1887

Abstract

Allele mining on susceptibility factors offers opportunities to find new sources of resistance among crop wild relatives for breeding purposes. As a proof of concept, we used available RNAseq data to investigate polymorphisms among the four tomato genes encoding translation initiation factors [eIF4E1 and eIF4E2, eIFiso4E and the related gene new cap-binding protein(nCBP)] to look for new potential resistance alleles to potyviruses. By analysing polymorphism among RNAseq data obtained for 20 tomato accessions, 10 belonging to the cultivated type Solanum lycopersicum and 10 belonging to the closest related wild species Solanum pimpinellifolium, we isolated one new eIF4E1 allele, in the S. pimpinellifolium LA0411 accession, which encodes a potential new resistance allele, mainly due to a polymorphism associated with an amino acid change within eIF4E1 region II. We confirmed that this new allele, pot1 , is indeed associated with resistance to potato virus Y, although with a restricted resistance spectrum and a very low durability potential. This suggests that mutations occurring in eIF4E region II only may not be sufficient to provide efficient and durable resistance in plants. However, our study emphasizes the opportunity brought by RNAseq data to mine for new resistance alleles. Moreover, this approach could be extended to seek for putative new resistance alleles by screening for variant forms of susceptibility genes encoding plant host proteins known to interact with viral proteins.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000609
2016-11-10
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/11/3063.html?itemId=/content/journal/jgv/10.1099/jgv.0.000609&mimeType=html&fmt=ahah

References

  1. Andersen M. M., Landes X., Xiang W., Anyshchenko A., Falhof J., Østerberg J. T., Olsen L. I., Edenbrandt A. K., Vedel S. E. et al.( 2015;). Feasibility of new breeding techniques for organic farming. . Trends Plant Sci 20: 426–434. [CrossRef] [PubMed]
    [Google Scholar]
  2. Ayme V., Souche S., Caranta C., Jacquemond M., Chadoeuf J., Palloix A., Moury B..( 2006;). Different mutations in the genome-linked protein VPg of potato virus Y confer virulence on the pvr23 resistance in pepper. . Mol Plant Microbe Interact 19: 557–563. [CrossRef] [PubMed]
    [Google Scholar]
  3. Barabaschi D., Tondelli A., Desiderio F., Volante A., Vaccino P., Valè G., Cattivelli L..( 2016;). Next generation breeding. . Plant Sci 242: 3–13. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bernacchi D., Tanksley S. D..( 1997;). An interspecific backcross of Lycopersicon esculentum × L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. . Genetics 147: 861–877.[PubMed]
    [Google Scholar]
  5. Browning K. S., Bailey-Serres J..( 2015;). Mechanism of cytoplasmic mRNA translation. . Arabidopsis Book 13: e0176. [CrossRef] [PubMed]
    [Google Scholar]
  6. Cavatorta J. R., Savage A. E., Yeam I., Gray S. M., Jahn M. M..( 2008;). Positive Darwinian selection at single amino acid sites conferring plant virus resistance. . J Mol Evol 67: 551–559. [CrossRef] [PubMed]
    [Google Scholar]
  7. Chandrasekaran J., Brumin M., Wolf D., Leibman D., Klap C., Pearlsman M., Sherman A., Arazi T., Gal-On A..( 2016;). Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. . Mol Plant Pathol 17: 1140–1153. [CrossRef] [PubMed]
    [Google Scholar]
  8. Charron C..( 2007;). Caractérisation fonctionnelle et évolution moléculaire des gènes codant pour les facteurs d'initiation de la traduction eIF4E: des facteurs clés dans la résistance des plantes aux potyvirus. PhD thesis, Aix Marseille 2 University, Marseille, France;.
  9. Charron C., Nicolaï M., Gallois J.-L., Robaglia C., Moury B., Palloix A., Caranta C..( 2008;). Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. . Plant J 54: 56–68. [CrossRef] [PubMed]
    [Google Scholar]
  10. Danecek P., Auton A., Abecasis G., Albers C. A., Banks E., DePristo M. A., Handsaker R. E., Lunter G., Marth G. T. et al.( 2011;). The variant call format and VCFtools. . Bioinformatics 27: 2156–2158. [CrossRef] [PubMed]
    [Google Scholar]
  11. Devisetty U. K., Covington M. F., Tat A. V., Lekkala S., Maloof J. N..( 2014;). Polymorphism identification and improved genome annotation of Brassica rapa through deep RNA sequencing. . G3 (Bethesda) 4: 2065–2078. [CrossRef] [PubMed]
    [Google Scholar]
  12. Duprat A., Caranta C., Revers F., Menand B., Browning K. S., Robaglia C..( 2002;). The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. . Plant J 32: 927–934. [CrossRef] [PubMed]
    [Google Scholar]
  13. Elena S. F., Rodrigo G..( 2012;). Towards an integrated molecular model of plant–virus interactions. . Curr Opin Virol 2: 719–724. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fraser R. S. S..( 1990;). The genetics of resistance to plant viruses. . Annu Rev Phytopathol 28: 179–200. [CrossRef]
    [Google Scholar]
  15. Gao Z., Johansen E., Eyers S., Thomas C. L., Ellis T. H. N., Maule A. J..( 2004;). The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. . Plant J 40: 376–385. [CrossRef] [PubMed]
    [Google Scholar]
  16. Gauffier C., Lebaron C., Moretti A., Constant C., Moquet F., Bonnet G., Caranta C., Gallois J. L..( 2016;). A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy. . Plant J 85: 717–729. [CrossRef] [PubMed]
    [Google Scholar]
  17. Goodwin S., McPherson J. D., McCombie W. R..( 2016;). Coming of age: ten years of next-generation sequencing technologies. . Nat Rev Genet 17: 333–351. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hofinger B. J., Russell J. R., Bass C. G., Baldwin T., dos Reis M., Hedley P. E., Li Y., Macaulay M., Waugh R. 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. . Mol Ecol 20: 3653–3668. [CrossRef] [PubMed]
    [Google Scholar]
  19. Huang X. F., Wu J., Lv J. N., Zhang X., Jin Z. B..( 2015;). Identification of false-negative mutations missed by next-generation sequencing in retinitis pigmentosa patients: a complementary approach to clinical genetic diagnostic testing. . Genet Med 17: 307–311. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hwang J., Li J., Liu W.-Y., An S. J., Cho H., Her N. H., Yeam I., Kim D., Kang B.-C..( 2009;). Double mutations in eIF4E and eIFiso4E confer recessive resistance to Chilli veinal mottle virus in pepper. . Mol Cells 27: 329–336. [CrossRef] [PubMed]
    [Google Scholar]
  21. Ibiza V. P., Cañizares J., Nuez F..( 2010;). EcoTILLING in Capsicum species: searching for new virus resistances. . BMC Genomics 11: 631. [CrossRef] [PubMed]
    [Google Scholar]
  22. Jeong H.-J., Kwon J.-K., Pandeya D., Hwang J., Hoang N. H., Bae J.-H., Kang B.-C..( 2011;). A survey of natural and ethyl methane sulfonate-induced variations of eIF4E using high-resolution melting analysis in Capsicum. . Mol Breed 29: 349–360. [CrossRef]
    [Google Scholar]
  23. Koenig D., Jiménez-Gómez J. M., Kimura S., Fulop D., Chitwood D. H., Headland L. R., Kumar R., Covington M. F., Devisetty U. K. et al.( 2013;). Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. . Proc Natl Acad Sci U S A 110: E2655E2662. [CrossRef] [PubMed]
    [Google Scholar]
  24. Konečná E., Šafářová D., Navrátil M., Hanáček P., Coyne C., Flavell A., Vishnyakova M., Ambrose M., Redden R., Smýkal P..( 2014;). Geographical gradient of the eIF4E alleles conferring resistance to potyviruses in pea (Pisum) germplasm. . PLoS One 9: e90394. [CrossRef] [PubMed]
    [Google Scholar]
  25. Legnani R., Selassie K. G., Womdim R. N., Gognalons P., Moretti A., Laterrot H., Marchoux G..( 1995;). Evaluation and inheritance of the Lycopersicon hirsutum resistance against potato virus Y. . Euphytica 86: 219–226.
    [Google Scholar]
  26. Legnani R., Gognalons P., Moretti A., Marchoux G., Selassie K. G., Laterrot H..( 1996;). Identification and characterization of resistance to Tobacco etch virus in Lycopersicon species. . Plant Dis 80: 306. [CrossRef]
    [Google Scholar]
  27. Li H., Durbin R..( 2009;). Fast and accurate short read alignment with Burrows–Wheeler transform. . Bioinformatics 25: 1754–1760. [CrossRef] [PubMed]
    [Google Scholar]
  28. Martin M..( 2011;). Cutadapt removes adapter sequences from high-throughput sequencing reads. . EMBnet J 17: 10–12. [CrossRef]
    [Google Scholar]
  29. Martínez F., Rodrigo G., Aragonés V., Ruiz M., Lodewijk I., Fernández U., Elena S. F., Daròs J.-A..( 2016;). Interaction network of tobacco etch potyvirus NIa protein with the host proteome during infection. . BMC Genomics 17: 87. [CrossRef] [PubMed]
    [Google Scholar]
  30. Mazier M., Flamain F., Nicolaï M., Sarnette V., Caranta C..( 2011;). Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. . PLoS One 6: e29595. [CrossRef] [PubMed]
    [Google Scholar]
  31. McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S. et al.( 2010;). The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. . Genome Res 20: 1297–1303. [CrossRef] [PubMed]
    [Google Scholar]
  32. Moury B., Morel C., Johansen E., Guilbaud L., Souche S., Ayme V., Caranta C., Palloix A., Jacquemond M..( 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: 322–329. [CrossRef] [PubMed]
    [Google Scholar]
  33. Nabholz B., Sarah G., Sabot F., Ruiz M., Adam H., Nidelet S., Ghesquière A., Santoni S., David J., Glémin S..( 2014;). Transcriptome population genomics reveals severe bottleneck and domestication cost in the African rice (Oryza glaberrima). . Mol Ecol 23: 2210–2227. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nicaise V., German-Retana S., Sanjuán R., Dubrana M. P., Mazier M., Maisonneuve B., Candresse T., Caranta C., LeGall O..( 2003;). The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. . Plant Physiol 132: 1272–1282. [CrossRef] [PubMed]
    [Google Scholar]
  35. Nicaise V., Gallois J.-L., Chafiai F., Allen L. M., Schurdi-Levraud V., Browning K. S., Candresse T., Caranta C., Le Gall O., German-Retana S..( 2007;). Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsis thaliana. . FEBS Lett 581: 1041–1046. [CrossRef] [PubMed]
    [Google Scholar]
  36. Nieto C., Piron F., Dalmais M., Marco C. F., Moriones E., Gómez-Guillamón M. L., Truniger V., Gómez P., Garcia-Mas J. et al.( 2007;). EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. . BMC Plant Biol 7: 34. [CrossRef] [PubMed]
    [Google Scholar]
  37. Ouibrahim L., Mazier M., Estevan J., Pagny G., Decroocq V., Desbiez C., Moretti A., Gallois J.-L., Caranta C..( 2014;). Cloning of the Arabidopsis rwm1 gene for resistance to Watermelon mosaic virus points to a new function for natural virus resistance genes. . Plant J 79: 705–716. [CrossRef] [PubMed]
    [Google Scholar]
  38. Park J. Y., Clark P., Londin E., Sponziello M., Kricka L. J., Fortina P..( 2015;). Clinical exome performance for reporting secondary genetic findings. . Clin Chem 61: 213–220. [CrossRef] [PubMed]
    [Google Scholar]
  39. Parrella G., Ruffel S., Moretti A., Morel C., Palloix A., Caranta C..( 2002;). Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes. . Theor Appl Genet 105: 855–861. [CrossRef] [PubMed]
    [Google Scholar]
  40. Pavan S., Jacobsen E., Visser R. G., Bai Y..( 2010;). Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. . Mol Breed 25: 1–12. [CrossRef] [PubMed]
    [Google Scholar]
  41. Pease J. B., Haak D. C., Hahn M. W., Moyle L. C..( 2016;). Phylogenomics reveals three sources of adaptive variation during a rapid radiation. . PLoS Biol 14: e1002379. [CrossRef] [PubMed]
    [Google Scholar]
  42. Piron F., Nicolaï M., Minoïa S., Piednoir E., Moretti A., Salgues A., Zamir D., Caranta C., Bendahmane A..( 2010;). An induced mutation in tomato eIF4E leads to immunity to two potyviruses. . PLoS One 5: e11313. [CrossRef] [PubMed]
    [Google Scholar]
  43. Pyott D. E., Sheehan E., Molnar A..( 2016;). Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. . Mol Plant Pathol 17: 1276–1288. [CrossRef] [PubMed]
    [Google Scholar]
  44. Quenouille J., Saint-Felix L., Moury B., Palloix A..( 2016;). Diversity of genetic backgrounds modulating the durability of a major resistance gene. Analysis of a core collection of pepper landraces resistant to Potato virus Y. . Mol Plant Pathol 17: 296–302. [CrossRef] [PubMed]
    [Google Scholar]
  45. Robaglia C., Caranta C..( 2006;). Translation initiation factors: a weak link in plant RNA virus infection. . Trends Plant Sci 11: 40–45. [CrossRef] [PubMed]
    [Google Scholar]
  46. Ruffel S., Dussault M.-H., Palloix A., Moury B., Bendahmane A., Robaglia C., Caranta C..( 2002;). A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). . Plant J 32: 1067–1075. [CrossRef] [PubMed]
    [Google Scholar]
  47. Ruffel S., Gallois J. L., Lesage M. L., Caranta C..( 2005;). The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. . Mol Genet Genomics 274: 346–353. [CrossRef] [PubMed]
    [Google Scholar]
  48. Ruffel S., Gallois J. L., Moury B., Robaglia C., Palloix A., Caranta C..( 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: 2089–2098. [CrossRef] [PubMed]
    [Google Scholar]
  49. Ruud K. A., Kuhlow C., Goss D. J., Browning K. S..( 1998;). Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. . J Biol Chem 273: 10325–10330. [CrossRef] [PubMed]
    [Google Scholar]
  50. Sarah G., Homa F., Pointet S., Contreras S., Sabot F., Nabholz B., Santoni S., Sauné L., Ardisson M. et al.( 2016;). A large set of 26 new reference transcriptomes dedicated to comparative population genomics in crops and wild relatives. . Mol Ecol Resour (in press), doi: [CrossRef] [PubMed]
    [Google Scholar]
  51. Sato M., Nakahara K., Yoshii M., Ishikawa M., Uyeda I..( 2005;). Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. . FEBS Lett 579: 1167–1171. [CrossRef] [PubMed]
    [Google Scholar]
  52. Schaad M. C., Anderberg R. J., Carrington J. C..( 2000;). Strain-specific interaction of the tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. . Virology 273: 300–306. [CrossRef] [PubMed]
    [Google Scholar]
  53. Tomato Genome Consortium( 2012;). The tomato genome sequence provides insights into fleshy fruit evolution. . Nature 485: 635–641. [CrossRef] [PubMed]
    [Google Scholar]
  54. van Schie C. C., Takken F. L..( 2014;). Susceptibility genes 101: how to be a good host. . Annu Rev Phytopathol 52: 551–581. [CrossRef] [PubMed]
    [Google Scholar]
  55. Wang A., Krishnaswamy S..( 2012;). Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement: eIF4E-mediated resistance to plant viruses. . Mol Plant Pathol 13: 795–803.[CrossRef]
    [Google Scholar]
  56. Yang P., Lüpken T., Habekuss A., Hensel G., Steuernagel B., Kilian B., Ariyadasa R., Himmelbach A., Kumlehn J. et al.( 2014;). Protein disulfide isomerase like 5-1 is a susceptibility factor to plant viruses. . Proc Natl Acad Sci U S A 111: 2104–2109. [CrossRef] [PubMed]
    [Google Scholar]
  57. Yeam I., Cavatorta J. R., Ripoll D. R., Kang B. C., Jahn M. M..( 2007;). Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. . Plant Cell 19: 2913–2928. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000609
Loading
/content/journal/jgv/10.1099/jgv.0.000609
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error