Scientia Agricultura Sinica ›› 2018, Vol. 51 ›› Issue (16): 3040-3059.doi: 10.3864/j.issn.0578-1752.2018.16.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Progresses of Resistance on Soybean Mosaic Virus in Soybean

WANG DaGang1, LI Kai2, ZHI HaiJian2   

  1. 1Crop Institute of Anhui Academy of Agricultural Sciences/Key Laboratory of Crop Quality Improvement of Anhui Province,  Hefei 230031; 2Soybean Research Institute of Nanjing Agriculture University/National Center for Soybean Improvement/    National Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing 210095
  • Received:2018-04-07 Online:2018-08-16 Published:2018-08-16

Abstract: Soybean mosaic virus disease, caused by soybean mosaic virus (SMV), is one of the most serous pathogens of soybean (Glycine max (L.) Merr.), which give rise to the loss of yield and quality in soybean production worldwide. During the recent decade, the studies on soybean against SMV stress have made some progress, includes the mapping of SMV resistant genes, the functional analysis of candidate resistance genes, and the progress in dissecting the SMV resistant signaling pathways in soybean. There are two kinds of resistance to SMV in soybean, quantitative resistance and qualitative resistance. The quantitative resistance to SMV is controlled by an additive major gene plus additive-dominant polygenes, and the qualitative resistance is mainly controlled by a dominant resistance gene. Research showed that the quantitative trait loci (QTL) were mainly on chromosome 6, 10 and 13. So far, 22 SMV qualitative resistance loci have been successively mapped on soybean chromosome 2, 6, 13 and 14. And most of the physical distance between the markers on both sides of the SMV resistance gene loci is within 1 Mb. Among them, there are 8 gene loci (Rsv4, RSC5, RSC6, RSC7 and RSC8 etc.) located on chromosome 2, 10 loci (Rsv1, Rsv5, RSC3Q, RSC11 and RSC12 etc.) on chromosome 13, 2 loci on chromosome 6 (RSC15 and RSC18) and 14 (Rsv3 and RSC4), respectively. According to the Williams 82 whole genomic sequence (http://www.phytozome.net/soybean), the putative candidate genes of SMV qualitative resistance loci were subsequently narrowed down based on their predicted functions, expression patterns and sequence comparison etc. Among these genes, Glyma.02G121400, Glyma.02G121500, Glyma.02G121600, Glyma.02G121800, Glyma.02G121900, Glyma.02G122000, Glyma.02G122100 and Glyma.02G122200 et al. eight genes were considered potential resistance candidate genes to SMV on chromosome 2; Glyma.06G182600 as the most promising candidate gene on chromosome 6; Glyma.13G184800, Glyma.13G184900, Glyma.13G187900, Glyma.13G190000, Glyma.13G190300, Glyma.13G190400, Glyma.13G190800, Glyma.13G194700, Glyma. 13G195100 et al. nine genes and Glyma.14G204500, Glyma.14G204600, Glyma.14G204700, Glyma.14G205000, Glyma.14G205200, Glyma.14G205300 et al. six genes were the putative candidate genes to SMV on chromosome 13 and 14, respectively. Using virus induced gene silencing (VIGS) and transgenic technology etc. analyzed the functions of the candidate genes. The results showed genes GmHSP40, GmPP2C3a, GmAKT2, GmCnx1, GmSN1, Glyma.14G204500, Glyma.14G204600 and Glyma.14G204700 can participate to SMV resistance in soybean as positive regulator. After knocked down GmEF1A and GmeIF5A, viral accumulation level of SMV and pathogenicity increased. They were considered negative regulator to SMV resistance. Based on the research results of SMV resistance gene, regulated model were built for Rsv1 and Rsv3 mediating extreme resistance (ER) against SMV. Rsv1-mediated ER has provided new insight into the soybean signaling network required for ER against SMV. The primary mechanism of Rsv3-mediated ER against viruses was the inhibition of viral cell-to-cell movement by callose deposition in an ABA signaling-dependent manner. In this report, the research progress on the mapping and function analysis of SMV resistance genes and the future research directions of SMV resistance in soybean are summarized. It will provide a basis for molecular design breeding and mechanism research of resistance genes to SMV in soybean.

Key words: soybean, soybean mosaic virus, resistance gene, marker location, functional research

[1]    李凯, 刘志涛, 李海朝, 张锴, 王成坤, 任锐, 卢为国, 智海剑. 国家大豆区域试验品种对SMV和SCN的抗性分析. 大豆科学, 2013, 32(5): 670-675.
LI K, LIU Z T, Li H C, ZHANG K, WANG C K, REN R, LU W G, ZHI H J. Resistance to soybean mosaic virus and soybean cyst nematode of soybean cultivars from China national soybean uniform trials. Soybean Science, 2013, 32(5): 670-675. (in Chinese)
[2]    王大刚, 智海剑, 张磊. 大豆抗大豆花叶病毒研究进展. 中国油料作物学报, 2013, 35(3): 341-348.
WANG D G, ZHI H J, ZHANG L. Review on resistance to soybean mosaic virus in soybean. Chinese Journal of Oil Crop Sciences, 2013, 35(3): 341-348. (in Chinese)
[3]    李凯, 智海剑. 大豆对大豆花叶病毒病抗性的研究进展. 大豆科学, 2016, 35(4): 525-530.
LI K, ZHI H J. Advances in resistance to soybean mosaic virus disease in soybean. Soybean Science, 2016, 35(4): 525-530. (in Chinese)
[4]    智海剑, 盖钧镒. 大豆对SMV数量抗性的表现形式与种质鉴定. 中国农业科学, 2004, 37(10): 1422-1427.
ZHI H J, GAI J Y. Performances and germplasm evaluation of quantitative resistance to soybean mosaic virus in soybeans. Scientia Agricultura Sinica, 2004, 37(10): 1422-1427. (in Chinese)
[5]    智海剑, 盖钧镒, 何小红. 大豆对SMV数量(程度)抗性的综合分级方法研究. 大豆科学, 2005, 24(2): 5-11.
ZHI H J, GAI J Y, HE X H. Study on methods of classification of quantitative resistance to soybean mosaic virus in soybean. Soybean Science, 2005, 24(2): 5-11. (in Chinese)
[6]    郭丹丹, 陈海峰, 杨中路, 单志慧, 朱晓玲, 陈水莲, 周新安, 周蓉. 大豆对SMV SC-3株系的抗性遗传和QTL分析. 大豆科学, 2012, 31(4): 511-516.
GUO D D, CHEN H F, YANG Z L, SHAN Z H, ZHU X L, CHEN S L, ZHOU X A, ZHOU R. Analysis of resistance inheritance to soybean mosaic virus (SMV) strain SC-3 and mapping related QTL in soybean. Soybean Science, 2012, 31(4): 511-516. (in Chinese)
[7]    KIIHL R A S, HARTWIG E E. Inheritance of reaction to a soybean mosaic virus in soybeans. Crop Science, 1979, 19(3): 372-375.
[8]    LIM S M. Resistance to soybean mosaic virus in soybeans. Phytopathology, 1985, 75(2): 199-201.
[9]    陈怡, 杜维广, 栾晓燕, 张桂茹, 黄承运, 满为群, 谷秀芝, 王彬 如. 大豆对两个大豆花叶病毒株系的抗性遗传研究. 黑龙江农业科学, 1991(5): 21-24.
CHEN Y, DU W G, LUAN X Y, ZHANG G R, HUANG C Y, MAN W Q, GU X Z, WANG B R. Inheritance of resistance to two soybean mosaic virus strains in soybean. Heilongjiang Agricultural Sciences, 1991(5): 21-24. (in Chinese)
[10]   李海朝, 智海剑, 白丽, 杨华, 马莹, 刘宁, 王大刚. 大豆对SMV株系SC-11的抗性遗传及抗性基因的等位性研究. 大豆科学, 2006, 25(4): 365-368.
LI H C, ZHI H J, BAI L, YANG H, MA Y, LIU N, WANG D G. Studies on inheritance and allelism of resistance genes to SMV strain SC-11 in soybean. Soybean Science, 2006, 25(4): 365-368. (in Chinese)
[11]   白丽, 李海朝, 马莹, 王大刚, 刘宁, 智海剑. 大豆对大豆花叶病毒SC11株系抗性的遗传及基因定位. 大豆科学, 2009, 28(1): 1-6.
BAI L, LI H C, MA Y, WANG D G, LIU N, ZHI H J. Inheritance and gene mapping of resistance to soybean mosaic virus strain SC11 in soybean. Soybean Science, 2009, 28(1): 1-6. (in Chinese)
[12]   王大刚, 马莹, 刘宁, 郑桂杰, 杨中路, 杨永庆, 智海剑. 大豆花叶病毒(SMV)株系SC4和SC8的抗性遗传分析. 作物学报, 2012, 38(2): 202-209.
WANG D G, MA Y, LIU N, ZHENG G J, YANG Z L, YANG Y Q, ZHI H J. Inheritance of resistances to soybean mosaic virus strains SC4 and SC8 in soybean. Acta Agronomica Sinica, 2012, 38(2): 202-209. (in Chinese)
[13]   BUZZELL R I, TU J C. Inheritance of soybean resistance to soybean mosaic virus. Heredity, 1984, 75(1): 82.
[14]   CHEN P Y, BUSS G R, TOLIN S A. Resistance to soybean mosaic virus conferred by two independent dominant genes in PI486355. Journal of Heredity, 1993, 84(1): 25-28.
[15]   Yu Y G, SAGHAI MAROOF M A, BUSS G R, MAUGHAN P J, TOLIN S A. RFLP and microsatellite mapping of a gene for soybean mosaic virus resistance. Phytopathology, 1994, 84(1): 60-64.
[16]   GUNDUZ I, BUSS G R, MA G, CHEN P Y, TOLIN S A. Genetic analysis of resistance to soybean mosaic virus in OX670 and Harosoy soybean. Crop Science, 2001, 41(6): 1785-1791.
[17]   GUNDUZ I, BUSS G R, CHEN P Y, TOLIN S A. Genetic and phenotypic analysis of soybean mosaic virus resistance in PI88788 soybean. Phytopathology, 2004, 94(7): 687-692.
[18]   GORE M A, HAYES A J, JEONG S C, YUE Y G, BUSS G R, SAGHAI MAROOF M A. Mapping tightly linked genes controlling potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome, 2002, 45(3): 592-599.
[19]   JEONG S C, KRISTIPATI S, HAYES A J, MAUGHAN P J, NOFFSINGER S L, GUNDUZ I, BUSS G R, SAGHAI MAROOF M A. Genetic and sequence analysis of markers tightly linked to the soybean mosaic virus resistance gene, Rsv3. Crop Science, 2002, 42(1): 265-270.
[20]   CHEN P Y, BUSS G R, TOLIN S A, GUNDUZ I, CICEK M. A valuable gene in Suweon 97 soybean for resistance to soybean mosaic virus. Crop Science, 2002, 42(2): 333-337.
[21]   WANG Y, NELSON R L, HU Y. Genetic analysis of resistance to soybean mosaic virus in four soybean cultivars from China. Crop Science, 1998, 38(4): 922-925.
[22]   CHEN P Y, MA G, BUSS G R, GUNDUZ I, ROANE C W, TOLIN S A. Inheritance and allelism tests of Raiden soybean for resistance to soybean mosaic virus. Journal of Heredity, 2001, 92(1): 51-55.
[23]   GUNDUZ I, BUSS G R, MA G, CHEN P Y, TOLIN S A. Genetic and phenotypic analysis of soybean mosaic virus resistance in PI88788 soybean. Phytopathology,2004, 94(7): 687-692.
[24]   JEONG S C, SAGHAI MAROOGF M A. Detection and genotyping of SNPs tightly linked to two disease resistance loci, Rsv1 and Rsv3, of soybean. Plant Breeding, 2004, 123(4): 305-310.
[25]   SHI A N, CHEN P Y, LI D X, ZHENG C M, HOU A F, ZHANG B. Genetic confirmation of two independent genes for resistance to soybean mosaic virus in J05 soybean using SSR markers. Journal of Heredity, 2008, 99(6): 598-603.
[26]   SUH S J, BOWMAN B C, JEONG N, YANG K, KASTL C, TOLIN S A, SAGHAI MAROOF M A, JEONG S C. 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, 2011, 4(1): 55-64.
[27]   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, KIM N, MOON J K, SAGHAI MAROOF M A, GORE M A, JEONG S C. Identification of haplotypes at the Rsv4 genomic region in soybean associated with durable resistance to soybean mosaic virus. Theoretical & Applied Genetics, 2016, 129(3): 453-468.
[28]   KLEPADLO M, CHEN P Y, SHI A N, MASON R E, KORTH K L, SRIVASTAVA V S, WU C J. Two tightly linked genes for soybean mosaic virus resistance in soybean. Crop Science, 2017, 57(4): 1-10.
[29]   FU S X, ZHAN Y, ZHI H J, GAI Y J, YU D Y. Mapping of SMV resistance gene Rsc-7 by SSR markers in soybean. Genetica, 2006, 128(1/3): 63-69.
[30]   LI H C, ZHI H J, GAI J Y, GUO D Q, WANG Y W, LI K, LI B, YANG H. Inheritance and gene mapping of resistance to soybean mosaic virus strain SC14 in soybean. Journal of Integrative Plant Biology, 2006, 48(12): 1466-1472.
[31]   MA Y, LI H C, WANG D G, LIU N, ZHI H J. Molecular mapping and marker assisted selection of soybean mosaic virus resistance gene RSC12 in soybean. Legume Genomics & Genetics, 2010, 1(8): 41-46.
[32]   MA Y, WANG D G, LI H C, ZHENG G J, YANG Y Q, LI H W, ZHI H J. Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus in soybean. Euphytica, 2011, 181(1): 127-135.
[33]   WANG D G, MA Y, YANG Y Q, LIU N, LI C Y, SONG Y P, ZHI H J. Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theoretical & Applied Genetics, 2011, 122(3): 555-565.
[34]   WANG D G, MA Y, LIU N, YANG Z L, ZHENG G J, ZHI H J. Fine mapping and identification of the soybean RSC4 resistance candidate gene to soybean mosaic virus. Plant Breeding, 2011, 130(6): 653-659.
[35]   YANG Q H, GAI J Y. Identification, inheritance and gene mapping of resistance to a virulent soybean mosaic virus strain SC15 in soybean. Plant Breeding, 2011, 130(2): 128-132.
[36]   李春燕, 杨永庆, 王大刚, 李华伟, 郑桂杰, 王涛, 智海剑. 大豆对SMV株系SC10的抗性遗传及抗病基因的定位研究. 中国农业科学, 2012, 45(21): 4335-4342.
LI C Y, YANG Y Q, WANG D G, LI H W, ZHENG G J, WANG T, ZHI H J. Studies on mapping and inheritance of resistance genes to SMV strain SC10 in soybean. Scientia Agricultura Sinica, 2012, 45(21): 4335-4342. (in Chinese)
[37]   YANG Y Q, ZHENG G J, HAN L, WANG D G, YANG X F, YUAN Y, HUANG S H, ZHI H J. Genetic analysis and mapping of genes for resistance to multiple strains of soybean mosaic virus in a single resistant soybean accession PI96983. Theoretical & Applied Genetics, 2013, 126(7): 1783-1791.
[38]   阳小凤, 杨永庆, 郑桂杰, 智海剑, 李晓红. 大豆对大豆花叶病毒株系SC6和SC17抗病基因的精细定位. 作物学报, 2013, 39(2): 216-221.
YANG X F, YANG Y Q, ZHENG G J, ZHI H J, LI X H. Fine mapping of resistance genes to SMV strains SC6 and SC17 in soybean. Acta Agronomica Sinica, 2013, 39(2): 216-221. (in Chinese)
[39]   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. Fine mapping and candidate gene analysis of resistance gene RSC3Q to soybean mosaic virus in Qihuang 1. Journal of Integrative Agriculture, 2014, 13(12): 2608-2615.
[40]   LI K, REN R, ADHIMOOLAM K, GAO L, YUAN Y, LIU Z T, ZHONG Y K, ZHI H J. Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [Glycine max (L.) Merr]. Plant Breeding, 2015, 134(6): 684-695.
[41]   YAN H L, WANG H, CHENG H, HU Z B, CHU S S, ZHANG G Z, YU D Y. Detection and fine-mapping of SC7 resistance genes via linkage and association analysis in soybean. Journal of Integrative Plant Biology, 2015, 57(8): 722-729.
[42]   LI C, ADHIMOOLAM K, YUAN Y, YIN J L, REN R, YANG Y Q, ZHI H J. Identification of candidate genes for resistance to soybean mosaic virus strain SC3by using fine mapping and transcriptome analyses. Crop & Pasture Science, 2017, 68(2): 156-166.
[43]   ZHAO L, WANG D G, ZHANG H Y, SHEN Y C, YANG Y Q, LI K, WANG L Q, YANG Y H, ZHI H J. Fine mapping of the RSC8 locus and expression analysis of candidate SMV resistance genes in soybean. Plant Breeding, 2016, 135(6): 701-706.
[44]   ADHIMOOLAM K, LI K, JIANG H, REN R, LI G, ZHI H J, CHEN S Y, GAI J Y. Inheritance, fine-mapping, and candidate gene analyses of resistance to soybean mosaic virus strain SC5in soybean. Molecular Genetics & Genomics, 2017, 292(4): 811-822.
[45]   ADHIMOOLAM K, LI K, LI C, YIN J L, LI N, YANG Y H, SONG Y P, REN R, ZHI H J, GAI J Y. Fine-mapping and identifying candidate genes conferring resistance to soybean mosaic virus strain SC20 in soybean. Theoretical & Applied Genetics, 2018, 131(2): 461-476.
[46]   REN R, LIU S C, ADHIMOOLAM K, WANG T, NIU H P, YIN J L, YANG Y H, WANG L Q, YANG Q H, ZHI H J, LI K. Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to soybean mosaic virus. Theoretical & Applied Genetics, 2017, 130(11): 2395-2410.
[47]   李凯, 任锐, 王涛, 高乐, 落金艳, 刘士超, 智海剑, 盖钧镒. 大豆对大豆花叶病毒SC18株系的抗性遗传和基因定位. 大豆科学, 2017, 36(2): 187-192.
LI K, REN R, WANG T, GAO L, LUO J Y, LIU S C, ZHI H J, GAI J Y. Genetic analysis and mapping of soybean mosaic virus resistance genes to SC18 in soybean. Soybean Science, 2017, 36(2): 187-192. (in Chinese)
[48]   MA F F, WU X Y, CHEN Y X, LIU Y N, SHAO Z Q, WU P, WU M, LIU C C, WU W P, YANG J Y, LI D X, CHEN J Q, WANG B. 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. Theoretical & Applied Genetics, 2016, 129(11): 2227-2236.
[49]   HAYES A J, MA G, BUSS G R, SAGHAI MAROOF A S. Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Science, 2000, 40(5): 1434-1437.
[50]   HWANG T Y, MOON J K, YU S, YANG K, MOHANKUMAR S, YU Y H, LEE Y H, KIM S H, KIM H M, SAGHAI MAROOF M A, JEONG S C. Application of comparative genomics in developing molecular markers tightly linked to the virus resistance gene Rsv4 in soybean. Genome, 2006, 49(4): 380-388.
[51]   SAGHAI MAROOF M A, TUCKER D M, SKONECZKA J A, BOWMEN B C, TRIPATHY S, TOLIN S A. Fine mapping and candidate gene discovery of the soybean mosaic virus resistance gene, Rsv4. Plant Genome, 2010, 3(1): 14-22.
[52]   CHEN P Y, BUSS G R, ROANE C W, TOLIN S A. Allelism among genes for resistance to soybean mosaic virus in strain-differential soybean cultivars. Crop Science, 1991, 31(2): 305-309.
[53]   LI K, YANG Q H, ZHI H J, GAI J Y. Identification and distribution of soybean mosaic virus strains in Southern China. Plant Disease, 2010, 94(3): 351-357.
[54]   王大刚, 田震, 李凯, 李华伟, 黄志平, 胡国玉, 张磊, 智海剑. 鲁豫皖大豆产区大豆花叶病毒株系的鉴定及动态变化分析. 大豆科学, 2013, 32(6): 806-809.
WANG D G, TIAN Z, LI K, LI H W, HUANG Z P, HU G Y, ZHANG L, ZHI H J. Identification and variation analysis of soybean mosaic virus strains in Shandong, Henan and Anhui provinces of China. Soybean Science, 2013, 32(6): 806-809. (in Chinese)
[55]   蔡春梅, 姜骁, 赵春梅, 马建新. 中国大豆花叶病毒SC7外壳蛋白基因的序列测定及其与美国株系的比较. 病毒学报, 2014, 30(5): 489-494.
CAI C M, JIANG X, ZHAO C M, MA J X. Sequence analysis of the coat protein gene of Chinese soybean mosaic virus strain SC7and comparison with those of SMV strains from the USA. Chinese Journal of Virology, 2014, 30(5): 489-494. (in Chinese)
[56]   郭东全, 王延伟, 智海剑, 盖钧镒, 李海朝, 李凯. 大豆对SMV SC-13株系群的抗性遗传及基因定位的研究. 大豆科学, 2007, 26(1): 21-24.
GUO D Q, WANG Y W, ZHI H J, GAI J Y, LI H C, LI K. Inheritance and gene mapping of resistance to SMV strain group SC-13in soybean. Soybean Science, 2007, 26(1): 21-24. (in Chinese)
[57]   CHE Z J, LIU H L, YI F L, CHENG H, YANG Y M, WANG L, DU J Y, ZHANG P P, WANG J, YU D Y. Genome-wide association study reveals novel loci for SC7 resistance in a soybean mutant panel. Frontiers in Plant Science, 2017, 8: 1-12.
[58]   HAYES A J, JEONG S C, GORE M A, YU Y G, BUSS G R, TOLIN S A, SAGHAI MAROOF M A. Recombination within a nucleotide- binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics,2004, 166(1): 493-503.
[59]   SHAO Z Q, ZHANG Y M, HANG Y Y, XUE J Y, ZHOU G C, WU P, WU X Y, WU X Z, WANG Q, WANG B, CHEN J Q. Long-term evolution of nucleotide-binding site-leucine-rich repeat genes: understanding gained from and beyond the legume family. Plant Physiology, 2014, 166(1): 217-234.
[60]   REDEKAR N R, CLEBINGER E M, LASKAR M A, BIYASHEV R M, ASHFIELD T, JENSEN R V, JEONG S C, TOLIN S A, SAGHAI MAROOF M A. Candidate gene sequence analyses toward identifying Rsv3-type resistance to soybean mosaic virus. Plant Genome, 2016, 9(2): 1-12.
[61]   贺超英, 张志永, 陈受宜. 大豆中NBS类抗性基因同源序列的分离与鉴定. 科学通报, 2001, 46(12): 1017-1021.
HE C Y, ZHANG Z Y, CHEN S Y. Isolation and identification of NBS type resistance gene analogs in soybean. Chinese Science Bulletin, 2001, 46(12): 1017-1021. (in Chinese)
[62]   WANG B J, WANG Y J, WANG Q, LUO G Z, ZHANG Z G, HE C Y, HE S J, ZHANG J S, GAI J Y, CHEN S Y. Characterization of an NBS-LRR resistance gene homologue from soybean. Journal of Plant Physiology, 2004, 161(7): 815-822.
[63]   HE C Y, TIAN A G, ZHANG J S, ZHANG Z Y, GAI J Y, CHEN S Y. Isolation and characterization of a full-length resistance gene homolog from soybean. Theoretical & Applied Genetics, 2003, 106(5): 786-793.
[64]   WANG Y J, LI Y D, TIAN A G, WANG H WM ZHANG J S, CHR S Y. Cloning and characterization of an HDZip I gene GmHZ1 from soybean. Planta, 2005, 221(6): 831-843.
[65]   CHENG H, YANG H, ZHANG D, GAI J Y, YU D Y. Polymorphisms of soybean isoflavone synthase and flavanone 3-hydroxylase genes are associated with soybean mosaic virus resistance. Molecular Breeding, 2010, 25(1): 13-24.
[66]   ZHANG G Y, CHEN M, CHEN X P, XU Z S, LI L C, GUO J M, MA Y Z. Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Molecular Biology Reports, 2010, 37(2): 809-818.
[67]   陈华涛, 陈新, 顾和平, 张红梅, 袁星星, 崔晓燕. 大豆GmPR10基因克隆与植物表达载体的构建. 江苏农业学报, 2011, 27(3): 494-499.
CHEN H T, CHEN X, GU H P, ZHANG H M, YUAN X X, CUI X Y. Cloning and plant expression vector construction of GmPR10 in soybean. Jiangsu Journal of Agricultural Sciences, 2011, 27(3): 494-499. (in Chinese)
[68]   HE H L, YANG X D, XUN H W, LOU X , LI S Z, ZHANG Z B, JIANG L L, DONG Y S, WANG S C, PANG J S, LIU B. Over-expression of GmSN1 enhances virus resistance in Arabidopsis and soybean. Plant Cell Reports, 2017, 36(9): 1441-1455.
[69]   LIU J Z, HORSTMAN H D, BRAUM E, GRAHAM M A, ZHANG C, NAVARRE D, QIU L W, LEE Y, NETTLETON D, HILL J H, WHITHAM S A. Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiology,2011, 157(3): 1363-1378.
[70]   LIU J Z, BRAUN E, QIU W L, SHI Y F, MARCELINO- GUIMARAES F C, NAVARRE D, HILL J H, WHITHAM S A. Positive, and negative roles for soybean MPK6 in regulating defense responses. Molecular Plant-Microbe Interactions, 2014, 27(8): 824-834.
[71]   LIU J Z, WHITHAM S A. Overexpression of a soybean nuclear localized type-III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance. The Plant Journal, 2013, 74(1): 110-121.
[72]   SEO J K, KWON S J, CHO W K, CHOI H S, KIM K H. Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Scientific Reports, 2014, 4: 5905-5913.
[73]   ZHOU L, HE H L, LIU R F, HAN Q, SHOU H X, LIU B. Overexpression of GmAKT2 potassium channel enhances resistance to soybean mosaic virus. BMC Plant Biology, 2014, 14(1): 154-165.
[74]   ZHOU Z, HE H L, MA L P, YU X Q, MI Q, PANG J S, TANG G X, LIU B. Overexpression of a GmCnx1 gene enhanced activity of nitrate reductase and aldehyde oxidase, and boosted mosaic virus resistance in soybean. Plos One, 2015, 10(4): 1-15.
[75]   LI N, YIN J L, LI C, WANG D G, YANG Y Q, ADHIMOOLAM K, LUAN H X, ZHI H J. NB-LRR gene family required for Rsc4- mediated resistance to soybean mosaic virus. Crop and Pasture Science, 2016, 67(5): 541-552.
[76]   TRAN P T, WIDYASARI K, SEO J K, KIM K H. Isolation and validation of a candidate Rsv3 gene from a soybean genotype that confers strain-specific resistance to soybean mosaic virus. Virology, 2017, 513: 153-159.
[77]   LUAN H X, SHINE M B, CUI X Y, CHEN X, MA N, KACHROO P, ZHI H J, KARCHROO A. The potyviral P3 protein targets eukaryotic elongation factor 1A to promote the unfolded protein response and viral pathogenesis. Plant Physiology, 2016, 172(1): 221-234.
[78]   CHEN H, ARSOVSKI A A, Yu K F, Wang A M. 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. Molecular Plant Pathology, 2016, 18(3): 391-404.
[79]   ZHANG C Q, GROSIC S, WHITHAM S A, HILL J H. The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to soybean mosaic virus. Molecular Plant-Microbe Interactions, 2012, 25(10): 1307-1313.
[80]   FU D Q, GHABRIAL S, KACHROO A. GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Molecular Plant-Microbe Interactions, 2009, 22(1): 86-95.
[81]   LI W L, ZHAO Y S, LIU C J, YAO G B, WU S S, HOU C Y, ZHANG M C, WANG D M. Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of soybean mosaic virus. Plant Cell Reports, 2012, 31(5): 905-916.
[82]   SAGHAI MAROOF M A, JEONG S C, GUNDUZ I, TOLIN S. Pyramiding of soybean mosaic virus resistance genes by marker-assisted selection. Crop Science, 2008, 48(2): 517-526.
[83]   SHI A N, CHEN P Y, LI D X, ZHENG C M, ZHANG B, HOU A F. Pyramiding multiple genes for resistance to soybean mosaic virus in soybean using molecular markers. Molecular Breeding, 2009, 23(1): 113-124.
[84]   WANG D G, ZHAO L, LI K, MA Y, WANG L Q, YANG Y Q, YANG Q H, ZHI H J. Marker-assisted pyramiding of soybean resistance genes RSC4, RSC8, and RSC14Qto soybean mosaic virus. Journal of Integrative Agriculture, 2017, 16(11): 2413-2420.
[85]   郑桂杰. 齐黄1号对大豆花叶病毒抗性基因的精细定位、育种应用及候选基因表达分析[D]. 南京: 南京农业大学, 2012.
ZHENG G J. Fine mapping, expression analysis and breeding application of resistance genes to soybean mosaic virus in Qihuang No.1[D]. Nanjing: Nanjing Agriculture University, 2012. (in Chinese)
[86]   徐冉, 石传娥, 张礼凤, 王彩洁, 聂翠琴, 李建和. 黄淮海大豆优异种质齐黄1号的育种应用. 植物遗传资源学报, 2004, 5(2): 170-175.
XU R, SHI C E, ZHANG L F, WANG C J, NIE C Q, LI J H. Utilization of Qihuang 1 in soybean breeding in the Huanghuaihai region. Journal of Plant Genetic Resources, 2004, 5(2): 170-175. (in Chinese)
[87]   张孟臣, 张磊, 刘学义, 李卫东. 黄淮海大豆改良种质. 北京: 中国农业出版社, 2014.
ZHANG M C, ZHANG L, LIU X Y, LI W D. Huanghuaihai soybean improvement germplasm. Beijing: China Agriculture Press, 2014. (in Chinese)
[88]   CHOI B K, KOO J M, AHN H J, YUM H J, CHOI C W, RYU K H, CHEN P Y, TOLIN S A. Emergence of Rsv-resistance breaking soybean mosaic virus isolates from Korean soybean cultivars. Virus Research, 2005, 112(1): 42-51.
[89]   KOO J M, CHOI B K, AHN H J, YUM H J, CHOI C W. First report of an Rsv resistance-breaking isolate of soybean mosaic virus in Korea. Plant Pathology, 2005, 54(4): 573.
[90]   SARUTA M, KIKUCHI A, OKABE A, SASAYA T. Molecular characterization of A2 and D strains of soybean mosaic virus, which caused a recent virus outbreak in soybean cultivar Sachiyutaka in Chugoku and Shikoku regions of Japan. Journal of General Plant Pathology, 2005, 71(6): 431-435.
[91]   GAGARINOVA A G, BABU M, POYSA V, HILL J H, WANG A M. Identification and molecular characterization of two naturally occurring soybean mosaic virus isolates that are closely related but differ in their ability to overcome Rsv4 resistance. Virus Research, 2008, 138(1/2): 50-56.
[92]   WANG Y, HAJIMORAD M R. Gain of virulence by soybean mosaic virus on Rsv4-genotype soybeans is associated with a relative fitness loss in a susceptible host. Molecular Plant Pathology, 2016, 17(7): 1154-1159.
[93]   YANG Y Q, LIN J, ZHENG G J, ZHANG M C, ZHI H J. Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Archives of Virology, 159(7): 1793-1796.
[94]   YANG Y Q, GONG J W, LI H W, LI C Y, WANG D G, LI K, ZHI H J. Identification of a novel soybean mosaic virus isolate in China that contains a unique5' terminus sharing high sequence homology with bean common mosaic virus. Virus Research, 2011, 157(1): 13-18.
[95]   ZHOU G C, SHAO Z Q, MA F F, WU P, WU X Y, XIA Z Y, YU D Y, CHENG H, LIU Z H, JIANG Z F, CHEN Q S, WANG B, CHEN J Q. The evolution of soybean mosaic virus: An updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Research, 2015, 208: 189-198.
[96]   董英山. 中国野生大豆研究进展. 吉林农业大学学报, 2008, 30(4): 394-400.
DONG Y S. Advances of research on wild soybean in China. Journal of Jilin Agricultural University, 2008, 30(4): 394-400. (in Chinese)
[97]   WEN Z X, DING Y L, ZHAO T J, GAI J Y. Genetic diversity and peculiarity of annual wild soybean (G. soja Sieb. et Zucc.) from various eco-regions in China. Theoretical & Applied Genetics, 2009, 119(2): 371-381.
[98]   ZHOU Z K, JIANG Y, WANG Z, GOU Z H, YU J L, LI W Y, YU Y J, SHU L P, ZHAO Y J, MA Y M, FANG C, SHEN Y T, LIU T F, LI C C, GAO Y D, XIANG H, ZHU B G, LEE S H, WANG W, TIAN Z X. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nature Biotechnology, 2015, 33(4): 408-414.
[1] DONG YongXin,WEI QiWei,HONG Hao,HUANG Ying,ZHAO YanXiao,FENG MingFeng,DOU DaoLong,XU Yi,TAO XiaoRong. Establishment of ALSV-Induced Gene Silencing in Chinese Soybean Cultivars [J]. Scientia Agricultura Sinica, 2022, 55(9): 1710-1722.
[2] LI YiLing,PENG XiHong,CHEN Ping,DU Qing,REN JunBo,YANG XueLi,LEI Lu,YONG TaiWen,YANG WenYu. Effects of Reducing Nitrogen Application on Leaf Stay-Green, Photosynthetic Characteristics and System Yield in Maize-Soybean Relay Strip Intercropping [J]. Scientia Agricultura Sinica, 2022, 55(9): 1749-1762.
[3] GUO ShiBo,ZHANG FangLiang,ZHANG ZhenTao,ZHOU LiTao,ZHAO Jin,YANG XiaoGuang. The Possible Effects of Global Warming on Cropping Systems in China XIV. Distribution of High-Stable-Yield Zones and Agro-Meteorological Disasters of Soybean in Northeast China [J]. Scientia Agricultura Sinica, 2022, 55(9): 1763-1780.
[4] MA XiaoYan,YANG Yu,HUANG DongLin,WANG ZhaoHui,GAO YaJun,LI YongGang,LÜ Hui. Annual Nutrients Balance and Economic Return Analysis of Wheat with Fertilizers Reduction and Different Rotations [J]. Scientia Agricultura Sinica, 2022, 55(8): 1589-1603.
[5] LIU Jiao,LIU Chang,CHEN Jin,WANG MianZhi,XIONG WenGuang,ZENG ZhenLing. Distribution Characteristics of Prophage in Multidrug Resistant Escherichia coli as well as Its Induction and Isolation [J]. Scientia Agricultura Sinica, 2022, 55(7): 1469-1478.
[6] ZHANG YaLing, GAO Qing, ZHAO Yuhan, LIU Rui, FU Zhongju, LI Xue, SUN Yujia, JIN XueHui. Evaluation of Rice Blast Resistance and Genetic Structure Analysis of Rice Germplasm in Heilongjiang Province [J]. Scientia Agricultura Sinica, 2022, 55(4): 625-640.
[7] JIANG FenFen, SUN Lei, LIU FangDong, WANG WuBin, XING GuangNan, ZHANG JiaoPing, ZHANG FengKai, LI Ning, LI Yan, HE JianBo, GAI JunYi. Geographic Differentiation and Evolution of Photo-Thermal Comprehensive Responses of Growth-Periods in Global Soybeans [J]. Scientia Agricultura Sinica, 2022, 55(3): 451-466.
[8] HU ChaoYue, WANG FengTao, LANG XiaoWei, FENG Jing, LI JunKai, LIN RuiMing, YAO XiaoBo. Resistance Analyses on Wheat Stripe Rust Resistance Genes to the Predominant Races of Puccinia striiformis f. sp. tritici in China [J]. Scientia Agricultura Sinica, 2022, 55(3): 491-502.
[9] TANG ZiYun,HU JianXin,CHEN Jin,LU YiXing,KONG LingLi,DIAO Lu,ZHANG FaFu,XIONG WenGuang,ZENG ZhenLing. Relationship Between Biofilm Formation and Molecular Typing of Staphylococcus aureus from Animal Origin [J]. Scientia Agricultura Sinica, 2022, 55(3): 602-612.
[10] YAN Qiang,XUE Dong,HU YaQun,ZHOU YanYan,WEI YaWen,YUAN XingXing,CHEN Xin. Identification of the Root-Specific Soybean GmPR1-9 Promoter and Application in Phytophthora Root-Rot Resistance [J]. Scientia Agricultura Sinica, 2022, 55(20): 3885-3896.
[11] WANG QiaoJuan,HE Hong,LI Liang,ZHANG Chao,CAI HuanJie. Research on Soybean Irrigation Schedule Based on AquaCrop Model [J]. Scientia Agricultura Sinica, 2022, 55(17): 3365-3379.
[12] YUAN Cheng,ZHANG MingCong,WANG MengXue,HUANG BingLin,XIN MingQiang,YIN XiaoGang,HU GuoHua,ZHANG YuXian. Effects of Intertillage Time and Depth on Photosynthetic Characteristics and Yield Formation of Soybean [J]. Scientia Agricultura Sinica, 2022, 55(15): 2911-2926.
[13] ZHAO DingLing,WANG MengXuan,SUN TianJie,SU WeiHua,ZHAO ZhiHua,XIAO FuMing,ZHAO QingSong,YAN Long,ZHANG Jie,WANG DongMei. Cloning of the Soybean Single Zinc Finger Protein Gene GmSZFP and Its Functional Analysis in SMV-Host Interactions [J]. Scientia Agricultura Sinica, 2022, 55(14): 2685-2695.
[14] REN JunBo,YANG XueLi,CHEN Ping,DU Qing,PENG XiHong,ZHENG BenChuan,YONG TaiWen,YANG WenYu. Effects of Interspecific Distances on Soil Physicochemical Properties and Root Spatial Distribution of Maize-Soybean Relay Strip Intercropping System [J]. Scientia Agricultura Sinica, 2022, 55(10): 1903-1916.
[15] HanXi LIU,Hao LÜ,GuangYu GUO,DongXu LIU,Yan SHI,ZhiJun SUN,ZeXin ZHANG,YanJiao ZHANG,YingNan WEN,JieQi WANG,ChunYan LIU,QingShan CHEN,DaWei XIN,JinHui WANG. Effect of rhcN Gene Mutation on Nodulation Ability of Soybean Rhizobium HH103 [J]. Scientia Agricultura Sinica, 2021, 54(6): 1104-1111.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!