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Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range

Abstract

A rust fungus collected from common ragweed (Ambrosia artemisiifolia) in Texas, USA, was identified as belonging to the Puccinia xanthii morphospecies based on its nrDNA ITS sequence. Pathogenicity studies carried out with this rust accession under quarantine conditions in the UK showed that the fungus was highly virulent on A. artemisiifolia plants from Australia. Recently, P. xanthii has been proposed as a potential classical biological control agent (CBCA) for common ragweed in its invasive range, focusing on Europe, despite previous doubts about its biocontrol potential. The results of the pathogenicity tests reported here support the suitability of this pathogen as a CBCA for common ragweed.

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References

  • Alaei, H., De Backer, M., Nuytinck, J., Maes, M., Höfte, M., & Heungens, K. (2009). Phylogenetic relationships of puccinia horiana and other rust pathogens of chrysanthemum × morifolium based on rDNA ITS sequence analysis. Mycological Research, 113, 668–683.

    CAS  Article  PubMed  Google Scholar 

  • Alcorn, J. L. (1976). Host range of puccinia xanthii. Transactions of the British Mycological Society, 66, 365–367.

    Article  Google Scholar 

  • Batra, S. W. T. (1981). Puccinia xanthii forma specialis ambrosia-trifidae. Mycopathologia, 73, 61–64.

    Article  Google Scholar 

  • Chauvel, B., Dessaint, F., Cardinal-Legrand, C., & Bretagnolle, F. (2006). The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. Journal of Biogeography, 33, 665–673.

    Article  Google Scholar 

  • Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research, 16, 10881–10890.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Evans, H. C. (1997). Parthenium hysterophorus: a review of its weed status and the possibilities for biological control. Biocontrol News and Information, 18, 89–98.

    Google Scholar 

  • Evans, H. C. (1998). Major Indian weeds of Neotropical origin and the possibilities for collaborative biocontrol projects. In: P. Ferrar, R. Muniappan, K. P. Jayanth (Eds.), Proceedings of the Fourth International Workshop on Biological Control and Management of Chromolaena odorata (pp. 55–62). Mangilao, Guam: Publication No. 216, Agricultural Experiment Station, University of Guam.

  • Evans, H. C. (2013). Biological control of weeds with fungi. In F. Kempken (Ed.), The mycota XI. Agricultural applications (pp. 145–172). Berlin-Heidelberg: Springer.

    Chapter  Google Scholar 

  • Evans, H. C., & Ellison, C. A. (1990). Classical biological control of weeds with micro-organisms: past, present, prospects. Aspects of Applied Biology, 24, 39–49.

    Google Scholar 

  • Farr, D. F., & Rossman, A. Y. (2015). Fungal databases, systematic mycology and microbiology laboratory. USDA: ARS Retrieved May 2, 2015, from http://nt.ars-grin.gov/fungaldatabases/.

    Google Scholar 

  • Feau, N., Vialle, A., Allaire, M., Maier, W., & Hamelin, R. C. (2011). DNA barcoding in the rust genus chrysomyxa and its implications for the phylogeny of the genus. Mycologia, 103, 1250–1266.

    Article  PubMed  Google Scholar 

  • Filatov, D. A. (2002). ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Molecular Ecology Notes, 2, 621–624.

    CAS  Article  Google Scholar 

  • Gaudeul, M., Giraud, T., Kiss, L., Shykoff, J. A. (2011). Nuclear and chloroplast microsatellites show multiple introductions in the worldwide invasion history of common ragweed, Ambrosia artemisiifolia (Asteraceae). PLOS ONE, 6:(3), e17658. doi:10.1371/journal.pone.0017658.

  • Gerber, E., Schaffner, U., Gassmann, A., Hinz, H. L., Seier, M., & Mueller-Schaerer, H. (2011). Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past. Weed Research, 51, 559–573.

    Article  Google Scholar 

  • Ginns, J. H. (1986). Compendium of plant disease and decay fungi in Canada 1960-1980. Research branch, publication 1813. Ottawa: Agriculture Canada.

  • Gladieux, P., Giraud, T., Kiss, L., Genton, B. J., Jonot, O., & Shykoff, J. A. (2011). Distinct invasion sources of common ragweed (Ambrosia artemisiifolia) in eastern and western Europe. Biological Invasions, 13, 933–944.

    Article  Google Scholar 

  • Kiss, L. (2007a). Why is biocontrol of common ragweed (Ambrosia artemisiifolia), the most allergenic weed in eastern Europe, still only a hope? In C. Vincent, M. Goettel, & G. Lazarovits (Eds.), Biological control - a global perspective (pp. 80–91). Wallingford, UK: CABI Publishing International.

    Chapter  Google Scholar 

  • Kiss, L. (2007b). Is puccinia xanthii a suitable biological control agent of Ambrosia artemisiifolia? Biocontrol Science and Technology, 17, 535–539.

    Article  Google Scholar 

  • Kovács, G. M., Balázs, T., & Pénzes, Z. (2007). Molecular study of arbuscular mycorrhizal fungi colonizing the sporophyte of the eusporangiate rattlesnake fern (botrychium virginianum, ophioglossaceae). Mycorrhiza, 17, 597–605.

    Article  PubMed  Google Scholar 

  • Lu, G.-Z., Yang, H., Sun, X.-D., Yang, R.-X., & Zhao, Z.-H. (2004). Puccinia xanthii f. sp. ambrosiae-trifidae, a newly recorded rust taxon on ambrosia in China. Mycosystema, 23, 310–311.

    Google Scholar 

  • Morin, L., Auld, B. A., & Brown, J. F. (1993). Host range of puccinia xanthii and postpenetration development on xanthium occidentale. Canadian Journal of Botany, 71, 959–965.

    Google Scholar 

  • Morin, L., van der Merwe, M., Hartley, D., & Muller, P. (2009). Putative natural hybrid between puccinia lagenophorae and an unknown rust fungus on senecio madagascariensis in KwaZulu-Natal, South Africa. Mycological Research, 113, 725–736.

    CAS  Article  PubMed  Google Scholar 

  • Parmelee, J. A. (1977). Puccinia xanthii. Fungi canadenses no. 99. National mycological herbarium, biosystematics research institute. Ottawa: Agriculture Canada.

    Google Scholar 

  • Pfunder, M., Schürch, S., & Roy, B. A. (2001). Sequence variation and geographic distribution of pseudoflower-forming rust fungi (uromyces pisi s. lat.) on euphorbia cyparissias. Mycological Research, 105, 57–66.

    CAS  Article  Google Scholar 

  • Seier, M. K. (2005). Exotic beneficials in classical biological control of invasive alien weeds: friends or foes? In D. V. Alford & G. F. Backhaus (Eds.) BCPC Symposium Proceedings No. 81; Plant Protection and Plant Health in Europe: Introduction and Spread of Invasive Species (pp. 191–196). Hampshire, UK: The British Crop Protection Council.

  • Seier, M. K., Harvey, J. L., Romero, A., & Kinnersley, R. P. (1997). Safety testing of the rust puccinia melampodii as a potential biocontrol agent of Parthenium hysterophorus L. In M. Mahadevappa, & V. C. Patil (Eds.), Proceedings of the first international conference on parthenium management (pp. 63–69). Dharwad, Karnataka, India: University of Agricultural Sciences.

    Google Scholar 

  • Seier, M. K., Morin, L., Van der Merwe, M., Evans, H. C., & Romero, A. (2009). Are the microcyclic rust species puccinia melampodii and puccinia xanthii conspecific? Mycological Research, 113, 1271–1282.

    CAS  Article  PubMed  Google Scholar 

  • Staden, R., Beal, K. F., & Bonfield, J. K. (2000). The staden package, 1998. Methods in Molecular Biology, 132, 115–130.

    CAS  PubMed  Google Scholar 

  • Tanner, R. A., Ellison, C. A., Seier, M. K., Kovács, G. M., Kassai-Jáger, E., Berecky, Z., Varia, S., Djeddour, D., Chand Singh, M., Csiszár, A., Csontos, P., Kiss, L., & Evans, H. C. (2015). Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (impatiens glandulifera). European Journal of Plant Pathology, 141, 247–266.

    Article  Google Scholar 

  • Tomley, A., Evans, H., Ellison, C., Seier, M., Thomas, S., & Djeddour, D. (2004). Release strategies and associated factors affecting the establishment of four rust fungi introduced into Australia between 1991 and 2001 for the biocontrol of Parthenium hysterophorus, cryptostegia grandiflora and lantana camara. In J. M. Cullen, D. T. Briese, D. J. Kriticos, W. M. Lonsdale, L. Morin, & J. K. Scott (Eds.), Proceedings of the XI international symposium on biological control of weeds (p. 612). Canberra, Australia: CSIRO.

    Google Scholar 

  • Zhang, P., Lu, G. Z., Sun, X. D., Zhang, W., Qu, B., & Tian, X. L. (2011). The infection process of puccinia xanthii f. sp. ambrosiae-trifidae on ambrosia trifida. Botany, 89, 771–777.

    Article  Google Scholar 

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Acknowledgments

We thank W. A. (Bill) Palmer (Queensland Department of Lands) for sending herbarium material of the North American rust. We acknowledge the support of the EU COST Action FA1203 ‘Sustainable management of Ambrosia artemisiifolia in Europe (SMARTER)’.

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Correspondence to Levente Kiss.

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Kassai-Jáger, E., Seier, M.K., Evans, H.C. et al. Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range. Eur J Plant Pathol 145, 81–87 (2016). https://doi.org/10.1007/s10658-015-0815-4

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  • DOI: https://doi.org/10.1007/s10658-015-0815-4

Keywords

  • Allergenic weed
  • Classical biological control
  • Fungal species concept
  • Pucciniaceae
  • Pucciniomycetes
  • Invasive alien species