Abstract
Soybean [Glycine max (L.) Merr.] is a short-day, photoperiod-sensitive crop. The vegetative growth period (V), reproductive growth period (R), whole growth period (V + R) and the ratio of growth period structure (R/V) are photoperiod traits critical to adaptability and yield in soybean. To thoroughly dissect the genetic basis of these growth period traits and their correlations, a panel of 277 soybean accessions were genotyped with a single nucleotide polymorphisms (SNPs) panel and phenotyped at three field environments over three years. A genome-wide association study found 28 SNPs on fifteen chromosomes with 33 significant marker-trait associations, eleven, eight, four and ten for V, R, V + R and R/V, respectively. Two SNPs, Map-6077 and -6502, showed pleiotropy in three and two traits, respectively. Map-6077, associated with V, R, and V + R, was a synonymous SNP of the GmMFT, a member of PEBP family that has been reported to inhibit seed germination and regulate oil content. These results provide candidate SNP markers and genes for further functional experiments to advance molecular marker-assisted breeding.
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The datasets analyzed during the current study are available in this article in Additional Tables S1 and S2.
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Abbreviations
- GWAS:
-
Genome-wide association study
- SNP:
-
Single nucleotide polymorphism
- QTL:
-
Quantitative trait loci
References
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint XXXaXXXrXiXXXv:14065823
Bernard RL (1971) Two major genes for time of flowering and maturity in soybeans 1. Crop Sci 11:242–244. https://doi.org/10.2135/cropsci1971.0011183X001100020022x
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Buzzell R, Voldeng H (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-daylength conditions. Can J Genet Cytol 13:703–707. https://doi.org/10.1139/g71-100
Chen Y, Lubberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15:454–461. https://doi.org/10.1016/j.tplants.2010.05.004
Cheng L et al (2011) Genetic analysis and QTL detection of reproductive period and post-flowering photoperiod responses in soybean. Theor Appl Genet 123:421–429. https://doi.org/10.1007/s00122-011-1594-8
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. https://doi.org/10.1007/s00122-009-1228-6
Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Fang C et al (2017) Genome-wide association studies dissect the genetic networks underlying agronomical traits in soybean. Genome Biol 18:161. https://doi.org/10.1186/s13059-017-1289-9
Fehr WR, Caviness CE (1977) Stages of soybean development. Special Report. 87
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill 1. Crop Sci 11:929–931. https://doi.org/10.2135/cropsci1971.0011183X001100060051x
Gabriel S, Ziaugra L, Tabbaa D (2009) SNP genotyping using the Sequenom MassARRAY iPLEX platform. Current Protocols in Human Genetics 60:2.12. 11–12.12
Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19:460–470. https://doi.org/10.1016/j.tplants.2014.01.010
Garner WW, Allard HA (1927) Effect of short alternating periods of light and darkness on plant growth. Science 66:40–42. https://doi.org/10.1126/science.66.1697.40
Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR, Dean C (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 17:73–78. https://doi.org/10.1016/j.cub.2006.11.052
Haider W (2014) Exploring flowering gene networks in soybean and arabidopsis through transcriptome analysis. University of Illinois at Urbana-Champaign
Han T, Wu C, Tong Z, Mentreddy RS, Tan K, Gai J (2006) Postflowering photoperiod regulates vegetative growth and reproductive development of soybean. Environ Exp Bot 55:120–129. https://doi.org/10.1016/j.envexpbot.2004.10.006
Henderson CR (1975) Best linear unbiased estimation and prediction under a selection model. Biometrics 31:423–447
Hu Z, Zhang D, Zhang G, Kan G, Hong D, Yu D (2014) Association mapping of yield-related traits and SSR markers in wild soybean (Glycine soja Sieb. and Zucc.). Breed Sci 63:441–449. https://doi.org/10.1270/jsbbs.63.441
Jian SZTPW (1990) Preliminary study on the growth period structure of soybean varieties in the northeast of China. Soybean Science 3
Jung CH, Wong CE, Singh MB, Bhalla PL (2012) Comparative genomic analysis of soybean flowering genes. PLoS ONE 7:e38250. https://doi.org/10.1371/journal.pone.0038250
Kaeuffer R, Reale D, Coltman DW, Pontier D (2007) Detecting population structure using STRUCTURE software: effect of background linkage disequilibrium. Heredity (edinb) 99:374–380. https://doi.org/10.1038/sj.hdy.6801010
Kim KH et al (2020) Genome-wide association and epistatic interactions of flowering time in soybean cultivar. PloS one 15:e0228114
Kong FJ et al (2014) A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Sci 54:2529–2535. https://doi.org/10.2135/cropsci2014.03.0228
Kong LP et al (2018) Quantitative trait locus mapping of flowering time and maturity in soybean using Next-Generation Sequencing-Based analysis. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00995
Li C et al (2020) A domestication-associated gene GmPRR3b regulates the circadian clock and flowering time in soybean. Mol Plant 13:745–759. https://doi.org/10.1016/j.molp.2020.01.014
Li Q, Fan C, Zhang X, Wang X, Wu F, Hu R, Fu Y (2014) Identification of a soybean MOTHER OF FT AND TFL1 homolog involved in regulation of seed germination. PLoS ONE 9:e99642. https://doi.org/10.1371/journal.pone.0099642
Li YH et al (2018) Genome-wide association mapping of QTL underlying seed oil and protein contents of a diverse panel of soybean accessions. Plant Sci 266:95–101. https://doi.org/10.1016/j.plantsci.2017.04.013
Li YH, Reif JC, Ma YS, Hong HL, Liu ZX, Chang RZ, Qiu LJ (2015) Targeted association mapping demonstrating the complex molecular genetics of fatty acid formation in soybean. BMC Genomics 16:841. https://doi.org/10.1186/s12864-015-2049-4
Lin X, Liu B, Weller JL, Abe J, Kong F (2021) Molecular mechanisms for the photoperiodic regulation of flowering in soybean. J Integr Plant Biol 63:981–994. https://doi.org/10.1111/jipb.13021
Liu B et al (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol 153:198–210. https://doi.org/10.1104/pp.109.150607
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767
Liu X et al (2017) Genetic variation of world soybean maturity date and geographic distribution of maturity groups. Breed Sci 67:221–232. https://doi.org/10.1270/jsbbs.16167
Lu S et al (2017) Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet 49:773–779. https://doi.org/10.1038/ng.3819
Mao T et al (2017) Association mapping of loci controlling genetic and environmental interaction of soybean flowering time under various photo-thermal conditions. BMC Genomics 18:415. https://doi.org/10.1186/s12864-017-3778-3
Marcolino-Gomes J et al (2017) Functional characterization of a putative Glycine max ELF4 in transgenic Arabidopsis and its role during flowering control. Front Plant Sci 8:618. https://doi.org/10.3389/fpls.2017.00618
Matsumura H, Liu B, Abe J, Takahashi R (2008) AFLP mapping of soybean maturity gene E4. J Hered 99:193–197. https://doi.org/10.1093/jhered/esm114
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. https://doi.org/10.2135/cropsci1999.3961642x
Purcell S, Cherny SS, Sham PC (2003) Genetic Power Calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19:149–150. https://doi.org/10.1093/bioinformatics/19.1.149
Qiu L, Chang R, Liu Z, Guan R, Li Y (2006) Descriptors and data standard for soybean (Glycine spp.). China Agriculture Press, Beijing
Qiu L-J, Li Y-H, Guan R-X, Liu Z-X, Wang L-X, Chang R-Z (2009) Establishment, representative testing and research progress of soybean core collection and mini core collection. Acta Agron Sin 35:571–579. https://doi.org/10.3724/sp.J.1006.2009.00571
Qiu LJ, Xing LL, Guo Y, Wang J, Jackson SA, Chang RZ (2013) A platform for soybean molecular breeding: the utilization of core collections for food security. Plant Mol Biol 83:41–50. https://doi.org/10.1007/s11103-013-0076-6
Ray JD, Hinson K, Mankono JEB, Malo MF (1995) Genetic-control of a Long-Juvenile trait in soybean. Crop Sci 35:1001–1006. https://doi.org/10.2135/cropsci1995.0011183X003500040012x
Saindon G, Beversdorf WD, Voldeng HD (1989a) Adjustment of the soybean phenology using the E 4 locus. Crop Sci 29:1361–1365. https://doi.org/10.2135/cropsci1989.0011183X002900060006x
Saindon G, Voldeng HD, Beversdorf WD, Buzzell RI (1989b) Genetic control of long daylength response in soybean. Crop Sci 29:1436–1439. https://doi.org/10.2135/cropsci1989.0011183X002900060021x
Samanfar B et al (2017) Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean. Theor Appl Genet 130:377–390. https://doi.org/10.1007/s00122-016-2819-7
Sedivy EJ, Wu F, Hanzawa Y (2017) Soybean domestication: the origin, genetic architecture and molecular bases. New Phytol 214:539–553. https://doi.org/10.1111/nph.14418
Shu Y, Yu D, Wang D, Guo D, Guo C (2013) Genome-wide survey and expression analysis of the MADS-box gene family in soybean. Mol Biol Rep 40:3901–3911. https://doi.org/10.1007/s11033-012-2438-6
Si L et al (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447–456. https://doi.org/10.1038/ng.3518
Sonah H, O’Donoughue L, Cober E, 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. https://doi.org/10.1111/pbi.12249
Sung S, Schmitz RJ, Amasino RM (2006) A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20:3244–3248. https://doi.org/10.1101/gad.1493306
Suo H et al (2016) The AtDREB1A transcription factor up-regulates expression of a vernalization pathway gene, GmVRN1-like, delaying flowering in soybean. Acta Physiol Plant 38:137
Takeshima R et al (2016) A soybean quantitative trait locus that promotes flowering under long days is identified as FT5a, a FLOWERING LOCUS T ortholog. J Exp Bot 67:5247–5258. https://doi.org/10.1093/jxb/erw283
Tsubokura Y et al (2014) Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot 113:429–441. https://doi.org/10.1093/aob/mct269
Wang X et al (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48:1233–1241. https://doi.org/10.1038/ng.3636
Wang Y, Cheng LR, Leng JT, Wu CX, Shao GH, Hou WS, Han TF (2015a) Genetic analysis and quantitative trait locus identification of the reproductive to vegetative growth period ratio in soybean (Glycine max (L.) Merr.). Euphytica 201:275–284. https://doi.org/10.1007/s10681-014-1209-y
Wang Y, Wu C-X, Zhang X-M, Wang Y-P, Han T-F (2008) Effects of soybean major maturity genes under different photoperiods. Acta Agron Sin 34:1160–1168
Wang Z et al (2015b) Functional evolution of phosphatidylethanolamine binding proteins in soybean and Arabidopsis. Plant Cell 27:323–336. https://doi.org/10.1105/tpc.114.135103
Watanabe S, Harada K, Abe J (2012) Genetic and molecular bases of photoperiod responses of flowering in soybean. Breed Sci 61:531–543. https://doi.org/10.1270/jsbbs.61.531
Watanabe S et al (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262. https://doi.org/10.1534/genetics.108.098772
Watanabe S et al (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. https://doi.org/10.1534/genetics.110.125062
Xia Z et al (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:E2155-2164. https://doi.org/10.1073/pnas.1117982109
Xue WY et al (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767. https://doi.org/10.1038/ng.143
Yamamoto Y et al (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol 44:1119–1130. https://doi.org/10.1093/pcp/pcg148
Yang G et al (2017) QTL effects and epistatic interaction for flowering time and branch number in a soybean mapping population of JapanesexChinese cultivars. J Integr Agric 16:1900–1912
Yang Y, Gai J, Ma Y (1994) Differential inheritance of crowth period traits under different planting seasons in soybean. Zhongguo Nongye Kexue 27:1–6
Yue Y et al (2017) A Single nucleotide eeletion in J encoding GmELF3 confers long juvenility and is associated with adaption of tropic soybean. Mol Plant 10:656–658. https://doi.org/10.1016/j.molp.2016.12.004
Zeng X et al (2018) Soybean MADS-box gene GmAGL1 promotes flowering via the photoperiod pathway. BMC Genomics 19:51. https://doi.org/10.1186/s12864-017-4402-2
Zhang J, Song Q, Cregan PB, Nelson RL, Wang X, Wu J, Jiang GL (2015) Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genomics 16:217. https://doi.org/10.1186/s12864-015-1441-4
Zhang X et al (2018) Genome-wide association studies of soybean seed hardness in the Chinese Mini Core Collection. Plant Mol Biol Report 36:605–617. https://doi.org/10.1007/s11105-018-1102-2
Zhao C et al (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 Biol 16:20. https://doi.org/10.1186/s12870-016-0704-9
Zhou L et al (2016) Identification and validation of candidate genes associated with domesticated and improved traits in soybean. Plant Genome. https://doi.org/10.3835/plantgenome2015.09.0090
Acknowledgements
This research was supported by the National Key R & D Program for Crop Breeding (2020YFE0202300 and 2016YFD0100201), the Platform of National Crop Germplasm Resources of China (No. 2016-004 and 2017-004) and the Agricultural Science and Technology Innovation Program (ASTIP) of Chinese Academy of Agricultural Sciences (CAAS-ZDRW202109).
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Y-F.L., Y-H.L., S.J., and L.Q. conceived the study and jointly wrote the paper; Y-F.L. performed the GWAS, genotype data processing, population structure analysis and relative analyses. H.H. and Z.L. carried out the phenotypic evaluation; Y.M. analyzed the phenotypic data; All authors read and approved the final manuscript.
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Li, Y., Li, Yh., Hong, H. et al. Dissecting four correlated growth period traits using a genome-wide association study approach in soybean. Genet Resour Crop Evol 69, 1147–1162 (2022). https://doi.org/10.1007/s10722-021-01293-3
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DOI: https://doi.org/10.1007/s10722-021-01293-3