et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 2010, 42, 1053–1059.
25. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 1983, 105, 437–460.
26. Watterson, G. On the number of segregating sites in genetical models without recombination. Theor. Pop. Biol. 1975, 7, 188–193.
27. Cannon, S.B.; Shoemaker, R.C. Evolutionary and comparative analyses of the soybean genome. Breed Sci. 2012, 61, 437–444.
28. Schlueter, J.A.; Scheffler, B.E.; Schlueter, S.D.; Shoemaker, R.C. Sequence conservation of homeologous bacterial artificial chromosomes and transcription of homeologous genes in soybean (Glycine max L. Merr.). Genetics 2006, 174, 1017–1028.
29. Lin, J.Y.; Stupar, R.M.; Hans, C.; Hyten, D.L.; Jackson, S.A. Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. Plant Cell 2010, 22, 2545–2561.
30. Hecht, V.; Foucher, F.; Ferrándiz, C.; Macknight, R.; Navarro, C.; Morin, J.; Vardy, M.E.; Ellis, N.; Beltran, J.P.; Rameau, C.; Weller, J.L. Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 2005, 137, 1420–1434.
31. Casal, J.J.; Sanchez, R.A.; Yanovsky, M.J. The function of phytochrome A. Plant Cell Environ. 1997, 20, 813–819.
32. Franklin, K.A.; Allen, T.; Whitelam, G.C. Phytochrome A is an irradiance-dependent red light sensor. Plant J. 2007, 50, 108–117.
33. Franklin, K.A.; Whitelam, G.C. Phytochrome A function in red light sensing. Plant Signal. Behav. 2007, 2, 383–385.
34. Weller, J.L.; Murfet, I.C.; Reid, J.B. Pea mutants with reduced sensitivity to far-red light define an important role for phytochrome A in day-length detection. Plant Physiol. 1997, 114, 1225–1236.
35. Weller, J.L.; Beauchamp, N.; Kerckhoffs, H.J.; Platten, D.; Reid, J.B. Interaction of phytochrome A and B in the control of de-etiolation and flowering in pea. Plant J. 2001, 26, 283–294.
36. Takano, M.; Kanegae, H.; Shinomura, T.; Miyano, A.; Hirochika, H.; Furuya, M. Isolation and characterization of rice phytochrome A mutants. Plant Cell 2001, 13, 521–534.
37. Takano, M.; Inagaki, N.; Xie, X.; Yuzurihara, N.; Hihara, F.; Ishizuka, T.; Yano, M.; Nishimura, M.; Miyano, A.; Hirochika, H.; et al. Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 2005, 17, 3311–3325.
38. Tian, Z.; Wang, X.; Lee, R.; Li, Y.; Specht, J.E.; Nelson, R.L.; McClean, P.E.; Qiu, L.; Ma, J. Artificial selection for determinate growth habit in soybean. Proc. Natl. Acad. Sci. USA 2010, 107, 8563–8568.
39. Liu, B.; Watanabe, S.; Uchiyama, T.; Kong, F.; Kanazawa, A.; Xia, Z.; Nagamatsu, A.; Arai, M.; Yamada, T.; Kitamura, K.; et al. The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER 1. Plant Physiol. 2010, 153, 198–210.
40. Winter, D.; Vinegar, B.; Nahal, H.; Ammar, R.; Wilson, G.V.; Provart, N. An “electronic fluorescent pictograph” browser for exploring and analyzing large-Scale biological data sets. PloS One 2007, 8, e718.
41. Available online: http://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi (accessed on 10 December 2012).
42. Abe, J.; Ohara, M.; Shimamoto, Y. New electrophoretic mobility variants observed in wild soybean (Glycine soja) distributed in Japan and Korea. Soybean Genet. Newsl. 1992, 19, 63–72.
43. Abe, J.; Xu, D.H.; Suzuki, Y.; Kanazawa, A.; Shimamoto, Y. Soybean germplasm pools in Asia revealed by nuclear SSRs. Theor. Appl. Genet. 2003, 106, 445–453.
44. Doyle, J.J.; Doyle, J.L. Isolation of plant DNA from fresh tissue. Focus 1990, 12, 13–15.
45. Felsenstein, J. PHYLIP (Phylogeny Inference Package), version 3.57c; University of Washington Press: Seattle WA, USA, 1997.
46. Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673–4680.
47. Librado, P.; Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25, 1451–1452.