1887

Abstract

Recombination events are frequently inferred from the increasing number of sequenced viral genomes, but their impact on natural viral populations has rarely been evidenced. TYLCV-IS76 is a recombinant (,) between the Israel strain of tomato yellow leaf curl virus (TYLCV-IL) and the Spanish strain of tomato yellow leaf curl Sardinia virus (TYLCSV-ES) that was generated most probably in the late 1990s in southern Morocco (Souss). Its emergence in the 2000s coincided with the increasing use of resistant tomato cultivars bearing the gene, and led eventually to the entire displacement of both parental viruses in the Souss. Here, we provide compelling evidence that this viral population shift was associated with selection of TYLCV-IS76 viruses in tomato plants and particularly in -bearing cultivars. Real-time quantitative PCR (qPCR) monitoring revealed that TYLCV-IS76 DNA accumulation in -bearing plants was significantly higher than that of representatives of the parental virus species in single infection or competition assays. This advantage of the recombinant in -bearing plants was not associated with a fitness cost in a susceptible, nearly isogenic, cultivar. In competition assays in the resistant cultivar, the DNA accumulation of the TYLCV-IL clone – the parent less affected by the gene in single infection – dropped below the qPCR detection level at 120 days post-infection (p.i.) and below the whitefly vector () transmissibility level at 60 days p.i. The molecular basis of the selective advantage of TYLCV-IS76 is discussed in relation to its non-canonical recombination pattern, and the RNA-dependent RNA polymerase encoded by the gene.

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2016-12-16
2020-04-02
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References

  1. Barbieri M., Acciarri N., Sabatini E., Sardo L., Accotto G., Pecchioni N.. 2010; Introgression of resistance to two Mediterranean virus species causing tomato yellow leaf curl into a valuable traditional tomato variety. J Plant Pathol92:485–493
    [Google Scholar]
  2. Belabess Z., Dallot S., El-Montaser S., Granier M., Majde M., Tahiri A., Blenzar A., Urbino C., Peterschmitt M.. 2015; Monitoring the dynamics of emergence of a non-canonical recombinant of Tomato yellow leaf curl virus and displacement of its parental viruses in tomato. Virology486:291–306 [CrossRef][PubMed]
    [Google Scholar]
  3. Butterbach P., Verlaan M. G., Dullemans A., Lohuis D., Visser R. G., Bai Y., Kormelink R.. 2014; Tomato yellow leaf curl virus resistance by Ty-1 involves increased cytosine methylation of viral genomes and is compromised by cucumber mosaic virus infection. Proc Natl Acad Sci U S A111:12942–12947 [CrossRef][PubMed]
    [Google Scholar]
  4. Carrasco P., de la Iglesia F., Elena S. F.. 2007; Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco Etch virus. J Virol81:12979–12984 [CrossRef][PubMed]
    [Google Scholar]
  5. Chakraborty S., Vanitharani R., Chattopadhyay B., Fauquet C. M.. 2008; Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J Gen Virol89:818–828 [CrossRef][PubMed]
    [Google Scholar]
  6. Condra J. H., Schleif W. A., Blahy O. M., Gabryelski L. J., Graham D. J., Quintero J. C., Rhodes A., Robbins H. L., Roth E. et al. 1995; In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature374:569–571 [CrossRef][PubMed]
    [Google Scholar]
  7. Davino S., Napoli C., Dellacroce C., Miozzi L., Noris E., Davino M., Accotto G. P.. 2009; Two new natural begomovirus recombinants associated with the tomato yellow leaf curl disease co-exist with parental viruses in tomato epidemics in Italy. Virus Res143:15–23 [CrossRef][PubMed]
    [Google Scholar]
  8. Davino S., Miozzi L., Panno S., Rubio L., Davino M., Accotto G. P.. 2012; Recombination profiles between tomato yellow leaf curl virus and tomato yellow leaf curl Sardinia virus in laboratory and field conditions: evolutionary and taxonomic implications. J Gen Virol93:2712–2717 [CrossRef][PubMed]
    [Google Scholar]
  9. Dellaporta S. L., Wood J., Hicks J. B.. 1983; A plant DNA minipreparation: Version II. Plant Mol Biol Report1:19–21 [CrossRef]
    [Google Scholar]
  10. Fernández-Cuartero B., Burgyán J., Aranda M. A., Salánki K., Moriones E., García-Arenal F.. 1994; Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology203:373–377 [CrossRef][PubMed]
    [Google Scholar]
  11. Fondong V. N., Pita J. S., Rey M. E., de Kochko A., Beachy R. N., Fauquet C. M.. 2000; Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J Gen Virol81:287–297 [CrossRef][PubMed]
    [Google Scholar]
  12. García-Andrés S., Tomás D. M., Navas-Castillo J., Moriones E.. 2009; Resistance-driven selection of begomoviruses associated with the tomato yellow leaf curl disease. Virus Res146:66–72 [CrossRef][PubMed]
    [Google Scholar]
  13. García-Andrés S., Monci F., Navas-Castillo J., Moriones E.. 2006; Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology350:433–442 [CrossRef][PubMed]
    [Google Scholar]
  14. García-Andrés S., Accotto G. P., Navas-Castillo J., Moriones E.. 2007a; Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology359:302–312 [CrossRef]
    [Google Scholar]
  15. García-Andrés S., Tomás D. M., Sánchez-Campos S., Navas-Castillo J., Moriones E.. 2007b; Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology365:210–219 [CrossRef]
    [Google Scholar]
  16. Gómez P., Sempere R. N., Elena S. F., Aranda M. A.. 2009; Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J Virol83:12378–12387 [CrossRef][PubMed]
    [Google Scholar]
  17. Hillung J., Cuevas J. M., Elena S. F.. 2015; Evaluating the within-host fitness effects of mutations fixed during virus adaptation to different ecotypes of a new host. Philos Trans R Soc B Biol Sci370:20140292 [CrossRef]
    [Google Scholar]
  18. Lapidot M., Friedmann M., Pilowsky M., Ben-Joseph R., Cohen S.. 2001; Effect of host plant resistance to Tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector. Phytopathology91:1209–1213 [CrossRef][PubMed]
    [Google Scholar]
  19. Larder B. A.. 1994; Interactions between drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase. J Gen Virol75:951–957 [CrossRef][PubMed]
    [Google Scholar]
  20. Lefeuvre P., Moriones E.. 2015; Recombination as a motor of host switches and virus emergence: geminiviruses as case studies. Curr Opin Virol10:14–19 [CrossRef][PubMed]
    [Google Scholar]
  21. Michelson I., Zamir D., Czosnek H.. 1994; Accumulation and translocation of Tomato yellow Leaf curl virus (TYLCV) in a Lycopersicon esculentum breeding line containing the L. chilense TYLCV tolerance gene Ty-1. Phytopathology84:928–933 [CrossRef]
    [Google Scholar]
  22. Monci F., Sánchez-Campos S., Navas-Castillo J., Moriones E.. 2002; A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology303:317–326 [CrossRef][PubMed]
    [Google Scholar]
  23. Moudy R. M., Meola M. A., Morin L. L., Ebel G. D., Kramer L. D.. 2007; A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg77:365–370[PubMed]
    [Google Scholar]
  24. Pérez de Castro A., Díez M. J., Nuez F.. 2005; Evaluation of breeding tomato lines partially resistant to Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus derived from Lycopersicon chilense. Can J Plant Pathol27:268–275 [CrossRef]
    [Google Scholar]
  25. Péréfarres F., Thébaud G., Lefeuvre P., Chiroleu F., Rimbaud L., Hoareau M., Reynaud B., Lett J.-M.. 2014; Frequency-dependent assistance as a way out of competitive exclusion between two strains of an emerging virus. Proc Biol Sci281:20133374 [CrossRef][PubMed]
    [Google Scholar]
  26. R_Development_Core_Team. 2010; R: A Language and Environment for Statistical Computing Vienna: R Foundation for Statistical Computing;
    [Google Scholar]
  27. Richman D. D., Havlir D., Corbeil J., Looney D., Ignacio C., Spector S. A., Sullivan J., Cheeseman S., Barringer K. et al. 1994; Nevirapine resistance mutations of human immunodeficiency virus type 1 selected during therapy. J Virol68:1660–1666[PubMed]
    [Google Scholar]
  28. Rodríguez-Negrete E. A., Carrillo-Tripp J., Rivera-Bustamante R. F.. 2009; RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol83:1332–1340 [CrossRef][PubMed]
    [Google Scholar]
  29. Sánchez-Campos S., Navas-Castillo J., Camero R., Soria C., Díaz J. A., Moriones E.. 1999; Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology89:1038–1043 [CrossRef][PubMed]
    [Google Scholar]
  30. Sahu P. P., Sharma N., Puranik S., Prasad M.. 2014; Post-transcriptional and epigenetic arms of RNA silencing: a defense machinery of naturally tolerant tomato plant against Tomato leaf curl New Delhi virus. Plant Mol Biol Report32:1015–1029 [CrossRef]
    [Google Scholar]
  31. Shi M., Holmes E. C., Brar M. S., Leung F. C.-C.. 2013; Recombination is associated with an outbreak of novel highly pathogenic porcine reproductive and respiratory syndrome viruses in China. J Virol87:10904–10907 [CrossRef][PubMed]
    [Google Scholar]
  32. Tahiri A., Sekkat A., Bennani A., Granier M., Delvare G., Peterschmitt M.. 2006; Distribution of tomato-infecting begomoviruses and Bemisia tabaci biotypes in Morocco. Ann Appl Biol149:175–186 [CrossRef]
    [Google Scholar]
  33. Tahiri A., Halkett F., Granier M., Gueguen G., Peterschmitt M.. 2013; Evidence of gene flow between sympatric populations of the Middle East-Asia Minor 1 and Mediterranean putative species of Bemisia tabaci. Ecol Evol3:2619–2633 [CrossRef]
    [Google Scholar]
  34. Tromas N., Zwart M. P., Poulain M., Elena S. F.. 2014; Estimation of the in vivo recombination rate for a plant RNA virus. J Gen Virol95:724–732 [CrossRef][PubMed]
    [Google Scholar]
  35. Urbino C., Gutiérrez S., Antolik A., Bouazza N., Doumayrou J., Granier M., Martin D. P., Peterschmitt M.. 2013; Within-host dynamics of the emergence of Tomato yellow leaf curl virus recombinants. PLoS One8:e58375 [CrossRef][PubMed]
    [Google Scholar]
  36. Vu T. T., Holmes E. C., Duong V., Nguyen T. Q., Tran T. H., Quail M., Churcher C., Parkhill J., Cardosa J. et al. 2010; Emergence of the Asian 1 genotype of dengue virus serotype 2 in Viet Nam: in vivo fitness advantage and lineage replacement in South-East Asia. PLoS Negl Trop Dis4:e757 [CrossRef][PubMed]
    [Google Scholar]
  37. Vuillaume F., Thébaud G., Urbino C., Forfert N., Granier M., Froissart R., Blanc S., Peterschmitt M.. 2011; Distribution of the phenotypic effects of random homologous recombination between two virus species. PLoS Pathog7:e1002028 [CrossRef][PubMed]
    [Google Scholar]
  38. Wain-Hobson S., Renoux-Elbé C., Vartanian J. P., Meyerhans A.. 2003; Network analysis of human and simian immunodeficiency virus sequence sets reveals massive recombination resulting in shorter pathways. J Gen Virol84:885–895 [CrossRef][PubMed]
    [Google Scholar]
  39. Worobey M., Holmes E. C.. 1999; Evolutionary aspects of recombination in RNA viruses. J Gen Virol80:2535–2543 [CrossRef][PubMed]
    [Google Scholar]
  40. Yadav R. K., Chattopadhyay D.. 2011; Enhanced viral intergenic region-specific short interfering RNA accumulation and DNA methylation correlates with resistance against a geminivirus. Mol Plant Microbe Interact24:1189–1197 [CrossRef][PubMed]
    [Google Scholar]
  41. Yang X., Wang Y., Guo W., Xie Y., Xie Q., Fan L., Zhou X.. 2011; Characterization of small interfering RNAs derived from the geminivirus/betasatellite complex using deep sequencing. PLoS One6:e16928 [CrossRef][PubMed]
    [Google Scholar]
  42. Zhou X., Liu Y., Calvert L., Munoz C., Otim-Nape G. W., Robinson D. J., Harrison B. D.. 1997; Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol78:2101–2111 [CrossRef][PubMed]
    [Google Scholar]
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