Abstract
The soybean mosaic virus (SMV) is a viral pathogen caused by Potyvirus reported in the major soybean growing areas of the world. SMV strain SC-15 is the most virulent and predominant strain that infects all soybean differentials and is widely distributed throughout southern China. In this study, three elite SMV-resistant soybean varieties that possess better comprehensive traits were identified through a screening test. A mapping population containing 163 F8 recombinant inbred lines derived from a Zhonghuang24 (resistant) × Huaxia3 (susceptible) cross was used to locate the resistance gene for SMV strain SC-15. A high-density genetic linkage map was developed containing 2639 recombination bins using the restriction site-associated DNA sequencing (RAD-seq) method. Results revealed a novel resistance gene, RSC15ZH identified in a 63 kb region of chromosome 13. This locus was further characterized by quantitative real-time PCR (qRT-PCR). Four candidate resistance genes were identified that were possibly involved in regulating SMV resistance, especially Glyma13g24461. These results provide a basic foundation for soybean breeding programs to improve resistance to SMV strain SC-15 and for positional cloning of SMV resistant candidate genes.
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References
Chaturvedi R, Shah J (2007) Salicylic acid in plant disease resistance. Salicylic Acid A Plant Horm. https://doi.org/10.1007/1-4020-5184-0_12
Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69(5):467–470. https://doi.org/10.1094/Phyto-69-467
Cho EK, Goodman RM (1982) Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Sci 22(6):1133–1136. https://doi.org/10.2135/cropsci1982.0011183X002200060012x
Dielen AS, Badaoui S, Candresse T, Germanretana S (2010) The ubiquitin/26S proteasome system in plant–pathogen– interactions: a never-ending hide-and-seek game. Mol Plant Pathol 11:293–308. https://doi.org/10.3390/ijms14047302
Fu SX, Zhan Y, Zhi HJ, Yu DY (2006) Mapping of SMV resistance gene Rsc7 by SSR markers in soybean. Genetica 128(1–3):63–69. https://doi.org/10.1007/s10709-005-5535-9
Gore MA, Hayes AJ, Jeong SC, Yue YG, Buss GR, Maroof MS (2002) Mapping tightly linked genes controlling potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome 45(3):592–599. https://doi.org/10.1139/g02-009
Guo DQ, Zhi HJ, Wang YW, Gai JY, Zhou XA, Yang ZK, Li K, Li HC (2005) Identification and distribution of soybean mosaic virus strains in Middle and Northern Huang-huai region of China. Chin J Oil Crop Sci 27(4):64–68. https://doi.org/10.3321/j.issn:1007-9084.2005.04.015
Hayes AJ, Ma GR, Buss GR, Maroof MS (2000) Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Sci 40(5):1434–1437. https://doi.org/10.2135/cropsci2000.4051434x
Hayes AJ, Jeong SC, Gore MA, Yue YG, Buss GR, Tolin SA, Maroof MS (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(1):493–503. https://doi.org/10.1534/genetics.166.1.493
Hwang TY, Moon JK, Yu S, Yang K, Mohankumar S, Yu YH, Lee YH, Kim HS, Kim HM, Maroof MS, Jeong SH (2006) Application of comparative genomics in developing molecular markers tightly linked to the virus resistance gene Rsv4 in soybean. Genome 49:380–388. https://doi.org/10.2174/138955706776073457
Ilut DC, Lipka AE, Jeong N, Bae DN, Kim DH, Kim JH, Redekar N, Yang K, Park W, Kang ST, Kim N, Moon JK, Maroof MS, Gore MA, Jeong SC (2016) Identification of haplotypes at the Rsv4 genomic region in soybean associated with durable resistance to soybean mosaic virus. Theor Appl Genet 129(3):453–468. https://doi.org/10.1007/s00122-015-2640-8
Jeong SC, Kristipati S, Hayes AJ, Maughan PJ, Noffsinger SL, Gunduz I, Buss GR, Maroof MS (2002) Genetic and sequence analysis of markers tightly linked to the soybean mosaic virus resistance gene, Rsv3. Crop Sci 42(1):265–270. https://doi.org/10.2135/cropsci2002.0265
Karthikeyan A, Li K, Li C, Yin JL, Li N, Yang YH, Song YP, Ren R, Zhi HJ, Gai JY (2018) Fine-mapping and identifying candidate genes conferring resistance to soybean mosaic virus strain SC20 in soybean. Theor Appl Genet 131(2):461–476. https://doi.org/10.1007/s00122-017-3014-1
Kato S, Takada Y, Shimamura S, Hirata K, Sayama T, Taguchi-Shiobara F, Ishimoto M, Kikuchi A, Nishio T (2016) Transfer of the Rsv3 locus from ‘Harosoy’ for resistance to soybean mosaic virus strains C and D in Japan. Breed Sci 66(2):319–327. https://doi.org/10.1270/jsbbs.66.319
Lee S, Jun TH, Michel AP, Mian MAF (2015) SNP markers linked to QTL conditioning plant height, lodging, and maturity in soybean. Euphytica 203(3):521–532. https://doi.org/10.1007/s10681-014-1252-8
Li HC, Zhi HJ, Gai JY, Guo DQ, Wang WY, Li K, Bai L, Yang H (2006a) Inheritance and gene mapping of resistance to soybean mosaic virus strain SC14 in soybean. J Integr Plant Biol 48(12):1466–1472. https://doi.org/10.1111/j.1744-7909.2006.00365.x
Li ZJ, Shi JG, Yang TZ (2006b) Research on salicylic acid-mediated signal transduction pathway of systemic acquired resistance in plant. Chin Agric Sci Bull 22(12):84–89. https://doi.org/10.3969/j.issn.1000-6850.2006.12.021
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009a) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li R, Yu C, Li YR, Lam TW, Yiu SM, Kristiansen K, Wang J (2009b) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25(15):1966–1967. https://doi.org/10.1093/bioinformatics/btp336
Li D, Chen P, Alloatti J, Shi A, Chen YF (2010a) Identification of new alleles for resistance to soybean mosaic virus in soybean. Crop Sci 50(2):649–655. https://doi.org/10.2135/cropsci2009.06.0302
Li K, Yang QH, Zhi HJ, Gai JY (2010b) Identification and distribution of soybean mosaic virus strains in southern China. Plant Dis 94(3):351–357. https://doi.org/10.1094/pdis-94-3-0351
Li K, Ren R, Karthikeyan A, Yuan Y, Liu ZT, Zhong YK, Zhi HJ (2015) Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [Glycine max (L.) Merr.]. Plant Breed 134(6):684–695. https://doi.org/10.1111/pbr.12315
Liu MS, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang CL, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, Mitchum MG, Meksem K (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492(7428):256–260. https://doi.org/10.1038/nature11651
Liu NX, Li M, Hu XB, Ma QB, Mu YH, Tan ZY, Xia QJ, Zhang GY, Nian H (2017) Construction of high-density genetic map and QTL mapping of yield-related and two quality traits in soybean RILs population by RAD-sequencing. BMC Genom 18(1):466. https://doi.org/10.1186/s12864-017-3854-8
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001
Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen PJ, Bendahmane A, Day L, Baulcombe DC (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22(21):5690–5699. https://doi.org/10.1093/emboj/cdg546
Ma Y, Li HC, Wang DG, Liu N, Zhi HJ (2010) Molecular mapping and marker assisted selection of soybean mosaic virus resistance gene RSC12 in soybean. Legume Genom Genet 1(8):41–46. https://doi.org/10.5376/lgg.2010.01.0008
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(1):127–135. https://doi.org/10.1007/s10681-011-0457-3
Maroof MS, Tucker DM, Skoneczka JA, Bowman BC, Tripathy S, Tolin S (2010) Fine mapping and candidate gene discovery of the soybean mosaic virus resistance gene, Rsv4. Plant Genome 3(1):14–22. https://doi.org/10.3835/plantgenome2009.07.0020
Murakami T, Matsuba S, Funatsuki H, Kawaguchi K, Saruyama H, Tanida M, Sato Y (2004) Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol Breed 13(2):165–175. https://doi.org/10.1023/b:molb.0000018764.30795.c1
Rui R, Liu S, Karthikeyan A, Wang T, Niu HP, Yin JL, Yang YH, Wang LQ, Yang QH, Zhi HJ, Li K (2017) Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to soybean mosaic virus. Theor Appl Genet 130(11):1–16. https://doi.org/10.1007/s00122-017-2966-5
Shi AN, Chen PY, Zheng CM, Hou AF, Zhang B (2008) A PCR-based marker for the Rsv1 locus conferring resistance to soybean mosaic virus. Crop Sci 48(1):262–268. https://doi.org/10.2135/cropsci2007.02.0076
Sun HH, Xue F, Chen JS (2007) Advances in study on soybean mosaic virus (SMV). Chin Bull Life Sci 19(3):338–345. https://doi.org/10.3969/j.issn.1004-0374.2007.03.017
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang YJ, Dongfang Y, Wang XQ, Yang YL, Yu DY, Gai JY, Wu XL, He CY, Zhang JS, Chen SY (2004) Mapping of five genes resistant to SMV strains in soybean. Acta Genet Sin 31(1):87–90
Wang DG, Ma Y, Liu N, Yang ZL, Zheng GJ, Zhi HJ (2011a) Fine mapping and identification of the soybean RSC4 resistance candidate gene to soybean mosaic virus. Plant Breed 130(6):653–659. https://doi.org/10.1111/j.1439-0523.2011.01888.x
Wang DG, Ma Y, Yang YQ, Liu N, Li CY, Song YP, Zhi HJ (2011b) Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theor Appl Genet 122(3):555–565. https://doi.org/10.1007/s00122-010-1469-4
Wang DG, Zhi HJ, Zhang L (2013) Review on resistance to soybean mosaic virus in soybean. Chin J Oil Crop Sci 35(3):341–348. https://doi.org/10.7505/j.issn.1007-9084.2013.03.020
Wang DG, Li K, Zhi HJ (2018) Progresses of resistance on soybean mosaic virus in soybean. Sci Agric Sin 51(16):3040–3059. https://doi.org/10.3864/j.issn.0578-1752.2018.16.002
Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC (2000) Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12(4):569–582. https://doi.org/10.1105/tpc.12.4.569
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(8):722–729. https://doi.org/10.1111/jipb.12323
Yang QH, Gai JY (2011) Identification, inheritance and gene mapping of resistance to a virulent soybean mosaic virus strain SC15 in soybean. Plant Breed 130(2):128–132. https://doi.org/10.1111/j.1439-0523.2010.01797.x
Yang YQ, Zheng GJ, Han L, Wang DG, Yang XF, Yuan Y, Huang SH, Zhi HJ (2011) Genetic analysis and mapping of genes for resistance to multiple strains of soybean mosaic virus in a single resistant soybean accession PI96983. Theor Appl Genet 126(7):1783–1791. https://doi.org/10.1007/s00122-013-2092-y
Yu YG, Maroof MS, Buss GR, Maughan PJ, Tolin SA (1994) RFLP and microsatellite mapping of a gene for soybean mosaic virus resistance. Phytopathology 84(1):60–64. https://doi.org/10.1094/Phyto-84-60
Yue YL, Liu NX, Jiang BJ, Li M, Wang HJ, Jiang Z, Pan HT, Xia QJ, Ma QB, Han TF, Nian H (2017) A single nucleotide deletion in J encoding GmELF3 confers long juvenility and is associated with adaption of tropic soybean. Mol Plant 10(4):656–658. https://doi.org/10.1016/j.molp.2016.12.004
Zeng Z (1993) Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci USA 90(23):10972–10976. https://doi.org/10.1073/pnas.90.23.10972
Zhan Y, Zhi HJ, Yu DG, Gai JY (2006) Identification and distribution of SMV strains in Huang-Huai Valleys. Sci Agric Sin 39(10):2009–2015. https://doi.org/10.3321/j.issn:0578-1752.2006.10.009
Zhang CG, Jing HM, Zheng HL, Zhao ZQ (2001) Progress in plant resistance induced by salicylic acid. Life Sci Res 5(z1):185–189. https://doi.org/10.3969/j.issn.1007-7847.2001.z1.039
Zhang CQ, Grosic S, Whitham SA, Hill JH (2012) The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to soybean mosaic virus. Mol Plant Microbe Interact 25(10):1307–1313. https://doi.org/10.1094/MPMI-02-12-0046-R
Zhao L, Wang DG, Zhang HY, Shen YC, Yang YQ, Li K, Wang LQ, Yang YH, Zhi HJ (2016) Fine mapping of the RSC8 locus and expression analysis of candidate SMV resistance genes in soybean. Plant Breed 135(6):701–706. https://doi.org/10.1111/pbr.12428
Zheng GJ, Yang YQ, Ma Y, Yang XF, Chen SY, Ren R, Wang DG, Yang ZL, Zhi HJ (2014) Fine mapping and candidate gene analysis of resistance gene RSC3Q to soybean mosaic virus in Qihuang 1. J Integr Agric 13(12):2608–2615. https://doi.org/10.1016/S2095-3119(13)60738-8
Acknowledgements
We wish to thank Professor Haijian Zhi (Nanjing Agricultural University, People’s Republic of China) for kindly supplying the SMV of SC-15 strain and the susceptible soybean accession Nannong1138-2. We also thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript. This work was supported by the Science and Technology Projects of Guangzhou City (201804020015); the China Agricultural Research System (CARS-04-PS09) and the Research Project of the State Key Laboratory of Agricultural and Biological Resources Protection and Utilization in Subtropics.
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ML and HN designed and directed the project. ML, NL, and QM participated in the analysis of phenotypic data. TL and ZC helped perform experiments. TL and QM was responsible for mapping the QTLs. ML and ZC performed the qRT-PCR analysis. ML and NL wrote the manuscript with input from all authors. NL designed the figures and tables in the manuscript. HN helped supervise the project. All authors discussed the results and contributed to the final manuscript.
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Li, M., Liu, N., Ma, Q. et al. Fine mapping and analyses of the RSC15ZH resistance candidate gene for the soybean mosaic virus. Euphytica 216, 47 (2020). https://doi.org/10.1007/s10681-020-02581-2
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DOI: https://doi.org/10.1007/s10681-020-02581-2