Abstract
Flowering time, as an important ecological trait related to photoperiod response, maturity, and final yield, is a complex trait conferred by multiple genes. To further elucidate the genetic mechanism for the flowering time, quantitative trait loci (QTLs) related to the flowering time and maturity were identified utilizing specific-locus amplified fragment sequencing (SLAF-Seq) technology. In total, we identified three QTLs on chromosomes 5, 6, and 7 from a recombinant inbred line (RIL) population of 171 individuals derived from a cross between Minsoy and Archer soybeans. Of these QTLs, one new QTL on chromosome 7, called E11, was simultaneously detected in an ~ 1.03 Mb region from the F6 and F8 generations of the RIL population, and accounted for ~ 15% of the total phenotypic variation over 2 years. The gene symbol E11e11 had been approved by the soybean genetic committee. The segregation patterns observed in residual heterozygous lines (RHLs) at the E11 locus revealed that early flowering was controlled by a single dominant gene. The gene was fine-mapped to an ~ 138 kb interval, including 11 genes based on the reference genome. Through amino acid sequence analysis, three most likely candidate genes, Glyma.07 g048500, Glyma.07 g049000, and Glyma.07 g049200, were identified. The phenotypes detected from two near-isogenic lines (NILs) revealed that NILs for E11 allele significantly promoted the flowering time and maturity than NILs for the e11 under the long-day (LD) conditions. These results suggest that E11 is a new flowering time gene that will be valuable in improving our understanding of the mechanism for the flowering time and molecular breeding.





Similar content being viewed by others
References
Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
Armbruster U, Labs M, Pribil M, Viola S, Xu W, Scharfenberg M, Hertle AP, Rojahn U, Jensen PE, Rappaport F, Joliot P, Dörmann P, Wanner G, Leister D (2013) Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25:2661–2678
Arrivault S, Senger T, Krämer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376
Berkman SJ, Roscoe EM, Bourret JC (2018) Comparing self-directed methods for training staff to create graphs using Graphpad prism. J Appl Behav Anal 52:188–204
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 News 17:26–29
Buzzell RI (1971) Inheritance of a soybean flowering response to fluorescent day length conditions. Can J Genet Cytol 13:703–707
Cao D, Takeshima R, Zhao C, Liu B, Jun A, Kong F (2017) Molecular mechanisms of flowering under long days and stem growth habit in soybean. J Exp Bot 68:1873–1884
Cheng CK, Cheung MK, Nong W, Law PT, Qin J, Ling JM, Kam KM, Cheung WM, Kwan HS (2015) Next generation genome sequencing reveals phylogenetic clades with different level of virulence among Salmonella Typhimurium clinical human isolates in Hong Kong. BMC Genomics 16:688
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 (2001) A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Sci 41:698–701
Cober ER, Tanner JW, Voldeng HD (1996) Genetic control of photoperiod response in early-maturing, near-isogenic soybean lines. Crop Sci 36:601–605
Cober ER, Molnar SJ, Charette M, Voldeng HD (2010) A new locus for early maturity in soybean. Crop Sci 50:524–527
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379
Fehr WR (1987) Principles of cultivar development. Macmillan, London
Fehr WR, Caviness CE, Bumood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max L. Merrill. Crop Sci 11:929–931
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550
Githiri SM, Yang D, Khan NA, Xu D, Komatsuda T, Takahashi R (2007) QTL analysis of low temperature induced browning in soybean seed coats. J Hered 98:360–366
Han YP, Li DM, Zhu D, Li HY, Li XP, Teng WL, Li WB (2012) QTL analysis of soybean seed weight across multi-genetic backgrounds and environments. Theor Appl Genet 125:671–683
Hansson M, Vener AV (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2:550–559
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
Kong L, Lu S, Wang Y, Fang C, Wang F, Nan H, Su T, Li S, Zhang F, Li X, Zhao X, Yuan X, Liu B, Kong F (2018) Quantitative trait locus mapping of flowering time and maturity in soybean using next-generation sequencing-based analysis. Front Plant Sci 9:995
Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 4:713–714
Li S, Li R, Li H, Lu J, Li Y, Bolund L, Schierup MH, Wang J (2013) SOAPindel: efficient identification of indels from short paired reads. Genome Res 23:195–200
Li B, Tian L, Zhang J, Huang L, Han F, Yan S, Wang L, Zheng H, Sun J (2014) Construction of a high-density genetic map based on large-scale markers developed by specific length amplified fragment sequencing (SLAF-seq) and its application to QTL analysis for isoflavone content in Glycine max. BMC Genomics 15:1086
Li X, Fang C, Xu M, Zhang F, Lu S, Nan H et al (2017) Quantitative trait locus mapping of soybean maturity gene E6. Crop Sci 57:1–8
Liu B, Fujita T, Yan ZH, Sakamoto S, Xu D, Abe J (2007) QTL mapping of domestication-related traits in soybean (Glycine max). Ann Bot 100:1027–1038
Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome a gene. Genetics 180:995–1007
Liu D, Ma C, Hong W, Huang L, Liu M, Liu H, Zeng H, Deng D, Xin H, Song J, Xu C, Sun X, Hou X, Wang X, Zheng H (2014) Construction and analysis of high-density linkage map using high throughput sequencing data. PLoS One 9:e98855
Liu D, Yan Y, Fujita Y, Xu D (2018) A major QTL (qFT12.1) allele from wild soybean delays flowering time. Mol Breed 38:45
Lu SJ, Zhao XH, Hu YL, Liu SL, Nan HY, Li XM, Fang C, Cao D, Shi XY, Kong LP, Su T, Zhang FG, Li SC, Wang Z, Yuan XH, Cober ER, Weller JL, Liu BH, Hou XL, Tian ZX, Kong FJ (2017) Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet 49:773–779
Manly KF, Cudmore RH Jr, Meer JM (2001) Map manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932
Mansur LM, Lark KG, Kross H, Oliveira A (1993) Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean (Glycine max L.). Theor Appl Genet 86:907–13
McBlain BA, Bernard RL (1987) A new gene affecting the time of flowering and maturity in soybeans. J Hered 78:160–162
Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carré IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641
Orf JH, Chase K, Jarvik T, Mansur LM, Cregan PB, Adler FR, Lark KG (1999) Genetics of soybean agronomic traits: I comparison of three related recombinant inbred populations. Crop Sci 39:1642–1651
Panthee DR, Pantalone VR, Saxton AM, West DR, Sams CE (2007) Quantitative trait loci for agronomic traits in soybean. Plant Breed 126:51–57
Ray JD, Hinson K, Mankono JEB, Malo MF (1995) Genetic control of a long-juvenile trait in soybean. Crop Sci 35:1001–1006
Rychel S, Książkiewicz M, Tomaszewska M, Bielski W, Wolko B (2019) FLOWERING LOCUS T, GIGANTEA, SEPALLATA, and FRIGIDA homologs are candidate genes involved in white lupin (Lupinus albus L.) early flowering. Mol Breed 39:43
Samanfar B, Molnar SJ, Charette M, Schoenrock A, Dehne F, Golshani A, Belzile F, Cober ER (2017) Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean. Theor Appl Genet 130:377–390
Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229
Spensley M, Kim JY, Picot E, Reid J, Ott S, Helliwell C, Carré IA (2009) Evolutionarily conserved regulatory motifs in the promoter of the Arabidopsis clock gene LATE ELONGATED HYPOCOTYL. Plant Cell 21:2606–2623
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8:e58700
Tsubokura Y, Matsumura H, Xu M, Liu B, Nakashima H, Anai T, Kong F, Yuan X, Kanamori H, Katayose Y, Takahashi R, Harada K, Abe J (2013) Genetic variation in soybean at the maturity locus E4 is involved in adaptation to long days at high latitudes. Agronomy 3:117–134
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
Van Ooijen JW (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen
Wang D, Graef GL, Procopiuk AM, Diers BW (2004) Identification of putative QTL that underlie yield in interspecific soybean backcross populations. Theor Appl Genet 108:458–467
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
Watanabe S, Harada K, Abe J (2012) Genetic and molecular bases of photoperiod responses of flowering in soybean. Breed Sci 61:531–543
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 U S A 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(9):91
Xu G, Jiang Z, Wang H, Lin R (2018) The central circadian clock proteins CCA1 and LHY regulate iron homeostasis in Arabidopsis. J Integr Plant Biol 61:168–181
Ye K, Schulz MH, Long Q, Apweiler R, Ning Z (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25:2865–2871
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
Acknowledgments
We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Funding
This work was funded by the Natural Key R&D Program of China (2017YFE0111000 and 2016YFD0100400), the National Natural Science Foundation of China (No.31725021, 31701445, 31801384, 31771815), and the National Natural Science Foundation of Heilongjiang Province (No. QC2014C036).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
The authors declare that this study complies with the current laws of the countries in which the experiments were performed.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 182 kb)
ESM 2
Fig. S1 Frequency distribution of days to flowering in two RHL families, (A) #13 and (B) #131, grown during 2017 in Harbin, China. Fig. S2 Frequency distribution of days to maturity in two RHL families, (A) #13 and (B) #131, grown during 2017 in Harbin, China. Fig. S3 The genotypes of the NILs for E11 derived from the cross between Minsoy and Archer. Molecular markers and their genomic positions were shown in Chr7. (PDF 98 kb)
Rights and permissions
About this article
Cite this article
Wang, F., Nan, H., Chen, L. et al. A new dominant locus, E11, controls early flowering time and maturity in soybean. Mol Breeding 39, 70 (2019). https://doi.org/10.1007/s11032-019-0978-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-019-0978-3


