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Volume 95, Issue 1

Alternative mutational pathways, outside the VPg, of rice yellow mottle virus to overcome eIF(iso)4G-mediated rice resistance under strong genetic constraints Free

Abstract

The adaptation of rice yellow mottle virus (RYMV) to -mediated resistance has been reported to involve mutations in the viral genome-linked protein (VPg). In this study, we analysed several cases of resistance breakdown by an isolate with low adaptability. Surprisingly, in these rarely occurring resistance-breaking (RB) genotypes, mutations were detected outside the VPg, in the ORF2a/ORF2b overlapping region. The causal role of three mutations associated with resistance breakdown was validated via directed mutagenesis of an infectious clone. In resistant plants, these mutations increased viral accumulation as efficiently as suboptimal RB mutations in the VPg. Interestingly, these mutations are located in a highly conserved, but unfolded, domain. Altogether, our results indicate that under strong genetic constraints, unfit genotypes can follow alternative mutational pathways, i.e. outside the VPg, to overcome resistance.

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© 2014 SGM
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2014-01-01
2024-04-25
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References

  1. Abdul-Razzak A., Guiraud T., Peypelut M., Walter J., Houvenaghel M.-C., Candresse T., Le Gall O., German-Retana S. 2009; Involvement of the cylindrical inclusion (CI) protein in the overcoming of an eIF4E-mediated resistance against Lettuce mosaic potyvirus. Mol Plant Pathol 10:109–113 [View Article][PubMed]
     [Google Scholar]
  2. Albar L., Bangratz-Reyser M., Hébrard E., Ndjiondjop M. N., Jones M., Ghesquière A. 2006; Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. . Plant J 47:417–426 [View Article][PubMed]
     [Google Scholar]
  3. Camps M., Herman A., Loh E., Loeb L. A. 2007; Genetic constraints on protein evolution. Crit Rev Biochem Mol Biol 42:313–326 [View Article][PubMed]
     [Google Scholar]
  4. Domingo E., Sheldon J., Perales C. 2012; Viral quasispecies evolution. Microbiol Mol Biol Rev 76:159–216 [View Article][PubMed]
     [Google Scholar]
  5. Fargette D., Pinel A., Abubakar Z., Traoré O., Brugidou C., Fatogoma S., Hébrard E., Choisy M., Séré Y. other authors 2004; Inferring the evolutionary history of Rice yellow mottle virus from genomic, phylogenetic, and phylogeographic studies. J Virol 78:3252–3261 [View Article][PubMed]
     [Google Scholar]
  6. Fargette D., Pinel A., Rakotomalala M., Sangu E., Traoré O., Sérémé D., Sorho F., Issaka S., Hébrard E. other authors 2008; Rice yellow mottle virus, an RNA plant virus, evolves as rapidly as most RNA animal viruses. J Virol 82:3584–3589 [View Article][PubMed]
     [Google Scholar]
  7. Harrison B. D. 2002; Virus variation in relation to resistance-breaking in plants. Euphytica 124:181–192 [View Article]
     [Google Scholar]
  8. Hébrard E., Bessin Y., Michon T., Longhi S., Uversky V. N., Delalande F., Van Dorsselaer A., Romero P., Walter J. other authors 2009; Intrinsic disorder in viral proteins genome-linked: experimental and predictive analyses. Virol J 6:23 [View Article][PubMed]
     [Google Scholar]
  9. Hébrard E., Poulicard N., Gérard C., Traoré O., Wu H. C., Albar L., Fargette D., Bessin Y., Vignols F. 2010; Direct interaction between the Rice yellow mottle virus (RYMV) VPg and the central domain of the rice eIF(iso)4G1 factor correlates with rice susceptibility and RYMV virulence. Mol Plant Microbe Interact 23:1506–1513 [View Article][PubMed]
     [Google Scholar]
  10. Librado P., Rozas J. 2009; DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452 [View Article][PubMed]
     [Google Scholar]
  11. Ling R., Pate A. E., Carr J. P., Firth A. E. 2013; An essential fifth coding ORF in the sobemoviruses. Virology 446:397–408 [View Article][PubMed]
     [Google Scholar]
  12. Nair S., Savithri H. S. 2010a; Natively unfolded nucleic acid binding P8 domain of SeMV polyprotein 2a affects the novel ATPase activity of the preceding P10 domain. FEBS Lett 584:571–576 [View Article][PubMed]
     [Google Scholar]
  13. Nair S., Savithri H. S. 2010b; Processing of SeMV polyproteins revisited. Virology 396:106–117 [View Article][PubMed]
     [Google Scholar]
  14. Nakahara K. S., Shimada R., Choi S. H., Yamamoto H., Shao J., Uyeda I. 2010; Involvement of the P1 cistron in overcoming eIF4E-mediated recessive resistance against Clover yellow vein virus in pea. Mol Plant Microbe Interact 23:1460–1469 [View Article][PubMed]
     [Google Scholar]
  15. Obradovic Z., Peng K., Vucetic S., Radivojac P., Dunker A. K. 2005; Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 61:Suppl 7176–182 [View Article][PubMed]
     [Google Scholar]
  16. Pinel-Galzi A., Rakotomalala M., Sangu E., Sorho F., Kanyeka Z., Traoré O., Sérémé D., Poulicard N., Rabenantoandro Y. other authors 2007; Theme and variations in the evolutionary pathways to virulence of an RNA plant virus species. PLoS Pathog 3:e180 [View Article][PubMed]
     [Google Scholar]
  17. Poulicard N., Pinel-Galzi A., Hébrard E., Fargette D. 2010; Why Rice yellow mottle virus, a rapidly evolving RNA plant virus, is not efficient at breaking rymv1-2 resistance. Mol Plant Pathol 11:145–154 [View Article][PubMed]
     [Google Scholar]
  18. Poulicard N., Pinel-Galzi A., Traoré O., Vignols F., Ghesquière A., Konaté G., Hébrard E., Fargette D. 2012; Historical contingencies modulate the adaptability of Rice yellow mottle virus. PLoS Pathog 8:e1002482 [View Article][PubMed]
     [Google Scholar]
  19. Prilusky J., Felder C. E., Zeev-Ben-Mordehai T., Rydberg E. H., Man O., Beckmann J. S., Silman I., Sussman J. L. 2005; FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21:3435–3438 [View Article][PubMed]
     [Google Scholar]
  20. Rakotomalala M., Pinel-Galzi A., Albar L., Ghesquière A., Rabenantaondro Y., Ramavovololona P., Fargette D. 2008; Resistance to Rice yellow mottle virus in the rice germplasm in Madagascar. Eur J Plant Pathol 122:277–286 [View Article]
     [Google Scholar]
  21. Rakotomalala M., Pinel-Galzi A., Mpunami A., Randrianasolo A., Ramavovololona P., Rabenantoandro Y., Fargette D. 2013; Rice yellow mottle virus in Madagascar and in the Zanzibar Archipelago; island systems and evolutionary time scale to study virus emergence. Virus Res 171:71–79 [View Article][PubMed]
     [Google Scholar]
  22. Rancurel C., Khosravi M., Dunker A. K., Romero P. R., Karlin D. 2009; Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83:10719–10736 [View Article][PubMed]
     [Google Scholar]
  23. Sanjuán R., Nebot M. R. 2008; A network model for the correlation between epistasis and genomic complexity. PLoS ONE 3:e2663 [View Article][PubMed]
     [Google Scholar]
  24. Satheshkumar P. S., Lokesh G. L., Savithri H. S. 2004; Polyprotein processing: cis and trans proteolytic activities of Sesbania mosaic virus serine protease. Virology 318:429–438 [View Article][PubMed]
     [Google Scholar]
  25. Satheshkumar P. S., Gayathri P., Prasad K., Savithri H. S. 2005; “Natively unfolded” VPg is essential for Sesbania mosaic virus serine protease activity. J Biol Chem 280:30291–30300 [View Article][PubMed]
     [Google Scholar]
  26. Simon-Loriere E., Holmes E. C., Pagán I. 2013; The effect of gene overlapping on the rate of RNA virus evolution. Mol Biol Evol 30:1916–1928 [View Article][PubMed]
     [Google Scholar]
  27. Traoré O., Pinel-Galzi A., Issaka S., Poulicard N., Aribi J., Aké S., Ghesquière A., Séré Y., Konaté G. other authors 2010; The adaptation of Rice yellow mottle virus to the eIF(iso)4G-mediated rice resistance. Virology 408:103–108 [View Article][PubMed]
     [Google Scholar]
  28. Truniger V., Aranda M. A. 2009; Recessive resistance to plant viruses. Adv Virus Res 75:119–159 [View Article][PubMed]
     [Google Scholar]
  29. Uversky V. N. 2013; The most important thing is the tail: multitudinous functionalities of intrinsically disordered protein termini. FEBS Lett 587:1891–1901 [View Article][PubMed]
     [Google Scholar]
  30. 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 13:795–803 [View Article][PubMed]
     [Google Scholar]
  31. Weinreich D. M., Watson R. A., Chao L. 2005; Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174[PubMed] [CrossRef]
     [Google Scholar]
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Alternative mutational pathways, outside the VPg, of rice yellow mottle virus to overcome eIF(iso)4G-mediated rice resistance under strong genetic constraints
J. Gen. Virol. 95, 219 (2014); https://doi.org/10.1099/vir.0.057810-0
/content/journal/jgv/10.1099/vir.0.057810-0
/content/journal/jgv/10.1099/vir.0.057810-0
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