Skip to main content
Log in

Progress and challenges in systematics of downy mildews and white blister rusts: new insights from genes and morphology

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Recent advances in the classification of downy mildews and white blister rusts are presented from ordinal to species level. Using molecular data (mainly LSU of nuclear ribosomal DNA and ITS rDNA data, but also cox2, beta-tubulin and NADH genes), ordinal, family and generic circumscriptions have been reconsidered and changed during the last years; species circumscription and concepts are also changing. These rearrangements also lead to a reevaluation of the traditional morphological characters used for classification. The recent changes have various implications for applied sciences (phytopathology, molecular biology) mainly at the species level; besides name changes for some taxa, revised species circumscriptions and improved species identification using genetic markers have important consequences on host ranges, source inocula and risk assessment of phytopathologically important taxa. However, there are also some substantial unresolved problems which need to be addressed in the future with new data and methods. These include the systematic position of some rarely sampled taxa, the phylogenetic relationships of the main downy mildew lineages to each other, more detailed molecular studies on speciation processes to develop appropriate sound species concepts and circumscriptions, and the development of a molecular bar coding system for downy mildews enabling reliable species identification. Applying molecular methods has the potential to greatly enhance our knowledge on the overall biodiversity of downy mildews.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Belbahri, L., Calmin, G., Pawlowski, J., & Lefort, F. (2005). Phylogenetic analysis and real time PCR detection of a presumably undescribed Peronospora species on sweet basil and sage. Mycological Research, 109, 1276–1287.

    Article  PubMed  CAS  Google Scholar 

  • Blair, J. E., Coffey, M. D., Park, S.-Y., Geiser, D. M., & Kang, S. (2008). A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology, 45, 266–277.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y.-J., Hong, S.-B., & Shin, H.-D. (2003). Diversity of the Hyaloperonospora parasitica complex from core brassicaceous hosts based on ITS rDNA sequences. Mycological Research, 107, 1314–1322.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y.-J., Hong, S.-B., & Shin, H.-D. (2005). A reconsideration of Pseudoperonospora cubensis and P. humuli based on molecular and morphological data. Mycological Research, 109, 841–848.

    Article  PubMed  CAS  Google Scholar 

  • 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 mt DNA sequences. Molecular Phylogenetics and Evolution, 40, 400–409.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y.-J., Constantinescu, O., & Shin, H.-D. (2007a). A new downy-mildew of the Rosaceae: Peronospora oblongispora sp. nov. (Chromista, Peronosporales). Nova Hedwigia, 85, 93–101.

    Article  Google Scholar 

  • Choi, Y.-J., Hong, S.-B., & Shin, H.-D. (2007b). Extreme size and sequence variation in the ITS rDNA of Bremia lactucae. Mycopathologia, 163, 91–95.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y.-J., Hong, S.-B., & Shin, H.-D. (2007c). Re-consideration of Peronospora farinosa infecting Spinacia oleracea as distinct species, Peronospora effusa. Mycological Research, 110, 381–391.

    Article  CAS  Google Scholar 

  • Choi, Y.-J., Shin, H.-D., Hong, S.-B., & Thines, M. (2007d). Morphological and molecular discrimination among Albugo candida materials infecting Capsella bursa-pastoris world-wide. Fungal Diversity, 27, 11–34.

    Google Scholar 

  • Choi, Y.-J., Denchev, C. M., & Shin, H.-D. (2008a). Morphological and molecular analyses support the existence of host-specific Peronospora species infecting Chenopodium. Mycopathologia, 168, 155–164.

    Article  CAS  Google Scholar 

  • Choi, Y.-J., Shin, H.-D., Ploch, S., & Thines, M. (2008b). Evidence for uncharted biodiversity in the Albugo candida complex, with the description of a new species. Mycological Research (in press).

  • Constantinescu, O. (1989). Peronospora complex on Compositae. Sydowia, 41, 79–107.

    Google Scholar 

  • Constantinescu, O. (1991a). Bremiella sphaerosperma sp. nov. and Plasmopara borreriae comb. nov. Mycologia, 83, 473–479.

    Article  Google Scholar 

  • Constantinescu, O. (1991b). An annotated list of Peronospora names. Thunbergia, 15, 1–110.

    Google Scholar 

  • Constantinescu, O. (1998). A revision of Basidiophora (Chromista, Peronosporales). Nova Hedwigia, 66, 251–265.

    Google Scholar 

  • Constantinescu, O. (2004). The nomenclature of Plasmopara (Chromista, Peronosporales) parasitic on Geraniaceae. Taxon, 53, 523–525.

    Article  Google Scholar 

  • Constantinescu, O., & Faheti, J. (2002). Peronospora-like fungi (Chromista, Peronosporales) parasitic on Brassicaceae and related hosts. Nova Hedwigia, 74, 291–338.

    Article  Google Scholar 

  • Constantinescu, O., Voglmayr, H., Fatehi, J., & Thines, M. (2005). Plasmoverna gen. nov., and the taxonomy and nomenclature of Plasmopara (Chromista, Peronosporales). Taxon, 54, 813–821.

    Google Scholar 

  • Constantinescu, O., & Thines, M. (2006). Dimorphism of sporangia in Albuginaceae (Chromista, Peronosporomycetes). Sydowia, 58, 178–190.

    Google Scholar 

  • Cooke, D. E. L., Drenth, A., Duncan, J. M., Wagels, G., & Brasier, C. M. (2000). A molecular phylogeny of Phytophthora and related Oomycetes. Fungal Genetics and Biology, 30, 17–32.

    Article  PubMed  CAS  Google Scholar 

  • Cooke, D. E. L., Williams, N. A., Williamson, B., & Duncan, J. M. (2002). An ITS-based phylogenetic analysis of the relationships between Peronospora and Phytophthora. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.), Advances in downy mildew research, Vol 1 (pp. 161–165). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Cunnington, J. H. (2006). DNA sequence variation supports multiple host-specialised taxa in the Peronospora viciae complex (Chromista: Peronosporales). Nova Hedwigia, 82, 23–29.

    Article  Google Scholar 

  • de Bary, A. (1863). Recherches sur le développement de quelques champignons parasites. Annales Des Sciences Naturelles. Botanique, Sér., 4(20), 5–148.

    Google Scholar 

  • Dick, M. W. (1995). Sexual reproduction in the Peronosporomycetes (chromistan fungi). Canadian Journal of Botany, 73(Suppl. 1), S712–S724.

    Article  Google Scholar 

  • Dick, M. W. (2001). The Peronosporomycetes. In D. J. McLaughlin, E. G. McLaughlin, & P. A. Lemke (Eds.), The Mycota, Vol VII A (pp. 39–72). Berlin: Springer.

    Google Scholar 

  • Dick, M. W. (2002). Towards an understanding of the evolution of the downy mildews. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.), Advances in downy mildew research, Vol 1 (pp. 1–57). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Dick, M. W., Wong, P. T. W., & Clark, G. (1984). The identity of the oomycete causing ‘Kikuyu Yellows’, with a reclassification of the downy mildews.. Botanical Journal of the Linnean Society, 89, 171–197.

    Article  Google Scholar 

  • Dick, M. W., Croft, B. J., Margarey, R. C., DeCock, A. W. A. M., & Clark, G. (1989). A new genus of the Verrucalvaceae (Oomycetes). Botanical Journal of the Linnean Society, 99, 97–113.

    Article  Google Scholar 

  • Dick, M. W., Vick, M. C., Gibbings, J. G., Hedderson, T. A., & Lopez Lastra, C. C. (1999). 18S rDNA for species of Leptolegnia and other Peronosporomycetes: Justification of the subclass taxa Saprolegniomycetidae and Peronosporomycetidae and division of the Saprolegniaceae sensu lato into the Leptolegniaceae and Saprolegniaceae. Mycological Research, 103, 1119–1125.

    Article  CAS  Google Scholar 

  • Fraymouth, J. (1956). Haustoria of the Peronosporales. Transactions of the British Mycological Society, 39, 79–107.

    Article  Google Scholar 

  • García-Blázquez, G., Göker, M., Voglmayr, H., Martín, M. P., Tellería, M. T., & Oberwinkler, F. (2008). Phylogeny of Peronospora, parasitic on Fabaceae, based on ITS sequences. Mycological Research, 112, 502–512.

    Article  PubMed  CAS  Google Scholar 

  • Gäumann, E. (1918). Über die Formen der Peronospora parasitica (Pers.) Fries. Beihefte zum Botanischen Centralblatt, 35, 395–533.

    Google Scholar 

  • Gäumann, E. (1923). Beiträge zu einer Monographie der Gattung Peronospora Corda. Beiträge zur Kryptogamenflora der Schweiz, 5, 1–360.

    Google Scholar 

  • Göker, M., Riethmüller, A., Voglmayr, H., Weiß, M., & Oberwinkler, F. (2004). Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycological Progress, 3, 83–94.

    Article  Google Scholar 

  • Göker, M., & Stamatakis, A. (2006). Maximum likelihood phylogenetic inference: An empirical comparison on a multi-locus dataset. (Poster presented at the German Conference on Bioinformatics 2006, Tübingen, Germany.) Retrieved June 12, 2007 from http://diwww.epfl.ch/∼stamatak/index-Dateien/publications/GCB2006_Poster.pdf.

  • Göker, M., Voglmayr, H., Riethmüller, A., & Oberwinkler, F. (2007). How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genetics and Biology, 44, 105–122.

    Article  PubMed  CAS  Google Scholar 

  • Göker, M., Voglmayr, H., Riethmüller, A., Weiß, M., & Oberwinkler, F. (2003). Taxonomic aspects of Peronosporaceae inferred from Bayesian molecular phylogenetics. Canadian Journal of Botany, 81, 672–683.

    Article  Google Scholar 

  • Hall, G. S. (1996). Modern approaches to species concepts in downy mildews. Plant Pathology, 45, 1009–1026.

    Article  Google Scholar 

  • Hudspeth, D. S. S., Nadler, S. A., & Hudspeth, M. E. S. (2000). A cox2 molecular phylogeny of the Peronosporomycetes. Mycologia, 92, 674–684.

    Article  CAS  Google Scholar 

  • Hudspeth, D. S. S., Stenger, D. C., & Hudspeth, M. E. S. (2003). A cox2 phylogenetic hypothesis for the downy mildews and white rusts. Fungal Diversity, 13, 47–57.

    Google Scholar 

  • Hukkanen, A., Pietikäinen, L., Kärenlampi, S., & Kokko, H. (2006). Quantification of downy mildew (Peronospora sparsa) in Rubus species using real-time PCR. European Journal of Plant Pathology, 116, 225–235.

    Article  CAS  Google Scholar 

  • Kirk, P. M., Cannon, P. F., David, J. C., & Stalpers, J. A. (2001). Ainsworth & Bisby’s dictionary of the fungi (9th ed.). Wallingford: CAB International.

    Google Scholar 

  • Komjáti, H., Walcz, I., Virányi, F., Zipper, R., Thines, M., & Spring, O. (2007). Characteristics of a Plasmopara angustiterminalis isolate from Xanthium strumarium. European Journal of Plant Pathology, 119, 421–428.

    Article  Google Scholar 

  • Lamour, K. H., Win, J., & Kamoun, S. (2007). Oomycete genomics: New insights and future directions. FEMS Microbiology Letters, 274, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Landa, B. B., Montes-Borrego, M., Muñoz-Ledesma, F. J., & Jiménez-Díaz, R. M. (2007). Phylogenetic analysis of downy mildew pathogens of opium poppy and PCR-based in planta and seed detection of Peronospora arborescens. Phytopathology, 97, 1380–1390.

    Article  CAS  PubMed  Google Scholar 

  • Larran, S., Ronco, L., Mónaco, C., & Andreau, R. H. (2006). First report of Peronospora parasitica on rocket (Eruca sativa) in Argentina. Australasian Plant Pathology, 35, 377–378.

    Article  Google Scholar 

  • Lecointre, G., & Le Guyader, H. (2006). The tree of life: A phylogenetic classification. Cambridge, MA: The Belknap Press of Harvard University Press.

    Google Scholar 

  • Petersen, A. B., & Rosendahl, S. (2000). Phylogeny of the Peronosporomycetes (Oomycota) based on partial sequences of the large ribosomal subunit (LSU rDNA). Mycological Research, 104, 1295–1303.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Riethmüller, A., Weiβ, M., & Oberwinkler, F. (1999). Phylogenetic studies of Saprolegniomycetidae and related groups based on nuclear large subunit DNA sequences. Canadian Journal of Botany, 77, 1790–1800.

    Article  Google Scholar 

  • Scott, J. B., Hay, F. S., & Wilson, C. R. (2004). Phylogenetic analysis of the downy mildew pathogen of oilseed poppy in Tasmania, and its detection by PCR. Mycological Research, 108, 198–205.

    Article  PubMed  CAS  Google Scholar 

  • Skalický, V. (1966). Taxonomie der Gattungen der Familie Peronosporaceae. Preslia (Praha), 38, 117–129.

    Google Scholar 

  • Spring, O. (2004). Potential and limits for the use of new characters in the systematics of biotrophic oomycetes. In P. Spencer-Phillips, & M. Jeger (Eds.), Advances in downy mildew research, Vol 2 (pp. 211–231). Dordrecht: Kluwer.

    Google Scholar 

  • Spring, O., Bachofer, M., Thines, M., Riethmüller, A., Göker, M., & Oberwinkler, F. (2006). Intraspecific relationship of Plasmopara halstedii isolates differing in pathogenicity and geographic origin based on ITS sequence data. European Journal of Plant Pathology, 114, 309–315.

    Article  Google Scholar 

  • Spring, O., Haas, K., Lamla, I., Thurnhofer, S., & Vetter, W. (2005). The composition and taxonomic significance of fatty acid patterns in three white rust species: Albugo amaranthi, A. candida and A. tragopogonis (Peronosporales, Albuginaceae). Mycological Progress, 4, 179–184.

    Article  Google Scholar 

  • Spring, O., & Thines, M. (2004). On the necessity of new characters for classification and systematics of biotrophic Peronosporomycetes. Planta, 219, 910–914.

    Article  PubMed  CAS  Google Scholar 

  • Spring, O., Voglmayr, H., Riethmüller, A., & Oberwinkler, F. (2003). Characterization of a Plasmopara isolate from Helianthus x laetiflorus based on cross infection, morphological, fatty acids, and molecular phylogenetic data. Mycological Progress, 2, 163–170.

    Article  Google Scholar 

  • Thines, M. (2006). Evaluation of characters available from herbarium vouchers for the phylogeny of the downy mildew genera (Chromista, Peronosporales), with focus on scanning electron microscopy. Mycotaxon, 97, 195–218.

    Google Scholar 

  • Thines, M. (2007a). Characterisation and phylogeny of repeated elements giving rise to exceptional length of ITS2 in several downy mildew genera (Peronosporaceae). Fungal Genetics and Biology, 44, 199–207.

    Article  PubMed  CAS  Google Scholar 

  • Thines, M. (2007b). Use of scanning electron microscopy in downy mildew systematics. In A. Lebeda, & P. Spencer-Phillips (Eds.), Advances in downy mildew research, Vol 3 (pp. 17–23). Olomouc: Palacký University and Kostelec na Hané, JOLA, v.o.s.

  • Thines, M. (2007c). Repeats of the ITS2 of Plasmopara species and their relevance for phylogenetic studies. In A. Lebeda, & P. Spencer-Phillips (Eds.), Advances in downy mildew research, Vol 3 (pp. 31–35). Olomouc: Palacký University and Kostelec na Hané, JOLA, v.o.s.

  • Thines, M., Göker, M., & Oberwinkler, F. (2006). A revision of Bremia graminicola. Mycological Research, 110, 646–656.

    Article  PubMed  Google Scholar 

  • Thines, M., Göker, M., Oberwinkler, F., & Spring, O. (2007). A revision of Plasmopara penniseti, with implications for the host range of the downy mildews with pyriform haustoria. Mycological Research, 111, 1377–1385.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Thines, M., Komjáti, H., & Spring, O. (2005). Exceptional length of ITS in Plasmopara halstedii is due to multiple repetitions in the ITS-2 region. European Journal of Plant Pathology, 112, 395–398.

    Article  CAS  Google Scholar 

  • Thines, M., & Spring, O. (2005). A revision of Albugo (Chromista, Peronosporomycetes). Mycotaxon, 92, 443–458.

    Google Scholar 

  • Voglmayr, H. (2003). Phylogenetic study of Peronospora and related genera based on nuclear ribosomal ITS sequences. Mycological Research, 107, 1132–1142.

    Article  PubMed  CAS  Google Scholar 

  • Voglmayr, H., & Constantinescu, O. (2008). Revision and reclassification of three Plasmopara species based on morphological and molecular phylogenetic data. Mycological Research, 112, 487–501.

    Article  PubMed  CAS  Google Scholar 

  • Voglmayr, H., Fatehi, J., & Constantinescu, O. (2006). Revision of Plasmopara (Chromista, Peronosporales) parasitic on Geraniaceae. Mycological Research, 110, 633–645.

    Article  PubMed  Google Scholar 

  • Voglmayr, H., & Greilhuber, J. (1998). Genome size determination in Peronosporales (Oomycota) by Feulgen image analysis. Fungal Genetics and Biology, 25, 181–195.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Voglmayr, H., Riethmüller, A., Göker, M., Weiß, M., & Oberwinkler, F. (2004). Phylogenetic relationships of Plasmopara, Bremia and other genera of downy mildews with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence data. Mycological Research, 108, 1011–1024.

    Article  PubMed  CAS  Google Scholar 

  • Voglmayr, H., & Thines, M. (2007). Phylogenetic relationships and nomenclature of Bremiella sphaerosperma (Chromista, Peronosporales). Mycotaxon, 100, 11–20.

    Google Scholar 

  • Waterhouse, G. M. (1973). 10. Peronosporales. In G. C. Ainsworth, F. K. Sparrow, & A. S. Sussman (Eds.), The fungi—An advanced treatise (pp. 165–183). New York: Academic.

    Google Scholar 

  • Yerkes, W. D., & Shaw, C. G. (1959). Taxonomy of Peronospora species on Cruciferae and Chenopodiaceae. Phytopathology, 49, 499–507.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hermann Voglmayr.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voglmayr, H. Progress and challenges in systematics of downy mildews and white blister rusts: new insights from genes and morphology. Eur J Plant Pathol 122, 3–18 (2008). https://doi.org/10.1007/s10658-008-9341-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-008-9341-y

Keywords

Navigation