The genetic variability of grapevine Pinot gris virus (GPGV) in Australia.

GPGV Median joining network Metagenomic HTS Phylogenetic analysis Population genetics Recombination

Journal

Virology journal
ISSN: 1743-422X
Titre abrégé: Virol J
Pays: England
ID NLM: 101231645

Informations de publication

Date de publication:
13 09 2023
Historique:
received: 02 05 2023
accepted: 28 08 2023
medline: 15 9 2023
pubmed: 14 9 2023
entrez: 13 9 2023
Statut: epublish

Résumé

Grapevine Pinot gris virus (GPGV; genus Trichovirus in the family Betaflexiviridae) was detected in Australia in 2016, but its impact on the production of nursery material and fruit in Australia is still currently unknown. This study investigated the prevalence and genetic diversity of GPGV in Australia. GPGV was detected by reverse transcription-polymerase chain reaction (RT-PCR) in a range of rootstock, table and wine grape varieties from New South Wales, South Australia, and Victoria, with 473/2171 (21.8%) samples found to be infected. Genomes of 32 Australian GPGV isolates were sequenced and many of the isolates shared high nucleotide homology. Phylogenetic and haplotype analyses demonstrated that there were four distinct clades amongst the 32 Australian GPGV isolates and that there were likely to have been at least five separate introductions of the virus into Australia. Recombination and haplotype analysis indicate the emergence of new GPGV strains after introduction into Australia. When compared with 168 overseas GPGV isolates, the analyses suggest that the most likely origin of Australian GPGV isolates is from Europe. There was no correlation between specific GPGV genotypes and symptoms such as leaf mottling, leaf deformation, and shoot stunting, which were observed in some vineyards, and the virus was frequently found in symptomless grapevines.

Identifiants

pubmed: 37705082
doi: 10.1186/s12985-023-02171-3
pii: 10.1186/s12985-023-02171-3
pmc: PMC10500770
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

211

Informations de copyright

© 2023. BioMed Central Ltd., part of Springer Nature.

Références

Giampetruzzi A, Roumi V, Roberto R, Malossini U, Yoshikawa N, La Notte P, et al. A new grapevine virus discovered by deep sequencing of virus-and viroid-derived small RNAs in Cv Pinot gris. Virus Res. 2012;163(1):262–8. https://doi.org/10.1016/j.virusres.2011.10.010 .
doi: 10.1016/j.virusres.2011.10.010 pubmed: 22036729
Bertazzon N, Forte V, Filippin L, Causin R, Maixner M, Angelini E. Association between genetic variability and titre of Grapevine Pinot gris virus with disease symptoms. Plant Pathol. 2017;66(6):949–59. https://doi.org/10.1111/ppa.12639 .
doi: 10.1111/ppa.12639
Eichmeier A, Peňázová E, Muljukina N. Survey of Grapevine Pinot gris virus in certified grapevine stocks in Ukraine. Eur Found Plant Pathol. 2018;152(2):555–60. https://doi.org/10.1007/s10658-018-1497-5 .
doi: 10.1007/s10658-018-1497-5
Glasa M, Predajňa L, Komínek P, Nagyová A, Candresse T, Olmos A. Molecular characterization of divergent grapevine Pinot gris virus isolates and their detection in Slovak and Czech grapevines. Adv Virol. 2014;159(8):2103–7. https://doi.org/10.1007/s00705-014-2031-5 .
doi: 10.1007/s00705-014-2031-5
Hily J-M, Poulicard N, Candresse T, Vigne E, Beuve M, Renault L, et al. Datamining, genetic diversity analyses, and phylogeographic reconstructions redefine the worldwide evolutionary history of Grapevine Pinot gris virus and Grapevine berry inner necrosis virus. Phytobiomes J. 2020;4(2):165–77. https://doi.org/10.1094/PBIOMES-10-19-0061-R .
doi: 10.1094/PBIOMES-10-19-0061-R
Saldarelli P, Giampetruzzi A, Morelli M, Malossini U, Pirolo C, Bianchedi P, et al. Genetic variability of Grapevine Pinot gris virus and its association with grapevine leaf mottling and deformation. Phytopathology. 2015;105(4):555–63. https://doi.org/10.1094/PHYTO-09-14-0241-R .
doi: 10.1094/PHYTO-09-14-0241-R pubmed: 25423070
Eichmeier A, Penazova E, Nebish A. First report of grapevine pinot gris virus on grapevines in Armenia. Plant Dis. 2020;104(3):1000. https://doi.org/10.1094/PDIS-09-19-1944-PDN .
doi: 10.1094/PDIS-09-19-1944-PDN
Eichmeier A, Peňázová E, Čechová J, Berraf-Tebbal A. Survey and diversity of grapevine pinot gris virus in algeria and comprehensive high-throughput small rna sequencing analysis of two isolates from vitis vinifera cv. Sabel revealing high viral diversity. Genes. 2020;11(9):1110. https://doi.org/10.3390/genes11091110 .
doi: 10.3390/genes11091110 pubmed: 32971929 pmcid: 7563602
Pleško IM, Marn MV, Seljak G, Žežlina I. First report of Grapevine Pinot gris virus infecting grapevine in Slovenia. Plant Dis. 2014;98(7):1014. https://doi.org/10.1094/PDIS-11-13-1137-PDN .
doi: 10.1094/PDIS-11-13-1137-PDN pubmed: 30708883
Saldarelli P, Beber R, Covelli L, Bianchedi P, Credi R, Giampetruzzi A, et al. Studies on a new grapevine disease in Trentino vineyards. J Plant Pathol. 2013;95(S4):60.
Bertazzon N, Forte V, Filippin L, Angelini E, editors. Studies on Grapevine Pinot gris virus (GPGV) presence and its association with an emergent disease of grapevine. Proceedings of the 18th Congress of ICVG; 2015.
Malossini U, Bianchedi P, Beber R, Credi R, Saldarelli P, Gualandri V, editors. Spread of GPGV-associated disease in two vineyards in Trentino (Italy). ICVG18: 18th Conference of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine; 2015.
Malossini U, Bianchedi P, Roman T, Varner M, Gualandri V, Nicolini G, editors. An updating about the performances of Pinot Gris and Traminer vines affected by the GPGV trichovirus-related grapevine disease. 37th World Congress of Vine and Wine, 12th General Assembly of the OIV" Southern Vitiviniculture, a Confluence of Knowledge and Nature"; 2014.
Malossini U, Bianchedi P, Villegas TR, Varner M, Gualandri V, Nicolini G. Aggiornamento sulle performance di viti Pinot grigio e Traminer affette dalla fitopatologia correlata al Trichovirus GPGV.
Tarquini G, Zaina G, Ermacora P, De Amicis F, Franco-Orozco B, Loi N, et al. Agroinoculation of Grapevine Pinot Gris Virus in tobacco and grapevine provides insights on viral pathogenesis. PLoS ONE. 2019;14(3):e0214010. https://doi.org/10.1371/journal.pone.0214010 .
doi: 10.1371/journal.pone.0214010 pubmed: 30889228 pmcid: 6424481
Eichmeier A, Komínková M, Komínek P, Baránek M. Comprehensive virus detection using next generation sequencing in grapevine vascular tissues of plants obtained from the wine regions of Bohemia and Moravia (Czech Republic). PLoS ONE. 2016;11(12):e0167966. https://doi.org/10.1371/journal.pone.0167966 .
doi: 10.1371/journal.pone.0167966 pubmed: 27959951 pmcid: 5154529
Bertazzon N, Filippin L, Forte V, Angelini E. Grapevine Pinot gris virus seems to have recently been introduced to vineyards in Veneto, Italy. Arch Virol. 2016;161(3):711–4. https://doi.org/10.1007/s00705-015-2718-2 .
doi: 10.1007/s00705-015-2718-2 pubmed: 26666440
Tarquini G, Ermacora P, Firrao G. Polymorphisms at the 3’end of the movement protein (MP) gene of grapevine Pinot gris virus (GPGV) affect virus titre and small interfering RNA accumulation in GLMD disease. Virus Res. 2021;302:198482. https://doi.org/10.1016/j.virusres.2021.198482 .
doi: 10.1016/j.virusres.2021.198482 pubmed: 34119570
Tarquini G, De Amicis F, Martini M, Ermacora P, Loi N, Musetti R, et al. Analysis of new grapevine Pinot gris virus (GPGV) isolates from Northeast Italy provides clues to track the evolution of a newly emerging clade. Adv Virol. 2019;164(6):1655–60. https://doi.org/10.1007/s00705-019-04241-w .
doi: 10.1007/s00705-019-04241-w
Tarquini G, Ermacora P, Bianchi G, De Amicis F, Pagliari L, Martini M, et al. Localization and subcellular association of Grapevine Pinot Gris Virus in grapevine leaf tissues. Int J Anim Fungal Plant Cell Biol. 2018;255(3):923–35. https://doi.org/10.1007/s00709-017-1198-5 .
doi: 10.1007/s00709-017-1198-5
Tarquini G, Pagliari L, Ermacora P, Musetti R, Firrao G. Trigger and suppression of antiviral defenses by grapevine Pinot gris virus (GPGV): novel insights into virus-host interaction. Mol Plant Microbe Interact. 2021;34(9):1010–23. https://doi.org/10.1094/MPMI-04-21-0078-R .
doi: 10.1094/MPMI-04-21-0078-R pubmed: 33983824
Bertazzon N, Forte V, Angelini E. Fast transmission of grapevine ‘Pinot gris’ virus (GPGV) in vineyard. Vitis. 2020;59(1):29–34. https://doi.org/10.5073/vitis.2020.59.29-34 .
doi: 10.5073/vitis.2020.59.29-34
Constable F, Tassie E, McLoughlin S. A comprehensive review of Grapevine Pinot gris virus (GPGV). 2019.
Buoso S, Pagliari L, Musetti R, Fornasier F, Martini M, Loschi A, et al. With or without you: Altered plant response to boron-deficiency in hydroponically grown grapevines infected by Grapevine Pinot gris virus suggests a relation between grapevine leaf mottling and deformation symptom occurrence and boron plant availability. Front Plant Sci. 2020;11:226. https://doi.org/10.3389/fpls.2020.00226 .
doi: 10.3389/fpls.2020.00226 pubmed: 32194603 pmcid: 7062799
Malagnini V, De Lillo E, Saldarelli P, Beber R, Duso C, Raiola A, et al., editors. Preliminary data on the transmission of grapevine pinot Gris virus by Colomerus vitis. Proceedings of the 18th congress of ICVG; 2015: Turkey Ankara. https://doi.org/10.13140/RG.2.1.1445.3208
Wu Q, Habili N. The recent importation of Grapevine Pinot gris virus into Australia. Virus Genes. 2017;53(6):935–8. https://doi.org/10.1007/s11262-017-1475-6 .
doi: 10.1007/s11262-017-1475-6 pubmed: 28612275
Constable F, Joyce P, Rodoni B. A survey of key Australian pome fruit growing districts for exotic and endemic pathogens. Austral Plant Pathol. 2007;36(2):165–72.
doi: 10.1071/AP07003
Thompson JR, Wetzel S, Klerks M, Vašková D, Schoen C, Špak J, et al. Multiplex RT-PCR detection of four aphid-borne strawberry viruses in Fragaria spp. in combination with a plant mRNA specific internal control. J Virol Methods. 2003;111(2):85–93. https://doi.org/10.1016/S0166-0934(03)00164-2 .
doi: 10.1016/S0166-0934(03)00164-2 pubmed: 12880923
Bianchi G, De Amicis F, De Sabbata L, Di Bernardo N, Governatori G, Nonino F, et al. Occurrence of grapevine pinot gris virus in Friuli Venezia Giulia (Italy): field monitoring and virus quantification by real-time RT-PCR. EPPO Bull. 2015;45(1):22–32. https://doi.org/10.1111/epp.12196 .
doi: 10.1111/epp.12196
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77.
doi: 10.1089/cmb.2012.0021 pubmed: 22506599 pmcid: 3342519
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.
doi: 10.1016/S0022-2836(05)80360-2 pubmed: 2231712
Morelli M, Catarino AdM, Susca L, Saldarelli P, Gualandri V, Martelli G. First report of grapevine pinot gris virus from table grapes in Southern Italy. J Plant Pathol. 2014. https://doi.org/10.4454/JPP.V96I2.039 .
doi: 10.4454/JPP.V96I2.039
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547. https://doi.org/10.1093/molbev/msy096 .
doi: 10.1093/molbev/msy096 pubmed: 29722887 pmcid: 5967553
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. https://doi.org/10.1093/nar/gkh340 .
doi: 10.1093/nar/gkh340 pubmed: 15034147 pmcid: 390337
Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows. Nucleic Acids Symp Ser. 1999;41(41):95–8.
Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE. 2014;9(9):e108277.
doi: 10.1371/journal.pone.0108277 pubmed: 25259891 pmcid: 4178126
King AM, Lefkowitz E, Adams MJ, Carstens EB. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses: Elsevier; 2011.
Silva JMF, Melo FL, Elena SF, Candresse T, Sabanadzovic S, Tzanetakis IE, et al. Virus classification based on in-depth sequence analyses and development of demarcation criteria using the Betaflexiviridae as a case study. J Gener Virol. 2022;103(11):001806. https://doi.org/10.1099/jgv.0.001806 .
doi: 10.1099/jgv.0.001806
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19(18):2496–7. https://doi.org/10.1093/bioinformatics/btg359 .
doi: 10.1093/bioinformatics/btg359 pubmed: 14668244
Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123(3):585–95.
doi: 10.1093/genetics/123.3.585 pubmed: 2513255 pmcid: 1203831
Hudson RR, Slatkin M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992;132(2):583–9.
doi: 10.1093/genetics/132.2.583 pubmed: 1427045 pmcid: 1205159
Tsompana M, Abad J, Purugganan M, Moyer J. The molecular population genetics of the Tomato spotted wilt virus (TSWV) genome. Mol Ecol. 2005;14(1):53–66. https://doi.org/10.1111/j.1365-294X.2004.02392.x .
doi: 10.1111/j.1365-294X.2004.02392.x pubmed: 15643950
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015. https://doi.org/10.1093/ve/vev003 .
doi: 10.1093/ve/vev003 pubmed: 27774281 pmcid: 5014477
Kinoti WM, Nancarrow N, Dann A, Rodoni BC, Constable FE. Updating the quarantine status of prunus infecting viruses in Australia. Viruses. 2020;12(2):246. https://doi.org/10.3390/v12020246 .
doi: 10.3390/v12020246 pubmed: 32102210 pmcid: 7077234
Kehoe MA, Coutts BA, Buirchell BJ, Jones RA. Split personality of a Potyvirus: to specialize or not to specialize? PLoS ONE. 2014;9(8):e105770. https://doi.org/10.1371/journal.pone.0105770 .
doi: 10.1371/journal.pone.0105770 pubmed: 25148372 pmcid: 4141833
Wylie S, Jones R. Role of recombination in the evolution of host specialization within Bean yellow mosaic virus. Phytopathology. 2009;99(5):512–8. https://doi.org/10.1094/PHYTO-99-5-0512 .
doi: 10.1094/PHYTO-99-5-0512 pubmed: 19351247
Ohshima K, Yamaguchi Y, Hirota R, Hamamoto T, Tomimura K, Tan Z, et al. Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol. 2002;83(6):1511–21. https://doi.org/10.1099/0022-1317-83-6-1511 .
doi: 10.1099/0022-1317-83-6-1511 pubmed: 12029167
Elena S, Agudelo-Romero P, Carrasco P, Codoner F, Martin S, Torres-Barceló C, et al. Experimental evolution of plant RNA viruses. Heredity. 2008;100(5):478–83. https://doi.org/10.1038/sj.hdy.6801088 .
doi: 10.1038/sj.hdy.6801088 pubmed: 18253158
García-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol. 2001;39:157. https://doi.org/10.1146/annurev.phyto.39.1.157 .
doi: 10.1146/annurev.phyto.39.1.157 pubmed: 11701863
Malagnini V, de Lillo E, Saldarelli P, Beber R, Duso C, Raiola A, et al. Transmission of grapevine Pinot gris virus by Colomerus vitis (Acari: Eriophyidae) to grapevine. Adv Virol. 2016;161(9):2595–9. https://doi.org/10.1007/s00705-016-2935-3 .
doi: 10.1007/s00705-016-2935-3
Michalska K, Skoracka A, Navia D, Amrine JW. Behavioural studies on eriophyoid mites: an overview. Exp Appl Acarol. 2010;51(1):31–59.
doi: 10.1007/s10493-009-9319-2 pubmed: 19779863
Marra M, Giampetruzzi A, Abou Kubaa R, de Lillo E, Saldarelli P. Grapevine pinot gris virus variants in vines with chlorotic mottling and leaf deformation. J Plant Pathol. 2020;102(2):531. https://doi.org/10.1007/s42161-019-00418-z .
doi: 10.1007/s42161-019-00418-z
Shvets D, Vinogradova S. Occurrence and genetic characterization of grapevine pinot gris virus in Russia. Plants. 2022;11(8):1061. https://doi.org/10.3390/plants11081061 .
doi: 10.3390/plants11081061 pubmed: 35448789 pmcid: 9028157
Vu M, Vemulapati BM, McFadden-Smith W, Fall ML, Úrbez-Torres JR, Moreau DL, et al. Phylogenetic and evolutionary studies of grapevine pinot gris virus isolates from Canada. Viruses. 2023;15(3):735. https://doi.org/10.3390/v15030735 .
doi: 10.3390/v15030735 pubmed: 36992444 pmcid: 10057519
Vončina D, Al Rwahnih M, Rowhani A, Gouran M, Almeida RP. Viral diversity in autochthonous croatian grapevine cultivars. Plant Dis. 2017;101(7):1230–5. https://doi.org/10.1094/PDIS-10-16-1543-RE .
doi: 10.1094/PDIS-10-16-1543-RE pubmed: 30682947
Porotikova E, Terehova U, Volodin V, Yurchenko E, Vinogradova S. Distribution and genetic diversity of grapevine viruses in Russia. Plants. 2021;10(6):1080. https://doi.org/10.3390/plants10061080 .
doi: 10.3390/plants10061080 pubmed: 34072229 pmcid: 8229536
Angelini E, Bazzo I, Bertazzon N, Filippin L, Forte V. A New Disease In Italian Vineyards. Wines & Vines, September. 2015; https://www.winesandvines.com/features/article/156977
Constable F, Tassie L, McLoughlin S. Pests and diseases: GPGV knowledge boost. Austr NZ Grapegrower Winemak. 2019. https://doi.org/10.3316/informit.318610880360548 .
doi: 10.3316/informit.318610880360548
Morán F, Olmos A, Lotos L, Predajňa L, Katis N, Glasa M, et al. A novel specific duplex real-time RT-PCR method for absolute quantitation of grapevine pinot gris virus in plant material and single mites. PLoS ONE. 2018;13(5):e0197237. https://doi.org/10.1371/journal.pone.0197237 .
doi: 10.1371/journal.pone.0197237 pubmed: 29763449 pmcid: 5953474
Berger K, Truog E. Boron availability in relation to soil reaction and organic matter content. Soil Sci Soc Am J. 1946;10(c):113–6. https://doi.org/10.2136/sssaj1946.03615995001000C00018x .
doi: 10.2136/sssaj1946.03615995001000C00018x
Constable F, Connellan J, Nicholas P, Rodoni B. The reliability of woody indexing for detection of grapevine virus-associated diseases in three different climatic conditions in A ustralia. Aust J Grape Wine Res. 2013;19(1):74–80. https://doi.org/10.1111/j.1755-0238.2012.00204.x .
doi: 10.1111/j.1755-0238.2012.00204.x
Kiss T, Kocanová M, Vavřiník A, Tekielska D, Pečenka J, Hakalová E, et al. Incidence of GLMD-like symptoms on grapevines naturally infected by grapevine Pinot gris virus, boron content and gene expression analysis of boron metabolism genes. Agronomy. 2021;11(6):1020. https://doi.org/10.3390/agronomy11061020 .
doi: 10.3390/agronomy11061020
Mikhail EH, Martin JJ. Soils of the Nangiloc-Colignan Irrigation Area: Department of Agriculture and Rural Affairs; 1986.
Penman F, Hubble GD, Taylor JK, Hooper PD. A soil survey of the Mildura Irrigation Settlement, Victoria: T. Rider, government printer; 1940.

Auteurs

Kamalpreet Kaur (K)

School of Applied Systems Biology, La Trobe University, Bundoora, VIC, Australia. kamalpreet.kaur@agriculture.vic.gov.au.
Agriculture Victoria Research, Department of Energy, Environment and Climate Action, Melbourne, VIC, Australia. kamalpreet.kaur@agriculture.vic.gov.au.

Amy Rinaldo (A)

The Australian Wine Research Institute, Adelaide, SA, Australia.

David Lovelock (D)

Agriculture Victoria Research, Department of Energy, Environment and Climate Action, Melbourne, VIC, Australia.

Brendan Rodoni (B)

School of Applied Systems Biology, La Trobe University, Bundoora, VIC, Australia.
Agriculture Victoria Research, Department of Energy, Environment and Climate Action, Melbourne, VIC, Australia.

Fiona Constable (F)

School of Applied Systems Biology, La Trobe University, Bundoora, VIC, Australia.
Agriculture Victoria Research, Department of Energy, Environment and Climate Action, Melbourne, VIC, Australia.

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