Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (3): 644-653    DOI: 10.1016/S2095-3119(20)63569-9
Special Issue: 油料作物合辑Oil Crops
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Fine mapping and genetic analysis of resistance genes, Rsc18, against soybean mosaic virus
LIU Sang-lin1, 2, CHENG Yan-bo1, 2, MA Qi-bin1, 2, LI Mu1, 2, 3, JIANG Ze1, 2, XIA Qiu-ju4, NIAN Hai1, 2
1 The State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, Guangzhou 510642, P.R.China 
2 The Key Laboratory of Plant Molecular Breeding of Guangdong Province, College of Agriculture, South China Agricultural University, Guangzhou 510642, P.R.China 
3 Maize Research Institute, Jilin Academy of Agricultural Sciences, Gongzhuling 130033, P.R.China 
4 Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen 518086, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

大豆花叶病毒(SMV)病是一种世界性病害,严重影响大豆(Glycine max(L.)Merr.)产量和品质。SC18是华南地区主要的大豆花叶病毒株系之一,但其抗性遗传机制尚不完全清楚。本研究利用中黄24(抗性)和华夏3号(感性)的杂交后代F1,F2和168个F11重组自交系(RILs)群体,利用高密度遗传图谱对抗病品种中黄24的SC18株系抗性基因进行精细定位,并分析其遗传机理。根据F2(3R:1S)和重组自交系(RILs)群体(1R:1S)的分离比例,单个显性基因调控中黄24对SC18的抗性。复合区间作图法(CIM)将抗性基因位点定位在第13号染色体上415.357 kb区域,LOD值为37.43,表型变异解释率达62.01%。根据定位区间内基因的功能注释,鉴定了三个可能与SC18抗性有关的候选基因,包括一个NBS-LRR型基因和两个丝氨酸/苏氨酸蛋白基因。与对照相比,这些基因在抗性材料中表达上调,其中NBS-LRR型基因在亲本外显子非同义SNV区域存在单碱基替换。这项研究为大豆分子抗病育种以及SC18抗性基因定位和功能验证提供参考。

Abstract  Soybean mosaic virus (SMV) affects seed quality and production of soybean (Glycine max (L.) Merr.) worldwide.  SC18 is one of the dominant SMV strains in South China, and accession Zhonghuang 24 displayed resistance to SC18.  The F1, F2 and 168 F11 recombinant inbred lines (RILs) population derived from a hybridization between Zhonghuang 24 (resistant, R) and Huaxia 3 (susceptible, S) were used in this study.  According to the segregation ratios of the F2 generation (3R:1S) and the recombinant inbred lines (RILs) population (1R:1S), one dominant locus may regulate the resistance to SC18 in Zhonghuang 24.  By using composite interval mapping (CIM), Rsc18 was mapped to a 415.357-kb region on chromosome 13.  Three candidate genes, including one NBS-LRR type gene and two serine/threonine protein type genes, were identified according to the genetic annotations, which may be related to the resistance to SC18.  The qRT-PCR demonstrated that these genes were up-regulated in the R genotype compared to the control.  In conclusion, the findings of this research enhanced the understanding about the R genes at the Rsc18 locus.  Moreover, our results will provide insights for designing molecular markers to improve marker-assisted selection and developing new varieties with resistance to SC18.
Keywords:  soybean mosaic virus (SMV)       fine mapping       recombinant inbred lines (RILs)       resistance gene  
Received: 03 July 2020   Accepted: 24 November 2020
Fund: This work was supported by the projects of the Key-Areas Research and Development Program of Guangdong Province, China (2020B020220008), the China Agriculture Research System of MOF and MARA (CARS-04-PSO9), the Major Project of New Varieties Cultivation of Genetically Modified Varieties, China (2016ZX08004002-007), the National Key R&D Program of China (2017FYD0101500), and the National Natural Science Foundation of China (31971966).
About author:  Correspondence NIAN Hai, Tel: +86-20-85280203, E-mail:

Cite this article: 

LIU Sang-lin, CHENG Yan-bo, MA Qi-bin, LI Mu JIANG Ze, XIA Qiu-ju, NIAN Hai. 2022. Fine mapping and genetic analysis of resistance genes, Rsc18, against soybean mosaic virus. Journal of Integrative Agriculture, 21(3): 644-653.

Brueggeman R, Rostoks N, Kudrna D, Kilian A, Kleinhofs A. 2002. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proceedings of the National Academy of Sciences of the United States of America, 99, 9328–9333.
Che Z J, Liu H L, Lei Y F, Hao C, Ming Y Y, Li W, Yi D J, Pei Z P, Jiao W, Yue Y D. 2017. Genome-wide association study reveals novel loci for SC7 resistance in a soybean mutant panel. Frontiers in Plant Science, 8, 1771–1780.
Chen P, Buss G R, Roane C W, Tolin S A. 1991. Allelism among genes for resistance to soybean mosaic virus in strain-differential soybean cultivars. Crop Science, 31, 305–309.
Cho E K, Goodman R M. 1982. Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Science, 22, 1133–1136.
Demirbas A, Rector B G, Lohnes D G, Fioritto R J, Graef G L, Cregan P B, Shoemaker R C, Specht J E. 2001. Simple sequence repeat markers linked to the soybean Rps genes for phytophthora resistance. Crop Science, 41, 1220–1227.
Dixon M S, Jones D A, Keddie J S, Thomas C M, Jones J D G. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell, 84, 451–459.
Feuillet C, Schachermayr G, Keller B. 1997. Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. The Plant Journal, 11, 45–52.
Gore M A, Hayes A J, Jeong S C, Yue Y G, Buss G R, Maroof S. 2002. Mapping tightly linked genes controlling Potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome, 45, 592–599.
Hayes A J, Jeong S C, Gore M A, Yu Y G, Buss G R, Tolin S A, Maroof M A S. 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.
Hayes A J, Ma G, Buss G R, Maroof M A S. 2000. Molecular marker mapping of RSV4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Science, 40, 1434–1437.
Hill J H, Alleman R, Hogg D B, Grau C R. 2001. First report of transmission of soybean mosaic virus and alfalfa mosaic virus by aphis glycines in the new world. Plant Disease, 85, 561.
Huang X H, Feng Q, Qian Q, Zhao Q, Wang L, Wang A H, Guan J P, Fan D L, Weng Q J, Huang T, Dong G J, Sang T, Han B. 2009. High-throughput genotyping by whole-genome resequencing. Genome Research, 19, 1068–1076.
Ilut D C, Lipka A E, Jeong N, Bae D N, Kim D H, Kim J H, Redekar N, Yang K, Park W, Kang S T. 2016. Identification of haplotypes at the Rsv4 genomic region in soybean associated with durable resistance to soybean mosaic virus. Theoretical and Applied Genetics, 129, 453–468.
Iyer A S, Mccouch S R. 2005. The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Molecular Plant Microbe Interactions, 17, 1348–1354.
Jeong S C, Kristipati S, Hayes A J, Maughan P J, Noffsinger S L, Gunduz I, Buss G R, Maroof M A. 2002. Genetic and sequence analysis of markers tightly linked to the soybean mosaic virus resistance gene, Rsv3. Crop Science, 42, 265–270.
Jeong S C, Maroof M A S. 2004. Detection and genotyping of SNPs tightly linked to two disease resistance loci, Rsv1 and Rsv3, of soybean. Plant Breeding, 123, 305–310.
Karthikeyan A, Li K, Li C, Yin J L, Li N, Yang Y H, Song Y P, Ren R, Zhi H J, Gai J Y. 2018. Fine-mapping and identifying candidate genes conferring resistance to Soybean mosaic virus strain SC20 in soybean. Theoretical and Applied Genetics, 131, 461–476.
Li C, Karthikeyan A, Yuan Y, Yin J L, Ren R, Yang Y Q, Zhi H J. 2017. Identification of candidate genes for resistance to Soybean mosaic virus strain SC3 by using fine mapping and transcriptome analyses. Crop and Pasture Science, 68, 156–166.
Li D, Chen P, Alloatti J, Shi A, Chen Y F. 2010. Identification of new alleles for resistance to in soybean. Crop Science, 50, 649–655.
Li K, Yang Q H, Zhi H J, Gai J Y. 2010. Identification and distribution of soybean mosaic virus strains in southern China. Plant Disease, 94, 351–357.
Li K, Zhi H J. 2016. Advances in resistance to soybean mosaic virus disease in soybean. Soybean Science, 4, 525–530. (in Chinese)
Liu H Z, Wang X E, Zhang H J, Yang Y Y, Ge X C, Song F M. 2008. A rice serine carboxypeptidase-like gene OsBISCPL1 is involved in regulation of defense responses against biotic and oxidative stress. Gene, 420, 57–65.
Liu N X, Mu L, Hu X B, Ma Q B, Mu Y H, Tan Z Y, Xia Q J, Zhang G Y, 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 Genomics, 18, 466–479.
Ma Y, Wang D G, Li H C, Zheng G J, Yang Y Q, Li H W, Zhi H J. 2011. Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus in soybean. Euphytica, 181, 127–135.
Maroof M A S, Tucker D M, Skoneczka J A, Bowman B C, Tripathy S, Tolin S A. 2010. Fine mapping and candidate gene discovery of the soybean mosaic virus resistance gene, Rsv4. Plant Genome, 3, 14–22.
Martin G B, Brommonschenkel S H, Chunwongse J, Frary A, Ganal M W, Spivey R, Wu T, Earle E D, Tanksley S D. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science, 262, 1432–1436.
Michelmore R W, Christopoulou M, Caldwell K S. 2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annual Review of Phytopathology, 51, 291–319.
Mohan M, Nair S, Bhagwat A, Krishna T G, Yano M, Bhatia C R, Sasaki T. 1997. Genome mapping, molecular markers and marker-assisted selection in crop plants. Molecular Breeding, 3, 87–103.
Nadeem M A, Nawaz M A, Shahid M Q, Doğan Y, Comertpay G, Yıldız M, Hatipoğlu R, Ahmad F, Alsaleh A, Labhane N, Özkan H, Chung G, Baloch F S. 2018. DNA molecular markers in plant breeding: Current status and recent advancements in genomic selection and genome editing. Biotechnology and Biotechnological Equipment, 32, 261–285.
Rech S S, Heidt S, Requena N. 2013. A tandem Kunitz protease inhibitor (KPI106)-serine carboxypeptidase (SCP1) controls mycorrhiza establishment and arbuscule development in Medicago truncatula. The Plant Journal, 75, 711–725.
Ronald P C, Beutler B. 2010. Plant and animal sensors of conserved microbial signatures. Science, 330, 1061–1064.
Rui R, Liu S C, Karthikeyan A, Wang T, Niu H P, Yin J L, Yang Y H, Wang L Q, Yang Q H, Zhi H J, Li K. 2017. Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to Soybean mosaic virus. Theoretical and Applied Genetics, 130, 2395–2410.
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.
Song W Y, Wang G L, Chen L L, Kim H S, Pi L Y, Holsten T, Gardner J, Wang B, Zhai W X, Zhu L H. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science, 270, 1804–1806.
Su J S, Bowman B C, Jeong N, Yang K, Kastl C, Tolin S A, Maroof M A S, Jeong S C. 2011. The Rsv3 locus conferring resistance to soybean mosaic virus is associated with a cluster of coiled-coil nucleotide-binding leucine-rich repeat genes. Plant Genome, 4, 55–64.
Sun X L, Cao Y L, Yang Z F, Xu C G, Li X H, Wang S P, Zhang Q F. 2004. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. The Plant Journal, 37, 517–527.
Wang D G, Li H W, Zhi H J, Tian Z, Hu C, Hu G Y, Huang Z P, Zhang L. 2014. Identification of strains and screening of resistance resources to soybean mosaic virus in Anhui Province. Chinese Journal of Oil Crop Sciences, 36, 374–379. (in Chinese)
Wang D G, Ma Y, Liu N, Yang Z L, Zheng G J, Zhi H J. 2011a. Fine mapping and identification of the soybean RSC4 resistance candidate gene to soybean mosaic virus. Plant Breeding, 130, 653–659.
Wang D G, Ma Y, Yang Y Q, Liu N, Li C Y, Song Y P, Zhi H J. 2011b. Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theoretical and Applied Genetics, 122, 555–565.
Wang H H, Waller L C, Tripathy S, St Martin S K, Zhou L C, Krampis K, Tucker D M, Mao Y C, Hoeschele I, Maroof M A S. 2010. Analysis of genes underlying soybean quantitative trait loci conferring partial resistance to Phytophthora sojae. Plant Genome, 3, 23–40.
Whitham S, Dinesh-Kumar S P, Choi D, Hehl R, Corr C, Baker B. 1994. The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell, 78, 1101–1115.
Yan H L, Wang H, Cheng H, Hu Z B, Chu S S, Zhang G Z, Yu D Y. 2015. Detection and fine-mapping of SC7 resistance genes via linkage and association analysis in soybean. Journal of Integrative Plant Biology, 57, 722–729.
Yang Q H, Gai J Y. 2011. Identification, inheritance and gene mapping of resistance to a virulent soybean mosaic virus strain SC15 in soybean. Plant Breeding, 130, 128–132.
Yang Y Q, Zheng G J, Han L, Wang D G. 2013. Genetic analysis and mapping of genes for resistance to multiple strains of Soybean mosaic virus in a single resistant soybean accession PI96983. Theoretical and Applied Genetics, 126, 1783–1791.
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang Z X, Kono I, Kurata N, Yano M, Iwata N, Sasaki T. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proceedings of the National Academy of Sciences of the United States of America, 95, 1663–1668.
Zhan Y, Zhi H J, Yu D Y, Gai J Y. 2006. Identification and distribution of SMV strains in Huang-Huai Valleys. Scientia Agricultural Sinica, 39, 2009–2015. (in Chinese)
Zheng G J, Yang Y Q, Ma Y, Yang X F, Chen S Y, Ren R, Wang D G, Yang Z L, Zhi H J. 2014. Fine mapping and candidate gene analysis of resistance gene RSC3Q to soybean mosaic virus in Qihuang 1. Journal of Integrative Agriculture, 13, 2608–2615.
Zhi H J, Yuan Y, Gao L E, Liu Z T, Kai L I, Zhong Y K, Rui R, Karthikeyan A. 2016. Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [Glycine max (L.) Merr]. Plant Breeding, 134, 684–695.
[1] WU Xian-xin, ZANG Chao-qun, ZHANG Ya-zhao, XU Yi-wei, WANG Shu, LI Tian-ya, GAO Li.

Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1740-1749.

[2] Carlos Kwesi TETTEY, YAN Zhi-yong, MA Hua-yu, ZHAO Mei-sheng, GENG Chao, TIAN Yan-ping, LI Xiang-dong . Tomato mottle mosaic virus: characterization, resistance gene effectiveness, and quintuplex RT-PCR detection system[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2641-2651.
[3] WANG Chao-nan, LUAN Fei-shi, LIU Hong-yu, Angela R. DAVIS, ZHANG Qi-an, DAI Zu-yun, LIU Shi. Mapping and predicting a candidate gene for flesh color in watermelon[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2100-2111.
[4] MA Dong-fang, HOU Lu, SUN Cai, ZHANG Xing, YIN Jun-liang, GUO Qing-yun, ZHU Yong-xing. Molecular mapping of stripe rust resistance gene YrH9017 in wheat-Psathyrostachys huashanica introgression line H9017-14-16-5-3[J]. >Journal of Integrative Agriculture, 2019, 18(1): 108-114.
[5] WANG Bao-hua, Daniel J. Ebbole, WANG Zong-hua. The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes[J]. >Journal of Integrative Agriculture, 2017, 16(12): 2746-2760.
[6] WANG Da-gang, ZHAO Lin, LI Kai, MA Ying, WANG Li-qun, YANG Yong-qing, YANG Yun-hua, ZHI Hai-jian. Marker-assisted pyramiding of soybean resistance genes RSC4, RSC8, and RSC14Q to soybean mosaic virus[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2413-2420.
[7] XIE Jing-zhong, WANG Li-li, WANG Yong, ZHANG Huai-zhi, ZHOU Sheng-hui, WU Qiu-hong, CHEN Yong-xing, WANG Zhen-zhong, WANG Guo-xin, ZHANG De-yun, ZHANG Yan, HU Tie-zhu, LIU Zhi-yong. Fine mapping of powdery mildew resistance gene PmTm4 in wheat using comparative genomics[J]. >Journal of Integrative Agriculture, 2017, 16(03): 540-550.
[8] GONG Hong-bing, ZENG Sheng-yuan, XUE Xiang, ZHANG Ya-fang, CHEN Zong-xiang, ZUO Shi-min, LI Chuang, LIN Tian-zi, JING De-dao, YU Bo, QIAN Hua-fei, PAN Xue-biao, SHENG Sheng-lan . Fine mapping of a novel wax crystal-sparse leaf3 gene in rice[J]. >Journal of Integrative Agriculture, 2017, 16(02): 497-502.
[9] LIU Zhong-xian, CUI Yu, WANG Zhong-wei, XIE Yuan-hua, SANG Xian-chun, YANG Zheng-lin, ZHANG Chang-wei, ZHAO Fang-ming, HE Guang-hua, LING Ying-hua. Phenotypic characterization and fine mapping of mps1, a premature leaf senescence mutant in rice (Oryza sativa L.)[J]. >Journal of Integrative Agriculture, 2016, 15(9): 1944-1954.
[10] WANG Yan, ZHAO Jia-ming, ZHANG Li-xia, WANG Ping, WANG Shi-wei, WANG Hui, WANG Xiao-xi, LIU Zhi-heng, ZHENG Wen-jing. Analysis of the diversity and function of the alleles of the rice blast resistance genes Piz-t, Pita and Pik in 24 rice cultivars[J]. >Journal of Integrative Agriculture, 2016, 15(7): 1423-1431.
[11] XIAO Wu-ming, LUO Li-xin, WANG Hui, GUO Tao, LIU Yong-zhu, ZHOU Ji-yong, ZHU Xiao-yuan, YANG Qi-yun, CHEN Zhi-qiang. Pyramiding of Pi46 and Pita to improve blast resistance and to evaluate the resistance effect of the two R genes[J]. >Journal of Integrative Agriculture, 2016, 15(10): 2290-2298.
[12] HAN Liu-sha, LI Zai-feng, WANG Jia-zhen, SHI Ling-zhi, ZHU Lin, LI Xing, LIU Da-qun, Syed J A Shah. Molecular mapping of leaf rust resistance genes in the wheat line Yu 356-9[J]. >Journal of Integrative Agriculture, 2015, 14(7): 1223-1228.
[13] ZHANG Dong, OUYANG Shu-hong, WANG Li-li, CUI Yu, WU Qiu-hong, LIANG Yong, WANG Zhen-zhong, XIE Jing-zhong, ZHANG De-yun, WANG Yong, CHEN Yong-xing, LIU Zhi-yong. Comparative genetic mapping revealed powdery mildew resistance gene MlWE4 derived from wild emmer is located in same genomic region of Pm36 and Ml3D232 on chromosome 5BL[J]. >Journal of Integrative Agriculture, 2015, 14(4): 603-609.
[14] PAN Yu, CHEN Xu-qing, XIE Hua, DENG Lei, LI Xiang-long, ZHANG Xiao-dong, HAN Li-xin, YANG Feng-ping, XUE Jing, ZHANG Li-quan. A maize bundle sheath defective mutation mapped on chromosome 1 between SSR markers umc1395 and umc1603[J]. >Journal of Integrative Agriculture, 2015, 14(10): 1949-1957.
[15] ZHANG Kun, XU Jian-fei, DUAN Shao-guang, PANG Wan-fu, BIAN Chun-song, LIU Jie and JIN. NBS Profiling Identifies Potential Novel Locus from Solanum demissum That Confers Broad-Spectrum Resistance to Phytophthora infestans[J]. >Journal of Integrative Agriculture, 2014, 13(8): 1662-1671.
No Suggested Reading articles found!