Confirmation of Peronospora agrimoniae as a distinct species

Abstract

Leaves with typical symptoms of downy mildew were found on common agrimony in the Czech Republic in 2014 and 2015 and at several locations in Germany from 2010 to 2014. The causal agent of downy mildew of agrimony was often reported as Peronospora agrimoniae, but sometimes also as P. sparsa. Morphological characteristics of the pathogens found in both countries are in the range of previous works for P. agrimoniae, but also other downy mildews parasitic on Rosaceae, rendering their discrimination based on published observations difficult. For molecular identification sequencing of several loci (nrITS rDNA, cox1 and cox2) was performed. Phylogenetic analyses based on nrITS rDNA clearly separated P. agrimoniae from other Peronospora species infecting Rosaceae. Thus, considering P. agrimoniae as separate species seems justified. Two German specimens were identical to two Czech samples in both nrITS rDNA and cox1 mtDNA sequences, but differed in a single nucleotide substitution in cox2 region. To our knowledge, this is the first verified record of P. agrimoniae on common agrimony in the Czech Republic.

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References

  1. Bonants, P., de Weerdt, M. H., van Gent Pelzer, M., Lacourt, I., Cooke, D., & Duncan, J. (1997). Detection and identification of Phytophtora fragariae Hickman by the polymerase chain reaction. European Journal of Plant Pathology, 103, 345–355.

    CAS  Article  Google Scholar 

  2. Bontea, V. (1953). Ciuperci Parazite si Saprofite din Republica Populara Romana. Bucharest: Editura Academiei R. P. R.

    Google Scholar 

  3. Brandenburger, W., & Hagedorn, G. (2006). Zur Verbreitung von Peronosporales (inkl. Albugo, ohne Phytophthora) in Deutschland. Mitteilungen aus der Biologischen Bundesanstalt für Land– und Forstwirtschaft Berlin–Dahlem, 405, 1–174.

    Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  6. Choi, Y. J., Shin, H. D., & Thines, M. (2009). Two novel Peronospora species are associated with recent reports of downy mildew on sages. Mycological Research, 113, 1340–1350.

    CAS  Article  PubMed  Google Scholar 

  7. Choi, Y. J., Beakes, G., Glockling, S., Kruse, J., Nam, B., Nigrelli, L., Ploch, S., Shin, H. D., Shivas, R. G., Telle, S., Voglmayr, H., & Thines, M. (2015a). Towards a universal barcode of oomycetes—a comparison of the cox1 and cox2 loci. Molecular Ecology Resources, 15, 1275–1288.

    CAS  Article  PubMed  Google Scholar 

  8. Choi, Y. J., Klosterman, S. J., Kummer, V., Voglmayr, H., Shin, H. D., & Thines, M. (2015b). Multi-locus tree and species tree approaches toward resolving a complex clade of downy mildews (Straminipila, Oomycota), including pathogens of beet and spinach. Molecular Phylogenetics and Evolution, 86, 24–34.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  10. Constantinescu, O., & Negrean, G. (1983). Check-list of Romanian Peronosporales. Mycotaxon, 16, 537–556.

    Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  12. De Vienne, D. M., Giraud, T., & Martin, O. C. (2007). A congruence index for testingtopological similarity between trees. Bioinformatics, 23, 3119–3124.

    Article  PubMed  Google Scholar 

  13. Dick, M. W. (2001). Straminipilous fungi: Systematics of the Peronosporomycetes, including accounts of the marine straminipilous protists, the plasmodiophorids and similar organisms. Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  14. Duke, J. A., Bogenschutz-Godwin, M. J., duCellier, J., & Duke, P. A. K. (2002). Handbook of medicinal herbs. Boca Raton: CRC Press.

    Google Scholar 

  15. Edgar, R. (2004). Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Edwards, K., Johnstone, C., & Thompson, C. (1991). A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research, 19, 1349.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

  18. Francis, S. M. (1981). Peronospora sparsa. CMI Descriptions of Pathogenic Fungi and Bacteria, 690, 1–2.

    Google Scholar 

  19. Gäumann, E. A. (1923). Beiträge zu einer Monographie der Gattung Peronospora Corda. Zürich: Gebr. Fretz.

    Google Scholar 

  20. Gustavsson, A. (1959). Studies on Nordic Peronosporas. I. Taxonomic revision. Opera Botanica, 3, 1–271.

    Google Scholar 

  21. Hall, G. (1991). Peronospora potentillae. IMI Descriptions of Fungi and Bacteria, 1061, 1–2.

    Google Scholar 

  22. Hatfield, G. (2004). Encyclopedia of folk medicine: Old world and new world traditions. Santa Barbara: ABC-CLIO.

    Google Scholar 

  23. Hirilovich, I. S., & Lemeza, N. A. (2010). Species structure and distribution of micromycetes order Peronosporales in vicinities of geostation “West Beresina”. Proceedings of the National Academy of Science of Belarus, Biological Series 2010 N 4, 27–35.

  24. Horst, R. K. (2001). Westcott’s plant disease handbook. Boston: Kluwer Academic Publishers.

    Google Scholar 

  25. Hruby, J. (1930). Beiträge zur Pilzflora Mährens und Schlesiens. Hedwigia, 69, 173–211.

    Google Scholar 

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

    CAS  Article  Google Scholar 

  27. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    CAS  Article  PubMed  Google Scholar 

  28. Iwata, Y. (1942). Specialization in Pseudoperonospora cubensis (Berk. et Curt.) Rostov. II. Comparative studies of the morphologies of the fungi from Cucumis sativus L. and Cucurbita moschata Duchesne. Annals of the Phytopathological Society of Japan, 11, 172–185.

    Article  Google Scholar 

  29. Jermalaviciute, S. (1962). Nauja medziaga Lietuvos TSR Peronosporainiams grybams (Peronosporales) pazinti. Lietuvos TSR Mokslu Akademija, Darbai Ser. C, 3(29), 13–22.

    Google Scholar 

  30. Jung, T., & Burgess, T. I. (2009). Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species. Phytophthora plurivora sp. nov. Persoonia, 22, 95–110.

    CAS  PubMed  Google Scholar 

  31. Kitner, M., Lebeda, A., Sharma, R., Runge, F., Dvořák, P., Tahir, A., Choi, Y. J., Sedláková, B., & Thines, M. (2015). Coincidence of virulence shifts and population genetic changes of Pseudoperonospora cubensis in the Czech Republic. Plant Pathology, 64, 1461–1670.

    CAS  Article  Google Scholar 

  32. Kruse, J. (2014). Diversität der pflanzenpathogenen Kleinpilze im Ökologisch-Botanischen Garten der Universität Bayreuth. Zeitschrift für Mykologie, 80, 169–226.

    Google Scholar 

  33. Kućmierz, J. (1966). Parasitic fungi of the Ojcow National Park. Part II. Archimycetes, Phycomycetes, Ustilaginales. Fragmenta Floristica et Geobotanica, 12, 497–511.

    Google Scholar 

  34. Martin, F. N., & Tooley, P. W. (2003). Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia, 95, 269–284.

    CAS  Article  PubMed  Google Scholar 

  35. Mishra, B., & Thines, M. (2014). siMBa—a simple graphical user interface for the Bayesian inference program MrBayes. Mycological Progress, 13, 1255–1258.

    Article  Google Scholar 

  36. Moncalvo, J. M., Wang, H. H., & Hseu, R. S. (1995). Phylogenetic relationships in Ganoderma inferred from the internal transcribed spacers and 25S ribosomal DNA sequences. Mycologia, 87, 223–238.

    CAS  Article  Google Scholar 

  37. Mordue, J. E. M. (1989). Peronospora rubi. CMI Descriptions of Pathogenic Fungi and Bacteria, 976, 1–2.

    Google Scholar 

  38. Mulenko, W., Majewski, T., & Ruszkiewicz-Michalska, M. (2008). Preliminary checklist of micromycetes in Poland. Biodiversity of Poland 9. Krakow: W. Szafer Institute of Botany, Polish Academy of Sciences.

    Google Scholar 

  39. Müller, J., & Kokeš, P. (2008). Extended checklist of downy mildews of Moravia and Czech Silesia. Czech Mycology, 60, 91–104.

    Google Scholar 

  40. Petrželová, I., Dušek, K., & Dušková, E. (2013). Monitoring of pests and diseases in the field collections of medicinal, aromatic and culinary plants (MAPs)—preliminary results. Olomouc Biotech 2013 Plant Biotechnology: Green for Good II, Book of Abstracts, 93.

  41. Pirondi, A., Kitner, M., Iotti, M., Sedláková, B., Lebeda, A., & Collina, M. (2016). Genetic structure and phylogeny of Italian and Czech populations of the cucurbit powdery mildew fungus Golovinomyces orontii inferred by Multilocus Sequence Typing. Plant Pathology, 65, 959–967.

    Article  Google Scholar 

  42. Robideau, G. P., de Cock, A. W. A. M., Coffey, M. D., Voglmayr, H., Brouwer, H., Bala, K., Chitty, D. W., Désaulniers, N., Eggertson, Q. A., Gachon, C. M. M., Hu, C. H., Küpper, F. C., Rintoul, T. L., Sarhan, E., Verstappen, E. C. P., Zhang, Y., Bonants, P. J. M., Ristaino, J. B., & Lévesque, C. A. (2011). DNAbarcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources, 11, 1002–1011.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Runge, F., Ndambi, B., Thines, M. (2012). Which morphological characteristics are most influenced by the host matrix in downy mildews? A case study in Pseudoperonospora cubensis. PLoS One, 7, e44863.

  44. Savulescu, T. (1948). Les especes de Peronospora Corda de Roumanie. Sydowia, 2, 255–307.

    Google Scholar 

  45. Skalický, V. (1983). The revision of species of the genus Peronospora on host plants of the family Rosaceae with respect to Central European species. Folia Geobotanica et Phytotaxonomica, 18, 71–101.

    Article  Google Scholar 

  46. Skalický, V. (1995). Agrimonia L.—řepík. In B. Slavík (Ed.), Květena České republiky 4 (Flora of the Czech Republic) (pp. 233–238). Praha: Academia (in Czech).

    Google Scholar 

  47. Smith, S., Roberson, S., & Cochran, K. (2014). First report of downy mildew on blackberry caused by Peronospora sparsa in Arkansas. Plant Disease, 98, 1585.

    Article  Google Scholar 

  48. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 4.0.. Molecular Biology and Evolution, 30, 2725–2729.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Thines, M., Telle, S., Ploch, S., & Runge, F. (2009). Identity of the downy mildew pathogens of basil, coleus, and sage with implications for quarantine measures. Mycological Research, 113, 532–540.

    Article  PubMed  Google Scholar 

  51. Tošovská, M., & Buchtová, I. (2012). Situační a výhledová zpráva léčivé, aromatické a kořeninové rostliny (Situation and Outlook Report Medicinal, Aromatic and Culinary Plants). Praha: Ministry of Agriculture (in Czech).

    Google Scholar 

  52. Voglmayr, H., Choi, Y. J., & Shin, H. D. (2014). Multigene phylogeny, taxonomy and reclassification of Hyaloperonospora on Cardamine. Mycological Progress, 13, 131–144.

    Article  PubMed  Google Scholar 

  53. Waller, J. M., Lenné, J. M., & Waller, S. J. (2001). Plant pathologist’s pocketbook. Wallingford: CABI Publishing.

    Google Scholar 

  54. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, H. Gelfand, J. S. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic.

    Google Scholar 

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Acknowledgments

Research was supported by: grant No. LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, MEYS, Czech Republic; Internal Grant Agency of Palacký University in Olomouc, the Czech Republic (IGA 2016-001); fellowship from the Alexander von Humboldt foundation; LOEWE, Landesinitiative zur Entwicklung wissenschaftlich-ökonmischer Exzellenz, a funding program of the Government of Hessen, Germany, in the framework of the IPF—Integrative Fungal Research Cluster and the BiK-F—Biodiversity and Climate Research Centre. Authors thank to Prof. Aloisie Poulíčková for providing DIC microscopy photograph of P. agrimoniae conidiophore.

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Correspondence to Miloslav Kitner.

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Petrželová, I., Choi, Y., Jemelková, M. et al. Confirmation of Peronospora agrimoniae as a distinct species. Eur J Plant Pathol 147, 887–896 (2017). https://doi.org/10.1007/s10658-016-1058-8

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Keywords

  • Downy mildew of agrimony
  • Morphology
  • Molecular identification
  • Obligate biotrophs
  • Peronospora
  • Rosaceae