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Transmission modes affect the population structure of potato virus Y in potato


Autoři: Washington da Silva aff001;  Denis Kutnjak aff003;  Yi Xu aff002;  Yimin Xu aff006;  James Giovannoni aff006;  Santiago F. Elena aff004;  Stewart Gray aff002
Působiště autorů: Department of Pathology and Ecology, The Connecticut Agricultural Experiment Station, New Haven, Connecticut, United States of America aff001;  School of Integrative Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, New York, United States of America aff002;  Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, Slovenia aff003;  Instituto de Biología Integrativa de Sistemas (ISysBio), CSIC-Universitat de València, Paterna, València, Spain aff004;  Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China aff005;  Boyce Thompson Institute, Cornell University, Ithaca, New York, United States of America aff006;  Emerging Pests & Pathogens Research Unit, USDA, ARS, Ithaca, New York, United States of America aff007;  The Santa Fe Institute, Santa Fe, New Mexico, United States of America aff008
Vyšlo v časopise: Transmission modes affect the population structure of potato virus Y in potato. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008608
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008608

Souhrn

Transmission is a crucial part of a viral life cycle and transmission mode can have an important impact on virus biology. It was demonstrated that transmission mode can influence the virulence and evolution of a virus; however, few empirical data are available to describe the direct underlying changes in virus population structure dynamics within the host. Potato virus Y (PVY) is an RNA virus and one of the most damaging pathogens of potato. It comprises several genetically variable strains that are transmitted between plants via different transmission modes. To investigate how transmission modes affect the within-plant viral population structure, we have used a deep sequencing approach to examine the changes in the genetic structure of populations (in leaves and tubers) of three PVY strains after successive passages by horizontal (aphid and mechanical) and vertical (via tubers) transmission modes. Nucleotide diversities of viral populations were significantly influenced by transmission modes; lineages transmitted by aphids were the least diverse, whereas lineages transmitted by tubers were the most diverse. Differences in nucleotide diversities of viral populations between leaves and tubers were transmission mode-dependent, with higher diversities in tubers than in leaves for aphid and mechanically transmitted lineages. Furthermore, aphid and tuber transmissions were shown to impose stronger genetic bottlenecks than mechanical transmission. To better understand the structure of virus populations within the host, transmission mode, movement of the virus within the host, and the number of replication cycles after transmission event need to be considered. Collectively, our results suggest a significant impact of virus transmission modes on the within-plant diversity of virus populations and provide quantitative fundamental data for understanding how transmission can shape virus diversity in the natural ecosystems, where different transmission modes are expected to affect virus population structure and consequently its evolution.

Klíčová slova:

Leaves – Nicotiana – Population genetics – Potato – Species diversity – Tubers – Viral evolution – Viral structure


Zdroje

1. Lambrechts L, Scott TW. Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proc R Soc B Biol Sci. 2009;276: 1369–1378. doi: 10.1098/rspb.2008.1709 19141420

2. Stewart AD, Logsdon JM, Kelley SE. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution. 2005;59: 730–739. doi: 10.1111/j.0014-3820.2005.tb01749.x 15926685

3. Pagán I, Montes N, Milgroom MG, García-Arenal F. Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host. PLoS Pathog. 2014;10: 23–25. doi: 10.1371/journal.ppat.1004293 25077948

4. Boissot N, Schoeny A, Vanlerberghe-Masutti F. Vat, an amazing gene conferring resistance to aphids and viruses they carry: From molecular structure to field effects. Front Plant Sci. 2016;7: 1–18. doi: 10.3389/fpls.2016.00001

5. Pybus OG, Tatem AJ, Lemey P. Virus evolution and transmission in an ever more connected world. Proc R Soc B Biol Sci. 2015;282: 20142878. doi: 10.1098/rspb.2014.2878 26702033

6. Hull R, editor. Front Matter. Matthews’ Plant Virology (Fourth Edition). London: Academic Press; 2002. p. iii. https://doi.org/10.1016/B978-0-12-361160-4.50078-5

7. Hamelin FM, Allen LJS, Prendeville HR, Hajimorad MR, Jeger MJ. The evolution of plant virus transmission pathways. J Theor Biol. 2016;396: 75–89. doi: 10.1016/j.jtbi.2016.02.017 26908348

8. Moury B, Fabre F, Senoussi R. Estimation of the number of virus particles transmitted by an insect vector. Proc Natl Acad Sci. 2007;104: 17891–17896. doi: 10.1073/pnas.0702739104 17971440

9. Ali A, Li H, Schneider WL, Sherman DJ, Gray S, Smith D, et al. Analysis of genetic bottlenecks during horizontal transmission of Cucumber mosaic virus. J Virol. 2006;80: 8345–8350. doi: 10.1128/JVI.00568-06 16912285

10. Power AG. Insect transmission of plant viruses: A constraint on virus variability. Curr Opin Plant Biol. 2000;3: 336–340. doi: 10.1016/s1369-5266(00)00090-x 10873852

11. Fabre F, Moury B, Johansen EI, Simon V, Jacquemond M, Senoussi R. Narrow bottlenecks affect Pea seedborne mosaic virus populations during vertical seed transmission but not during leaf colonization. PLoS Pathog. 2014;10. doi: 10.1371/journal.ppat.1003833 24415934

12. Sacristan S, Fraile A, García-Arenal F. Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J Virol Methods. 2011;85: 4974–4981. doi: 10.1128/JVI.00057-11 21367909

13. Domingo E, Sheldon J, Perales C. Viral quasispecies evolution. Microbiol Mol Biol Rev. 2012;76: 159–216. doi: 10.1128/MMBR.05023-11 22688811

14. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature. 2006;439: 344–348. doi: 10.1038/nature04388 16327776

15. García-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol. 2001;39: 157–186. doi: 10.1146/annurev.phyto.39.1.157 11701863

16. 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. doi: 10.1146/annurev-virology-100114-055135 26958911

17. Beerenwinkel N, Zagordi O. Ultra-deep sequencing for the analysis of viral populations. Curr Opin Virol. 2011;1: 413–418. doi: 10.1016/j.coviro.2011.07.008 22440844

18. Acevedo A, Andino R. Library preparation for highly accurate population sequencing of RNA viruses. Nat Protoc. 2014;9: 1760–1769. doi: 10.1038/nprot.2014.118 24967624

19. Posada-Cespedes S, Seifert D, Beerenwinkel N. Recent advances in inferring viral diversity from high-throughput sequencing data. Virus Res. 2017;239: 17–32. doi: 10.1016/j.virusres.2016.09.016 27693290

20. Kutnjak D, Elena SF, Ravnikar M. Time-Sampled Population Sequencing Reveals the Interplay of Selection and Genetic Drift in Experimental Evolution of Potato Virus Y. J Virol. 2017;91: e00690–17. doi: 10.1128/JVI.00690-17 28592544

21. Karasev A, Gray S. Continuous and Emerging Challenges of Potato virus Y in Potato. Annu Rev Phytopathol. 2013;51: 571–586. doi: 10.1146/annurev-phyto-082712-102332 23915135

22. Karasev A V, Hu X, Brown CJ, Kerlan C, Nikolaeva O V, Crosslin JM, et al. Genetic diversity of the ordinary strain of Potato virus Y (PVY) and origin of recombinant PVY strains. Phytopathology. 2011;101: 778–785. doi: 10.1094/PHYTO-10-10-0284 21675922

23. Urcuqui-Inchima S, Haenni A-L, Bernardi F. Potyvirus proteins: a wealth of functions. Virus Res. 2001;74: 157–175. doi: 10.1016/s0168-1702(01)00220-9 11226583

24. Chung BY-W, Miller WA, Atkins JF, Firth AE. An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci. 2008;105: 5897–5902. doi: 10.1073/pnas.0800468105 18408156

25. Lacomme C, Glais L, Bellstedt DU, Dupuis B, Karasev A V., Jacquot E. Transmission and Epidemiology of Potato virus Y. Potato Virus Y: Biodiversity, Pathogenicity, Epidemiology and Management. 2017. pp. 141–176. doi: 10.1007/978-3-319-58860-5

26. da Silva WL, Ingram J, Hackett CA, Coombs JJ, Douches D, Bryan GJ, et al. Mapping loci that control tuber and foliar symptoms caused by PVY in autotetraploid potato (Solanum tuberosum L.). G3 Genes, Genomes, Genet. 2017;7. doi: 10.1534/g3.117.300264 28903982

27. Boodley JW, Sheldrake R. “Cornell peat-like mixes for commercial plant growing.” Cornell Inf. Bull. 43. 1982.

28. Ali MC, Maoka T, Natsuaki KT, Natsuaki T. The simultaneous differentiation of Potato virus Y strains including the newly described strain PVYNTN-NW by multiplex PCR assay. J Virol Methods. 2010;165: 15–20. doi: 10.1016/j.jviromet.2009.12.010 20025905

29. Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y, et al. High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc. 2011; 940–949. doi: 10.1101/pdb.prot5652 21807852

30. Nelson CW, Moncla LH, Hughes AL. SNPGenie: Estimating evolutionary parameters to detect natural selection using pooled next-generation sequencing data. Bioinformatics. 2015;31: 3709–3711. doi: 10.1093/bioinformatics/btv449 26227143

31. Ferrer-Admetlla A, Leuenberger C, Jensen JD, Wegmann D. An approximate markov model for the wright–fisher diffusion and its application to time series data. Genetics. 2016;203: 831–846. doi: 10.1534/genetics.115.184598 27038112

32. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.: R Foundation for Statistical Computing; 2019.

33. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, et al. gplots: Various R Programming Tools for Plotting Data. R package version 3.0.1.1. https://CRAN.R-project.org/package=gplots. 2019.

34. Mello AFS, Olarte RA, Gray SM, Perry KL. Transmission efficiency of Potato virus Y strains PVY o and PVY N-Wi by five aphid species. Plant Dis. 2011;95: 1279–1283. doi: 10.1094/PDIS-11-10-0855 30731697

35. Mondal S, Wenninger EJ, Hutchinson PJS, Whitworth JL, Shrestha D, Eigenbrode SD, et al. Comparison of transmission efficiency of various isolates of Potato virus Y among three aphid vectors. Entomol Exp Appl. 2016;158: 258–268. doi: 10.1111/eea.12404

36. Mondal S, Lin YH, Carroll JE, Wenninger EJ, Bosque-Pérez NA, Whitworth JL, et al. Potato virus Y transmission efficiency from potato infected with single or multiple virus strains. Phytopathology. 2017;107: 491–498. doi: 10.1094/PHYTO-09-16-0322-R 27938241

37. Fox A, Collins LE, Macarthur R, Blackburn LF, Northing P. New aphid vectors and efficiency of transmission of Potato virus A and strains of Potato virus Y in the UK. Plant Pathol. 2017;66: 325–335. doi: 10.1111/ppa.12561

38. Verbeek M, Piron PGM, Dullemans AM, Cuperus C, Van Der Vlugt RAA. Determination of aphid transmission efficiencies for N, NTN and Wilga strains of Potato virus Y. Ann Appl Biol. 2010;156: 39–49. doi: 10.1111/j.1744-7348.2009.00359.x

39. 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. doi: 10.1128/jvi.77.18.9906-9911.2003 12941900

40. Ali A, Roossinck MJ. Genetic bottlenecks during systemic movement of Cucumber mosaic virus vary in different host plants. Virology. 2010;404: 279–283. doi: 10.1016/j.virol.2010.05.017 20542533

41. Li H, Roossinck MJ. Genetic Bottlenecks Reduce Population Variation in an Experimental RNA Virus Population. J Virol. 2004;78: 10582–10587. doi: 10.1128/JVI.78.19.10582-10587.2004 15367625

42. Dunham JP, Simmons HE, Holmes EC, Stephenson AG. Analysis of viral (zucchini yellow mosaic virus) genetic diversity during systemic movement through a Cucurbita pepo vine. Virus Res. 2014;191: 172–179. doi: 10.1016/j.virusres.2014.07.030 25107623

43. Tromas N, Zwart MP, Lafforgue G, Elena SF. Within-Host Spatiotemporal Dynamics of Plant Virus Infection at the Cellular Level. PLoS Genet. 2014;10. doi: 10.1371/journal.pgen.1004186 24586207

44. Pleydell DRJ, Soubeyrand S, Dallot S, Labonne G, Chadœuf J, Jacquot E, et al. Estimation of the dispersal distances of an aphid-borne virus in a patchy landscape. PLoS Comput Biol. 2018;14: 1–24. doi: 10.1371/journal.pcbi.1006085 29708968

45. Rousseau E, Moury B, Mailleret L, Senoussi R, Palloix A, Simon V, et al. Estimating virus effective population size and selection without neutral markers. PLoS Pathog. 2017;13: 1–25. doi: 10.1371/journal.ppat.1006702 29155894


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