Skip to main content
Genetics logoLink to Genetics
. 2004 Jan;166(1):493–503. doi: 10.1534/genetics.166.1.493

Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans.

A J Hayes 1, S C Jeong 1, M A Gore 1, Y G Yu 1, G R Buss 1, S A Tolin 1, M A Saghai Maroof 1
PMCID: PMC1470674  PMID: 15020438

Abstract

The soybean Rsv1 gene for resistance to soybean mosaic virus (SMV; Potyvirus) has previously been described as a single-locus multi-allelic gene mapping to molecular linkage group (MLG) F. Various Rsv1 alleles condition different responses to the seven (G1-G7) described strains of SMV, including extreme resistance, localized and systemic necrosis, and mosaic symptoms. We describe the cloning of a cluster of NBS-LRR resistance gene candidates from MLG F of the virus-resistant soybean line PI96983 and demonstrate that multiple genes within this cluster interact to condition unique responses to SMV strains. In addition to cloning 3gG2, a strong candidate for the major Rsv1 resistance gene from PI96983, we describe various unique resistant and necrotic reactions coincident with the presence or absence of other members of this gene cluster. Responses of recombinant lines from a high-resolution mapping population of PI96983 (resistant) x Lee 68 (susceptible) demonstrate that more than one gene in this region of the PI96983 chromosome conditions resistance and/or necrosis to SMV. In addition, the soybean cultivars Marshall and Ogden, which carry other previously described Rsv1 alleles, are shown to possess the 3gG2 gene in a NBS-LRR gene cluster background distinct from PI96983. These observations suggest that two or more related non-TIR-NBS-LRR gene products are likely involved in the allelic response of several Rsv1-containing lines to SMV.

Full Text

The Full Text of this article is available as a PDF (335.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Banerjee D., Zhang X., Bent A. F. The leucine-rich repeat domain can determine effective interaction between RPS2 and other host factors in arabidopsis RPS2-mediated disease resistance. Genetics. 2001 May;158(1):439–450. doi: 10.1093/genetics/158.1.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bendahmane A., Kanyuka K., Baulcombe D. C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell. 1999 May;11(5):781–792. doi: 10.1105/tpc.11.5.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buell C. R., Somerville S. C. Use of Arabidopsis recombinant inbred lines reveals a monogenic and a novel digenic resistance mechanism to Xanthomonas campestris pv campestris. Plant J. 1997 Jul;12(1):21–29. doi: 10.1046/j.1365-313x.1997.12010021.x. [DOI] [PubMed] [Google Scholar]
  4. Collins N., Drake J., Ayliffe M., Sun Q., Ellis J., Hulbert S., Pryor T. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell. 1999 Jul;11(7):1365–1376. doi: 10.1105/tpc.11.7.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Creusot F., Macadré C., Ferrier Cana E., Riou C., Geffroy V., Sévignac M., Dron M., Langin T. Cloning and molecular characterization of three members of the NBS-LRR subfamily located in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris. Genome. 1999 Apr;42(2):254–264. doi: 10.1139/g98-134. [DOI] [PubMed] [Google Scholar]
  6. Ellis J., Dodds P., Pryor T. Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol. 2000 Aug;3(4):278–284. doi: 10.1016/s1369-5266(00)00080-7. [DOI] [PubMed] [Google Scholar]
  7. Gore M. A., Hayes A. J., Jeong S. C., Yue Y. G., Buss G. R., Maroof Saghai. Mapping tightly linked genes controlling potyvirus infection at the Rsv1 and Rpv1 region in soybean. Genome. 2002 Jun;45(3):592–599. doi: 10.1139/g02-009. [DOI] [PubMed] [Google Scholar]
  8. Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
  9. Kanazin V., Marek L. F., Shoemaker R. C. Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11746–11750. doi: 10.1073/pnas.93.21.11746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leister D., Ballvora A., Salamini F., Gebhardt C. A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet. 1996 Dec;14(4):421–429. doi: 10.1038/ng1296-421. [DOI] [PubMed] [Google Scholar]
  11. Meyers B. C., Dickerman A. W., Michelmore R. W., Sivaramakrishnan S., Sobral B. W., Young N. D. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 1999 Nov;20(3):317–332. doi: 10.1046/j.1365-313x.1999.t01-1-00606.x. [DOI] [PubMed] [Google Scholar]
  12. Michelmore R. W., Meyers B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998 Nov;8(11):1113–1130. doi: 10.1101/gr.8.11.1113. [DOI] [PubMed] [Google Scholar]
  13. Ori N., Eshed Y., Paran I., Presting G., Aviv D., Tanksley S., Zamir D., Fluhr R. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell. 1997 Apr;9(4):521–532. doi: 10.1105/tpc.9.4.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pan Q., Wendel J., Fluhr R. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol. 2000 Mar;50(3):203–213. doi: 10.1007/s002399910023. [DOI] [PubMed] [Google Scholar]
  15. Peñuela S., Danesh D., Young N. D. Targeted isolation, sequence analysis, and physical mapping of nonTIR NBS-LRR genes in soybean. Theor Appl Genet. 2002 Feb;104(2-3):261–272. doi: 10.1007/s00122-001-0785-0. [DOI] [PubMed] [Google Scholar]
  16. Richter T. E., Ronald P. C. The evolution of disease resistance genes. Plant Mol Biol. 2000 Jan;42(1):195–204. [PubMed] [Google Scholar]
  17. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  18. Shoemaker R. C., Polzin K., Labate J., Specht J., Brummer E. C., Olson T., Young N., Concibido V., Wilcox J., Tamulonis J. P. Genome duplication in soybean (Glycine subgenus soja). Genetics. 1996 Sep;144(1):329–338. doi: 10.1093/genetics/144.1.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sun Q., Collins N. C., Ayliffe M., Smith S. M., Drake J., Pryor T., Hulbert S. H. Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics. 2001 May;158(1):423–438. doi: 10.1093/genetics/158.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wang Z. X., Yano M., Yamanouchi U., Iwamoto M., Monna L., Hayasaka H., Katayose Y., Sasaki T. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 1999 Jul;19(1):55–64. doi: 10.1046/j.1365-313x.1999.00498.x. [DOI] [PubMed] [Google Scholar]
  21. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]
  22. Yu Y. G., Buss G. R., Maroof M. A. Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11751–11756. doi: 10.1073/pnas.93.21.11751. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES