1887

Journal of General Virology header logo

Volume 98, Issue 7

Quantitative trait loci in pepper control the effective population size of two RNA viruses at inoculation Free

Abstract

Infection of plants by viruses is a complex process involving several steps: inoculation into plant cells, replication in inoculated cells and plant colonization. The success of the different steps depends, in part, on the viral effective population size (), defined as the number of individuals passing their genes to the next generation. During infection, the virus population will undergo bottlenecks, leading to drastic reductions in and, potentially, to the loss of the fittest variants. Therefore, it is crucial to better understand how plants affect . We aimed to (i) identify the plant genetic factors controlling during inoculation, (ii) understand the mechanisms used by the plant to control and (iii) compare these genetic factors with the genes controlling plant resistance to viruses. was measured in a doubled-haploid population of . Plants were inoculated with either a (PVY) construct expressing the green fluorescent protein or a necrotic variant of (CMV). was assessed by counting the number of primary infection foci on cotyledons for PVY or the number of necrotic local lesions on leaves for CMV. The number of foci and lesions was correlated (=0.57) and showed a high heritability (=0.93 for PVY and =0.98 for CMV). The of the two viruses was controlled by both common quantitative trait loci (QTLs) and virus-specific QTLs, indicating the contribution of general and specific mechanisms. The PVY-specific QTL colocalizes with a QTL that reduces PVY accumulation and the capacity to break down a major-effect resistance gene.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bottlenecks , Capsicum annuum , Cucumber mosaic virus , effective population size , Potato virus Y , quantitative trait loci and virus infection
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000835
2017-07-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/7/1923.html?itemId=/content/journal/jgv/10.1099/jgv.0.000835&mimeType=html&fmt=ahah

References

  1. Mcdonald BA, Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 2002; 40:349–379 [View Article][PubMed]
     [Google Scholar]
  2. Rojas MR, Gilbertson RL. Emerging plant viruses: a diversity of mechanisms and opportunities. In: Plant Virus Evolution Berlin, Heidelberg: Springer; 2008 pp. 27–51 [CrossRef]
     [Google Scholar]
  3. Elena SF, Bedhomme S, Carrasco P, Cuevas JM, de La Iglesia F et al. The evolutionary genetics of emerging plant RNA viruses. Mol Plant Microbe Interact 2011; 24:287–293 [View Article][PubMed]
     [Google Scholar]
  4. Brown JK. Durable resistance of crops to disease: a Darwinian perspective. Annu Rev Phytopathol 2015; 53:513–539 [View Article][PubMed]
     [Google Scholar]
  5. García-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 2001; 39:157–186 [View Article][PubMed]
     [Google Scholar]
  6. Elena SF, Sanjuán R. Virus evolution: insights from an experimental approach. Annu Rev Ecol Evol Syst 2007; 38:27–52 [View Article]
     [Google Scholar]
  7. Sacristán S, Malpica JM, Fraile A, García-Arenal F. Estimation of population bottlenecks during systemic movement of tobacco mosaic virus in tobacco plants. J Virol 2003; 77:9906–9911 [View Article][PubMed]
     [Google Scholar]
  8. Rouzine IM, Rodrigo A, Coffin JM. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol Mol Biol Rev 2001; 65:151–185 [View Article][PubMed]
     [Google Scholar]
  9. Li H, Roossinck MJ. Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 2004; 78:10582–10587 [View Article][PubMed]
     [Google Scholar]
  10. Moury B, Fabre F, Senoussi R. Estimation of the number of virus particles transmitted by an insect vector. Proc Natl Acad Sci USA 2007; 104:17891–17896 [View Article][PubMed]
     [Google Scholar]
  11. Betancourt M, Fereres A, Fraile A, García-Arenal F. Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus. J Virol 2008; 82:12416–12421 [View Article][PubMed]
     [Google Scholar]
  12. Sacristán S, Díaz M, Fraile A, García-Arenal F. Contact transmission of tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J Virol 2011; 85:4974–4981 [View Article][PubMed]
     [Google Scholar]
  13. González-Jara P, Fraile A, Canto T, García-Arenal F. The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J Virol 2009; 83:7487–7494 [View Article][PubMed]
     [Google Scholar]
  14. Gutiérrez S, Pirolles E, Yvon M, Baecker V, Michalakis Y et al. The multiplicity of cellular infection changes depending on the route of cell infection in a plant virus. J Virol 2015; 89:9665–9675 [View Article][PubMed]
     [Google Scholar]
  15. Zwart MP, Elena SF. Matters of size: genetic bottlenecks in virus infection and their potential impact on evolution. Annu Rev Virol 2015; 2:161–179 [View Article][PubMed]
     [Google Scholar]
  16. Gutiérrez S, Michalakis Y, Blanc S. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr Opin Virol 2012; 2:546–555 [View Article][PubMed]
     [Google Scholar]
  17. Acosta-Leal R, Xiong Z. Complementary functions of two recessive R-genes determine resistance durability of tobacco ‘Virgin A Mutant’ (VAM) to Potato virus Y. Virology 2008; 379:275–283 [View Article][PubMed]
     [Google Scholar]
  18. Marczewski W, Flis B, Syller J, Schäfer-Pregl R, Gebhardt C. A major quantitative trait locus for resistance to Potato leafroll virus is located in a resistance hotspot on potato chromosome XI and is tightly linked to N-gene-like markers. Mol Plant Microbe Interact 2001; 14:1420–1425 [View Article][PubMed]
     [Google Scholar]
  19. Quenouille J, Paulhiac E, Moury B, Palloix A. Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants. Heredity 2014; 112:579–587 [View Article][PubMed]
     [Google Scholar]
  20. Quenouille J, Montarry J, Palloix A, Farther MB. Slower, stronger: how the plant genetic background protects a major resistance gene from breakdown: mechanisms of polygenic resistance durability. Mol Plant Pathol 2013; 14:109–118 [CrossRef]
     [Google Scholar]
  21. Zwart MP, Daròs JA, Elena SF. One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog 2011; 7:e1002122 [View Article][PubMed]
     [Google Scholar]
  22. Chao L. Fitness of RNA virus decreased by Muller's ratchet. Nature 1990; 348:454–455 [View Article][PubMed]
     [Google Scholar]
  23. Bald JG. The use of numbers of infections for comparing the concentration of plant virus suspensions: dilution experiments with purified suspensions. Ann Appl Biol 1937; 24:33–55 [View Article]
     [Google Scholar]
  24. Kleczkowski A. Interpreting relationships between the concentrations of plant viruses and numbers of local lesions. J Gen Microbiol 1950; 4:53–69 [View Article][PubMed]
     [Google Scholar]
  25. Lauffer MA, Price WC. Infection by viruses. Arch Biochem 1945; 8:449–450[PubMed]
     [Google Scholar]
  26. García-Arenal F, Fraile A. Population dynamics and genetics of plant infection by viruses. In Recent Advances in Plant Virology Norfolk, UK: Caister Academic Press; 2011
     [Google Scholar]
  27. Caranta C, Palloix A, Lefebvre V, Daubèze AM. QTLs for a component of partial resistance to cucumber mosaic virus in pepper: restriction of virus installation in host-cells. Theor Appl Genet 1997; 94:431–438 [View Article]
     [Google Scholar]
  28. Djian-Caporalino C, Lefebvre V, Sage-Daubèze A-M, Palloix A. Capsicum. In Singh RJ. (editor) Genetic Resources, Chromosome Engineering, and Crop Improvement: Vegetable Crops Florida, USA: CRC Press; 2006 pp. 185–243 [CrossRef]
     [Google Scholar]
  29. Ayme V, Souche S, Caranta C, Jacquemond M, Chadoeuf J et al. Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol Plant Microbe Interact 2006; 19:557–563 [View Article][PubMed]
     [Google Scholar]
  30. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003; 19:889–890 [View Article][PubMed]
     [Google Scholar]
  31. Voorrips RE. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 2002; 93:77–78 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000835
Loading
Quantitative trait loci in pepper control the effective population size of two RNA viruses at inoculation
J. Gen. Virol. 98, 1923 (2017); https://doi.org/10.1099/jgv.0.000835
/content/journal/jgv/10.1099/jgv.0.000835
/content/journal/jgv/10.1099/jgv.0.000835
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

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