Abstract
Key message
E10 is a new maturity locus in soybean and FT4 is the predicted/potential functional gene underlying the locus.
Abstract
Flowering and maturity time traits play crucial roles in economic soybean production. Early maturity is critical for north and west expansion of soybean in Canada. To date, 11 genes/loci have been identified which control time to flowering and maturity; however, the molecular bases of almost half of them are not yet clear. We have identified a new maturity locus called “E10” located at the end of chromosome Gm08. The gene symbol E10e10 has been approved by the Soybean Genetics Committee. The e10e10 genotype results in 5–10 days earlier maturity than E10E10. A set of presumed E10E10 and e10e10 genotypes was used to identify contrasting SSR and SNP haplotypes. These haplotypes, and their association with maturity, were maintained through five backcross generations. A functional genomics approach using a predicted protein–protein interaction (PPI) approach (Protein–protein Interaction Prediction Engine, PIPE) was used to investigate approximately 75 genes located in the genomic region that SSR and SNP analyses identified as the location of the E10 locus. The PPI analysis identified FT4 as the most likely candidate gene underlying the E10 locus. Sequence analysis of the two FT4 alleles identified three SNPs, in the 5′UTR, 3′UTR and fourth exon in the coding region, which result in differential mRNA structures. Allele-specific markers were developed for this locus and are available for soybean breeders to efficiently develop earlier maturing cultivars using molecular marker assisted breeding.
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Abbreviations
- GO:
-
Gene ontology
- MP-PIPE:
-
Massively parallel protein–protein interaction prediction engine
- PIPE:
-
Protein–protein interaction prediction engine
- PPIs:
-
Protein–protein interactions
- QTLs:
-
Quantitative trait loci
- SNP:
-
Single nucleotide polymorphism
- SSR:
-
Simple sequence repeat
References
Baraas RC, Hagen LA, Dees EW, Neitz M (2012) Substitution of isoleucine for threonine at position 190 of S-opsin causes S-cone-function abnormalities. Vision Res 73:1–9
Bernard RL (1971) Two major genes for time of flowering and maturity in soybeans. Crop Sci 11:242–247
Bonato ER, Vello NA (1999) E6 a dominant gene conditioning early flowering and maturity in soybeans. Genet Mol Biol 22:229–232
Buzzel RI, Voldeng HD (1980) Inheritance of insensitivity to long day length. Soybean Genet Newsl 7:26–29
Buzzell RI (1971) Inheritance of a soybean flowering response to fluorescent day length conditions. Can J Genet Cytol 13:703–707
Cober ER, Morrison MJ (2010) Regulation of seed yield and agronomic characters by photoperiod sensitivity and growth habit genes in soybean. Theor Appl Genet 120:1005–1012
Cober ER, Voldeng HD (2012) A retrospective look at short-season soybean cultivar development in Ontario. Can J Plant Sci 92:1239–1243
Cober ER, Molnar SJ, Charette M, Voldeng HD (2010) A new locus for early maturity in soybean. Crop Sci 50:524–527
Cober ER, Curtis DF, Stewart DW, Morrison MJ (2014) Quantifying the effects of photoperiod, temperature and daily irradiance on flowering time of soybean isolines. Plants 3:476–497
Cregan PB, Jarvik T, Bush AL, Shoemaker RC, Lark KG, Kahler AL, Kaya N, Van Toai TT, Lohnes DG, Chung J, Specht JE (1999) An integrated genetic linkage map of the soybean genome. Crop Sci 39:1464–1490
Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340:245–246
Garner WW, Allard HA (1927) Effect of short alternating periods of light and darkness on plant growth. Science 66:40–42
Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Natl Acad Sci USA (PNAS) 97:4168–4173
Jessulat M, Pitre S, Gui Y, Hooshyar M, Omidi K, Samanfar B, Tan LH, Alamgir M, Green J, Dehne F, Golshani A (2011) Recent advances in protein-protein interaction prediction: experimental and computational methods. Expert Opin Drug Discov 6:921–935
Kong F, Nan H, Cao D, Li Y, Wu F, Wang J, Lu S, Yuan X, Cober ER, Abe J, Liu B (2014) A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Sci 54:2529–2535
Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photo responses associated with duplication of the phytochrome A gene. Genetics 180:995–1007
Liu B, Watanabe S, Uchiyama T, Kong F, Kanazawa A, Xia Z, Nagamatsu A, Arai M, Yamada T, Kitamura K, Masuta C, Harada K, Abe J (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER 1. Plant Physiol 153:198–210
McBlain BA, Bernard RL (1987) A new gene affecting the time of flowering-maturity in soybeans. J Hered 178:68–70
McBlain BA, Hesketh JD, Bernard RL (1987) Genetic effects on reproductive phenology in soybean isolines differing in maturity genes. Can J Plant Sci 67:105–116
Molnar SJ, Rai S, Charette M, Cober ER (2003) Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome 46:1024–1036
Omidi K, Hooshyar M, Jessulat M, Samanfar B, Sanders M, Burnside D, Pitre S, Schoenrock A, Xu J, Babu M, Golshani A (2014) Phosphatase complex Pph3/Psy2 is involved in regulation of efficient non-homologous end-joining pathway in the yeast Saccharomyces cerevisiae. PLoS One 9(1):e87248
Park Y (2009) Critical assessment of sequence-based protein-protein interaction prediction methods that do not require homologous protein sequences. BMC Bioinform 10:419
Pepys MB, Hawkins PN, Booth DR, Vigushin DM, Tennent GA, Soutar AK, Totty N, Nguyen O, Blake CC, Terry CJ (1993) Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature 362:553–557
Pitre S, Dehne F, Chan A, Cheetham J, Duong A, Emili A, Gebbia M, Greenblatt J, Jessulat M, Krogan N, Luo X, Golshani A (2006) PIPE: a protein-protein interaction prediction engine based on the re-occurring short polypeptide sequences between known interacting protein pairs. BMC Bioinform 7:365
Pitre S, Alamgir M, Green JR, Dumontier M, Dehne F, Golshani A (2008) Computational methods for predicting protein-protein interactions. Adv Biochem Eng/Biotechnol 110:247–267
Pitre S, Hooshyar M, Schoenrock A, Samanfar B, Jessulat M, Green JR, Dehne F, Golshani A (2012) Short co-occurring polypeptide regions can predict global protein interaction maps. Sci Rep 2:239
Ray JD, Hinson K, Mankono JEB, Malo MF (1995) Genetic control of a long-juvenile trait in soybean. Crop Sci 35:1001–1006
Saindon G, Beversdorf WD, Voldeng HD (1989a) Adjusting of the soybean phenology using the E4 loci. Crop Sci 29:1361–1365
Saindon G, Voldeng HD, Beversdorf WD, Buzzell RI (1989b) Genetic control of long daylength response in soybean. Crop Sci 29:1436–1439
Schoenrock A, Samanfar B, Pitre S, Hooshyar M, Jin K, Phillips CA, Wang H, Phanse S, Omidi K, Gui Y, Alamgir M, Wong A, Barrenäs F, Babu M, Benson M, Langston MA, Green JR, Dehne F, Golshani A (2014) Efficient prediction of human protein-protein interactions at a global scale. BMC Bioinform 15:383
Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS One 8(1):e54603
Sonah H, O’Donoughue L, Cober ER, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13:211–221
Tian Z, Wang X, Lee R, Li Y, Specht JE, Nelson RL, McClean PE, Qiu L, Ma J (2010) Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci (PNAS) 107:8563–8568
Tsubokura Y, Watanabe S, Xia Z, Kanamori H, Yamagata H, Kaga A, Katayose Y, Abe J, Ishimoto M, Harada K (2014) Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot 113:429–441
Vlasblom J, Zuberi K, Rodriguez H, Arnold R, Gagarinova A, Deineko V, Kumar A, Leung E, Rizzolo K, Samanfar B, Chang L, Phanse S, Golshani A, Greenblatt JF, Houry WA, Emili A, Morris Q, Bader G, Babu M (2015) Novel function discovery with GeneMANIA: a new integrated resource for gene function prediction in Escherichia coli. Bioinformatics 31:306–310
Wang Z, Zhou Z, Liu Y, Liu T, Li Q, Ji Y, Li C, Fang C, Wang M, Wu M, Shen Y, Tang T, Ma J, Tian Z (2015) Functional evolution of phosphatidylethanolamine binding proteins in soybean and Arabidopsis. Plant Cell 27:323–336
Watanabe S, Hideshima R, Xia Z, Tsubokura Y, Sato S, Nakamoto Y, Yamanaka N, Takahashi R, Ishimoto M, Anai T, Tabata S, Harada K (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262
Watanabe S, Xia Z, Hideshima R, Tsubokura Y, Sato S, Yamanaka N, Takahashi R, Anai T, Tabata S, Kitamura K, Harada K (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
Wickland DP, Hanzawa Y (2015) The Flowering Locus T/Terminal Flower 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8:983–997
Xia Z, Watanabe S, Yamada T, Tsubokura Y, Nakashima H, Zhai H, Anai T, Sato S, Yamazaki T, Lü S, Wu H, Tabata S, Harada K (2012) Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc Natl Acad Sci USA 109:E2155–E2164
Xu M, Xu Z, Liu B, Kong F, Tsubokura Y, Watanabe S, Xia Z, Harada K, Kanazawa A, Yamada T, Abe J (2013) Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol 13:91
Xu M, Yamagishi N, Zhao C, Takeshima R, Kasai M, Watanabe S, Kanazawa A, Yoshikawa N, Liu B, Yamada T, Abe J (2015) The soybean-specific maturity gene E1 family of floral repressors controls night-break responses through down-regulation of flowering locus t orthologues. Plant Physiol 168:1735–1746
Zhai H, Lü S, Liang S, Wu H, Zhang X, Liu B, Kong F, Yuan X, Li J, Xia Z (2014) GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS One 9(2):e89030
Zhao C, Takeshima R, Zhu J, Xu M, Sato M, Watanabe S, Kanazawa A, Liu B, Kong F, Yamada T, Abe J (2016) A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a flowering locus T orthologue. BMC Plant Biol 16:20
Acknowledgements
This work was funded in part by the Canadian Field Crop Research Alliance (CFCRA) and Agriculture and Agri-Food Canada through the Growing Forward 2 Agri-Innovation Program and also by the Natural Sciences and Engineering Council of Canada (NSERC).
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Samanfar, B., Molnar, S.J., Charette, M. et al. Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean. Theor Appl Genet 130, 377–390 (2017). https://doi.org/10.1007/s00122-016-2819-7
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DOI: https://doi.org/10.1007/s00122-016-2819-7