Characterization and quantitative trait locus mapping of late-flowering from a Thai soybean cultivar introduced into a photoperiod-insensitive genetic background

English version

Autoři: Fei Sun ^aff001; Meilan Xu ^aff001; Cheolwoo Park ^aff001; Maria Stefanie Dwiyanti ^aff001; Atsushi J. Nagano ^aff003; Jianghui Zhu ^aff001; Satoshi Watanabe ^aff004; Fanjiang Kong ^aff005; Baohui Liu ^aff005; Tetsuya Yamada ^aff001; Jun Abe ^aff001
Působiště autorů: Research Faculty of Agriculture, Hokkaido University, Sapporo, Hokkaido, Japan ^aff001; Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, China ^aff002; Faculty of Agriculture, Ryukoku University, Otsu, Shiga, Japan ^aff003; Faculty of Agriculture, Saga University, Saga, Saga, Japan ^aff004; School of Life Sciences, Guangzhou University, Guangzhou, China ^aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226116

Souhrn

The timing of both flowering and maturation determine crop adaptability and productivity. Soybean (Glycine max) is cultivated across a wide range of latitudes. The molecular-genetic mechanisms for flowering in soybean have been determined for photoperiodic responses to long days (LDs), but remain only partially determined for the delay of flowering under short-day conditions, an adaptive trait of cultivars grown in lower latitudes. Here, we characterized the late-flowering (LF) habit introduced from the Thai cultivar K3 into a photoperiod-insensitive genetic background under different photo-thermal conditions, and we analyzed the genetic basis using quantitative trait locus (QTL) mapping. The LF habit resulted from a basic difference in the floral induction activity and from the suppression of flowering, which was caused by red light-enriched LD lengths and higher temperatures, during which FLOWERING LOCUS T (FT) orthologs, FT2a and FT5a, were strongly down-regulated. QTL mapping using gene-specific markers for flowering genes E2, FT2a and FT5a and 829 single nucleotide polymorphisms obtained from restriction-site associated DNA sequencing detected three QTLs controlling the LF habit. Of these, a QTL harboring FT2a exhibited large and stable effects under all the conditions tested. A resequencing analysis detected a nonsynonymous substitution in exon 4 of FT2a from K3, which converted the glycine conserved in FT-like proteins to the aspartic acid conserved in TERMINAL FLOWER 1-like proteins (floral repressors), suggesting a functional depression in the FT2a protein from K3. The effects of the remaining two QTLs, likely corresponding to E2 and FT5a, were environment dependent. Thus, the LF habit from K3 may be caused by the functional depression of FT2a and the down-regulation of two FT genes by red light-enriched LD conditions and high temperatures.

Klíčová slova:

Alleles – Gene mapping – Genetic loci – Habits – Latitude – Molecular genetics – Quantitative trait loci – Soybean

Zdroje

1. Watanabe S, Harada K, Abe J. Genetic and molecular bases of photoperiod responses of flowering in soybean. Breed Sci. 2012; 61(5): 531–543. doi: 10.1270/jsbbs.61.531 23136492

2. Cao D, Takeshima R, Zhao C, Liu B, Abe J, Kong F. Molecular mechanisms of flowering under long days and stem growth habit in soybean. J Exp Bot. 2017; 68(8): 1873–1884. doi: 10.1093/jxb/erw394 28338712

3. Zhang J, Song Q, Cregan PB, Nelson RL, Wang X, Wu J, et al. Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genomics. 2015; 16(1): 217.

4. Contreras-Soto RI, Mora F, Lazzari F, de Oliveira MAR, Scapim CA, Schuster I. Genome-wide association mapping for flowering and maturity in tropical soybean: implications for breeding strategies. Breed Sci. 2017; 67(4): 435–449.

5. Mao T, Li J, Wen Z, Wu C, Sun S, Jiang B, et al. Association mapping of loci controlling genetic and environmental interaction of soybean flowering time under various photo-thermal conditions. BMC Genomics. 2017; 18(1): 415. doi: 10.1186/s12864-017-3778-3 28549456

6. Copley TR, Duceppe MO, O’Donoughue LS. Identification of novel loci associated with maturity and yield traits in early maturity soybean plant introduction lines. BMC Genomics. 2018; 19(1): 167. doi: 10.1186/s12864-018-4558-4 29490606

7. Zhao L, Li M, Xu C, Yang X, Li D, Zhao X, et al. Natural variation in GmGBP1 promoter affects photoperiod control of flowering time and maturity in soybean. Plant J. 2018; 96(1): 147–162. doi: 10.1111/tpj.14025 30004144

8. Jiang B, Zhang S, Song W, Khan MAA, Sun S, Zhang C, et al. Natural variations of FT family genes in soybean varieties covering a wide range of maturity groups. BMC Genomics. 2019; 20(1): 230. doi: 10.1186/s12864-019-5577-5 30894121

9. Ogiso-Tanaka E, Shimizu T, Hajika M, Kaga A, Ishimoto M. Highly multiplexed AmpliSeq technology identifies novel variation of flowering time-related genes in soybean (Glycine max). DNA Res. 2019; 26(3): 243–260. doi: 10.1093/dnares/dsz005 31231761

10. Xu M, Yamagishi N, Zhao C, Takeshima R, Kasai M, Watanabe S, et al. The soybean-specific maturity gene E1 family of floral repressors controls night-break responses through down-regulation of FLOWERING LOCUS T orthologs. Plant Physiol. 2015; 168(4): 1735–1746. doi: 10.1104/pp.15.00763 26134161

11. Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genet. 2008; 180(2): 995–1007.

12. Watanabe S, Hideshima R, Xia Z, Tsubokura Y, Sato S, Nakamoto Y, et al. Map-based cloning of the gene associated with the soybean maturity locus E3. Genet. 2009; 182(4): 1251–1262.

13. Kong F, Liu B, Xia Z, Sato S, Kim B M, Watanabe S, et al. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 2010; 154(3): 1220–1231. doi: 10.1104/pp.110.160796 20864544

14. Xia Z, Watanabe S, Yamada T, Tsubokura Y, Nakashima H, Zhai H, et al. Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc Natl Acad Sci. 2012; 109(32): E2155–E2164. doi: 10.1073/pnas.1117982109 22619331

15. Watanabe S, Xia Z, Hideshima R, Tsubokura Y, Sato S, Yamanaka N, et al. A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genet. 2011; 188(2): 395–407.

16. Liu W, Kim MY, Van K, Lee YH, Li H, Liu X, et al. QTL identification of yield-related traits and their association with flowering and maturity in soybean. J Crop Sci Biotechnol. 2011; 14(1): 65–70.

17. Jia H, Jiang B, Wu C, Lu W, Hou W, Sun S, et al. Maturity group classification and maturity locus genotyping of early-maturing soybean varieties from high-latitude cold regions. PLoS One. 2014; 9(4): e94139. doi: 10.1371/journal.pone.0094139 24740097

18. Jiang B, Nan H, Gao Y, Tang L, Yue Y, Lu S, et al. Allelic combinations of soybean maturity loci E1, E2, E3 and E4 result in diversity of maturity and adaptation to different latitudes. PloS One. 2014; 9(8): e106042. doi: 10.1371/journal.pone.0106042 25162675

19. Langewisch T, Zhang H, Vincent R, Joshi T, Xu D, Bilyeu K. Major soybean maturity gene haplotypes revealed by SNPViz analysis of 72 sequenced soybean genomes. PloS One. 2014; 9(4): e94150. doi: 10.1371/journal.pone.0094150 24727730

20. Tsubokura Y, Watanabe S, Xia Z, Kanamori H, Yamagata H, Kaga A, et al. Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann. Bot. 2014; 113:429–41. doi: 10.1093/aob/mct269 24284817

21. Zhai H, Lü S, Wang Y, Chen X, Ren H, Yang J, et al. Allelic variations at four major maturity E genes and transcriptional abundance of the E1 gene are associated with flowering time and maturity of soybean cultivars. PloS One, 2014, 9(5): e97636. doi: 10.1371/journal.pone.0097636 24830458

22. Lu S, Li Y, Wang J, Srinives P, Nan H, Cao D, et al. QTL mapping for flowering time in different latitude in soybean. Euphytica. 2015; 206(3): 725–736.

23. Kurasch AK, Hahn V, Leiser WL, Vollmann J, Schori A, Bétrix CA, et al. Identification of mega‐environments in Europe and effect of allelic variation at maturity E loci on adaptation of European soybean. Plant Cell Environ. 2017; 40(5): 765–778. doi: 10.1111/pce.12896 28042879

24. Li J, Wang X, Song W, Huang X, Zhou J, Zeng H, et al. Genetic variation of maturity groups and four E genes in the Chinese soybean mini core collection. PloS One. 2017; 12(2): e0172106. doi: 10.1371/journal.pone.0172106 28207889

25. Xu M, Xu Z, Liu B, Kong F, Tsubokura Y, Watanabe S, et al. Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol. 2013; 13(1): 91.

26. Takeshima R, Hayashi T, Zhu J, Zhao C, Xu M, Yamaguchi N, et al. A soybean quantitative trait locus that promotes flowering under long days is identified as FT5a, a FLOWERING LOCUS T ortholog. J. Exp. Bot. 2016; 67(17): 5247–5258. doi: 10.1093/jxb/erw283 27422993

27. Zhu J, Takeshima R, Harigai K, Xu M, Kong F, Liu B, et al. Loss of function of the E1-Like-b gene associates with early flowering under long-day conditions in soybean. Front Plant Sci. 2018; 9: 1867. doi: 10.3389/fpls.2018.01867 30671065

28. Zhao C, Takeshima R, Zhu J, Xu M, Sato M, Watanabe S, et al. A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a FLOWERING LOCUS T ortholog. BMC Plant Biol. 2016; 16(1): 20.

29. Destro D, Carpentieri-Pípolo V, Kiihl RA de S, Almeida LA de. Photoperiodism and genetic control of the long juvenile period in soybean: A review. Crop Breed. Appl. Biotech. 2001; 1(1):72–92

30. Ray JD, Hinson K, Mankono J, Malo, MF. Genetic control of a long-juvenile trait in soybean. Crop Sci. 1995; 35(4): 1001–1006.

31. Bonato ER, Vello NA. E6, a dominant gene conditioning early flowering and maturity in soybeans. Genet Mol Biol. 1999; 22(2): 229–232.

32. Yue Y, Liu N, Jiang B, Li M, Wang H, Jiang Z, et al. A single nucleotide deletion in J encoding GmELF3 confers long juvenility and is associated with adaption of tropic soybean. Mol Plant. 2017; 10(4): 656–658. doi: 10.1016/j.molp.2016.12.004 27979775

33. Lu S, Zhao X, Hu Y, Liu S, Nan H, Li X, et al. Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat. Genet. 2017, 49(5): 773. doi: 10.1038/ng.3819 28319089

34. Li X, Fang C, Xu M, Zhang F, Lu S, Nan H, et al. Quantitative trait locus mapping of soybean maturity gene E6. Crop Sci. 2017; 57(5): 2547–2554.

35. Pooprompan P, Wasee S. Toojinda T, Abe J, Chanprame S, Srinives P. Molecular marker analysis of days to flowering in vegetable soybean (Glycine max (L.) Merrill). Kasetsart J. 2006, 40: 573–581.

36. Doyle JJ, Doyle JL. Isolation of plant DNA from fresh tissue. Focus. 1990; 12(13): 39–40.

37. Baird NA, Etter PD, Atwood TS, Curry MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PloS One. 2008; 3(10): e3376. doi: 10.1371/journal.pone.0003376 18852878

38. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE, et al. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PloS One. 2012; 7(5): e37135. doi: 10.1371/journal.pone.0037135 22675423

39. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15): 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

40. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012; 9(4): 357. doi: 10.1038/nmeth.1923 22388286

41. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20(9): 1297–1303. doi: 10.1101/gr.107524.110 20644199

42. Browning S R, Browning B L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007; 81(5): 1084–1097. doi: 10.1086/521987 17924348

43. Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007; 23(19): 2633–2635. doi: 10.1093/bioinformatics/btm308 17586829

44. Broman KW, Wu H, Sen Ś, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics, 2003, 19(7): 889–890. doi: 10.1093/bioinformatics/btg112 12724300

45. Wang J, Li H, Zhang L, Bilyeu K, Song JT, Lee JD. User’s manual of QTL IciMapping ver. 4.1. Quantitative Genetics group, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS): Beijing/Genetic Resources Program, International Maize and Wheat Improvement Center (CIMMYT): Mexico City, 2016.

46. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010; 463(7278): 178. doi: 10.1038/nature08670 20075913

47. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3): R25. doi: 10.1186/gb-2009-10-3-r25 19261174

48. Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999; 27, 297–300. doi: 10.1093/nar/27.1.297 9847208

49. Jiang B, Yue Y, Gao Y, Ma L, Sun S, Wu C, et al. GmFT2a polymorphism and maturity diversity in soybeans. PloS One. 2013; 8(10): e77474. doi: 10.1371/journal.pone.0077474 24155962

50. Wilkerson GG, Jones JW, Boote KJ, Buol GS. Photoperiodically sensitive interval in time to flower of soybean. Crop Sci. 1989; 29(3): 721–726.

51. Ellis RH, Collinson ST, Hudson D, Patefield WM. The analysis of reciprocal transfer experiments to estimate the durations of the photoperiod-sensitive and photoperiod-insensitive phases of plant development: an example in soya bean. Ann Bot. 1992; 70(1): 87–92.

52. Collinson ST, Summerfield RJ, Ellis RH, Roberts EH. Durations of the photoperiod-sensitive and photoperiod-insensitive phases of development to flowering in four cultivars of soyabean [Glycine max (L.) Merrill]. Ann Bot. 1993; 71(5): 389–394.

53. Upadhyay AP, Ellis RH, Summerfield RJ, Roberts EH, Qi A. Characterization of photothermal flowering responses in maturity isolines of soyabean [Glycine max (L.) Merrill] cv. Clark. Ann Bot. 1994; 74(1): 87–96. doi: 10.1093/aob/74.1.87 19700466

54. Cober ER. Long juvenile soybean flowering responses under very short photoperiods. Crop Sci. 2011; 51(1): 140–145.

55. Saindon G, Voldeng HD, Beversdorf WD, Buzzell RI. Genetic control of long daylength response in soybean. Crop Sci. 1989; 29(6): 1436–1439.

56. Cober ER, Tanner JW, Voldeng HD. Genetic control of photoperiod response in early-maturing, near-isogenic soybean lines. Crop Sci. 1996; 36(3): 601–605.

57. Buzzell RI, Voldeng H D. Inheritance of insensitivity to long daylength. Soyb Genet Newsl. 1980; 7(1): 13.

58. Buzzell RI. Inheritance of a soybean flowering response to fluorescent-daylength conditions. Can J Genet Cytol. 1971; 13(4): 703–707.

59. Kilen TC, Hartwig EE. Inheritance of a light-quality sensitive character in soybeans. Crop Sci. 1971; 11(4): 559–561.

60. Wu FQ, Fan CM, Zhang XM, Fu YF. The phytochrome gene family in soybean and a dominant negative effect of a soybean PHYA transgene on endogenous Arabidopsis PHYA. Plant Cell Rep. 2013; 32(12): 1879–1890. doi: 10.1007/s00299-013-1500-8 24013793

61. Zhang Q, Li H, Li R, Hu R, Fan C, Chen F, et al. Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc Natl Acad Sci. 2008; 105(52): 21028–21033. doi: 10.1073/pnas.0810585105 19106300

62. Matsumura H, Kitajima H, Akada S, Abe J, Minaka N, Takahashi R. Molecular cloning and linkage mapping of cryptochrome multigene family in soybean. Plant Genome. 2009; 2(3): 271–281.

63. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2006; 2(7): e106. doi: 10.1371/journal.pgen.0020106 16839183

64. Luan W, Chen H, Fu Y, Si H, Peng W, Song S, et al. The effect of the crosstalk between photoperiod and temperature on the heading-date in rice. PLoS One. 2009; 4(6): e5891. doi: 10.1371/journal.pone.0005891 19521518

65. Jagadish SV, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PV, Craufurd PQ. Implications of high temperature and elevated CO2 on flowering time in plants. Front Plant Sci. 2016; 7: 913. doi: 10.3389/fpls.2016.00913 27446143

66. Cober ER, Stewart DW, Voldeng HD. Photoperiod and temperature responses in early-maturing near-isogenic soybean lines. Crop Sci. 2001; 41: 721–727.

67. Wang Y, Gu Y, Gao H, Qiu L, Chang R, Chen S, et al. Molecular and geographic evolutionary support for the essential role of GIGANTEAa in soybean domestication of flowering time. BMC Evol Biol. 2016; 16: 79. doi: 10.1186/s12862-016-0653-9 27072125

68. Sun H, Jia Z, Cao D, Jiang B, Wu C, Hou W, et al. GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PloS One. 2011; 6.12: e29238.

69. Nan H, Cao D, Zhang D, Li Y, Lu S, Tang L, et al. GmFT2a and GmFT5a redundantly and differentially regulate flowering through interaction with and upregulation of the bZIP transcription factor GmFDL19 in soybean. PloS One. 2014; 9.5: e97669.

70. Cai Y, Chen L, Liu X, Guo C, Sun S, Wu C, et al. CRISPR/Cas9‐mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotech J. 2018; 16(1): 176–185.

71. Hanzawa Y, Money T, Bradley D. A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci. 2005; 102(21): 7748–7753. doi: 10.1073/pnas.0500932102 15894619

72. Ho WWH, Weigel D. Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell. 2014; 26(2): 552–564. doi: 10.1105/tpc.113.115220 24532592

73. Wang Z, Zhou Z, Liu Y, Liu T, Li Q, Ji Y, et al. Functional evolution of phosphatidylethanolamine binding proteins in soybean and Arabidopsis. Plant Cell. 2015; 27(2): 323–336. doi: 10.1105/tpc.114.135103 25663621

74. Kazan K, Manners JM. MYC2: the master in action. Mol Plant. 2013; 6(3): 686–703. doi: 10.1093/mp/sss128 23142764

75. Wang H, Li Y, Pan J, Lou D, Hu Y, Yu D. The bHLH transcription factors MYC2, MYC3, and MYC4 are required for jasmonate-mediated inhibition of flowering in Arabidopsis. Mol Plant. 2017; 10(11): 1461–1464. doi: 10.1016/j.molp.2017.08.007 28827172

Characterization and quantitative trait locus mapping of late-flowering from a Thai soybean cultivar introduced into a photoperiod-insensitive genetic background

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz