1887

Abstract

In this study 163 complete whole-genome sequences of the emerging pathogen grapevine red blotch virus (GRBV; genus , family ) were used to reconstruct phylogenies using Bayesian analyses on time-tipped (heterochronous) data. Using different combinations of priors, Bayes factors identified heterochronous datasets (3×200 million chains) generated from strict clock and exponential tree priors as being the most robust. Substitution rates of 3.2×10 subsitutions per site per year (95% HPD 4.3–2.1×10) across the whole of the GRBV genome were estimated, suggesting ancestral GRBV diverged from ancestral wild Vitis latent virus 1 around 9 000 years ago, well before the first documented arrival of in North America. Whole-genome analysis of GRBV isolates in a single infected field-grown grapevine across 12 years identified 12 single nucleotide polymorphisms none of which were fixed substitutions: an observation not discordant with the estimate. The substitution rate estimated here is lower than those estimated for other geminiviruses and is the first for a woody-host-infecting geminivirus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001789
2022-10-07
2024-05-05
Loading full text...

Full text loading...

References

  1. Power AG, Mitchell CE. Pathogen spillover in disease epidemics. Am Nat 2004; 164 Suppl 5:S79–89 [View Article]
    [Google Scholar]
  2. Gougherty AV, Davies TJ. Towards a phylogenetic ecology of plant pests and pathogens. Philos Trans R Soc Lond B Biol Sci 2021; 376:20200359 [View Article]
    [Google Scholar]
  3. Wasik BR, de Wit E, Munster V, Lloyd-Smith JO, Martinez-Sobrido L et al. Onward transmission of viruses: how do viruses emerge to cause epidemics after spillover?. Philos Trans R Soc Lond B Biol Sci 2019; 374:20190017 [View Article]
    [Google Scholar]
  4. Krenz B, Thompson JR, Fuchs M, Perry KL. Complete genome sequence of a new circular DNA virus from grapevine. J Virol 2012; 86:7715 [View Article]
    [Google Scholar]
  5. Rwahnih MA, Dave A, Anderson MM, Rowhani A, Uyemoto JK et al. Association of a DNA virus with grapevines affected by red blotch disease in California. Phytopathology® 2013; 103:1069–1076 [View Article]
    [Google Scholar]
  6. Yepes LM, Cieniewicz E, Krenz B, McLane H, Thompson JR et al. Causative role of grapevine red blotch virus in red blotch disease. Phytopathology 2018; 108:902–909 [View Article]
    [Google Scholar]
  7. Marwal A, Kumar R, Paul Khurana SM, Gaur RK. Complete nucleotide sequence of a new geminivirus isolated from vitis vinifera in india: a symptomless host of grapevine red blotch virus. VirusDis 2019; 30:106–111 [View Article]
    [Google Scholar]
  8. Luna F, Debat H, Moyano S, Zavallo D, Asurmendi S et al. First report of grapevine red blotch virus infecting grapevine in Argentina. J Plant Pathol 2019; 101:1239 [View Article]
    [Google Scholar]
  9. Lim S, Igori D, Zhao F, Moon JS, Cho I-S et al. First Report of Grapevine red blotch-associated virus on Grapevine in Korea. Plant Dis 2016; 100:1957 [View Article]
    [Google Scholar]
  10. Gasperin-Bulbarela J, Licea-Navarro AF, Pino-Villar C, Hernández- R, Carrillo-Tripp J. First report of grapevine red blotch virus in Mexico. Plant Dis 2019; 103:381 [View Article]
    [Google Scholar]
  11. Xiao H, Shabanian M, Moore C, Li C, Meng B. Survey for major viruses in commercial vitis vinifera wine grapes in ontario. Virol J 2018; 15:127 [View Article]
    [Google Scholar]
  12. Al Rwahnih M, Alabi OJ, Westrick NM, Golino D. Prunus geminivirus a: a novel grablovirus infecting prunus spp. Plant Dis In press 102:1246–1253 [View Article]
    [Google Scholar]
  13. Perry KL, McLane H, Thompson JR, Fuchs M. A novel grablovirus from non-cultivated grapevine (vitis sp.) in north america. Arch Virol 2018; 163:259–262 [View Article]
    [Google Scholar]
  14. Bahder BW, Zalom FG, Jayanth M, Sudarshana MR. Phylogeny of geminivirus coat protein sequences and digital PCR aid in identifying spissistilus festinus as a vector of grapevine red blotch-associated virus. Phytopathology® 2016; 106:1223–1230 [View Article]
    [Google Scholar]
  15. Cieniewicz E, Thompson JR, McLane H, Perry KL, Dangl GS et al. Prevalence and genetic diversity of rabloviruses in free-living vitis spp. Plant Dis 2018; 102:2308–2316 Epub 2018/09/13 [View Article]
    [Google Scholar]
  16. Flasco M, Hoyle V, Cieniewicz EJ, Roy BG, McLane HL et al. Grapevine red blotch virus is transmitted by the three-cornered alfalfa hopper in a circulative, nonpropagative mode with unique attributes. Phytopathology® 2021; 111:1851–1861 [View Article]
    [Google Scholar]
  17. Cieniewicz EJ, Qiu WP, Saldarelli P, Fuchs M. Believing is seeing: lessons from emerging viruses in grapevine. J Plant Pathol 2020; 102:619–632 [View Article]
    [Google Scholar]
  18. Cieniewicz E, Flasco M, Brunelli M, Onwumelu A, Wise A et al. Differential spread of grapevine red blotch virus in California and New York Vineyards. Phytobiomes Journal 2019; 3:203–211 [View Article]
    [Google Scholar]
  19. Qiu W, Petersen SM, Howard S. North american grape ‘norton’ is resistant to grapevine vein clearing irus. Plant Dis 2020; 104:2051–2053 [View Article]
    [Google Scholar]
  20. Rojas MR, Macedo MA, Maliano MR, Soto-Aguilar M, Souza JO et al. World management of geminiviruses. Annu Rev Phytopathol 2018; 56:637–677 Epub 2018/08/29 [View Article]
    [Google Scholar]
  21. Al Rwahnih M, Alabi OJ, Westrick NM, Golino D, Rowhani A. Description of a novel monopartite geminivirus and its defective subviral genome in grapevine. Phytopathology® 2017; 107:240–251 [View Article]
    [Google Scholar]
  22. Tabassum A, Ramesh SV, Zhai Y, Iftikhar R, Olaya C et al. Viruses without borders: global analysis of the population structure, haplotype distribution, and evolutionary pattern of iris yellow spot orthotospovirus (family tospoviridae, genus orthotospovirus). Front Microbiol 2021; 12:633710 [View Article]
    [Google Scholar]
  23. Thompson JR, Kamath N, Perry KL. An evolutionary analysis of the secoviridae family of viruses. PLoS One 2014; 9:e106305 [View Article]
    [Google Scholar]
  24. Fuentes S, Gibbs AJ, Adams IP, Hajizadeh M, Kreuze J et al. Phylogenetics and evolution of potato virus v: another potyvirus that originated in the andes. Plant Dis 2022; 106:691–700 [View Article]
    [Google Scholar]
  25. Gibbs AJ, Ohshima K, Yasaka R, Mohammadi M, Gibbs MJ et al. The phylogenetics of the global population of potato virus Y and its necrogenic recombinants. Virus Evol 2017; 3:vex002 [View Article]
    [Google Scholar]
  26. Pagán I, Holmes EC. Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. J Virol 2010; 84:6177–6187 [View Article] [PubMed]
    [Google Scholar]
  27. Pinel-Galzi A, Traoré O, Séré Y, Hébrard E, Fargette D. The biogeography of viral emergence: rice yellow mottle virus as a case study. Curr Opin Virol 2015; 10:7–13 [View Article]
    [Google Scholar]
  28. Xu Y, Zhang S, Shen J, Wu Z, Du Z et al. The phylogeographic history of tomato mosaic virus in eurasia. Virology 2021; 554:42–47 [View Article]
    [Google Scholar]
  29. Duffy S. Why are RNA virus mutation rates so damn high?. PLoS Biol 2018; 16:e3000003 [View Article]
    [Google Scholar]
  30. Peck KM, Lauring AS, Sullivan CS. Complexities of viral mutation rates. J Virol 2018; 92: [View Article]
    [Google Scholar]
  31. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol 2010; 84:9733–9748 [View Article]
    [Google Scholar]
  32. Sanjuán R, Domingo-Calap P. Mechanisms of viral mutation. Cell Mol Life Sci 2016; 73:4433–4448 [View Article]
    [Google Scholar]
  33. Shackelton LA, Parrish CR, Truyen U, Holmes EC. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci USA 2005; 102:379–384 [View Article]
    [Google Scholar]
  34. Sarker S, Patterson EI, Peters A, Baker GB, Forwood JK et al. Mutability dynamics of an emergent single stranded DNA virus in a naive host. PLoS ONE 2014; 9:e85370 [View Article]
    [Google Scholar]
  35. Sanjuán R, Agudelo-Romero P, Elena SF. Upper-limit mutation rate estimation for a plant RNA virus. Biol Lett 2009; 5:394–396 [View Article]
    [Google Scholar]
  36. 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; 82:957–965 [View Article]
    [Google Scholar]
  37. 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; 90:1539–1547 [View Article]
    [Google Scholar]
  38. Harkins GW, Martin DP, Duffy S, Monjane AL, Shepherd DN et al. Dating the origins of the maize-adapted strain of maize streak virus, MSV-A. J Gen Virol 2009; 90:3066–3074 [View Article]
    [Google Scholar]
  39. Harkins GW, Delport W, Duffy S, Wood N, Monjane AL et al. Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts. Virol J 2009; 6:104 [View Article]
    [Google Scholar]
  40. Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA et al. The spread of tomato yellow leaf curl virus from the middle east to the world. PLoS Pathog 2010; 6:e1001164 [View Article]
    [Google Scholar]
  41. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  42. Milne I, Lindner D, Bayer M, Husmeier D, McGuire G et al. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 2009; 25:126–127 [View Article] [PubMed]
    [Google Scholar]
  43. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2:vew007 [View Article] [PubMed]
    [Google Scholar]
  44. Gambino G, Perrone I, Gribaudo I. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 2008; 19:520–525 [View Article]
    [Google Scholar]
  45. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10(3):512–526 [View Article]
    [Google Scholar]
  46. Kass RE, Raftery AE. Bayes factors. J Am Stat Assoc 1995; 90:773–795 [View Article]
    [Google Scholar]
  47. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A, Penny D. Relaxed phylogenetics and dating with confidence. PLoS Biol 2006; 4:e88 Epub 2006/05/11 [View Article]
    [Google Scholar]
  48. Duchene S, Lemey P, Stadler T, Ho SYW, Duchene DA et al. Bayesian evaluation of temporal signal in measurably evolving populations. Mol Biol Evol 2020; 37:3363–3379 [View Article]
    [Google Scholar]
  49. van der Walt E, Rybicki EP, Varsani A, Polston JE, Billharz R et al. Rapid host adaptation by extensive recombination. J Gen Virol 2009; 90:734–746 [View Article]
    [Google Scholar]
  50. Carbone A, Quici L, Pica G. The age dynamics of vineyards: past trends affecting the future. Wine Economics and Policy 2019; 8:38–48 [View Article]
    [Google Scholar]
  51. Cieniewicz EJ, Pethybridge SJ, Loeb G, Perry K, Fuchs M. Insights into the ecology of grapevine red blotch virus in a diseased vineyard. Phytopathology 2018; 108:94–102 [View Article]
    [Google Scholar]
  52. Katsiani A, Maliogka V, Katis N, Svanella-Dumas L, Olmos A et al. High-throughput sequencing reveals further diversity of little cherry virus 1 with implications for diagnostics. Viruses 2018; 10:385 [View Article]
    [Google Scholar]
  53. Kinoti WM, Constable FE, Nancarrow N, Plummer KM, Rodoni B et al. Analysis of intra-host genetic diversity of prunus necrotic ringspot virus (PNRSV) using amplicon next generation sequencing. PLoS ONE 2017; 12:e0179284 [View Article]
    [Google Scholar]
  54. Liu W, Zhou Y, Hu Z, Sun T, Denise A et al. Regulation of splicing enhancer activities by RNA secondary structures. FEBS Lett 2010; 584:4401–4407 [View Article]
    [Google Scholar]
  55. Warf MB, Berglund JA. Role of RNA structure in regulating pre-mrna splicing. Trends Biochem Sci 2010; 35:169–178 [View Article]
    [Google Scholar]
  56. Buratti E, Baralle FE. Influence of RNA secondary structure on the pre-mRNA splicing process. Mol Cell Biol 2004; 24:10505–10514 [View Article]
    [Google Scholar]
  57. Blake Birchell D. New Mexico wine: an enchanting history Charleston, SC: American Palate; 2013
    [Google Scholar]
  58. Bertazzon N, Migliaro D, Rossa A, Filippin L, Casarin S et al. Grapevine red blotch virus is sporadically present in a germplasm collection in Northern Italy. J Plant Dis Prot 2021; 128:1115–1119 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001789
Loading
/content/journal/jgv/10.1099/jgv.0.001789
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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