Population Genomics of Plant Viruses

  • Israel Pagán
  • Fernando García-ArenalEmail author
Part of the Population Genomics book series (POGE)


For more than one century, studies of plant viruses have broken paths in many fields of biology. More recently, studies of plant viruses have also been pioneer in population genomics. In the past few decades, there has been a significant advance in the number, sophistication, and quality of molecular techniques and bioinformatics tools for the genetic characterization of virus populations. This has broadened current knowledge on the mechanisms that generate genetic diversity and on the evolutionary forces and ecological factors that shape the genetic structure and dynamics of plant virus populations. This chapter aims at summarizing this knowledge, and it is structured around three major levels at which plant virus populations have been studied:
  1. 1.

    The within-host level, that is, the analysis of the genetic diversity of virus populations during plant colonization and of how phenomena such as co-/superinfection exclusion and population bottlenecks determine population structure

  2. 2.

    The between-host level, which includes studies on genetic diversity of virus populations in the host plant population and on the ecological factors shaping the genetic structure of the virus populations

  3. 3.

    The community level, which adddresses current studies on the genetic diversity of virus communities in multiple infected hosts and of multi-host-multivirus interactions


In sum, we provide an overview of current understanding on the population genomics of plant viruses at every level of population organization.


Ecosystem biodiversity Genomics of plant viruses Multiplicity of infection Plant virome assembly Plant-virus coevolution Time scale of plant virus evolution Virus coinfection Virus-virus interactions 



IP was supported by grant (BIO2016-79165-R) and FGA was supported by grant (BFU2015-60418-R), both funded by Plan Nacional I + D + I, MINECO, Spain.


  1. Acosta-Leal R, Duffy S, Xiong Z, Hammond RW, Elena SF. Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology. 2011;101:1136–48.PubMedGoogle Scholar
  2. Agnew P, Koella JC, Michalakis Y. Host life-history responses to parasitism. Microbes Infect. 2000;2:891–6.PubMedGoogle Scholar
  3. Alí A, Roossinck MJ. Genetic bottlenecks during systemic movement of Cucumber mosaic virus vary in different host plants. Virology. 2010;404:279–83.PubMedGoogle Scholar
  4. Almeida RPP, Bennett GM, Anhalt MD, Tsai C-W, O’Grady P. Spread of an introduced vector-borne banana virus in Hawaii. Mol Ecol. 2009;18:136–46.PubMedGoogle Scholar
  5. de Assis Filho F, Sherwood J. Evaluation of seed transmission of turnip yellow mosaic virus and tobacco mosaic virus in Arabidopsis thaliana. Phytopathology. 2000;90:1233–8.PubMedGoogle Scholar
  6. Bedhomme S, Agnew P, Vital Y, Sidobre C, Michalakis Y. Prevalence-dependent costs of parasite virulence. PLoS Biol. 2005;2:e262.Google Scholar
  7. Bergua M, Zwart MP, El-Mohtar C, Shilts T, Elena SF, Folimonova SY. A viral protein mediates superinfection exclusion at the whole-organism level but is not required for exclusion at the cellular level. J Virol. 2014;88:11327–38.PubMedPubMedCentralGoogle Scholar
  8. Berzal-Herranz A, de la Cruz A, Tenllado F, Díaz-Ruíz JR, López L, Sanz AI, Vaquero C, Serra MT, García-Luque I. The Capsicum L 3 gene-mediated resistance against the tobamoviruses is elicited by the coat protein. Virology. 1995;209:498–505.PubMedGoogle Scholar
  9. Blawid R, Silva JMF, Nagata T. Discovering and sequencing new plant viral genomes by next-generation sequencing: description of a practical pipeline. Ann Appl Biol. 2017;170:301–14.Google Scholar
  10. Blok J, Mackenzie A, Guy P, Gibbs AJ. Nucleotide sequence comparisons of turnip yellow mosaic isolates from Australia and Europe. Arch Virol. 1987;97:283–95.PubMedGoogle Scholar
  11. Borer ET, Adams VT, Engler GA, Adams AL, Schumann CB, Seabloom EW. Aphid fecundity and grassland invasion: invader life history is the key. Ecol Appl. 2009;19:1187–96.PubMedGoogle Scholar
  12. Borer ET, Seabloom EW, Mitchell CE, Power AG. Local context drives infection of grasses by vector-borne generalist viruses. Ecol Lett. 2010;13:810–8.PubMedGoogle Scholar
  13. Bujarski J. Genetic recombination in plant-infecting messenger-sense RNA viruses: overview and research perspectives. Front Plant Sci. 2013;4:68.PubMedPubMedCentralGoogle Scholar
  14. Burdon JJ, Chilvers GA. Host density as a factor in plant-disease ecology. Annu Rev Phytopathol. 1982;20:143–66.Google Scholar
  15. Burdon JJ, Thrall PH. Pathogen evolution across the agro-ecological interface: implications for disease management. Evol Appl. 2008;1:57–65.PubMedPubMedCentralGoogle Scholar
  16. Carrasco P, de la Iglesia F, Elena SF. Distribution of fitness and virulence effects caused by single-nucleotide substitutions in tobacco etch virus. J Virol. 2007;81:12979–84.PubMedPubMedCentralGoogle Scholar
  17. Chao L. Fitness of RNA virus decreased by Muller’s ratchet. Nature. 1990;348:454–5.PubMedGoogle Scholar
  18. Chao L. Levels of selection, evolution of sex in RNA viruses, and the origin of life. J Theor Biol. 1991;153:229–46.PubMedGoogle Scholar
  19. Chen S, Huang Q, Wu L, Qian Y. Identification and characterization of a maize-associated mastrevirus in China by deep sequencing small RNA populations. Virol J. 2015;12:156.PubMedPubMedCentralGoogle Scholar
  20. Clarke DD. Tolerance of parasites and disease in plants and its significance in host-parasite interactions. Adv Plant Pathol. 1986;5:161–98.Google Scholar
  21. Coetzee B, Freeborough M-J, Maree HJ, Celton J-M, Rees DJG, Burger JT. Deep sequencing analysis of viruses infecting grapevines: virome of a vineyard. Virology. 2010;400:157–63.PubMedGoogle Scholar
  22. De Bruyn A, Villemot J, Lefeuvre P, Villar E, Hoareau M, Harimalala M, Abdoul-Karime AL, Abdou-Chakour C, Reynaud B, Harkins GW, Varsani A, Martin DP, Lett JM. East African cassava mosaic-like viruses from Africa to Indian Ocean islands: molecular diversity, evolutionary history and geographical dissemination of a bipartite begomovirus. BMC Evol Biol. 2012;12:228.PubMedPubMedCentralGoogle Scholar
  23. Delwart EL. Viral metagenomics. Rev Med Virol. 2007;17:115–31.PubMedGoogle Scholar
  24. Dietrich C, Maiss E. Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. J Gen Virol. 2003;84:2871–6.PubMedGoogle Scholar
  25. Divéki Z, Salánki K, Balázs E. Limited utility of blue fluorescent protein in monitoring plant virus movement. Biochimie. 2002;84:997–1002.PubMedGoogle Scholar
  26. Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C. Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology. 2009;392:203–14.PubMedGoogle Scholar
  27. Donaire L, Burgyán J, García-Arenal F. RNA silencing may play a role in but is not the only determinant of the multiplicity of infection. J Virol. 2016;90:553–61.PubMedGoogle Scholar
  28. Drake JW, Holland JJ. Mutation rates among RNA viruses. Proc Natl Acad Sci U S A. 1999;96:13910–3.PubMedPubMedCentralGoogle Scholar
  29. Drummond AJ, Pybus OG, Rambaut A, Forsberg R, Rodrigo AG. Measurably evolving populations. Trends Ecol Evol. 2003;18:481–8.Google Scholar
  30. Duffy S, Holmes EC. Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. J Virol. 2008;82:957–65.PubMedGoogle Scholar
  31. Duffy S, Holmes EC. Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol. 2009;90:1539–47.PubMedPubMedCentralGoogle Scholar
  32. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 2008;9:267–76.PubMedGoogle Scholar
  33. 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;191:172–9.PubMedPubMedCentralGoogle Scholar
  34. Elena SF, Sanjuán R. On the adaptive value of high mutation rates in RNA viruses: separating causes from consequences. J Virol. 2005;79:11555–8.PubMedPubMedCentralGoogle Scholar
  35. Elena SF, Fraile A, García-Arenal F. Evolution and emergence of plant viruses. Adv Virus Res. 2014;88:161–91.PubMedGoogle Scholar
  36. 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:e1003833.PubMedPubMedCentralGoogle Scholar
  37. Fargette D, Pinel A, Rakotomalala M, Sangu E, Traoré O, Sérémé D, Sorho F, Issaka S, Hébrard E, Séré Y, Kanyeka Z, Konaté G. Rice yellow mottle virus, an RNA plant virus, evolves as rapidly as most RNA animal viruses. J Virol. 2008a;82:3584–9.PubMedPubMedCentralGoogle Scholar
  38. Fargette D, Pinel-Galzi A, Sérémé D, Lacombe S, Hébrard E, Traoré O, Konaté G. Diversification of Rice yellow mottle virus and related viruses spans the history of agriculture from the Neolithic to the present. PLoS Pathog. 2008b;4:e1000125.PubMedPubMedCentralGoogle Scholar
  39. Fawcett HS. The importance of investigations on the effects of known mixtures of microorganisms. Phytopathology. 1931;2:545–50.Google Scholar
  40. Fraile A, García-Arenal F. The coevolution of plants and viruses: resistance and pathogenicity. Adv Virus Res. 2010;76:1–32.PubMedGoogle Scholar
  41. Fraile A, Pagán I, Anastasio G, Sáez E, García-Arenal F. Rapid genetic diversification and high fitness penalties associated with pathogenicity evolution in a plant virus. Mol Biol Evol. 2011;28:1425–37.PubMedGoogle Scholar
  42. Fraile A, Hily J-M, Pagán I, Pacios LF, García-Arenal F. Host resistance selects for traits unrelated to resistance-breaking that affect fitness in a plant virus. Mol Biol Evol. 2014;31:928–39.PubMedGoogle Scholar
  43. Fraile A, McLeish MJ, Pagán I, González-Jara P, Piñero P, García-Arenal F. Environmental heterogeneity and the evolution of plant-virus interactions: viruses in wild pepper populations. Virus Res. 2017;241:68–76.PubMedGoogle Scholar
  44. Frank SA. Multiplicity of infection and the evolution of hybrid incompatibility in segmented viruses. Heredity. 2001;87:522–9.PubMedGoogle Scholar
  45. French R, Stenger DC. Evolution of wheat streak mosaic virus: dynamics of population growth within plants may explain limited variation. Annu Rev Phytopathol. 2003;41:199–214.PubMedGoogle Scholar
  46. Friess N, Maillet J. Influence of cucumber mosaic virus infection on the intraspecific competitive ability and fitness of purslane (Portulaca oleracea). New Phytol. 1996;132:103–11.Google Scholar
  47. Froissart R, Wilke CO, Montville R, Remold SK, Chao L, Turner PE. Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics. 2004;168:9–19.PubMedPubMedCentralGoogle Scholar
  48. Froissart R, Roze D, Uzest M, Galibert L, Blanc S, Michalakis Y. Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol. 2005;3:e89.PubMedPubMedCentralGoogle Scholar
  49. Froissart R, Doumayrou J, Vuillaume F, Alizon S, Michalakis Y. The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Philos Trans R Soc B. 2010;365:1907–18.Google Scholar
  50. García-Andrés S, Tomás DM, Sánchez-Campos S, Navas-Castillo J, Moriones E. Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease associated begomoviruses. Virology. 2007;365:210–9.PubMedGoogle Scholar
  51. García-Arenal F, Fraile A. Questions and concepts in plant virus evolution: a historical perspective. In: Roossinck MJ, editor. Plant virus evolution. Berlin: Springer; 2008. p. 1–14.Google Scholar
  52. García-Arenal F, Fraile A. Population dynamics and genetics of plant infection by viruses. In: Caranta C, Aranda MA, Tepfer M, Lopez-Moya JJ, editors. Recent advances in plant virology. Norfolk: Caister Academic Press; 2011. p. 263–81.Google Scholar
  53. García-Arenal F, Fraile A. Trade-offs in host range evolution of plant viruses. Plant Pathol. 2013;62:S2–9.Google Scholar
  54. García-Arenal F, McDonald BA. An analysis of the durability of resistance to plant viruses. Phytopathology. 2003;93:941–52.PubMedGoogle Scholar
  55. García-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol. 2001;39:157–86.PubMedGoogle Scholar
  56. Ghoshal B, Sanfaçon H. Symptom recovery in virus-infected plants: revisiting the role of RNA silencing mechanisms. Virology. 2015;479–480:167–79.PubMedGoogle Scholar
  57. Giampetruzzi A, Roumi V, Roberto R, Malossini U, Yoshikawa N, La Notte P, Terlizzi F, Credi R, Saldarelli P. A new grapevine virus discovered by deep sequencing of virus- and viroid-derived small RNAs in Cv Pinot gris. Virus Res. 2012;163:262–8.PubMedGoogle Scholar
  58. Gibbs AJ. A plant virus that partially protects its wild legume host against herbivores. Intervirology. 1980;13:42–7.PubMedGoogle Scholar
  59. Gibbs AJ, Blok J, Coates DJ, Guy PL, Mackenzie A, Pigram N. Turnip yellow mosaic virus in an endemic Australian alpine Cardamine. In: Barlow BA, editor. Flora and Fauna of Alpine Australasia; ages and origins. Collingwood: CSIRO; 1986. p. 289–300.Google Scholar
  60. Gibbs AJ, Gibbs MJ, Ohshima K, García-Arenal F. More plant virus evolution; past present and future. In: Domingo E, Parrish CR, Holland JJ, editors. Origin and evolution of viruses. 2nd ed. London: Academic Press; 2008a.Google Scholar
  61. Gibbs AJ, Ohshima K, Phillips MJ, Gibbs MJ. The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. PLoS One. 2008b;3:e2523.PubMedPubMedCentralGoogle Scholar
  62. Gibbs AJ, Fargette D, García-Arenal F, Gibbs MJ. Time—the emerging dimension of plant virus studies. J Gen Virol. 2010;91:13–22.PubMedGoogle Scholar
  63. Gibbs AJ, Wood J, Garcia-Arenal F, Ohshima K, Armstrong JS. Tobamoviruses have probably co-diverged with their eudicotyledonous hosts for at least 110 million years. Virus Evol. 2015;1:vev019.PubMedPubMedCentralGoogle Scholar
  64. Gibbs AJ, Ohshima K, Yasaka R, Mohammadi M, Gibbs MJ, Jones RAC. The phylogenetics of the global population of potato virus Y and its necrogenic recombinants. Virus Evol. 2017;3:vex002.PubMedPubMedCentralGoogle Scholar
  65. Gómez P, Sempere RN, Elena SF, Aranda MA. Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J Virol. 2009;83:12378–87.PubMedPubMedCentralGoogle Scholar
  66. Gómez P, Sempere RN, Aranda MA, Elena SF. Phylodynamics of Pepino mosaic virus. Eur J Plant Pathol. 2012;134:445–9.Google Scholar
  67. 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;83:7487–94.PubMedPubMedCentralGoogle Scholar
  68. 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. Author’s correction. J Virol. 2013;87:2374.PubMedCentralGoogle Scholar
  69. Gutiérrez S, Yvon M, Thébaud G, Monsion B, Michalakis Y, Blanc S. Dynamics of the multiplicity of cellular infection in a plant virus. PLoS Pathog. 2010;6:e1001113.PubMedPubMedCentralGoogle Scholar
  70. Gutiérrez S, Michalakis Y, Blanc S. Virus population bottlenecks during within-host progression and host-to-host transmission. Curr Op Virol. 2012a;2:546–55.Google Scholar
  71. Gutiérrez S, Yvon M, Pirolles E, Garzo E, Fereres A, Michalakis Y, Blanc S. Circulating virus load determines the size of bottlenecks in viral populations progressing within a host. PLoS Pathog. 2012b;8:e1003009.PubMedPubMedCentralGoogle Scholar
  72. Gutiérrez S, Pirolles E, Yvon M, Baecker V, Michalakis Y, Blanc S. The multiplicity of cellular infection changes depending on the route of cell infection in a plant virus. J Virol. 2015;89:9665–75.PubMedPubMedCentralGoogle Scholar
  73. Guy P, Gibbs AJ. A tymovirus of Cardamine sp. from alpine Australia. Australas Plant Pathol. 1981;10:12–3.Google Scholar
  74. Hackett J, Muthukumar V, Wiley GB, Palmer MW, Roe BA, Melcher U. Viruses in Oklahoma Euphorbia marginata. Proc Oklahoma Acad Sci. 2009;89:49–54.Google Scholar
  75. Hadidi A, Flores R, Candresse T, Barba M. Next-generation sequencing and genome editing in plant virology. Front Microbiol. 2016;7:1325.PubMedPubMedCentralGoogle Scholar
  76. Hajimorad MR, Wen R-H, Eggenberger AL, Hill JH, Saghai Maroof MA. Experimental adaptation of an RNA virus mimics natural evolution. J Virol. 2011;85:2557–64.PubMedGoogle Scholar
  77. Hall JS, French R, Hein GL, Morris TJ, Stenger DC. Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology. 2001;282:230–6.PubMedGoogle Scholar
  78. Hall GS, Peters JS, Little DP, Power AG. Plant community diversity influences vector behavior and Barley yellow dwarf virus population structure. Plant Pathol. 2010;59:152–1158.Google Scholar
  79. Hamada H, Takeuchi S, Kiba A, Tsuda S, Hikichi Y, Okuno T. Amino acid changes in Pepper mild mottle virus coat protein that affect L 3 gene-mediated resistance in pepper. J Gen Plant Pathol. 2002;68:155–62.Google Scholar
  80. Hamada H, Tomita R, Iwadate Y, Kobayashi K, Minemura I, Takeuchi S, Hikichi Y, Suzuki K. Cooperative effect of two amino acid mutations in the coat protein of Pepper mild mottle virus overcomes L 3-mediated resistance in Capsicum plants. Virus Genes. 2007;34:205–14.PubMedGoogle Scholar
  81. Harkins GW, Delport W, Duffy S, Wood N, Monjane AL, Owor BE, Donaldson L, Saumtally S, Triton G, Briddon RW, Shepherd DN, Rybicki EP, Martin DP, Varsani A. Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts. Virol J. 2009;6:104.PubMedPubMedCentralGoogle Scholar
  82. Harrison BD. The infectivity of extracts made from leaves at intervals after inoculation with viruses. J Gen Microbiol. 1956;15:210–20.PubMedGoogle Scholar
  83. Hartl DL, Clark AG. Principles of population genetics. 4th ed. Sunderland: Sinauer; 2007.Google Scholar
  84. Hillung J, Cuevas JM, Elena SF. Evaluating the within-host fitness effects of mutations fixed during virus adaptation to different ecotypes of a new host. Philos Trans R Soc B. 2015;370:20140292.Google Scholar
  85. Hochberg ME. Population dynamic consequences of the interplay between parasitism and intraspecific competition for host-parasite systems. Oikos. 1991;61:297–306.Google Scholar
  86. Holmes EC. The evolution and emergence of RNA viruses. Oxford: Oxford University Press; 2009.Google Scholar
  87. Hughes AL. Small effective population sizes and rare nonsynonymous variants in potyviruses. Virology. 2009;393:127–34.PubMedPubMedCentralGoogle Scholar
  88. Hull R. Plant virology. 5th ed. San Diego: Academic Press; 2014.Google Scholar
  89. Hull R, Plaski A. Electron microscopy on the behaviour of two strains of Alfalfa mosaic virus in mixed infections. Virology. 1970;42:773–6.PubMedGoogle Scholar
  90. Hurwitz BL, Sullivan MB. The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One. 2013;8:e57355.PubMedPubMedCentralGoogle Scholar
  91. Ishibashi K, Kezuka Y, Kobayashi C, Kato M, Inoue T, Nonaka T, Ishikawa M, Matsumura H, Katoh E. Structural basis for the recognition-evasion arms race between Tomato mosaic virus and the resistance gene Tm-1. Proc Natl Acad Sci U S A. 2014;111:3486–95.Google Scholar
  92. Jenkins GM, Rambaut A, Pybus OG, Holmes EC. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol. 2002;54:156–65.PubMedGoogle Scholar
  93. Johnson PT, Ostfeld RS, Keesing F. Frontiers in research on biodiversity and disease. Ecol Lett. 2015;18:1119–33.PubMedPubMedCentralGoogle Scholar
  94. Jones RAC. Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res. 2009;141:113–30.PubMedGoogle Scholar
  95. Jridi C, Martin JF, Marie-Jeanne V, Labonne G, Blanc S. Distinct viral populations differentiate and evolve independently in a single perennial host plant. J Virol. 2006;80:2349–57.PubMedPubMedCentralGoogle Scholar
  96. Kay KM, Whittall JB, Hodges SA. A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol. 2006;6:36.PubMedPubMedCentralGoogle Scholar
  97. Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecol Lett. 2006;9:485–98.PubMedGoogle Scholar
  98. Keesing F, Belden LK, Daszk P, Dobson A, Harwell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–52.PubMedGoogle Scholar
  99. Kelly SE. Viral pathogens and the advantage of sex in the perennial grass Anthoxanthum odoratum: a review. Phil Trans R Soc Lond B. 1994;346:295–302.Google Scholar
  100. Kinoti WM, Constable FE, Nancarrow N, Plummer KM, Rodoni B. Analysis of intra-host genetic diversity of Prunus necrotic ringspot virus (PNRSV) using amplicon next generation sequencing. PLoS One. 2017;12:e0179284.PubMedPubMedCentralGoogle Scholar
  101. Kreuze JF, Pérez A, Untiveros M, Quispe D, Fuentes S, Barker I, Simon R. Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology. 2009;388:1–7.PubMedGoogle Scholar
  102. Lanfear R, Kokko H, Eyre-Walker A. Population size and the rate of evolution. Trends Ecol Evol. 2014;29:33–41.PubMedGoogle Scholar
  103. Lartey RT, Voss TC, Melcher U. Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol Biol Evol. 1996;13:1327–38.PubMedGoogle Scholar
  104. Lefeuvre P, Harkins GW, Lett J-M, Briddon RW, Chase MW, Moury B, Martin DP. Evolutionary time-scale of the begomoviruses: evidence from integrated sequences in the Nicotiana genome. PLoS One. 2011;6:e19193.PubMedPubMedCentralGoogle Scholar
  105. Levontin RC. The units of infection. Annu Rev Ecol Syst. 1970;1:1–18.Google Scholar
  106. Li H, Roossinck MJ. Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol. 2004;78:10582–7.PubMedPubMedCentralGoogle Scholar
  107. Lima ATM, Silva JCF, Silva FN, Castillo-Urquiza GP, Silva FF, Seah YM, Mizubuti ESG, Duffy S, Murilo Zerbini F. The diversification of begomovirus populations is predominantly driven by mutational dynamics. Virus Evol. 2017;3:vex005.PubMedPubMedCentralGoogle Scholar
  108. Lipkin WI. The changing face of pathogen discovery and surveillance. Nat Rev Microbiol. 2013;11:133–41.PubMedPubMedCentralGoogle Scholar
  109. Little TJ, Shuker DM, Colegrave N, Day N, Graham AL. The coevolution of virulence: tolerance in perspective. PLoS Pathog. 2010;6:e1001006.PubMedPubMedCentralGoogle Scholar
  110. Lively CM. The ecology of virulence. Ecol Lett. 2006;9:1089–95.PubMedGoogle Scholar
  111. Malmstrom CM, Alexander HM. Effects of crop viruses on wild plants. Curr Op Virol. 2016;19:30–6.Google Scholar
  112. Malmstrom CM, Hughes CC, Newton LA, Stoner CJ. Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytol. 2005a;168:217–30.PubMedGoogle Scholar
  113. Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia. 2005b;145:153–64.PubMedGoogle Scholar
  114. Malmstrom CM, Shu R, Linton EW, Newton LA, Cook MA. Barley yellow dwarf viruses (BYDVs) preserved in herbarium specimens illuminate historical disease ecology of invasive and native grasses. J Ecol. 2007;95:1153–66.Google Scholar
  115. Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, García-Arenal F. The rate and character of spontaneous mutation in an RNA virus. Genetics. 2002;162:1505–11.PubMedPubMedCentralGoogle Scholar
  116. Malpica JM, Sacristán S, Fraile A, García-Arenal F. Association and host selectivity in multi-host pathogens. PLoS One. 2006;1:e41.PubMedPubMedCentralGoogle Scholar
  117. Martín S, Elena SF. Application of game theory to the interaction between plant viruses during mixed infections. J Gen Virol. 2009;90:2815–20.PubMedGoogle Scholar
  118. Maskell LC, Raybould AF, Cooper JI, Edwards ML, Gray AJ. Effects of turnip mosaic virus and turnip yellow mosaic virus on the survival, growth and reproduction of wild cabbage (Brassica oleracea). Ann Appl Biol. 1999;135:401–7.Google Scholar
  119. Massart S, Olmos A, Jijakli H, Candresse T. Current impact and future directions of high throughput sequencing in plant virus diagnostics. Virus Res. 2014;188:90–6.PubMedGoogle Scholar
  120. Massart S, Candresse T, Gil J, Lacomme C, Predajna L, Ravnikar M, Reynard JS, Rumbou A, Saldarelli P, Škorić D, Vainio EJ, Valkonen JP, Vanderschuren H, Varveri C, Wetzel T. A framework for the evaluation of biosecurity, commercial, regulatory, and scientific impacts of plant viruses and viroids identified by NGS technologies. Front Microbiol. 2017;8:45.PubMedPubMedCentralGoogle Scholar
  121. McKinney HH. Evidence of virus mutation in the common mosaic of tobacco. J Agric Res. 1935;51:951–81.Google Scholar
  122. McLeish MJ, Sacristán S, Fraille A, García-Arenal F. Scale dependencies and generalism in host use shape virus prevalence. Proc. R. Soc. B, 2017;284: 20172066.PubMedGoogle Scholar
  123. Miyashita S, Kishino H. Estimation of the size of genetic bottlenecks in cell-to-cell movement of soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements. J Virol. 2010;84:1828–37.PubMedGoogle Scholar
  124. van Molken T, de Caluwe H, Hordijk CA, Leon-Reyes A, Snoeren TA, van Dam NM, Stuefer JF. Virus infection decreases the attractiveness of white clover plants for a non-vectoring herbivore. Oecologia. 2012;170:433–44.PubMedPubMedCentralGoogle Scholar
  125. Monsion B, Froissart R, Michalakis Y, Blanc S. Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization. PLoS Pathog. 2008;4:e1000174.PubMedPubMedCentralGoogle Scholar
  126. Moreno A, De Blas C, Biurrun R, Nebreda M, Palacios I, Duque M, Fereres A. The incidence and distribution of viruses infecting lettuce, cultivated Brassica and associated natural vegetation in Spain. Ann Appl Biol. 2004;144:339–46.Google Scholar
  127. Morse SS, Schluederberg A. Emerging viruses: the evolution of viruses and viral diseases. J Infect Dis. 1990;162:1–7.PubMedGoogle Scholar
  128. Moury B, Janzac B, Ruellan Y, Simon V, Ben Khalifa M, Fakhfakh H, Fabre F, Palloix A. Interaction patterns between Potato virus Y and eIF4E-mediated recessive resistance in the Solanaceae. J Virol. 2014;88:9799–807.PubMedPubMedCentralGoogle Scholar
  129. Moury B, Fabre F, Hébrard E, Froissart R. Determinants of host species range in plant viruses. J Gen Virol. 2017;98:862–73.PubMedGoogle Scholar
  130. Moya A, Rodríguez-Cerezo E, García-Arenal F. Genetic structure of natural populations of the plant RNA virus tobacco mild green mosaic virus. Mol Biol Evol. 1993;10:449–56.Google Scholar
  131. Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Annu Rev Microbiol. 2004;2:279–88.Google Scholar
  132. Nee S, Maynard-Smith J. The evolutionary biology of molecular parasites. Parasitology. 1990;100:S5–S18.PubMedGoogle Scholar
  133. Ng TFF, Duffy S, Polston JE, Bixby E, Vallad GE, Breitbart M. Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS One. 2011;6:e19050.PubMedPubMedCentralGoogle Scholar
  134. Nieberding CM, Olivieri I. Parasites: proxies for host genealogy and ecology? Trends Ecol Evol. 2007;22:156–65.PubMedGoogle Scholar
  135. Nsa IY, Kareem KT. Additive interactions of unrelated viruses in mixed infections of cowpea (Vigna unguiculata L. Walp). Front Plant Sci. 2015;6:812.PubMedPubMedCentralGoogle Scholar
  136. Nuismer SL, Jordano P, Bascompte J. Coevolution and the architecture of mutualistic networks. Evolution. 2013;67:338–54.PubMedGoogle Scholar
  137. Ostfeld RS, Keesing F. Effects of host diversity on infectious disease. Annu Rev Ecol Evol Syst. 2012;43:157–82.Google Scholar
  138. Ostfeld RS, Keesing F. Is biodiversity bad for your health? Ecosphere. 2017;8:e01676.Google Scholar
  139. Pagán I, Holmes EC. Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. J Virol. 2010;84:6177–87.PubMedPubMedCentralGoogle Scholar
  140. Pagán I, Alonso-Blanco C, García-Arenal F. The relationship of within-host multiplication and virulence in a plant-virus system. PLoS One. 2007;2:e786.PubMedPubMedCentralGoogle Scholar
  141. Pagán I, Alonso-Blanco C, García-Arenal F. Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathog. 2008;4:e1000124.PubMedPubMedCentralGoogle Scholar
  142. Pagán I, Alonso-Blanco C, García-Arenal F. Differential tolerance to direct and indirect density-dependent costs of viral infection in Arabidopsis thaliana. PLoS Pathog. 2009;5:e1000531.PubMedPubMedCentralGoogle Scholar
  143. Pagán I, Firth C, Holmes EC. Phylogenetic analysis reveals rapid evolutionary dynamics in the plant RNA virus genus Tobamovirus. J Mol Evol. 2010a;71:298–307.PubMedGoogle Scholar
  144. Pagán I, Fraile A, Fernández-Fuello E, Montes N, Alonso-Blanco C, García-Arenal F. Arabidopsis thaliana as a model for plant-virus co-evolution. Philos Trans R Soc B. 2010b;365:1983–95.Google Scholar
  145. Pagán I, González-Jara P, Moreno-Letelier A, Rodelo-Urrego M, Fraile A, Piñero D, García-Arenal F. Effect of biodiversity changes in disease risk: exploring disease emergence in a plant-virus system. PLoS Pathog. 2012;8:e1002796.PubMedPubMedCentralGoogle Scholar
  146. 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:e1004293.PubMedPubMedCentralGoogle Scholar
  147. Pagán I, Fraile A, García-Arenal F. Evolution of the interactions of viruses with their plant hosts. In: Weaver SC, Denison M, Roossink MJ, Vignuzzi M, editors. Virus evolution: current research and future directions. Norfolk: Caister Academic Press; 2016. p. 127–54.Google Scholar
  148. Pinel-Galzi AS, Rakotomalala M, Sangu E, Sorho F, Kanyeka Z, Traoré O, Sérémé D, Poulicard N, Rabenantoandro Y, Sere Y, Konaté G, Ghesquiere A, Hébrard E, Fargette D. Theme and variations in the evolutionary pathways to virulence of an RNA plant virus species. PLoS Pathog. 2007;3:e180.PubMedPubMedCentralGoogle Scholar
  149. Piry S, Wipf-Scheibel C, Martin J-F, Galan M, Berthier K. High throughput amplicon sequencing to assess within- and between-host genetic diversity in plant viruses. BioRXiv. 2017.
  150. Poulicard N, Pinel-Galzi A, Fargette D, Hébrard E. 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. 2014;95:219–24.PubMedGoogle Scholar
  151. Power AG, Mitchell CE. Pathogen spillover in disease epidemics. Am Nat. 2004;164:S79–89.PubMedGoogle Scholar
  152. Power AG, Borer ET, Hosseini P, Mitchell CE, Seabloom EW. The community ecology of barley/cereal yellow dwarf viruses in Western US grasslands. Virus Res. 2011;159:95–100.PubMedGoogle Scholar
  153. Prendeville HR, Ye XH, Morris TJ, Pilson D. Virus infections in wild plant populations are both frequent and often unapparent. Am J Bot. 2012;99:1033–42.PubMedGoogle Scholar
  154. Prendeville HR, Tenhumberg B, Pilson D. Effects of virus on plant fecundity and population dynamics. New Phytol. 2014;202:1346–56.PubMedGoogle Scholar
  155. Pressing J, Reanney DC. Divided genomes and intrinsic noise. J Mol Evol. 1984;20:135–46.PubMedGoogle Scholar
  156. Quenoiulle J, Vassilakos N, Moury B. Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Mol Plant Pathol. 2013;14:439–52.Google Scholar
  157. Randolph SE, Dobson DM. Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology. 2012;139:847–63.PubMedGoogle Scholar
  158. Rato S, Golumbeanu M, Telenti A, Ciuffi A. Exploring viral infection using single-cell sequencing. Virus Res. 2016;239:55–68.PubMedGoogle Scholar
  159. Rentería-Canett I, Xoconostle-Cázares B, Ruiz-Medrano R, Rivera-Bustamante RF. Geminivirus mixed infection on pepper plants: synergistic interaction between PHYVV and PepGMV. Virol J. 2011;8:104.PubMedPubMedCentralGoogle Scholar
  160. Rochow WF. The role of mixed infections in the transmission of plant viruses by aphids. Annu Rev Phytopatol. 1972;10:101–24.Google Scholar
  161. Rodelo-Urrego M, Pagán I, González-Jara P, Betancourt M, Moreno-Letelier A, Ayllón MA, Fraile A, Piñero D, García-Arenal F. Landscape heterogeneity shapes host-parasite interactions and results in apparent plant-virus codivergence. Mol Ecol. 2013;22:2325–40.PubMedGoogle Scholar
  162. Rodelo-Urrego M, García-Arenal F, Pagán I. The effect of ecosystem biodiversity on virus genetic diversity depends on virus species: a study of chiltepin-infecting begomoviruses in Mexico. Virus Evol. 2015;1:vev004.PubMedPubMedCentralGoogle Scholar
  163. Rodríguez-Nevado C, Montes N, Pagán I. Ecological factors affecting the infection risk and population genetic diversity of a novel potyvirus in its native wild ecosystem. Front Plant Sci. 2017;8:1958.PubMedPubMedCentralGoogle Scholar
  164. Roossinck MJ. Mechanisms of plant virus evolution. Annu Rev Phytopathol. 1997;35:191–209.PubMedGoogle Scholar
  165. Roossinck MJ. Symbiosis versus competition in plant virus evolution. Nat Rev Microbiol. 2005;3:917–24.PubMedGoogle Scholar
  166. Roossinck MJ. The big unknown: plant virus biodiversity. Curr Op Virol. 2011;1:63–7.Google Scholar
  167. Roossinck MJ. Plant virus metagenomics: biodiversity and ecology. Annu Rev Genet. 2012;46:357–67.Google Scholar
  168. Roossinck MJ. Deep sequencing for discovery and evolutionary analysis of plant viruses. Virus Res. 2017;239:82–6.PubMedGoogle Scholar
  169. Roossinck MJ, Saha P, Wiley GB, Quan J, White JD, Lai H, Chavarría F, Shen G, Roe BA. Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol Ecol. 2010;19:81–8.PubMedGoogle Scholar
  170. Roossinck MJ, Martin DP, Roumagnac P. Plant virus metagenomics: advances in virus discovery. Phytopatology. 2015;105:716–27.Google Scholar
  171. Sacristán S, García-Arenal F. The evolution of virulence and pathogenicity in plant pathogen populations. Mol Plant Pathol. 2008;9:369–84.PubMedGoogle Scholar
  172. 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;77:9906–11.PubMedPubMedCentralGoogle Scholar
  173. Salvaudon L, De Moraes CM, Mescher MC. Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proc R Soc Lon B. 2013;280:20122959.Google Scholar
  174. Sanjuán R, Agudelo-Romero P, Elena SF. Upper-limit mutation rate estimation for a plant RNA virus. Biol Lett. 2009;5:394–6.PubMedPubMedCentralGoogle Scholar
  175. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol. 2010;84:9733–48.PubMedPubMedCentralGoogle Scholar
  176. Sasu MA, Ferrari MJ, Du D, Winsor JA, Stephenson AG. Indirect costs of a nontarget pathogen mitigate the direct benefits of a virus-resistant transgene in wild Cucurbita. 2009;45:19067–71.Google Scholar
  177. Scholle SO, Ypma RJ, Lloyd AL, Koelle K. Viral substitution rate variation can Arise from the interplay between within-host and epidemiological dynamics. Am Nat. 2013;182:494–513.PubMedGoogle Scholar
  178. Shuckla A, Pagán I, García-Arenal F. Effective tolerance based on resource reallocation is a virus-specific defence in Arabidopsis thaliana. Mol Plant Pathol. Published on line 30 Jan 2018.Google Scholar
  179. Sicard A, Yvon M, Timchenko T, Gronenborn B, Michalakis Y, Gutierrez S, Blanc S. Gene copy number is differentially regulated in a multipartite virus. Nat Commun. 2013;4:2248.PubMedGoogle Scholar
  180. Sicard A, Michalakis Y, Gutierrez S, Blanc S. The strange lifestyle of multipartite viruses. PLoS Pathog. 2016;12:e1005819.PubMedPubMedCentralGoogle Scholar
  181. Simmons HE, Holmes EC, Stephenson AG. Rapid evolutionary dynamics of zucchini yellow mosaic virus. J Gen Virol. 2008;89:1081–5.PubMedGoogle Scholar
  182. Simmons HE, Dunham JP, Stack JC, Dickins BJA, Pagán I, Holmes EC, Stephenson AG. Deep sequencing reveals persistence of intra- and inter-host genetic diversity in natural and greenhouse populations of zucchini yellow mosaic virus. J Gen Virol. 2012;93:1831–40.PubMedGoogle Scholar
  183. Simon AE, Bujarski JJ. RNA-RNA recombination and evolution in virus infected plants. Annu Rev Phytopathol. 1994;32:337–62.Google Scholar
  184. Stenger DC, Seifers DL, French R. Patterns of polymorphism in wheat streak mosaic virus: sequence space explored by a clade of closely related viral genotypes rivals that between the most divergent strains. Virology. 2002;302:58–70.PubMedGoogle Scholar
  185. Stobbe AH, Roossinck MJ. Plant virus metagenomics: what we know and why we need to know more. Front Plant Sci. 2014;5:150.PubMedPubMedCentralGoogle Scholar
  186. Stobbe AH, Melcherl U, Palmer MW, Roossinck MJ, Shen G. Co-divergence and host-switching in the evolution of tobamoviruses. J Gen Virol. 2012;93:408–18.PubMedGoogle Scholar
  187. Stukenbrock EH, McDonald BA. The origin of plant pathogens in agro- ecosystems. Annu Rev Phytopathol. 2008;46:75–100.PubMedGoogle Scholar
  188. Syller J. Facilitative and antagonistic interactions between plant viruses in mixed infections. Mol Plant Pathol. 2012;13:204–16.PubMedGoogle Scholar
  189. Szathmáry E. Viral sex, levels of selection, and the origin of life. J Theor Biol. 1992;159:99–109.PubMedGoogle Scholar
  190. Taiwo MA, Kareem KT, Nsa IY, Hughes JD’A. Cowpea viruses: effect of single and mixed infections on symptomatology and virus concentration. Virol J. 2007;4:95.PubMedPubMedCentralGoogle Scholar
  191. Takahashi T, Sugawara T, Yamatsuta T, Isogai M, Natsuaki T, Yoshikawa N. Analysis of the spatial distribution or identical and two distinct virus populations differently labelled with cyan and yellow fluorescent proteins in coinfected plants. Phytopathology. 2007;97:1200–6.PubMedGoogle Scholar
  192. Takeshita M, Shigemune N, Kikuhara K, Takanami Y. Spatial analysis for exclusive interactions between subgroups I and II of cucumber mosaic virus in cowpea. Virology. 2004;328:45–51.PubMedGoogle Scholar
  193. Tepfer M. Risk assessment of virus-resistant transgenic plants. Annu Rev Phytopathol. 2002;40:467–91.PubMedGoogle Scholar
  194. Thébaud G, Michalakis Y. Comment on “Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization” by Monsion et al. (2008). PLoS Pathog. 2016;12:e1005512.PubMedPubMedCentralGoogle Scholar
  195. Thompson AD. Interactions between plant viruses. I Appearance of new strains after mixed infection with Potato virus X strains. Virology. 1961;13:507–14.Google Scholar
  196. Thompson JN. The geographic mosaic of coevolution. Chicago: University of Chicago Press; 2005.Google Scholar
  197. Thresh JM. Cropping practices and virus spread. Annu Rev Phytopathol. 1982;20:193–218.Google Scholar
  198. Tomita R, Murai J, Miura Y, Ishikara H, Liu S, Kubotera Y, Honda A, Hatta R, Kuroda T, Hamada H, Sakamoto M, Munemura I, Nunomura O, Ishikawa K, Genda Y, Kawasaki S, Suzuki K, Meksem K, Kobayashi K. Fine mapping and DNA fiber FISH analysis locates the tobamovirus resistance gene L 3 of Capsicum chinense in a 400-kb region of R-like genes cluster embedded in highly repetitive sequences. Theor Appl Genet. 2008;117:1107–18.PubMedPubMedCentralGoogle Scholar
  199. Tromas N, Elena SF. The rate and spectrum of spontaneous mutations in a plant RNA virus. Genetics. 2010;185:983–9.PubMedPubMedCentralGoogle Scholar
  200. Tromas N, Zwart MP, Lafforgue G, Elena SF. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLoS Genet. 2014a;10:e1004186.PubMedPubMedCentralGoogle Scholar
  201. Tromas N, Zwart MP, Poulain M, Elena SF. Estimation of the in vivo recombination rate for a plant RNA virus. J Gen Virol. 2014b;95:724–32.PubMedGoogle Scholar
  202. Trovão NS, Baele G, Vrancken B, Bielejec F, Suchard MA, Fargette D, Lemey P. Host ecology determines the dispersal patterns of a plant virus. Virus Evol. 2015;1:vev016.PubMedPubMedCentralGoogle Scholar
  203. Tsuda S, Kirita M, Watanabe Y. Characterization of a pepper mild mottle tobamovirus strain capable of overcoming the L 3 gene-mediated resistance, distinct from the resistance-breaking Italian isolate. Mol Plant Microbe Interact. 1998;11:327–31.PubMedGoogle Scholar
  204. Tugume AK, Mukasa SB, Valkonen JPT. Mixed infections of four viruses, the incidence and phylogenetic relationships of Sweet potato chlorotic fleck virus (Betaflexiviridae) isolates in wild species and sweetpotatoes in Uganda and evidence of distinct isolates in East Africa. PLoS One. 2016;11:e0167769.PubMedPubMedCentralGoogle Scholar
  205. van der Walt E, Martin DP, Varsani A, Polston JE, Rybicki EP. Experimental observations of rapid maize streak virus evolution reveal a strand-specific nucleotide substitution bias. Virol J. 2008;5:104.PubMedPubMedCentralGoogle Scholar
  206. Wang J, Moore NE, Deng Y-M, Eccles DA, Hall RJ. MinION nanopore sequencing of an influenza genome. Front Microbiol. 2017;6:766.Google Scholar
  207. Wanunu M. Nanopores: a journey towards DNA sequencing. Phys Life Rev. 2012;9:125–58.PubMedPubMedCentralGoogle Scholar
  208. Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet. 2002;32:569–77.PubMedGoogle Scholar
  209. Worobey M, Holmes EC. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999;80:2535–43.PubMedGoogle Scholar
  210. Wu X, Xu Z, Shaw JG. Uncoating of tobacco mosaic virus RNA in protoplasts. Virology. 1994;200:256–62.PubMedGoogle Scholar
  211. Wu B, Melcher U, Guo X, Wang X, Fan L, Zhou G. Assessment of codivergence of mastreviruses with their plant hosts. BMC Evol Biol. 2008;8:335.PubMedPubMedCentralGoogle Scholar
  212. Wu B, Blanchard-Letort A, Liu Y, Zhou G, Wang X, Elena SF. Dynamics of molecular evolution and phylogeography of Barley yellow dwarf virus-PAV. PLoS One. 2011;6:e16896.PubMedPubMedCentralGoogle Scholar
  213. Wu Q, Ding SW, Zhang Y, Zhu S. Identification of viruses and viroids by next-generation sequencing and homology-dependent and homology-independent algorithms. Annu Rev Phytopathol. 2015;53:425–44.PubMedGoogle Scholar
  214. Wylie SJ, Li H, Dixon KW, Richards H, Jones MGK. Exotic and indigenous viruses infect wild populations and captive collections of temperate terrestrial orchids (Diuris species) in Australia. Virus Res. 2013;171:22–32.PubMedGoogle Scholar
  215. Xu P, Chen F, Mannas JP, Feldman T, Sumner LW, Roossinck MJ. Virus infection improves drought tolerance. New Phytol. 2008;180:911–21.PubMedGoogle Scholar
  216. Yasaka R, Nguyen HD, Ho SYW, Duchêne S, Korkmaz S, Nikolaos K, Takahashi H, Gibbs AJ, Ohshima K. The temporal evolution and global spread of Cauliflower mosaic virus, a plant pararetrovirus. PLoS One. 2014;9:e85641.PubMedPubMedCentralGoogle Scholar
  217. Zwart MP, Willemsen A, Darós JA, Elena SF. Experimental evolution of pseudogenization and gene loss in a plant RNA virus. Mol Biol Evol. 2014;31:121–34.PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Centro de Biotecnología y Genómica de Plantas UPM-INIAUniversidad Politécnica de MadridPozuelo de Alarcón, MadridSpain
  2. 2.E.T.S. Ingeniería Agronómica, Alimentaria y de BiosistemasMadridSpain

Personalised recommendations