Theoretical and Applied Genetics

, Volume 130, Issue 11, pp 2395–2410 | Cite as

Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to Soybean mosaic virus

  • Ren Rui
  • Shichao Liu
  • Adhimoolam Karthikeyan
  • Tao Wang
  • Haopeng Niu
  • Jinlong Yin
  • Yunhua Yang
  • Liqun Wang
  • Qinghua Yang
  • Haijian Zhi
  • Kai Li
Original Article

Abstract

Key message

Rsc15, a novel locus underlying soybean resistance to SMV, was fine mapped to a 95-kb region on chromosome 6. The Rsc15- mediated resistance is likely attributed to the gene GmPEX14 , the relative expression of which was highly correlated with the accumulation of H 2 O 2 along with the activities of POD and CAT during the early stages of SMV infection in RN-9.

Abstract

Soybean mosaic virus (SMV) causes severe yield losses and seed quality deterioration in soybean [Glycine max (L.) Merr.] worldwide. A series of single dominant SMV resistance genes have been identified on respective soybean chromosomes 2, 13 and 14, while one novel locus, Rsc15, underlying resistance to the virulent SMV strain SC15 from soybean cultivar RN-9 has been recently mapped to a 14.6-cM region on chromosome 6. However, candidate gene has not yet been identified within this region. In the present study, we aimed to fine map the Rsc15 region and identify candidate gene(s) for this invaluable locus. High-resolution fine-mapping revealed that the Rsc15 gene was located in a 95-kb genomic region which was flanked by the two simple sequence repeat (SSR) markers SSR_06_17 and BARCSOYSSR_06_0835. Allelic sequence comparison and expression profile analysis of candidate genes inferred that the gene Glyma.06g182600 (designated as GmPEX14) was the best candidate gene attributing for the resistance of Rsc15, and that genes encoding receptor-like kinase (RLK) (i.e., Glyma.06g175100 and Glyma.06g184400) and serine/threonine kinase (STK) (i.e., Glyma.06g182900 and Glyma.06g183500) were also potential candidates. High correlations were established between the relative expression level of GmPEX14 and the hydrogen peroxide (H2O2) concentration and activities of catalase (CAT) and peroxidase (POD) during the early stages of SMV-SC15 infection in RN-9. The results of the present study will be useful in marker-assisted breeding for SMV resistance and will lead to further understanding of the molecular mechanisms of host resistance against SMV.

Notes

Acknowledgements

This work was financially supported through grants from the National Natural Science Foundation of China (Grant Nos. 31671718, 31371646, 31571690), the Fundamental Research Funds for the Central Universities (Y0201600115), the National Soybean Industrial Technology System of China (No. CARS-04), Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP), the Fund of Transgenic Breeding for Soybean Resistance to Soybean mosaic virus (No. 2008ZX08004-004) and Changjiang Scholars and Innovative Research Team in University (PCSIRT13073).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments were performed in compliance with the current laws of China.

Supplementary material

122_2017_2966_MOESM1_ESM.docx (26 kb)
Supplementary material 1 (DOCX 26 kb)
122_2017_2966_MOESM2_ESM.docx (59 kb)
Supplementary material 2 (DOCX 58 kb)
122_2017_2966_MOESM3_ESM.docx (88 kb)
Supplementary material 3 (DOCX 88 kb)
122_2017_2966_MOESM4_ESM.docx (157 kb)
Supplementary material 4 (DOCX 156 kb)

References

  1. Abdelmajid KM, Ramos L, Leandro L, Mbofung G, Hyten DL, Kantartzi SK, Grier I, Robert L, Njiti VN, Meksem K (2012) The ‘PI 438489B’by ‘Hamilton’ SNP-based genetic linkage map of soybean [Glycine max (L.) Merr.] identified quantitative trait loci that underlie seedling SDS resistance. J Plant Genome Sci 1:18–30CrossRefGoogle Scholar
  2. Ahangaran A, Habibi MK, Mohammadi G-HM, Winter S, García-Arenal F (2013) Analysis of Soybean mosaic virus genetic diversity in Iran allows the characterization of a new mutation resulting in overcoming Rsv4-resistance. J Gen Virol 94:2557–2568CrossRefPubMedGoogle Scholar
  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefPubMedGoogle Scholar
  4. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci 99:9328–9333CrossRefPubMedPubMedCentralGoogle Scholar
  5. Buzzell R, Tu J (1984) Inheritance of soybean resistance to soybean mosaic virus. J Hered 75:82CrossRefGoogle Scholar
  6. Buzzell R, Tu J (1989) Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic virus. J Hered 80:400–401CrossRefGoogle Scholar
  7. Chen P, Buss G, Roane C, Tolin S (1991) Allelism among genes for resistance to soybean mosaic virus in strain-differential soybean cultivars. Crop Sci 31:305–309CrossRefGoogle Scholar
  8. 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 18:391–404CrossRefPubMedGoogle Scholar
  9. Cho E-K, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467–470CrossRefGoogle Scholar
  10. Cho E, Choi S, Cho W (1983) Newly recognized soybean mosaic virus mutants and sources of resistance in soybeans. The research report of the Office of Rural Development Soil fertilizer, crop protection, mycology and farm products utilizationGoogle Scholar
  11. Choi B, Koo J, Ahn H, Yum H, Choi C, Ryu K, Chen P, Tolin S (2005) Emergence of Rsv-resistance breaking Soybean mosaic virus isolates from Korean soybean cultivars. Virus Res 112:42–51CrossRefPubMedGoogle Scholar
  12. Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131CrossRefGoogle Scholar
  13. Conover RA (1948) Studies of two viruses causing mosaic diseases in Soybean. Phytopathology 38:724–735Google Scholar
  14. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JD (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459CrossRefPubMedGoogle Scholar
  15. Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  16. 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. Plant J 11:45–52CrossRefPubMedGoogle Scholar
  17. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gore M, Hayes A, Jeong S, Yue Y, Buss G, Maroof MS (2002) Mapping tightly linked genes controlling potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome 45:592–599CrossRefPubMedGoogle Scholar
  19. Guo D, Zhi H, Wang Y (2005) Identification and distribution of soybean mosaic virus strains in Middle and Northern Huang Huai Region of China. Chin J Oil Crop Sci 27:64–68Google Scholar
  20. Hajimorad M, Hill J (2001) Rsv1-mediated resistance against Soybean mosaic virus-N is hypersensitive response-independent at inoculation site, but has the potential to initiate a hypersensitive response-like mechanism. Mol Plant Microbe Interact 14:587–598CrossRefPubMedGoogle Scholar
  21. Hayes AJ, Ma G, Buss GR, Maroof M (2000) Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of Soybean Mosaic Virus. Crop Sci 40:1434–1437CrossRefGoogle Scholar
  22. Hayes A, Jeong S, Gore M, Yu Y, Buss G, Tolin S, 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 166:493–503CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 94:134–148CrossRefGoogle Scholar
  24. Hill J, Bailey T, Benner H, Tachibana H, Durand D (1987) Soybean mosaic virus: effects of primary disease incidence on yield and seed quality. Plant Dis 71:237–239CrossRefGoogle Scholar
  25. Hossain M, Akamatsu H, Morishita M, Mori T, Yamaoka Y, Suenaga K, Soares R, Bogado A, Ivancovich A, Yamanaka N (2015) Molecular mapping of Asian soybean rust resistance in soybean landraces PI 594767A, PI 587905 and PI 416764. Plant Pathol 64:147–156CrossRefGoogle Scholar
  26. Huynh T, Bastien M, Iquira E, Turcotte P, Belzile F (2010) Identification of QTLs associated with partial resistance to white mold in soybean using field-based inoculation. Crop Sci 50:969–979CrossRefGoogle Scholar
  27. Hyten DL, Smith JR, Frederick RD, Tucker ML, Song Q, Cregan PB (2009) Bulked segregant analysis using the GoldenGate assay to locate the locus that confers resistance to soybean rust in soybean. Crop Sci 49:265–271CrossRefGoogle Scholar
  28. Ilut DC, Lipka AE, Jeong N, Bae DN, Kim DH, Kim JH, 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. Theor Appl Genet 129:453–468CrossRefPubMedGoogle Scholar
  29. Jeong S, Kristipati S, Hayes A, Maughan P, Noffsinger S, Gunduz I, Buss G, Maroof M (2002) Genetic and sequence analysis of markers tightly linked to the resistance gene, Rsv3. Crop Sci 42:265–270PubMedGoogle Scholar
  30. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793CrossRefPubMedGoogle Scholar
  31. Kang YJ, Kim KH, Shim S, Yoon MY, Sun S, Kim MY, Van K, Lee S-H (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:139CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kiihl RA, Hartwig E (1979) Inheritance of reaction to soybean mosaic virus in soybeans. Crop Sci 19:372–375CrossRefGoogle Scholar
  33. Li Q, Wan J (2005) SSRHunter: development of a local searching software for SSR sites. Hereditas 27:808–810PubMedGoogle Scholar
  34. Li K, Yang Q, Zhi H, Gai J (2010) Identification and distribution of soybean mosaic virus strains in southern China. Plant Dis 94:351–357CrossRefGoogle Scholar
  35. Li C, Yang Y, Wang D, Li H, Zheng G, Wang T, Zhi H (2012) Studies on mapping and inheritance of resistance genes to SMV strain SC10 in soybean. Scientia Agricultura Sinica 45:4335–4342Google Scholar
  36. Li H, Xiao Y, Cao L, Yan X, Li C, Shi H, Wang J, Ye Y (2013) Cerebroside C increases tolerance to chilling injury and alters lipid composition in wheat roots. PLoS One 8:e73380CrossRefPubMedPubMedCentralGoogle Scholar
  37. Li K, Xia Y, Wang D, Yang Y, Ren R, Gao L, Zhang K, Zhi H (2014) Analysis of dynamic change of soybean mosaic virus strains in Heilongjiang province of China. Soybean Sci 33:880–884Google Scholar
  38. Li N, Yin J, Li C, Wang D, Yang Y, Karthikeyan A, Luan H, Zhi H (2016) NB-LRR gene family required for Rsc4-mediated resistance to Soybean mosaic virus. Crop Pasture Sci 67:541–552CrossRefGoogle Scholar
  39. Liu J, Horstman HD, Braun E, Graham MA, Zhang C, Navarre D, Qiu W, Lee Y, Nettleton D, Hill JH (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol 157:1363–1378CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ma Y, Li H, Wang D, Liu N, Zhi H (2010) Molecular mapping and marker assisted selection of soybean mosaic virus resistance gene RSC12 in soybean. Legume Genom Genet 1:41–46Google Scholar
  41. Ma Y, Wang D, Li H, Zheng G, Yang Y, Li H, Zhi H (2011) Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus in soybean. Euphytica 181:127–135CrossRefGoogle Scholar
  42. Ma F, Wu X, Chen Y, Liu Y, Shao Z, Wu P, Wu M, Liu C, Wu W, Yang J (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 129:2227–2236CrossRefPubMedGoogle Scholar
  43. Maroof M, Tucker DM, Skoneczka JA, Bowman BC, Tripathy S, Tolin SA (2010) Fine mapping and candidate gene discovery of the soybean mosaic virus resistance gene, Rsv4. Plant Genome 3:14–22CrossRefGoogle Scholar
  44. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436CrossRefPubMedGoogle Scholar
  45. Molnar SJ, Rai S, Charette M, Cober ER (2003) Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome 46:1024–1036CrossRefPubMedGoogle Scholar
  46. Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47:829–834CrossRefGoogle Scholar
  47. Njiti V, Doubler T, Suttner RJ, Gray L, Gibson P, Lightfoot D (1998) Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycine in near-isogenic lines. Crop Sci 38:472–477CrossRefGoogle Scholar
  48. Nordgren M, Fransen M (2014) Peroxisomal metabolism and oxidative stress. Biochimie 98:56–62CrossRefPubMedGoogle Scholar
  49. Sandhu D, Tasma IM, Frasch R, Bhattacharyya MK (2009) Systemic acquired resistance in soybean is regulated by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol 9:105CrossRefPubMedPubMedCentralGoogle Scholar
  50. Seo J-K, Kwon S-J, Cho WK, Choi H-S, Kim K-H (2014) Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Sci Rep 4:5905CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shi A, Chen P, Zheng C, Hou A, Zhang B (2008) A PCR-based marker for the locus conferring resistance to Soybean Mosaic Virus. Crop Sci 48:262–268CrossRefGoogle Scholar
  52. Song W-Y, Wang G-L, Chen L-L, Kim H-S (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806CrossRefPubMedGoogle Scholar
  53. Song Q, Marek L, Shoemaker R, Lark KG, Concibido V, Delannay X, Specht JE, Cregan P (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128CrossRefPubMedGoogle Scholar
  54. Song Q, Jia G, Zhu Y, Grant D, Nelson RT, Hwang E-Y, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1. 0) in soybean. Crop Sci 50:1950–1960CrossRefGoogle Scholar
  55. Suh SJ, Bowman BC, Jeong N, Yang K, Kastl C, Tolin SA, Maroof M, 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 4:55–64CrossRefGoogle Scholar
  56. Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527CrossRefPubMedGoogle Scholar
  57. Van Ooijen J (2006) JoinMap 4: software for the calculation of genetic linkage maps in experimental populations. Wageningen, Kyazma BVGoogle Scholar
  58. van Zutphen T, Veenhuis M, van der Klei IJ (2008) Pex14 is the sole component of the peroxisomal translocon that is required for pexophagy. Autophagy 4:63–66CrossRefPubMedGoogle Scholar
  59. Viel C, Ide C, Cui X, Wang A, Farsi M, Michelutti R, Strümvik M (2009) Isolation, partial sequencing, and phylogenetic analyses of Soybean mosaic virus (SMV) in Ontario and Quebec. Can J Plant Pathol 31:108–113CrossRefGoogle Scholar
  60. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  61. Wang X, Gai J, Pu Z (2003) Classification and distribution of strain groups of Soybean mosaic virus in middle and lower Huang-Huai and Changjiang Valleys. Soybean Sci 22:102–107Google Scholar
  62. Wang Y, Zhi H, Guo D, Gai J, Chen Q, Li K, Li H (2004) Classification and distribution of strain groups of soybean mosaic virus in Northern China spring planting soybean region. Soybean Sci 24:263–268Google Scholar
  63. 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 130:653–659CrossRefGoogle Scholar
  64. 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 122:555–565CrossRefPubMedGoogle Scholar
  65. Wang D, Li H, Zhi H, Tian Z, Hu C, Hu G, Huang Z, Zhang L (2014) Identification of strains and screening of resistance resources to soybean mosaic virus in Anhui Province. Chin J Oil Crop Sci 36:374–379Google Scholar
  66. Whitham S, Dinesh-Kumar S, 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 78:1101–1115CrossRefPubMedGoogle Scholar
  67. Wrather J, Anderson T, Arsyad D, Tan Y, Ploper LD, Porta-Puglia A, Ram H, Yorinori J (2001a) Soybean disease loss estimates for the top ten soybean-producing countries in 1998. Can J Plant Pathol 23:115–121CrossRefGoogle Scholar
  68. Wrather J, Stienstra W, Koenning S (2001b) Soybean disease loss estimates for the United States from 1996 to 1998. Can J Plant Pathol 23:122–131CrossRefGoogle Scholar
  69. Xu Y, Li H-N, Li G-J, Wang X, Cheng L-G, Zhang Y-M (2011) Mapping quantitative trait loci for seed size traits in soybean (Glycine max L. Merr.). Theor Appl Genet 122:581–594CrossRefPubMedGoogle Scholar
  70. 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 57:722–729CrossRefPubMedGoogle Scholar
  71. Yang Y (2002) Classification and distribution of strains of Soybean mosaic virus in the middle and lower Changjiang River Valleys and the resistance to Soybean mosaic virus in soybeans. Master’s thesis, Nanjing Agricultural University, NanjingGoogle Scholar
  72. Yang Q, Gai J (2011) Identification, inheritance and gene mapping of resistance to a virulent Soybean mosaic virus strain SC15 in soybean. Plant Breed 130:128–132CrossRefGoogle Scholar
  73. Yang H, Huang Y, Zhi H, Yu D (2011) Proteomics-based analysis of novel genes involved in response toward soybean mosaic virus infection. Mol Biol Rep 38:511–521CrossRefPubMedGoogle Scholar
  74. 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 126:1783–1791CrossRefPubMedGoogle Scholar
  75. Yang Y, Lin J, Zheng G, Zhang M, Zhi H (2014) Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Adv Virol 159:1793–1796Google Scholar
  76. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134CrossRefGoogle Scholar
  77. Yong Z, Hao-Ru T, Ya L (2008) Variation in antioxidant enzyme activities of two strawberry cultivars with short-term low temperature stress. World J Agric Sci 4:458–462Google Scholar
  78. Yu Y, Saghai Maroof M, Buss G, Maughan P, Tolin S (1994) RFLP and microsatellite mapping of a gene for soybean mosaic virus resistance. Phytopathology 84:60–64CrossRefGoogle Scholar
  79. Zhan Y, Zhi H, Yu D, Gai J (2006) Identification and distribution of SMV strains in Huang-Huai valleys. Sci Agric Sin 39:2009–2015Google Scholar
  80. Zhang C, 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 25:1307–1313CrossRefPubMedGoogle Scholar
  81. Zhang D, Cheng H, Hu Z, Wang H, Kan G, Liu C, Yu D (2013) Fine mapping of a major flowering time QTL on soybean chromosome 6 combining linkage and association analysis. Euphytica 191:23–33CrossRefGoogle Scholar
  82. Zhao L, Wang D, Zhang H, Shen Y, Yang Y, Li K, Wang L, Yang Y, Zhi H (2016) Fine mapping of the RSC8 locus and expression analysis of candidate SMV resistance genes in soybean. Plant Breed 135:701–706CrossRefGoogle Scholar
  83. Zheng G, Yang Y, Ma Y, Yang X, Chen S, Ren R, Wang D, Yang Z, Zhi H (2014) Fine mapping and candidate gene analysis of resistance gene RSC3Q to soybean mosaic virus in Qihuang 1. J Integr Agric 13:2608–2615CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Ren Rui
    • 1
    • 2
  • Shichao Liu
    • 1
    • 2
  • Adhimoolam Karthikeyan
    • 1
    • 2
  • Tao Wang
    • 1
    • 2
  • Haopeng Niu
    • 1
    • 2
  • Jinlong Yin
    • 1
    • 2
  • Yunhua Yang
    • 1
    • 2
  • Liqun Wang
    • 1
    • 2
  • Qinghua Yang
    • 1
    • 2
  • Haijian Zhi
    • 1
    • 2
  • Kai Li
    • 1
    • 2
  1. 1.National Center for Soybean ImprovementKey Laboratory of Biology and Genetic Improvement of Soybean, Ministry of AgricultureNanjingPeople’s Republic of China
  2. 2.National Key Laboratory for Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanjingPeople’s Republic of China

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