Please wait a minute...
Journal of Integrative Agriculture  2017, Vol. 16 Issue (09): 1900-1912    DOI: 10.1016/S2095-3119(16)61539-3
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
QTL effects and epistatic interaction for flowering time and branch number in a soybean mapping population of Japanese×Chinese cultivars
YANG Guang1, 4*, ZHAI Hong2*, WU Hong-yan2, ZHANG Xing-zheng2, 3, LÜ Shi-xiang5, WANG Ya-ying2, 3, LI Yu-qiu2, 3, HU Bo2, WANG Lu2, 3, WEN Zi-xiang6, WANG De-chun6, WANG Shao-dong7, Kyuya Harada8, XIA Zheng-jun2, XIE Fu-ti1
1 Soybean Research Institute, Shenyang Agricultural University, Shenyang 110866, P.R.China
2 Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, P.R.China
3 University of Chinese Academy of Sciences, Beijing 100049, P.R.China
4 Institute of Economic Crop of Liaoning, Liaoyang 111000, P.R.China
5 Information Center, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, P.R.China
6 Department of Plant, Soil and Microbial Sciences, Michigan State University East Lansing, Michigan 48824, USA
7 National Research Center of Soybean Engineering and Technology, Northeast Agricultural University, Harbin 150028, P.R.China
8 Graduate School of Engineering, Osaka University, Suita 565-0871, Japan
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract     Flowering time and branching type are important agronomic traits related to the adaptability and yield of soybean. Molecular bases for major flowering time or maturity loci, E1 to E4, have been identified. However, more flowering time genes in cultivars with different genetic backgrounds are needed to be mapped and cloned for a better understanding of flowering time regulation in soybean. In this study, we developed a population of Japanese cultivar (Toyomusume)×Chinese cultivar (Suinong 10) to map novel quantitative trait locus (QTL) for flowering time and branch number. A genetic linkage map of a F2 population was constructed using 1 306 polymorphic single nucleotide polymorphism (SNP) markers using Illumina SoySNP8k iSelect BeadChip containing 7 189 (SNPs). Two major QTLs at E1 and E9, and two minor QTLs at a novel locus, qFT2_1 and at E3 region were mapped. Using other sets of F2 populations and their derived progenies, the existence of a novel QTL of qFT2_1 was verified. qBR6_1, the major QTL for branch number was mapped to the proximate to the E1 gene, inferring that E1 gene or neighboring genetic factor is significantly contributing to the branch number.
Keywords:  soybean        quantitative trait loci        SNP        flowering time        branch number  
Received: 22 August 2016   Accepted:

This work was supported by the National Key Research and Development Program of China (2016YFD0100201 and 2016YFD0101902), the Knowledge Innovation Project of Chinese Academy of Sciences (XDA08010105), and the National Natural Science Foundation of China (31471518 and 31301338).

Corresponding Authors:  Correspondence XIE Fu-ti, Tel/Fax: +86-24-88487135, E-mail:; XIA Zheng-jun, Tel: +86-451-87501708, Fax: +86-451-86603736, E-mail:    
About author:  YANG Guang, E-mail:;

Cite this article: 

YANG Guang, ZHAI Hong, WU Hong-yan, ZHANG Xing-zheng, Lü Shi-xiang, WANG Ya-ying, LI Yu-qiu, HU Bo, WANG Lu, WEN Zi-xiang, WANG De-chun, WANG Shao-dong, Kyuya Harada, XIA Zheng-jun, XIE Fu-ti. 2017. QTL effects and epistatic interaction for flowering time and branch number in a soybean mapping population of Japanese×Chinese cultivars. Journal of Integrative Agriculture, 16(09): 1900-1912.

Akond M, Liu S, Schoener L, Anderson J A, Kantartzi S K, Meksem K, Song Q, Wang D, Wen Z, Lightfoot D A. 2013. A SNP-based genetic linkage map of soybean using the SoySNP6K Illumina Infinium BeadChip genotyping array. Plant Genome Sciences, 1, 80–89.

Bernard R. 1971. Two major genes for time of flowering and maturity in soybeans. Crop Science, 11, 242–244.

Bonato E R, Vello N A. 1999. E-6, a dominant gene conditioning early flowering and maturity in soybeans. Genetics and Molecular Biology, 22, 229–232.

Buzzell R. 1971. Inheritance of a soybean flowering response to fluorescent-daylength conditions. Canadian Journal of Genetics and Cytology, 13, 703–707.

Buzzell R, Voldeng H. 1980. Inheritance of insensitivity to long daylength. Soybean Genetics Newsletter, 7, 26–29.

Carpenter A C, Board J E. 1997. Branch yield components controlling soybean yield stability across plant populations. Crop Science, 37, 885–891.

Chen Q S, Zhang Z C, Liu C Y, Xin D W, Qiu H M, Shan D P, Shan C Y, Hu G H. 2007. QTL analysis of major agronomic traits in soybean. Agricultural Sciences in China, 6, 399–405.

Choi I Y, Hyten D L, Matukumalli L K, Song Q J, Chaky J M, Quigley C V, Chase K, Lark K G, Reiter R S, Yoon M S, Hwang E Y, Yi S I, Young N D, Shoemaker R C, van Tassell C P, Specht J E, Cregan P B. 2007. A soybean transcript map: Gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics, 176, 685–696.

Cober E R, Molnar S J, Charette M, Voldeng H D. 2010. A new locus for early maturity in soybean. Crop Science, 50, 524–527.

Cober E R, Tanner J W, Voldeng H D. 1996a. Genetic control of photoperiod response in early-maturing, near-isogenic soybean lines. Crop Science, 36, 601–605.

Cober E R, Tanner J W, Voldeng H D. 1996b. Soybean photoperiod-sensitivity loci respond differentially to light quality. Crop Science, 36, 606–610.

Cober E R, Voldeng H D. 2001. A new soybean maturity and photoperiod-sensitivity locus linked to E1 and T. Crop Science, 41, 698–701.

Fan S X, Li B, Yu F K, Han F X, Yan S R, Wang L Z, Sun J M. 2015. Analysis of additive and epistatic quantitative trait loci underlying fatty acid concentrations in soybean seeds across multiple environments. Euphytica, 206, 689–700.

Fehr W R, Caviness C E, Burmood D T, Penningt J S. 1971. Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Science, 11, 929–931.

Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Coupland G, Putterill J. 1999. GIGANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. The EMBO Journal, 18, 4679–4688.

He Q Y, Yang H Y, Xiang S H, Wang W B, Xing G N, Zhao T J, Gai J Y. 2014. QTL mapping for the number of branches and pods using wild chromosome segment substitution lines in soybean [Glycine max (L.) Merr.]. Plant Genetic Resources-Characterization and Utilization, 12, S172–S177.

Hyten D L, Cannon S B, Song Q J, Weeks N, Fickus E W, Shoemaker R C, Specht J E, Farmer A D, May G D, Cregan P B. 2010a. High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genomics, 11, 38.

Hyten D L, Choi I Y, Song Q J, Specht J E, Carter T E, Shoemaker R C, Hwang E Y, Matukumalli L K, Cregan P B. 2010b. A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Science, 50, 960–968.

Kawasaki S, Murakami Y. 2000. Genome analysis of Lotus japonicus. Journal of Plant Research, 113, 497–506.

Kim M Y, Lee S, Van K, Kim T H, Jeong S C, Choi I Y, Kim D S, Lee Y S, Park D, Ma J, Kim W Y, Kim B C, Park S, Lee K A, Kim D H, Kim K H, Shin J H, Jang Y E, Do Kim K, Liu W X, et al. 2010. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proceedings of the National Academy of Sciences of the United States of America, 107, 22032–22037.

Kong F J, Liu B H, Xia Z J, Sato S, Kim B M, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, Abe J. 2010. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiology, 154, 1220–1231.

Kong F J, Nan H Y, Cao D, Li Y, Wu F F, Wang J L, Lu S J, Yuan X H, Cober E R, Abe J, Liu B H. 2014. A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Science, 54, 2529–2535.

Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart C J, Peeters A J M. 1998. Genetic interactions among late-flowering mutants of Arabidopsis. Genetics, 148, 885–892.

Kumar S, Roder M S, Tripathi S B, Kumar S, Chand R, Joshi A K, Kumar U. 2015. Mendelization and fine mapping of a bread wheat spot blotch disease resistance QTL. Molecular Breeding, 35, 218.

Lam H M, Xu X, Liu X, Chen W B, Yang G H, Wong F L, Li M W, He W M, Qin N, Wang B, Li J, Jian M, Wang J A, Shao G H, Wang J, Sun S S M, Zhang G Y. 2010. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics, 42, 1053–1059.

Li W, Zheng D H, Van K, Lee S H. 2008. QTL mapping for major agronomic traits across two years in soybean (Glycine max L. Merr.). Journal of Crop Science and Biotechnology, 11, 171–190.

Li Y H, Zhao S C, Ma J X, Li D, Yan L, Li J, Qi X T, Guo X S, Zhang L, He W M, Chang R Z, Liang Q S, Guo Y, Ye C, Wang X B, Tao Y, Guan R X, Wang J Y, Liu Y L, Jin L G, et al. 2013. Molecular footprints of domestication and improvement in soybean revealed by whole genome re-sequencing. BMC Genomics, 14, 579.

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.

Mcblain B A, Bernard R L. 1987. A new gene affecting the time of flowering and maturity in soybeans. Journal of Heredity, 78, 160–162.

Meng L, Li H, Zhang L, Wang J. 2015. QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. The Crop Journal, 3, 269–283.

Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, Coupland G. 2005. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. The Plant Cell, 17, 2255–2270.

Murray M G, Thompson W F. 1980. Rapid isolation of high molecular-weight plant DNA. Nucleic Acids Research, 8, 4321–4325.

Nelson R. 1996. The inheritance of a branching type in soybean. Crop Science, 36, 1150–1152.

Van Ooijen J. 2004. MapQTL®5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen.

Owen F V. 1927. Inheritance studies in soybeans. II. Glabrousness, color of pubescence, time of maturity, and linkage relations. Genetics, 12, 519–529.

Panthee D R, Pantalone V R, Saxton A M, West D R, Sams C E. 2007. Quantitative trait loci for agronomic traits in soybean. Plant Breeding, 126, 51–57.

Saindon G, Voldeng H, Beversdorf W, Buzzell R. 1989. Genetic control of long daylength response in soybean. Crop Science, 29, 1436–1439.

Sayama T, Hwang T Y, Yamazaki H, Yamaguchi N, Komatsu K, Takahashi M, Suzuki C, Miyoshi T, Tanaka Y, Xiao Z J, Tsubokura Y, Watanabe S, Harada K, Funatsuki H, Ishimoto M. 2010. Mapping and comparison of quantitative trait loci for soybean branching phenotype in two locations. Breeding Science, 60, 380–389.

Schmutz J, Cannon S B, Schlueter J, Ma J X, Mitros T, Nelson W, Hyten D L, Song Q J, Thelen J J, Cheng J L, Xu D, Hellsten U, May G D, Yu Y, Sakurai T, Umezawa T, Bhattacharyya M K, Sandhu D, Valliyodan B, Lindquist E, et al. 2010. Genome sequence of the palaeopolyploid soybean. Nature, 463, 178–183.

Song Q J, Hyten D L, Jia G F, Quigley C V, Fickus E W, Nelson R L, Cregan P B. 2013. Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLOS ONE, 8, e54985.

Song Q J, Hyten D L, Jia G F, Quigley C V, Fickus E W, Nelson R L, Cregan P B. 2015. Fingerprinting soybean germplasm and its utility in genomic research. G3: Genes Genomes Genetics, 5, 1999–2006.

Song Q J, Jia G F, Zhu Y L, Grant D, Nelson R T, Hwang E Y, Hyten D L, Cregan P B. 2010. Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Science, 50, 1950–1960.

Tsubokura Y, Watanabe S, Xia Z J, 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. Annals of Botany, 113, 429–441.

Wang D, Zhu J, Li Z, Paterson A. 1999. Mapping QTLs with epistatic effects and QTL×environment interactions by mixed linear model approaches. Theoretical and Applied Genetics, 99, 1255–1264.

Watanabe S, Hideshima R, Xia Z J, 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, Tajuddin T, Yamanaka N, Hayashi M, Harada K. 2004. Analysis of QTLs for reproductive development and seed quality traits in soybean using recombinant inbred lines. Breeding Science, 54, 399–407.

Watanabe S, Xia Z J, 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.

Xia Z, Tsubokura Y, Hoshi M, Hanawa M, Yano C, Okamura K, Ahmed T A, Anai T, Watanabe S, Hayashi M, Kawai T, Hossain K G, Masaki H, Asai K, Yamanaka N, Kubo N, Kadowaki K I, Nagamura Y, Yano M, Sasaki T, et al. 2007. An integrated high-density linkage map of soybean with RFLP, SSR, STS, and AFLP markers using a single F2 population. DNA Research, 14, 257–269.

Xia Z J, Watanabe S, Yamada T, Tsubokura Y, Nakashima H, Zhai H, Anai T, Sato S, Yamazaki T, Lu S X, Wu H Y, Tabata S, Harada K. 2012. 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, 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 Biology, 13, 91.

Yamanaka N, Ninomiya S, Hoshi M, Tsubokura Y, Yano M, Nagamura Y, Sasaki T, Harada K. 2001. An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. DNA Research, 8, 61–72.

Zhai H, Lu S X, Wang Y Q, Chen X, Ren H X, Yang J Y, Cheng W, Zong C M, Gu H P, Qiu H M, Wu H Y, Zhang X Z, Cui T T, Xia Z J. 2014. 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, 9, e97636.

Zhao C, Takeshima R, Zhu J, Xu M, Sato M, Watanabe S, Kanazawa A, Liu B, Kong F, Yamada T. 2016. 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 Biology, 16, 1.
[1] YANG Hong-jun, YE Wen-wu, YU Ze, SHEN Wei-liang, LI Su-zhen, WANG Xing, CHEN Jia-jia, WANG Yuan-chao, ZHENG Xiao-bo. Host niche, genotype, and field location shape the diversity and composition of the soybean microbiome[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2412-2425.
[2] XU Lei, ZHAO Tong-hua, Xing Xing, XU Guo-qing, XU Biao, ZHAO Ji-qiu.

Model fitting of the seasonal population dynamics of the soybean aphid, Aphis glycines Matsumura, in the field [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1797-1808.

[3] GAO Hua-wei, YANG Meng-yuan, YAN Long, HU Xian-zhong, HONG Hui-long, ZHANG Xiang, SUN Ru-jian, WANG Hao-rang, WANG Xiao-bo, LIU Li-ke, ZHANG Shu-zhen, QIU Li-juan. Identification of tolerance to high density and lodging in short petiolate germplasm M657 and the effect of density on yield-related phenotypes of soybean[J]. >Journal of Integrative Agriculture, 2023, 22(2): 434-446.
[4] QU Zheng, LI Yue-han, XU Wei-hui, CHEN Wen-jing, HU Yun-long, WANG Zhi-gang. Different genotypes regulate the microbial community structure in the soybean rhizosphere[J]. >Journal of Integrative Agriculture, 2023, 22(2): 585-597.
[5] GAO Hua-wei, SUN Ru-jian, YANG Meng-yuan, YAN Long, HU Xian-zhong, FU Guang-hui, HONG Hui-long, GUO Bing-fu, ZHANG Xiang, LIU Li-ke, ZHANG Shu-zhen, QIU Li-juan. Characterization of the petiole length in soybean compact architecture mutant M657 and the breeding of new lines[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2508-2520.
[6] ZHANG Hua, WU Hai-yan, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying. Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2521-2537.
[7] ZOU Jia-nan, ZHANG Zhan-guo, KANG Qing-lin, YU Si-yang, WANG Jie-qi, CHEN Lin, LIU Yan-ru, MA Chao, ZHU Rong-sheng, ZHU Yong-xu, DONG Xiao-hui, JIANG Hong-wei, WU Xiao-xia, WANG Nan-nan, HU Zhen-bang, QI Zhao-ming, LIU Chun-yan, CHEN Qing-shan, XIN Da-wei, WANG Jin-hui. Characterization of chromosome segment substitution lines reveals candidate genes associated with the nodule number in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2197-2210.
[8] PAN Wen-jing, HAN Xue, HUANG Shi-yu, YU Jing-yao, ZHAO Ying, QU Ke-xin, ZHANG Ze-xin, YIN Zhen-gong, QI Hui-dong, YU Guo-long, ZHANG Yong, XIN Da-wei, ZHU Rong-sheng, LIU Chun-yan, WU Xiao-xia, JIANG Hong-wei, HU Zhen-bang, ZUO Yu-hu, CHEN Qing-shan, QI Zhao-ming. Identification of candidate genes related to soluble sugar contents in soybean seeds using multiple genetic analyses[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1886-1902.
[9] LIU Chen, TIAN Yu, LIU Zhang-xiong, GU Yong-zhe, ZHANG Bo, LI Ying-hui, NA Jie, QIU Li-juan. Identification and characterization of long-InDels through whole genome resequencing to facilitate fine-mapping of a QTL for plant height in soybean (Glycine max L. Merr.)[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1903-1912.
[10] HUI Fang, XIE Zi-wen, LI Hai-gang, GUO Yan, LI Bao-guo, LIU Yun-ling, MA Yun-tao. Image-based root phenotyping for field-grown crops: An example under maize/soybean intercropping[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1606-1619.
[11] TIAN Yu, YANG Lei, LU Hong-feng, ZHANG Bo, LI Yan-fei, LIU Chen, GE Tian-li, LIU Yu-lin, HAN Jia-nan, LI Ying-hui, QIU Li-juan. QTL analysis for plant height and fine mapping of two environmentally stable QTLs with major effects in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(4): 933-946.
[12] LIU Sang-lin, CHENG Yan-bo, MA Qi-bin, LI Mu JIANG Ze, XIA Qiu-ju, NIAN Hai. Fine mapping and genetic analysis of resistance genes, Rsc18, against soybean mosaic virus[J]. >Journal of Integrative Agriculture, 2022, 21(3): 644-653.
[13] LIU Li-feng, GAO Le, ZHANG Li-xin, CAI Yu-peng, SONG Wen-wen, CHEN Li, YUAN Shan, WU Ting-ting, JIANG Bing-jun, SUN Shi, WU Cun-xiang, HOU Wen-sheng, HAN Tian-fu. Co-silencing E1 and its homologs in an extremely late-maturing soybean cultivar confers super-early maturity and adaptation to high-latitude short-season regions[J]. >Journal of Integrative Agriculture, 2022, 21(2): 326-335.
[14] OCHAR Kingsley, SU Bo-hong, ZHOU Ming-ming, LIU Zhang-xiong, GAO Hua-wei, SOBHI F. Lamlom, QIU Li-juan. Identification of the genetic locus associated with the crinkled leaf phenotype in a soybean (Glycine max L.) mutant by BSA-Seq technology[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3524-3539.
[15] JIA Jia, WANG Huan, CAI Zhan-dong, WEI Ru-qian, HUANG Jing-hua, XIA Qiu-ju, XIAO Xiao-hui, MA Qi-bin, NIAN Hai, CHENG Yan-bo. Identification and validation of stable and novel quantitative trait loci for pod shattering in soybean [Glycine max (L.) Merr.][J]. >Journal of Integrative Agriculture, 2022, 21(11): 3169-3184.
No Suggested Reading articles found!