Abstract
Soybean mosaic virus (SMV) threatens soybean (Glycine max (L.) Merr.) production and seed quality worldwide. Host plant resistance is the most environmentally friendly and economically effective method to deduce the damages of SMV. However, the use of limited resistant loci in SMV management will be conquered due to SMV strain shifts caused by evolutionary arms races. Thus, exploration of novel germplasms of SMV resistance and identification of novel resistant genes are necessary. In this study, we inoculated 219 soybean accessions with a SC3 virus strain in three environments. A genome-wide association study was conducted with 355K SoySNP array to dissect the genetic basis of SMV resistance. A total of 24 SNPs significantly associated with resistance to SC3 were identified, and these SNPs explained 25.54–33.60% of the phenotypic variations. Many significant SNPs were located near to the known SMV resistance loci Rsv1, Rsv4, and Rsv5. Furthermore, one SNP on chromosome 8 and four SNPs on chromosome 20 were novel loci. Three genes underlying these two novel loci with different genetic variation between resistant and susceptible accessions and with high expression levels in leaf were identified as promising candidate genes. Therefore, the novel loci and candidate genes were identified as new genetic sources for marker-assisted selection breeding in soybean.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams MJ, Antoniw JF, Fauquet CM (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150:459–479. https://doi.org/10.1007/s00705-004-0440-6
Bai L, Li HC, Ma Y et al (2009) Inheritance and gene mapping of resistance to soybean mosaic virus strain SC- 11 in soybean. Soybean Sci 28:1–6. https://doi.org/10.1111/j.1744-7909.2006.00365.x
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265. https://doi.org/10.1093/bioinformatics/bth457
Buss GR, Ma G, Chen P, Tolin SA (1997) Registration of LN92-12033 and LN92-12054 soybean germplasm lines near-isogenic for brown stem rot resistance gene Rbs2. Crop Sci 37:1987–1987. https://doi.org/10.2135/cropsci1997.0011183x003700060067x
Cai C, Jiang X, Zhao C, Ma J (2014) Sequence analysis of the coat protein gene of Chinese soybean mosaic virus strain SC7 and comparison with those of SMV strains from the USA. Bing Du Xue Bao 30:489–494. https://doi.org/10.13242/j.cnki.bingduxuebao.002537
Chang F, Guo C, Sun F, Zhang J, Wang Z, Kong J, He Q, Sharmin RA, Zhao T (2018) Genome-wide association studies for dynamic plant height and number of nodes on the main stem in summer sowing soybeans. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.01184
Che Z, Liu H, Yi F, Cheng H, Yang Y, Wang L, du J, Zhang P, Wang J, Yu D (2017) Genome-wide association study reveals novel loci for SC7 resistance in a soybean mutant panel. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.01771
Chen H, Adam Arsovski A, Yu K, Wang A (2017) Deep sequencing leads to the identification of eukaryotic translation initiation factor 5A as a key element in Rsv1-mediated lethal systemic hypersensitive response to soybean mosaic virus infection in soybean. Mol Plant Pathol 18:391–404. https://doi.org/10.1111/mpp.12407
Cho E-K, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467. https://doi.org/10.1094/Phyto-69-467
Chu S, Wang J, Zhu Y, Liu S, Zhou X, Zhang H, Wang CE, Yang W, Tian Z, Cheng H, Yu D (2017) An R2R3-type MYB transcription factor, GmMYB29, regulates isoflavone biosynthesis in soybean. PLoS Genet 13:1–26. https://doi.org/10.1371/journal.pgen.1006770
Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS One 9:9–13. https://doi.org/10.1371/journal.pone.0111988
Devarenne TP, Ekengren SK, Pedley KF, Martin GB (2006) Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J 25:255–265. https://doi.org/10.1038/sj.emboj.7600910
Ellis M, Wang H, Paul P et al (2012) Identification of soybean genotypes resistant to and genetic mapping of resistance quantitative trait loci in the cultivar Conrad. Crop Sci 52:2224–2233. https://doi.org/10.2135/cropsci2011.11.0624
Gong ZZ (2020) Flowering phenology as a core domestication trait in soybean. J Integr Plant Biol 62:546–549. https://doi.org/10.1111/jipb.12934
Gore MA, Hayes AJ, Jeong SC, Yue YG, Buss GR, Maroof MAS (2002) Mapping tightly linked genes controlling potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome 45:592–599. https://doi.org/10.1139/g02-009
Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326:1115–1117. https://doi.org/10.1126/science.1177837
Guo D, Zhi H, Wang Y et al (2005) Identification and distribution of strains of soybean mosaic virus in middle and northern of HuangHuai Region of China. Chin J Oil Crop Sci 27:64–68. https://doi.org/10.3321/j.issn:1007-9084.2005.04.015
Hayes AJ, Ma G, Buss GR, Maroof MAS (2000) Molecular marker mapping of RSV4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Sci 40:1434–1437. https://doi.org/10.2135/cropsci2000.4051434x
Hayes AJ, Jeong SC, Gore MA, Yu YG, Buss GR, Tolin SA, Maroof MAS (2004) Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics 166:493–503. https://doi.org/10.1534/genetics.166.1.493
Hernández JA, Gullner G, Clemente-Moreno MJ, Künstler A, Juhász C, Díaz-Vivancos P, Király L (2016) Oxidative stress and antioxidative responses in plant–virus interactions. Physiol Mol Plant Pathol 94:134–148. https://doi.org/10.1016/j.pmpp.2015.09.001
Hwang IS, Kim NH, Choi DS, Hwang BK (2012) Overexpression of Xanthomonas campestris pv. vesicatoria effector AvrBsT in Arabidopsis triggers plant cell death, disease and defense responses. Planta 236:1191–1204. https://doi.org/10.1007/s00425-012-1672-4
Hwang EY, Song Q, Jia G, Specht JE, Hyten DL, Costa J, Cregan PB (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15:1–12. https://doi.org/10.1186/1471-2164-15-1
Hyten DL, Choi IY, Song Q, Shoemaker RC, Nelson RL, Costa JM, Specht JE, Cregan PB (2007) Highly variable patterns of linkage disequilibrium in multiple soybean populations. Genetics 175:1937–1944. https://doi.org/10.1534/genetics.106.069740
Ishibashi K, Saruta M, Shimizu T, Shu M, Anai T, Komatsu K, Yamada N, Katayose Y, Ishikawa M, Ishimoto M, Kaga A (2019) Soybean antiviral immunity conferred by dsRNase targets the viral replication complex. Nat Commun 10:1–3. https://doi.org/10.1038/s41467-019-12052-5
Jiao Y, Vuong TD, Liu Y, Meinhardt C, Liu Y, Joshi T, Cregan PB, Xu D, Shannon JG, Nguyen HT (2015) Identification and evaluation of quantitative trait loci underlying resistance to multiple HG types of soybean cyst nematode in soybean PI 437655. Theor Appl Genet 128:15–23. https://doi.org/10.1007/s00122-014-2409-5
Karthikeyan A, Li K, Jiang H, Ren R, Li C, Zhi H, Chen S, Gai J (2017) Inheritance, fine-mapping, and candidate gene analyses of resistance to soybean mosaic virus strain SC5 in soybean. Mol Gen Genomics 292:811–822. https://doi.org/10.1007/s00438-017-1310-8
Kiihl RAS, Hartwig EE (1979) Inheritance of reaction to soybean mosaic virus in soybeans 1. Crop Sci 19:372–375. https://doi.org/10.2135/cropsci1979.0011183x001900030024x
Klepadlo M, Chen P, Shi A, Mason RE, Korth KL, Srivastava V, Wu C (2017) Two tightly linked genes for soybean mosaic virus resistance in soybean. Crop Sci 57:1844–1853. https://doi.org/10.2135/cropsci2016.05.0290
Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis 1. Crop Sci 25:192–194. https://doi.org/10.2135/cropsci1985.0011183x002500010046x
Li K, Yang QH, Zhi HJ, Gai JY (2010) Identification and distribution of soybean mosaic virus strains in southern China. Plant Dis 94:351–357. https://doi.org/10.1094/PDIS-94-3-0351
Li C, Yang Y, Wang D et al (2012) Tudies on mapping and inheritance of resistance genes to SMV strain SC10 in soybean. Sci Agric Sin 45:4335–4342. https://doi.org/10.3864/j.issn.0578-1752.2012.21.001
Li K, Ren R, Adhimoolam K, Gao L, Yuan Y, Liu Z, Zhong Y, Zhi H (2015) Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [Glycine max (L.) Merr]. Plant Breed 134:684–695. https://doi.org/10.1111/pbr.12315
Li C, Adhimoolam K, Yuan Y, Yin J, Ren R, Yang Y, Zhi H (2017) Identification of candidate genes for resistance to soybean mosaic virus strain SC3 by using fine mapping and transcriptome analyses. Crop Pasture Sci 68:156–166. https://doi.org/10.1071/CP16353
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399. https://doi.org/10.1093/bioinformatics/bts444
Liu JZ, Whitham SA (2013) Overexpression of a soybean nuclear localized type-III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance. Plant J 74:110–121. https://doi.org/10.1111/tpj.12108
Liu H, Che Z, Zeng X, Zhang G, Wang H, Yu D (2016) Identification of single nucleotide polymorphisms in soybean associated with resistance to common cutworm (Spodoptera litura Fabricius). Euphytica 209:49–62. https://doi.org/10.1007/s10681-016-1631-4
Lu SJ, Dong LD, Fang C, Liu S, Kong L, Cheng Q, Chen L, Su T, Nan H, Zhang D, Zhang L, Wang Z, Yang Y, Yu D, Liu X, Yang Q, Lin X, Tang Y, Zhao X, Yang X, Tian C, Xie Q, Li X, Yuan X, Tian Z, Liu B, Weller JL, Kong F (2020) Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat Genet 52:428–436. https://doi.org/10.1038/s41588-020-0604-7
Ma Y, Wang DG, Li HC, Zheng GJ, Yang YQ, Li HW, Zhi HJ (2011) Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus in soybean. Euphytica 181:127–135. https://doi.org/10.1007/s10681-011-0457-3
Ma FF, Wu XY, Chen YX, Liu YN, Shao ZQ, Wu P, Wu M, Liu CC, Wu WP, Yang JY, Li DX, Chen JQ, Wang B (2016) Fine mapping of the Rsv1-h gene in the soybean cultivar Suweon 97 that confers resistance to two Chinese strains of the soybean mosaic virus. Theor Appl Genet 129:2227–2236. https://doi.org/10.1007/s00122-016-2769-0
Ma Y, Ma W, Hu D, Zhang X, Yuan W, He X, Kan G, Yu D (2019) QTL mapping for protein and sulfur-containing amino acid contents using a high-density bin-map in soybean (Glycine max L. Merr.). J Agric Food Chem 67:12313–12321. https://doi.org/10.1021/acs.jafc.9b04497
Matsui H, Miyao A, Takahashi A, Hirochika H (2010) Pdk1 kinase regulates basal disease resistance through the OsOxi1-OsPti1a phosphorylation cascade in rice. Plant Cell Physiol 51:2082–2091. https://doi.org/10.1093/pcp/pcq167
Merk HL, Yarnes SC, Van Deynze A et al (2012) Trait diversity and potential for selection indices based on variation among regionally adapted processing tomato Germplasm. J Am Soc Hortic Sci 137:427–437. https://doi.org/10.21273/jashs.137.6.427
Pu Z, Cao Q, Fang D et al (1983) Resistance in soybean varieties to six strains of soybean mosaic virus. J Nanjing Agric Univ 3:41–45. https://doi.org/10.7685/j.issn.1000-2030.1983.03.006
R Core Team (2018) R: a language and environment for statistical computing. In: R Foundation for statistical computing. Austria. Available online at, Vienna https://www.R-project.org/
Ren R, Liu S, Karthikeyan A et al (2017) Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to soybean mosaic virus. Theor Appl Genet 130:2395–2410. https://doi.org/10.1007/s00122-017-2966-5
Shi A, Chen P, Li DX, Zheng C, Hou A, Zhang B (2008) Genetic confirmation of 2 independent genes for resistance to soybean mosaic virus in J05 soybean using SSR markers. J Hered 99:598–603. https://doi.org/10.1093/jhered/esn035
Tsan M-F, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85:905–910. https://doi.org/10.1189/jlb.0109005
Wang X, Gai J, Pu Z (2003) Classification and distribution of strains of soybean mosaic virus in middle and lower Huanghuai and Changjiang river valleys. Soybean Sci 22:102–107. https://doi.org/10.3969/j.issn.1000-9841.2003.04.001
Wang D, Ma Y, Liu N, Yang Z, Zheng G, Zhi H (2011a) Fine mapping and identification of the soybean RSC4 resistance candidate gene to soybean mosaic virus. Plant Breed 130:653–659. https://doi.org/10.1111/j.1439-0523.2011.01888.x
Wang D, Ma Y, Yang Y, Liu N, Li C, Song Y, Zhi H (2011b) Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theor Appl Genet 122:555–565. https://doi.org/10.1007/s00122-010-1469-4
Wang J, Chu S, Zhang H, Zhu Y, Cheng H, Yu D (2016) Development and application of a novel genome-wide SNP array reveals domestication history in soybean. Sci Rep 6:1–10. https://doi.org/10.1038/srep20728
Winter SMJ, Shelp BJ, Anderson TR, Welacky TW, Rajcan I (2007) QTL associated with horizontal resistance to soybean cyst nematode in Glycine soja PI464925B. Theor Appl Genet 114:461–472. https://doi.org/10.1007/s00122-006-0446-4
Wu L, Han Z, Wang S, Wang X, Sun A, Zu X, Chen Y (2013) Comparative proteomic analysis of the plant-virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J Proteome 89:124–140. https://doi.org/10.1016/j.jprot.2013.06.005
Yan H, Wang H, Cheng H, Hu Z, Chu S, Zhang G, Yu D (2015) Detection and fine-mapping of SC7 resistance genes via linkage and association analysis in soybean. J Integr Plant Biol 57:722–729. https://doi.org/10.1111/jipb.12323
Yang Y, Zheng G, Han L, Dagang W, Yang X, Yuan Y, Huang S, Zhi H (2013) Genetic analysis and mapping of genes for resistance to multiple strains of soybean mosaic virus in a single resistant soybean accession PI 96983. Theor Appl Genet 126:1783–1791. https://doi.org/10.1007/s00122-013-2092-y
Yano K, Yamamoto E, Aya K, Takeuchi H, Lo PC, Hu L, Yamasaki M, Yoshida S, Kitano H, Hirano K, Matsuoka M (2016) Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat Genet 48:927–934. https://doi.org/10.1038/ng.3596
Zhan Y, Zhi H-j, Yu D, Gai J (2015) Identification and distribution of SMV strains in Huang-Huai Valleys. Sci Agric Sin 39:2009–2015. https://doi.org/10.3321/j.issn:0578-1752.2006.10.009
Zhang D, Lü H, Chu S, Zhang H, Zhang H, Yang Y, Li H, Yu D (2017) The genetic architecture of water-soluble protein content and its genetic relationship to total protein content in soybean. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-04685-7
Zheng G-j, Yang Y q, Ma Y et al (2014) Fine mapping and candidate gene analysis of resistance gene RSC3Q to soybean mosaic virus in Qihuang 1. J Integr Agric 13:2608–2615. https://doi.org/10.1016/S2095-3119(13)60738-8
Funding
This work was supported in part by Ministry of Science and Technology (2017YFE0111000), Ministry of Agriculture (2016ZX08004-003), National Natural Science Foundation of China (31871649), and China Postdoctoral Science Foundation (2019M662842)
Author information
Authors and Affiliations
Contributions
DY designed the experiment. HY performed the experiment. ZC performed data analysis. ZC wrote the manuscript, and HL, HY, HD, YY, BL, and DY revised it. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Che, Z., Yan, H., Liu, H. et al. Genome-wide association study for soybean mosaic virus SC3 resistance in soybean. Mol Breeding 40, 69 (2020). https://doi.org/10.1007/s11032-020-01149-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-020-01149-1