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Theoretical and Applied Genetics

, Volume 126, Issue 11, pp 2849–2863 | Cite as

A series of eIF4E alleles at the Bc-3 locus are associated with recessive resistance to Clover yellow vein virus in common bean

  • John P. Hart
  • Phillip D. GriffithsEmail author
Original Paper

Abstract

Clover yellow vein virus (ClYVV) is capable of causing severe damage to common bean (Phaseolus vulgaris L.) production worldwide. The snap bean market class is particularly vulnerable because infection may lead to distortion and necrosis of the fresh green pods and rejection of the harvest. Three putatively independent recessive genes (cyv, desc, bc-3) have been reported to condition resistance to ClYVV; however, their allelic relationships have not been resolved. We identified, evaluated, and characterized the phenotypic and molecular genetic variation present in 21 informative common bean genotypes for resistance to ClYVV. Allelism testing phenotypes from multiple populations provided clear evidence that the three genes were a series of recessive alleles at the Bc-3 locus that condition unique potyvirus strain- and species-specific resistance spectra. Candidate gene analysis revealed complete association between the recessive resistance alleles and unique patterns of predicted amino acid substitutions in P. vulgaris eukaryotic translation initiation factor 4E (PveIF4E). This led to the discovery and characterization of two novel PveIF4E alleles associated with resistance to ClYVV, PveIF4E 3 , and PveIF4E 4 . We developed KASPar allele-specific SNP genotyping assays and demonstrated their ability to accurately detect and differentiate all of the PveIF4E haplotypes present in the germplasm, allelism testing, and in three separate segregating populations. The results contribute to an enhanced understanding and accessibility of the important potyvirus resistance conditioned by recessive alleles at Bc-3. The KASPar assays should be useful to further enable germplasm exploration, allelic discrimination, and marker-assisted introgression of bc-3 alleles in common bean.

Keywords

Common Bean Allelism Testing Bean Common Mosaic Virus Snap Bean Recessive Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors wish to thank James Kelly, Phil Miklas, Elise Vendeuvre, and Molly Welsh for provision of bean germplasm. A special thanks is due to Jason Cavatorta for his initial assistance with preliminary research and Michael Mazourek for providing laboratory space. We acknowledge the technical assistance of Matt Wavrick, and Sarah Durkee. We also thank two anonymous reviewers whose suggestions helped to improve the manuscript. This research was supported through funding from the New York State Vegetable Research Association. John Hart was provided with support from Pioneer Hi-Bred Intl. through Cornell University’s Department of Plant Breeding and Genetics, a Cornell Graduate School Fellowship, and the Bullis Fellowship of the NYSAES.

Supplementary material

122_2013_2176_MOESM1_ESM.docx (4.9 mb)
Supplementary material (DOCX 4987 kb)

References

  1. Afanador LK, Haley SD, Kelly JD (1993) Adoption of a mini-prep DNA extraction method for RAPD marker analysis in common bean (Phaseolus vulgaris L.). Annu Rep Bean Improv Coop 35:10–11Google Scholar
  2. Ali MA (1950) Genetics of resistance to the common bean mosaic virus in the bean (Phaseolus vulgaris L.). Phytopathol 40:69–79Google Scholar
  3. Andrade M, Abe Y, Nakahara KS, Uyeda I (2009) The cyv-2 resistance to Clover yellow vein virus in pea is controlled by the eukaryotic initiation factor 4E. J Gen Plant Pathol 75:241–249CrossRefGoogle Scholar
  4. Boodley JW, Sheldrake R (1972) Cornell peat-lite mixes for commercial plant growing. Cornell Info Bull 43:1–8Google Scholar
  5. Bos L, Lindsten K, Maat DZ (1977) Similarity of Clover yellow vein virus and Pea necrosis virus. Neth J Plant Pathol 83:97–108CrossRefGoogle Scholar
  6. Bruun-Rasmussen M, Moller IS, Tulinius G et al (2007) The same allele of translation initiation factor 4E mediates resistance against two Potyvrius spp. in Pisum sativum. Molec Plant Microb Interact 9:1075–1082CrossRefGoogle Scholar
  7. CABI/EPPO (2000) Clover yellow vein potyvirus. Distribution maps of plant diseases. CAB International, Wallingford, p 811Google Scholar
  8. Cavatorta JR, Savage AE, Yeam I, Gray SM, Jahn MM (2008) Positive darwinian selection at single amino-acid sites conferring plant virus resistance. J Mol Evol 67:551–559PubMedCrossRefGoogle Scholar
  9. Charron C, Nicolai M, Gallois JL et al (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68PubMedCrossRefGoogle Scholar
  10. Collmer CW, Marston MF, Taylor JC, Jahn M (2000) The I gene of bean: a dosage- dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to the Potyvirus Bean common mosaic virus. Molec Plant-Microbe Interact 13:1266–1270CrossRefGoogle Scholar
  11. Crnov R, Gilbertson RL (2001) Outbreak of Clover yellow vein virus in a bean field in Colusa County, California. Plant Dis 85:444CrossRefGoogle Scholar
  12. Diaz-Camino C, Annamalai P, Sanchez F et al (2011) An effective virus-based gene silencing method for functional genomics studies in common bean. Plant Methods 7:16PubMedCrossRefGoogle Scholar
  13. Diaz-Pendon JA, Truniger V, Nieto C et al (2004) Advances in understanding recessive resistance to plant viruses. Molec Plant Pathol 5:223–233CrossRefGoogle Scholar
  14. Dizadji A, Shahraeen N (2011) Occurrence, distribution and seasonal changes of viruses infecting common bean in northwestern Iran. Arch Phytopathol Plant Prot 44(17):1647–1654CrossRefGoogle Scholar
  15. Drijfhout E (1978) Genetic interaction between Phaseolus vulgaris and Bean common mosaic virus with implications for strain identification and breeding for resistance. Agric Res Rep 872:1–98Google Scholar
  16. Drijfhout E, Silbernagel MJ, Burke DW (1978) Differentiation of strains of Bean common mosaic virus. Neth J Plant Pathol 84:13–26CrossRefGoogle Scholar
  17. Forster RL, Strausbaugh CA, Stewart-Williams K, Myers JR (1994) Determination of resistance to BCMV in dry edible bean cultivars and breeding lines. Annu Rep Bean Improv Coop 37:1–8Google Scholar
  18. Gao A, Johansen E, Eyers S et al (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385PubMedCrossRefGoogle Scholar
  19. Halseth DE, Myers JR, Stewart-Williams K, Scully B (1998) Registration of ‘Black Knight’ black bean. Crop Sci 38:883CrossRefGoogle Scholar
  20. Hill JH, Alleman R, Hogg DB, Grau CR (2001) First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World. Plant Dis 85:561CrossRefGoogle Scholar
  21. Hjulsager CK, Lund OS, Johansen IE (2002) A new pathotype of pea seed-borne mosaic virus explained by properties of the P3-6K1 and viral genome-linked (VPg) coding regions. Mol Plant Microb Interact 15:169–171CrossRefGoogle Scholar
  22. Hofinger BJ, Jing HC, Hammond-Kossack KE, Kanyuka K (2009) High-resolution melting analysis of cDNA-derived PCR amplicons for rapid and cost-effective identifications of novel alleles in barley. Theor Appl Genet 119:851–865PubMedCrossRefGoogle Scholar
  23. Hofinger BJ, Russell JR, Bass CG et al (2011) An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Molec Ecol 20:3653–3668Google Scholar
  24. Hwang J, Li J, Liu W et al (2009) Double mutations in eIF4E and eIFiso4E confer recessive resistance to Chilli veinal mottle virus in Pepper. Mol Cells 27:329–336PubMedCrossRefGoogle Scholar
  25. Johnson WC, Guzman P, Mandala D, Mkandawire ABC, Temple S, Gilbertson RL, Gepts P (1997) Molecular tagging of the bc-3 gene for introgression into Andean common bean. Crop Sci 37:248–254CrossRefGoogle Scholar
  26. Kang BC, Yeam I, Jahn MM (2005a) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621PubMedCrossRefGoogle Scholar
  27. Kang BC, Yeam I, Frantz JD et al (2005b) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405PubMedCrossRefGoogle Scholar
  28. Keller KE, Johansen IE, Martin RR, Hampton RO (1998) Potyvirus genome-linked protein VPg determines pea-seed borne mosaic virus pathotype-specific virulence in Pisum sativum. Molec Plant Microb Interact 11:124–130CrossRefGoogle Scholar
  29. Kelly JD, Hosfield GL, Varner GV, Uebersax MA, Haley SD, Taylor J (1994) Registration of ‘Raven’ black bean. Crop Sci 34:1406–1407CrossRefGoogle Scholar
  30. Kelly JD, Afanador L, Haley SD (1995) Pyramiding genes for resistance to bean common mosaic virus. Euphytica 82:207–212CrossRefGoogle Scholar
  31. Kelly JD, Gepts P, Miklas PN, Coyne DP (2003) Tagging and mapping of genes and QTL and molecular-marker assisted selection for traits of economic importance in bean and cowpea. Field Crops Res 82:135–154CrossRefGoogle Scholar
  32. Larsen RC, Myers JR (2006) A pod necrosis disease (‘chocolate pod’) of snap bean (Phaseolus vulgaris) in Oregon caused by a strain of Clover yellow vein virus. Phytopathol 96:S169Google Scholar
  33. Larsen RC, Miklas PN, Eastwell CR et al (2002) A virus disease complex devastating late season snap bean production in the Midwest. Annu Rep Bean Improv Coop 45:36–37Google Scholar
  34. Larsen RC, Miklas PN, Druffel KL, Wyatt SD (2005) NL-3 K strain is a stable and naturally occurring interspecific recombinant derived from Bean common mosaic necrosis virus and Bean common mosaic virus. Phytopathol 95:1037–1042CrossRefGoogle Scholar
  35. Larsen RC, Miklas PN, Eastwell KC, Grau CR (2008) A strain of Clover yellow vein virus that causes severe pod necrosis disease in snap bean. Plant Dis 92:1026–1032CrossRefGoogle Scholar
  36. LeGall O, Aranda MA, Caranta C (2011) Plant resistance to viruses mediated by translation initiation factors. In: Caranta C et al (eds) Recent advances in plant virology. Caister Academic Press, Norfolk, pp 177–194Google Scholar
  37. Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051PubMedCrossRefGoogle Scholar
  38. Ling KS, Harris R, Meyer JDF (2009) Non-synonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to Zucchini yellow mosaic virus. Theor Appl Genet 120:191–200PubMedCrossRefGoogle Scholar
  39. McKern NM, Mink GI, Barnett OW, Mishra A, Whittaker LA, Silbernagel MJ, Ward CW, Shukla DD (1992) Isolates of bean common mosaic virus comprising two distinct potyviruses. Phytopathol 82:923–928CrossRefGoogle Scholar
  40. Miklas PN, Hang AN (1998) Release of cranberry dry bean germplasm lines USCR-7 and USCR-8 with resistance to bean common mosaic and necrosis viruses. Annu Rep Bean Improv Coop 41:227–228Google Scholar
  41. Miklas PN, Lambert S, Mink G, Silbernagel M (1998) Many beans with bc-3 resistance to BCMNV are susceptible to BCMV. Annu Rep Bean Improv Coop 41:33–34Google Scholar
  42. Miklas PN, Larsen RC, Riley R, Kelly J (2000) Potential marker-assisted selection for bc-1 2 resistance to bean common mosaic potyvirus in common bean. Euphtyica 116:211–219CrossRefGoogle Scholar
  43. Miklas PN, Hang AN, Kelly JD, Strausbaugh CA, Forster RL (2002) Registration of three kidney bean germplasm lines resistant to bean common mosaic and necrosis potyviruses: USLK-2 light red kidney, USDK-4 dark red kidney, and USWK-6 white kidney. Crop Sci 42:674–675CrossRefGoogle Scholar
  44. Morales FJ (2005) Bean common mosaic. In: Shwartz HF (ed) Compendium of Bean diseases. American Phytopathol Soc, St. Paul MN, pp 60–63Google Scholar
  45. Moury B, Morel C, Johansen E et al (2004) Mutations in potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact 17:322–329PubMedCrossRefGoogle Scholar
  46. Mukeshimana G, Paneda A, Rodriguez-Suarez C et al (2005) Markers linked to the bc-3 gene conditioning resistance to bean common mosaic potyviruses in common bean. Euphtyica 144:291–299CrossRefGoogle Scholar
  47. Naderpour M, Søgaard Lund O, Larsen R, Johansen E (2010) Potyviral resistance derived from cultivars of Phaseolus vulgaris carrying bc-3 is associated with the homozygotic presence of a mutated eIF4E allele. Mol Plant Pathol 11:255–263PubMedCrossRefGoogle Scholar
  48. Nault LR (1997) Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90:521–541Google Scholar
  49. Nault BA, Shah DA, Dillard HR, McFaul AC (2004) Seasonal and spatial dynamics of alate aphid dispersal in snap bean fields in proximity to alfalfa and implications for virus management. 33:1593–1601Google Scholar
  50. Nicaise V, German-Retana S, Sanjuán R et al (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132:1272–1282PubMedCrossRefGoogle Scholar
  51. Nicolas O, Dunnington SW, Gotow LF et al (1997) Variations in the VPg protein allow a potyvirus to overcome va gene resistance in tobacco. Virol 237:452–459CrossRefGoogle Scholar
  52. Ortiz V, Castro S, Romero J (2009) First report of Clover yellow vein virus in grain legumes in Spain. Plant Dis 93:106CrossRefGoogle Scholar
  53. Park SJ, Tu JC (1991) Inheritance and allelism of resistance to a severe strain of bean yellow mosaic virus in common bean. Can J Plant Pathol 13:7–10CrossRefGoogle Scholar
  54. Pedrosa-Harand A, Porch T, Gepts P (2008) Standard nomenclature for common bean chromosomes and linkage groups. Annu Rept Bean Improv Coop 51:106–107Google Scholar
  55. Phaseolus vulgaris V1.0, DOE-JGI and USDA-NIFA (2013) http://www.phytozome.net/commonbean. Accessed 08 May 2013
  56. Piron F, Nicolai M, Minoia S et al (2010) An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS One 5:e11313PubMedCrossRefGoogle Scholar
  57. Porch T (2009) List of genes—Phaseolus vulgaris L. Bean Improvement Cooperative. http://www.css.msu.edu/bic/PDF/Bean_Genes_List_2010.pdf. Accessed 23 Oct 2012
  58. Porch T (2012) Phaseolus Genes and Gene Symbol Nomenclature, Bean Improvement Cooperative Genetics Committee. www.css.msu.edu/bic/_pdf/Gene_Committee_Rules.pdf. Accessed 23 Oct 2012
  59. Provvidenti R (1987) List of genes in Phaseolus vulgaris for resistance to viruses. Annu Rep Bean Improv Coop 30:1–4Google Scholar
  60. Provvidenti R, Morales FJ (2005) Clover yellow vein. In: Shwartz HF (ed) Compendium of Bean Diseases. American Phytopathol Soc, St. Paul, pp 75–76Google Scholar
  61. Provvidenti R, Schroeder WT (1973) Resistance in Phaseolus vulgaris to the severe strain of Bean yellow mosaic virus. Phytopathol 63:196–197CrossRefGoogle Scholar
  62. Ragsdale DW, Voegtlin DJ, O’Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208CrossRefGoogle Scholar
  63. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45PubMedCrossRefGoogle Scholar
  64. Robinson P, Holmes J (2011) KASP version 4.0 SNP Genotyping Manual. Kbioscience. http://www.lgcgenomics.com/bbpPage/download/slug/kasp-technicalresources/link/337ad5493211ff491791f7d95469b0285eae1c1c.pdf. Accessed 23 Oct 2012
  65. Rozen S, Skaletsky HJ (2000) Primer3 on the www for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386Google Scholar
  66. Rubio M, Nicolai M, Caranta C, Palloix A (2009) Allele mining in the pepper gene pool provided new complementation effects between pvr2-eIF4E and pvr6-eIF(iso)4E alleles for resistance to pepper veinal mottle virus. J Gen Virol 90:2808–2814PubMedCrossRefGoogle Scholar
  67. Ruffel S, Dussault MH, Palloix A et al (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075PubMedCrossRefGoogle Scholar
  68. Ruffel S, Dussault MH, Palloix A et al (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Gen Genomics 274:346–353CrossRefGoogle Scholar
  69. Ruffel S, Gallois J, Moury B et al (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J Gen Virol 87:2089–2098PubMedCrossRefGoogle Scholar
  70. Sasaya T, Shimizu T, Nozu Y et al (1997) Biological, serological, and molecular variabilities of Clover yellow vein virus. Phtyopathol 87:1014–1019CrossRefGoogle Scholar
  71. Sato M, Masuta C, Uyeda I (2003) Natural resistance to Clover yellow vein virus in beans controlled by a single recessive locus. Molec Plant Microb Interact 16:994–1002CrossRefGoogle Scholar
  72. Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  73. Shah DA, Dillard HR, Mazumdar-Leighton S (2006) Incidence, spatial patterns, and associations among viruses in snap bean and alfalfa in New York. Plant Dis 90:203–210CrossRefGoogle Scholar
  74. Shail J, Taylor AG, Provvidenti R (2007) Bioassays to diagnose selected bean potyviruses. Annu Rep Bean Improv Coop 50:81–82Google Scholar
  75. Slater GSC, Birney E (2005) Automated generation of heuristics for biological sequence comparison. BMC Bioinforma 6:31CrossRefGoogle Scholar
  76. Stein N, Perovic D, Kumlehn J et al (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922PubMedCrossRefGoogle Scholar
  77. Strausbaugh CA, Miklas PN, Singh SP, Myers JR, Forster RL (2003) Genetic characterization of differential reactions among host group 3 common bean cultivars to NL-3 K strain of Bean common mosaic virus. Phytopathol 93:683–690CrossRefGoogle Scholar
  78. Tatchell SP, Baggett JR, Hampton RO (1985) Relationship between resistance to severe and type strains of Bean yellow mosaic virus. J Am Soc Hort Sci 110:96–99Google Scholar
  79. Tracy SL, Frenkel MJ, Gough KH et al (1992) Bean yellow mosaic, clover yellow vein, and pea mosaic are distinct potyviruses: evidence from coat protein gene sequences and molecular hybridization involving the 3′ non-coding regions. Arch Virol 122:249–261PubMedCrossRefGoogle Scholar
  80. Truniger V, Aranda MA (2009) Recessive resistance to plant viruses. Adv Virus Res 75:119–159PubMedCrossRefGoogle Scholar
  81. Tu JC (1980) Occurrence and identification of a flexuous rod virus from a mosaic complex of white beans in southern Ontario. Phytopathol Z 99:163–174CrossRefGoogle Scholar
  82. Tu JC (1983) Inheritance in Phaseolus vulgaris cv. Kentwood of resistance to a necrotic strain of bean yellow mosaic virus and to a severe bean strain of tobacco ringspot virus. Can J Plant Pathol 5:34–35CrossRefGoogle Scholar
  83. Tu JC (1988) Bean yellow mosaic: now the most severe virus disease of white beans in southwestern Ontario. Annu Rep Bean Improv Coop 31:143Google Scholar
  84. United States Department of Agriculture National Agricultural Statistics Service (USDA- NASS) (2011) Washington, DC. http://quickstats.nass.usda.gov/. Accessed 23 Oct 2012
  85. Uyeda I, Takahasi T, Shikata E (1991) Relatedness of the nucleotide sequence of the 3′- terminal region of clover yellow vein potyvirus RNA to bean yellow mosaic potyvirus RNA. Intervirol 32:234–245Google Scholar
  86. Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 7:795–803CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Plant Breeding and GeneticsCornell University, New York State Agricultural Experiment StationGenevaUSA

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