Abstract
Many potyviruses have been found in Australia. We analyzed a selected region of the coat protein genes of 37 of them to determine their relationships, and found that they fall into two groups. Half were isolated from cultivated plants and crops, and are also found in other parts of the world. Sequence comparisons show that the Australian populations of these viruses are closely related to, but less variable than, those in other parts of the world, and they represent many different potyvirus lineages. The other half of the potyviruses have only been found in Australia, and most were isolated from native plants. The sequences of these potyviruses, which are probably endemic, are on average five times more variable than those of the crop potyviruses, but surprisingly, most of the endemic potyviruses belong to one potyvirus lineage, the bean common mosaic virus lineage. We conclude that the crop potyviruses entered Australia after agriculture was established by European migrants two centuries ago, whereas the endemic plant potyviruses probably entered Australia before the Europeans. Australia, like the U.K., seems recently to have had c. one incursion of a significant crop potyvirus every decade. Our analysis suggests it is likely that potyviruses are transmitted in seed more frequently than experimental evidence indicates, and shows that understanding the sources of emerging pathogens and the frequency with which they ‘emerge’ is essential for proper national biosecurity planning.
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References
Brunt AA, Crabtree K, Dallwitz M, Gibbs A, Watson L (1996) Viruses of plants. C. A. B. International, UK
Buchen-Osmond C, Crabtree K, Gibbs A, McLean G (1988) Viruses of plants in Australia. Australian National University, Canberra
Carver M, Gross GF, Woodward TE (1991) Hemiptera (bugs, leafhoppers, cicadas, aphids, scale insects, etc). In: Naumann ID (ed) The insects of Australia, vol 1. Melbourne University Press, Melbourne
Chen J, Chen J, Adams MJ (2001) A universal PCR primer to detect members of the Potyviridae and its use to examine the taxonomic status of several members of the family. Arch Virol 146:757–766
Clemens WA, Richardson AJ, Baverstock PR (1989) Biogeography and phylogeny of the Metatheria. In: Walton DW, Richardson BJ (eds) Fauna of Australia vol IB Mammalia. Australian Government Publishing Service, Canberra, pp 527–548
Crisp MD (2001) Historical biogeography and patterns of diversity in plants, algae and fungi: introduction. J Biogeogr 28:153
Dwyer GI, Gibbs MJ, Gibbs AJ, Jones RAC (2007) Wheat streak mosaic virus in Australia: relationship to isolates from the Pacific Northwest of the USA and its dispersion via seed transmission. Plant Dis 91:164–170
Eastop V (1966) A taxonomic study of Australian Aphidoidea (Homoptera). Aust J Zool 14:399–592
Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus taxonomy: classification and nomenclature of viruses. 8th report of the international committee on the taxonomy of viruses. Elsevier-Academic Press, New York
Fourment M, Gibbs MJ (2006) PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol 6:1
Gibbs A, Guy P (1978) How long have there been plant viruses in Australia? Aust Plant Pathol 8:41–42
Gibbs AJ, Mackenzie AM, Gibbs MJ (2003) The ‘potyvirid primers’ will probably provide phylogenetically informative DNA fragments from all species of Potyviridae. J Virol Methods 112:41–44
Gibbs AJ, Ohshima K, Phillips MJ, Gibbs MJ (2008) The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. PLoS ONE (in press)
Gibbs MJ, Wayper P, Fourment ML, Wood JT, Ohshima K, Armstrong JS, Gibbs AJ (2006) The variable codons of H3 influenza A virus haemagglutinin genes. Arch Virol 52:11–24
Guindon S, Gascuel O (2003) PhyML—a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hancock JM (1995) The contribution of slippage-like processes to genome evolution. J Mol Evol 41:1038–1047
Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Holmes FO (1951) Indications of a new world origin of tobacco mosaic virus. Phytopathology 41:341–349
Jeanmougin F, Thompson JD, Gibson TJ, Gouy M, Higgins DG (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405
Jones DR, Baker RHA (2007) Introductions of non-native plant pathogens into Great Britain, 1970–2004. Plant Pathol 56:891–910
Jones RAC, Coutts BA, Mackie AE, Dwyer GI (2005) Seed transmission of wheat streak mosaic virus shown unequivocally in wheat. Plant Dis 89:1048–1050
Kiratyi-Angul S, Gibbs A (1992) Group-specific antiserum detects potyviruses in several wild plant species in S.E. Australia. Aust Plant Pathol 21:118–119
Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93
Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262
McLean GD, Price LK (1984) Virus, viroid, mycoplasma and rickettsial diseases of plants in Western Australia. Technical Bulletin. Department of Agriculture, Western Australia, Perth, vol 68, p 22
Murray RGE, Stackebrandt E (1995) Taxonomic Note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187
Robaglia C, Durand-Tardif M, Tronchet M, Boudazin G, Astier-Manifacier S, Casse-Delbart F (1989) Nucleotide sequence of potato virus Y (N Strain) genomic RNA. J Gen Virol 70:935–947
Sampson PJ, Walker J (1982) An annotated list of plant diseases in Tasmania. Department of Agriculture, Tasmania, p 121
Shukla DD, Ward CW, Brunt AA (1994) The potyviridae. CAB International, Wallingford
Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Possello-Mora R, Swings J, Trüper HG, Vauterin L, Ward A, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Ward CW, Weiller G, Shukla DD, Gibbs AJ (1995) Molecular systematics of the potyviridae, the largest plant virus family. In: Gibbs AJ, Calisher CH, Garcia-Arenal H (eds) Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 477–500
Webster CG, Coutts BA, Jones RAC, Jones MGK, Wylie SJ (2007) Virus impact at the ancient ecosystem-recent agroecosystem interface: studies on three legume-infecting potyviruses in the Southwest Australian floristic region. Plant Pathol 56(5):729–742
Weiller GF (1998) Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 15:326–335
White NH (1973) The geographic isolation of Australia in relation to plant viruses. Aust Plant Path Soc Newsl 2:32–33
Zheng L, Wayper PJ, Gibbs AJ, Fourment M, Rodoni BC, Gibbs MJ (2008) Accumulating variation at conserved sites in potyvirus genomes is driven by species discovery and affects degenerate primer design. PLoS ONE 3:e1586
Acknowledgments
We are very grateful for useful comments and information supplied by Carlye Baker, Mark Clements, Bryan Harrison, Roger Jones, Ramon Jordan, Terry Macfarlane, Rick Mumford, Kazusato Ohshima, Denis Persley, Brendan Rodoni, Len Tessorerio, Anupam Varma, Colin Ward, Les Watson, Josef Vetten. AJG is especially grateful to Pat Gibbs, and Drs. Ian Mills and Michael Pidcock for their special support.
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“The hypothesis is proposed that all plant viruses in Australia were introduced since European settlement of the Australia continent toward the end of the eighteenth century”, N. H. White 1973.
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Gibbs, A.J., Mackenzie, A.M., Wei, KJ. et al. The potyviruses of Australia. Arch Virol 153, 1411–1420 (2008). https://doi.org/10.1007/s00705-008-0134-6
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DOI: https://doi.org/10.1007/s00705-008-0134-6