Abstract
For almost all groups of pathogens, unusual and rare host species have been reported. Often, such associations are based on single or few collections only, which are frequently hard to access. Many of them later prove to be due to misidentification of the host, the pathogen, or both. Therefore, such reports are often disregarded, or treated anecdotally in taxonomic and phylogenetic studies, regardless of their potential importance to unravelling the evolution of the entire group. Concerning oomycete biotrophs there are several reports of unusual and rare hosts for hardly known pathogens. In the order Fabales, for example, a single species of Albugo, A. mauginii, was described as parasitic to Onobrychis crista-galli about 80 years ago, but not recorded again. All other confirmed members of Albugo s.str. are parasitic to representatives of the families Brassicaceae, Capparaceae, Cleomaceae, and Resedaceae in the order Brassicales. In the present study, molecular phylogenetic analysis of cox2 mtDNA sequences and morphological investigations on an original specimen confirmed the occurrence of a member of Albugo on Fabaceae hosts, with the characteristic thin wall of the secondary sporangia, which is almost uniform in thickness. In phylogenetic analyses the species results as embedded within Albugo s.str. Therefore, it is concluded that the natural host range of Albugo s.str. extends from Brassicales to Fabales via host jumping. Our results underscore that unrevised reports of pathogens from unusual hosts should be reconsidered carefully to obtain a more complete picture of pathogen diversity and evolution.
Similar content being viewed by others
References
Ahangarian, S., Kazempour, O. S., & Maassoumi, A. A. (2007). Molecular phylogeny of the tribe Hedysareae with special reference to Onobrychis (Fabaceae) as inferred from nrDNA ITS sequences. Iranian Journal of Botany, 13, 64–74.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
APG [Angiosperm Phylogeny Group]. (2009). An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, 161, 105–121.
Begerow, D., Stoll, M., & Bauer, R. (2006). A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia, 98, 906–916.
Biga, M. L. B. (1955). Review of the species of the genus Albugo based on the morphology of the conidia. Sydowia, 9, 339–358.
Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S., & Beynon, J. L. (2006). Trafficking arms: oomycete effectors enter host plant cells. Trends in Microbiology, 14, 8–11.
Choi, D., & Priest, M. J. (1995). A key to the genus Albugo. Mycotaxon, 53, 261–272.
Choi, Y. J., Hong, S. B., & Shin, H. D. (2005). A re-consideration of Pseudoperonospora cubensis and Ps. humuli based on molecular and morphological data. Mycological Research, 109, 841–848.
Choi, Y. J., Hong, S. B., & Shin, H. D. (2006). Genetic diversity within the Albugo candida complex (Peronosporales, Oomycota) inferred from phylogenetic analysis of ITS rDNA and COX2 mtDNA sequences. Molecular Phylogenetics and Evolution, 40, 400–409.
Choi, Y. J., Shin, H. D., Hong, S. B., & Thines, M. (2007). Morphological and molecular discrimination among Albugo candida materials infecting Capsella bursa-pastoris world-wide. Fungal Diversity, 27, 11–34.
Choi, Y. J., Shin, H. D., Ploch, S., & Thines, M. (2008). Evidence for uncharted biodiversity in the Albugo candida complex, with the description of a new species. Mycological Research, 112, 1327–1334.
Choi, Y. J., Shin, H. D., Ploch, S., & Thines, M. (2011). Three new phylogenetic lineages are the closest relatives of the widespread species Albugo candida. Fungal Biology. doi:10.1016/j.funbio.2011.02.006.
Choi, Y. J., Shin, H. D., & Thines, M. (2009). The host range of Albugo candida extends from Brassicaceae through Cleomaceae to Capparaceae. Mycological Progress, 8, 329–335.
Choi, Y. J., & Thines, M. (2010). Morphological and molecular confirmation of Albugo resedae (Albuginales; Oomycota) as a distinct species from A. candida. Mycological Progress. doi:10.1007/s11557-010-0683-4.
Constantinescu, O., & Thines, M. (2006). Dimorphism of sporangia in the Albuginaceae (Chromista, Peronosporomycetes). Sydowia, 58, 178–190.
El-Buni, A. M., & Rattan, S. S. (1981). Check-list of Libyan fungi. Tripolis: Al-Faateh University, Faculty of Science, Department of Botany.
Farris, J. S. (1989). The retention index and the rescaled consistency index. Cladistics, 5, 417–419.
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
Hudspeth, D. S. S., Nadler, S. A., & Hudspeth, M. E. S. (2000). A COX2 molecular phylogeny of the Peronosporomycetes. Mycologia, 92, 674–684.
Hudspeth, D. S. S., Stenger, D., & Hudspeth, M. E. S. (2003). A COX2 phylogenetic hypothesis of the downy mildews and white rusts. Fungal Diversity, 13, 47–57.
Inuma, T., Khodaparast, S. A., & Takamatsu, S. (2007). Multilocus phylogenetic analyses within Blumeria graminis, a powdery mildew fungus of cereals. Molecular Phylogenetics and Evolution, 44, 741–751.
Kemler, M., Göker, M., Oberwinkler, F., & Begerow, D. (2006). Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evolutionary Biology, 6, 35.
Kluge, A. G., & Farris, J. S. (1969). Quantitative phyletics and the evolution of anurans. Systematic Zoology, 30, 1–32.
Kranz, J. (1965). A list of plant pathogenic and other fungi of Cyrenaica (Libya). Phytopathology Papers, 6, 1–24.
Lee, S. B., & Taylor, J. W. (1990). Isolation of DNA from fungal mycelia and single spores. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 282–287). San Diego: Academic.
Matsuda, S., & Takamatsu, S. (2003). Evolution of host-parasite relationship of Golovinomyces (Ascomycetes: Erysiphales) inferred from nuclear rDNA sequences. Molecular Phylogenetics and Evolution, 27, 314–327.
Morgan, W., & Kamoun, S. (2007). RXLR effectors of plant pathogenic Oomycetes. Current Opinion in Microbiology, 10, 332–338.
Page, R. D. M. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357–358.
Parisi, S. (1926) [“1925”]. Di un Cystopus, dell Onobrychis Cristata-galli Lam. di Cirenaica. Bullettino dell’Orto Botanico della Regia Universitá di Napoli, 8, 217–221.
Ploch, S., Choi, Y. J., Rost, C., Shin, H. D., Schilling, E., & Thines, M. (2010). Evolution of diversity in Albugo is driven by high host specificity and multiple speciation events on closely related Brassicaceae. Molecular Phylogenetics and Evolution, 57, 812–820.
Riethmüller, A., Voglmayr, H., Göker, M., Weiß, M., & Oberwinkler, F. (2002). Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia, 94, 834–849.
Runge, F., Choi, Y.-J., & Thines, M. (2011). Host matrix has major impact on the morphology of Pseudoperonospora cubensis. European Journal of Plant Pathology, 129, 147–156.
Savile, D. B. O. (1979). Fungi as aids in higher plant classification. Botanical Review, 45, 377–503.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Sunderland: Sinauer.
Thines, M., Cano, L., & Kamoun, S. (2009a). Effector evolution in the Hyaloperonospora arabidopsidis species complex. Fungal Genetics Reports, 56(Supplement), 243.
Thines, M., Choi, Y. J., Kemen, E., Ploch, S., Holub, E. B., Shin, H. D., et al. (2009b). A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts (Albuginaceae). Persoonia, 22, 123–128.
Thines, M., Göker, M., Telle, S., Ryley, M., Mathur, K., Narayana, Y. D., et al. (2008). Phylogenetic relationships of graminicolous downy mildews based on cox2 sequence data. Mycological Research, 112, 345–351.
Thines, M., & Kamoun, S. (2010). Oomycete-plant coevolution: recent advances and future prospects. Current Opinion in Plant Biology, 13, 427–433.
Thines, M., & Spring, O. (2005). A revision of Albugo (Chromista, Peronosporomycetes). Mycotaxon, 92, 443–458.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882.
van der Merwe, M. M., Walker, J., Ericson, L., & Burdon, J. J. (2008). Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps. Mycological Progress, 112, 1387–1408.
Voglmayr, H., Piątek, M., & Mossebo, D. C. (2009). Pseudoperonospora cubensis causing downy mildew disease on Impatiens irvingii in Cameroon: a new host for the pathogen. Plant Pathology, 58, 394.
Voglmayr, H., & Riethmüller, A. (2006). Phylogenetic relationships of Albugo species (white blister rusts) based on LSU rDNA sequence and oospore data. Mycological Research, 110, 75–85.
Walker, J., & Priest, M. J. (2007). A new species of Albugo on Pterostylis (Orchidaceae) from Australia: confirmation of the genus Albugo on a monocotyledonous host. Australasian Plant Pathology, 36, 181–185.
White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). San Diego: Academic.
Acknowledgements
The authors are grateful to the curator at BPI for providing the Albugo specimen investigated. This work was financially supported by research grants from the Korea Research Foundation (KRF-2003-015-C00611) and the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of the State Ministry of Higher Education, Research, and the Arts (Hessen, Germany).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Choi, YJ., Thines, M. & Shin, HD. A new perspective on the evolution of white blister rusts: Albugo s.str. (Albuginales; Oomycota) is not restricted to Brassicales but also present on Fabales. Org Divers Evol 11, 193–199 (2011). https://doi.org/10.1007/s13127-011-0043-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-011-0043-5