Plant Protect. Sci., 2019, 55(3):149-158 | DOI: 10.17221/32/2019-PPS

Spreading and global pathogenic diversity of sunflower downy mildew - ReviewReview

Otmar Spring*
Institute of Botany, Faculty of Natural Science, University of Hohenheim, Stuttgart, Germany

Since almost a century, sunflower cultivation is endangered by Plasmopara halstedii (Farlow) Berlese & de Toni, a biotrophic oomycete causing downy mildew symptoms. The pathogen has conquered four of the five continents, and through high genetic plasticity recurrently avoided being reliably controlled by the introduction of resistant host cultivars in sunflower production. This paper attempts to retrace the historic routes of sunflower downy mildew spreading from its North American origin into Europe, South America, Asia and Africa. An update of the global diversity of pathotypes will be provided and critically discussed. Finally, the limits of the currently applied bioassay-based techniques for diversity assessment are pointed out and an alternative for continuous and area-wide monitoring is discussed.

Keywords: Plasmopara halstedii; sunflower downy mildew; pathotype diversity

Published: September 30, 2019  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Spring O. Spreading and global pathogenic diversity of sunflower downy mildew - Review. Plant Protect. Sci.. 2019;55(3):149-158. doi: 10.17221/32/2019-PPS.
Download citation

References

  1. Achbani E.H., Lamrhari A., Laamaraf N., Bahsine M., Serrhini M.N., Douira A., Tourvieille D.T. (2000): Downy mildew (Plasmopara halstedii): Importance and geographical distribution on sunflower in Morocco. Phytopathologia Mediterranea, 39: 283-288.
  2. Bán R., Kovács A., Körösi K., Perczel M., Turóczi G., Zalai M., Pálinkás Z., Égei M. (2018): First report on the occurrence of a globally new pathotype, 724, of Plasmopara halstedii causing sunflower downy mildew in Hungary. Plant Disease, 102: 1861. doi: 10.1094/PDIS-10-17-1609-PDN Go to original source... Go to PubMed...
  3. Batinica J., Bes A., Dimic N., Numic R., Radman L., Ristanovic M., Vaclav V. (1973): A contribution to the knowledge of harmful fauna and the causes of diseases of sunflower in the area of its cultivation in the republic of Bosnia and Hercegovina. Radovi Poljoprivrednog Fakulteta Univerziteta u Sarajevu, 21/22: 203-210.
  4. Bisby G.R., Buller A.H.R., Dearness J., Fraser W.E., Russell R. (1938): The Fungi of Manitoba and Saskatchawan. Otawa, Natural Research Council Canada.
  5. Bogovik I.V. (1953): Nesprazhiya muchna rosa Plasmopara halstedii I plyamistict listya Septoria helianthi na sopyashinku v Zakarpatskii URSR. Pidvisheniya produktivnosti laniv lysiv I girskiikh nasovish Zakhidnikh oblastei URSR.
  6. CMI (1988): Distribution Maps of Plant Diseases No. 286. 5th Ed. Wallingford, CAB International.
  7. Cohen Y., Sackston W.E. (1974): Seed infection and latent infection of sunflower by Plasmopara halstedii. Canadian Journal of Botany, 52: 231-238. Go to original source...
  8. Constantinescu O., Thines M. (2010): Plasmopara halstedii is absent from Australia and New Zealand. Polish Botanical Journal, 55: 293-298.
  9. Delanoe D. (1972): Biologie et epidemiologie du mildiou du tornesol. Cetiom Informations Techniques, 26: 1-61.
  10. Delmotte F., Giresse X., Richard-Cervera S., M'Baya J., Vear F., Tourvieille J., Walser P., Tourvieille de Labrouhe D. (2008): Single nucleotide polymorphisms reveal multiple introductions into France of Plasmopara halstedii, the plant pathogen causing sunflower downy mildew. Infection, Genetics and Evolution, 8: 534-540. Go to original source... Go to PubMed...
  11. Drábková Trojanová Z., Sedláøová M., Pospíchalová R., Lebeda A. (2018): Pathogenic variability of Plasmopara halstedii infecting sunflower in the Czech Republic. Plant Pathology, 67: 136-144. Go to original source...
  12. Farlow W.G. (1883): Note on some species in the third and eleventh centuries of Ellis's North American Fungi. Proceedings of the American Academy of Arts and Sciences, 18: 71-73. Go to original source...
  13. Farlow W.G., Seymour A.B. (1890): A Provisional Host-index of the Fungi of the USA. Cambridge, Library of Harvard.
  14. Ferreira L.P., Henning A.A., Yorinori J.T., França Neto J.B., Schuck E., Lemos E.C., Azeredo J.A.P. (1983): Ocorrência do míldio (Plasmopara halstedii) em girassol, no Brasil. In: Congresso Brasileiro de Sementes, 3, Campinas, Brasil, 1983: 93.
  15. Fucikovsky-Zak L. (1976): Enfermedades y Plagas del Girasol en Mexico. Chapingo, Escuela Nacional de Agricultura, Colegio de Postgraduados.
  16. Gascuel Q., Martinez Y., Boniface M.C., Vear F., Pichon M., Godiard L. (2015): The sunflower downy mildew pathogen Plasmopara halstedii. Molecular Plant Pathology, 16: 109-122. Go to original source... Go to PubMed...
  17. Gascuel Q., Bordat A., Sallet E., Pouilly N., Carrere S., Roux F., Vincourt P., Godiard L. (2016): Effector polymorphisms of the sunflower downy mildew pathogen Plasmopara halstedii and their use to identify pathotypes from field isolates. PLoS ONE, 11: e0148513. doi: 10.1371/journal.pone.0148513 Go to original source... Go to PubMed...
  18. Gindrat D., Frei P., Pellet D. (1997): Le mildiou du tournesol en Suisse. Revue Suisse d'Agriculture, 30: 62-66.
  19. Gomez-Menor J. (1936): Review of Applied Mycology. Kew, Commonwealth Mycological Institute.
  20. Gulya T.J. (1995): Proposal for a revised system of classifying races of sunflower downy mildew. In: Proceedings of the 17th Sunflower Research Workshop, Jan 12-13, 1995, Fargo, USA: 76-78.
  21. Gulya T.J. (1996): Sunflower diseases in the Northern Great Plains. In: Proceedings of the 18th Sunflower Research Workshop, Jan 11-12, 1996, Fargo, USA: 24-27.
  22. Gulya T.J. (2007): Distribution of Plasmopara halstedii races from sunflower around the world. In: Lebeda A., Spencer-Phillips P.T.N. (eds): Advances in Downy Mildew Research, Vol. 3. Proceedings of the 2 nd International Downy Mildew Symposium, July 2-6, 2007, Olomouc, Czech Republic: 121-134.
  23. Gulya T.J., Rashid K.Y., Masirevic S.M. (1997): Sunflower diseases. In: Schneider A.A. (ed.): Sunflower Technology and Production. Madison, American Society of Agronomy: 263-380. Go to original source...
  24. Gulya T.J., Miller J.F., Viranyi F., Sackston W.E. (1991a): Proposed internationally standardized methods for race identification of Plasmopara halstedii. Helia, 14: 11-20.
  25. Gulya T.J., Sackston W.E., Viranyi F., Masirevic S., Rashid K. (1991b): New races of the sunflower downy mildew pathogen in Europe and North and South America. Journal of Phytopathology, 132: 303-311. Go to original source...
  26. Gulya T.J., Tourvieille de Labrouhe D., Masirevic S., Penaud A., Rashid K., Viranyi F. (1998): Proposal for standardized nomenclature and identification of races of Plasmopara halstedii (sunflower downy mildew). In: ISA. Symposium III: Sunflower Downy Mildew, Jan 13-14, 1998, Fargo, USA: 130-136.
  27. Henry A.W., Gilbert H.C. (1924): Important fungous diseases of the common sunflower. Minnesota Studies in Plant Science, 5: 285-305.
  28. Hübner S., Bercovich N., Todesco M., Mandel J.R., Odenheimer J., Ziegler E., Lee J.S., Baute G.J., Owens G.L., Grassa C.J., Ebert D.P., Ostevik K.L., Moyers B.T., Yakimowski S., Masalia R.R., Gao L., Calic I., Bowers J.E., Kane N.C., Swanevelder D.Z.H., Kubach T., Muños S., Langlade N.B., Burke J.M., Rieseberg L.H. (2019): Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nature Plants, 5: 54-62. Go to original source... Go to PubMed...
  29. Ioos R., Laugustin L., Rose S., Tourvieille J., Tourvieille de Labrouhe D. (2007): Development of a PCR test to detect the downy mildew causal agent Plasmopara halstedii in sunflower seeds. Plant Pathology, 56: 209-218. Go to original source...
  30. Karel G. (1958): A Preliminary List of Plant Diseases in Turkey. Ankara, Ministry of Agriculture.
  31. Kola K. (1980): Comparative study of sunflower varieties to assess their resistance to fungal diseases in the Zadrima area. Buletini i Shkencave Bujqesore, 19: 87-94.
  32. Kucmierz J. (1976): Plasmopara helianthi Novot., a new fungus species for Poland. Fragmenta Floristica et Geobotanica, 22: 373-375.
  33. Leppik E.E. (1962): Distribution of downy mildew and some other seedborne pathogens on sunflower. FAO Plant Protection Bulletin, 10: 126-129.
  34. Leppik E.E. (1966): Origin and specialization of Plasmopara halstedii complex on Compositae. FAO Plant Protection Bulletin, 14: 72-76.
  35. Machavariani G.D. (1972): Features of the development of downy mildew of sunflower in Georgia and the measures for its control. Trudy Nauchno-Issledovatel' skogo Instituta Zashchity Rastenii Gruz SSR, 24: 223-226. https://doi.org/10.17221/32/2019-PPS Go to original source...
  36. Masirevic S. (1992): Races of downy mildew (Plasmopara halstedii) on sunflower present in our region and in the world. Zbornik Radova, 20: 405-408.
  37. Mayee C.D., Patil M.A. (1986): Downy mildew of sunflower. Indian Phytopathology, 39: 314.
  38. McTaggart A.R., Shuey L.S., McKenna S.G., Davis R.I., Shivas R.G. (2015): Plasmopara sphagneticolae sp. nov. (Peronosporales) on Sphagneticola (Asteraceae) in Australia. Australasian Plant Pathology, 44: 81-85. Go to original source...
  39. Melero-Vara J.M., Garcia-Baudin C., Lopez-Herrera C.J., Jimenez-Diaz R.M. (1982): Control of sunflower downy mildew with metalaxyl. Plant Disease, 66: 132-135. Go to original source...
  40. Mikhailova L.S. (1988): Nauchno-Tekhnicheskii Byulleten' Vsesoyuznogo Nauchno-Issledovatel'skogo Instituta Maslichnykh Kul'tur No. 2: 3-4.
  41. Novotelnova N.S. (1966): Downy Mildew of Sunflower. Moscow, Leningrad, Nauka.
  42. Pontis R., Feldman J., Klinger A. (1959): Downy Mildew of Sunflower in Argentina. Plant Disease Report No. 43. Beltsville, USDA Plant Industry Station.
  43. Rahmani Y., Madjidieh-Ghassemi S. (1975): Research on relative resistance of different varieties and inbred lines of sunflower to downy mildew Plasmopara helianthi Novt. in greenhouse and in the experimental field test, 1973. Iranian Journal of Plant Pathology, 11: 96-104. (in Persian)
  44. Sackston W.E. (1956): Observations and speculations on rust (Puccinia helianthi Schw.) and some other diseases of sunflowers in Chile. The Plant Disease Reporter, 40: 744-747.
  45. Sackston W.E. (1957): Dieseases of sunflower in Uruguay. The Plant Disease Reporter, 41: 885-889.
  46. Sackston W.E. (1992): On a treadmill: Breeding sunflowers for resistance to diseases. Annual Review of Phytopathology, 30: 529-551. Go to original source... Go to PubMed...
  47. Sackston W.E., Gulya T.J., Miller J.F. (1990): A proposed international system of designating races of Plasmopara halstedii. Plant Disease, 74: 721-723.
  48. Savulescu T., Savulescu O. (1951): Studiul morfologic, biologic, si sistematic al geurilor Sclerospora, Basidiophora, Plasmopara si Peronoplasmopara. Bulletin Scientifique, Section des Sciences Biologiques, Agronomiques, Géologiques etGéographiques, III: 400-409.
  49. Sedláøová M., Pospíchalová R., Drábková Trojanová Z., Bartù¹ek T., Slobodianová L., Lebeda A. (2016): First Report of Plasmopara halstedii new races 705 and 715 on sunflower from the Czech Republic - Short Communication. Plant Protection Science, 52: 182-187. Go to original source...
  50. Sharma R., Xia X., Cano L.M., Evangelisti E., Kemen E., Judelson H., Oome S., Sambles C., van den Hoogen D.J., Kitner M., Klein J., Meijer H.J.G., Spring O., Win J., Zipper R., Bode H.B., Govers F., Kamoun S., Schornack S., Studholme D.J., Van den Ackerveken G., Thines M. (2015): Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. BMC Genomics, 16: 741. doi: 10.1186/s12864-015-1904-7 Go to original source... Go to PubMed...
  51. Shin H.D. (1991): Occurrence of sunflower downy mildew in Korea. Korean Journal of Plant Pathology, 7: 192-194.
  52. Spring O. (2000): Homothallic sexual reproduction in Plasmopara halstedii, the downy mildew of sunflower. Helia, 23: 19-26. Go to original source...
  53. Spring O. (2001). Non-systemic infections of sunflower with Plasmopara halstedii and their putative role in the distribution of the pathogen. Journal of Plant Diseases and Protection, 108: 329-336.
  54. Spring O., Zipper R. (2006): Evidence for asexual genetic recombination in sunflower downy mildew, Plasmopara halstedii. Mycological Research, 110: 657-663. Go to original source... Go to PubMed...
  55. Spring O., Zipper R. (2016): Asexual recombinants of Plasmopara halstedii pathotypes from dual infection of sunflower. PLoS ONE, 11: e0167015. doi: 10.1371/journal.pone.0167015 Go to original source... Go to PubMed...
  56. Spring O., Zipper R. (2018): New highly aggressive pathotype 354 of Plasmopara halstedii in German sunflower fields. Plant Protection Science, 54: 83-86. Go to original source...
  57. Spring O., Benz A., Faust V. (1991): Impact of downy mildew (Plasmopara halstedii) infection on the development and metabolism of sunflower. Journal of Plant Diseases and Protection, 98: 597-604.
  58. Spring O., Gomez-Zeledon J., Hadziabdic D., Trigiano R.N., Thines M., Lebeda A. (2018): Biological characteristics and assessment of virulence diversity in pathosystems of economically important biotrophic oomycetes. Critical Reviews in Plant Sciences, 37: 439-495. Go to original source...
  59. Thanassoulopoulos C.C., Mappas C.B. (1992): First report of downy mildew of sunflower in Greece. Plant Disease, 76: 539. doi: 10.1094/PD-76-0539B Go to original source...
  60. Tourvieille D., Lafon S., Walser P., Raulic I. (2000): A new race of Plasmopara halstedii, pathogen of sunflower downy mildew. Oleagineux, 12: 85-93.
  61. Tourvieille de Labrouhe D., Gulya T., Masirevic S., Penaud A., Rashid K., Viranyi F. (2000): New nomenclature of races of Plasmopara halstedii (sunflower downy mildew). In: Proceedings of the 15th International Sunflower Conference, June 12-16, 2000, Toulouse, France: 61-66.
  62. Tourvieille de Labrouhe D., Walser P., Jolivot D., Roche S., Serre F., Leguillon M., Delmotte F., Bordat A., Godiard L., Vincourt P., Vear F. (2012): Proposal for improvement of sunflower downy mildew race nomenclature. In: Proceedings of the 18th International Sunflower Conference, Feb 27-March 1, 2012, Mar del Plata, Argentina: 322-327.
  63. Trojanová Z., Sedláøová M., Gulya T.J., Lebeda, A. (2017): Methodology of virulence screening and race characterization of Plasmopara halstedii, and resistance evaluation in sunflower - a review. Plant Pathology, 66: 171-185. Go to original source...
  64. Viljoen A., van Wyk P.S., Nowell D.C., Gulya T.J. (1997): Occurrence of downy mildew on sunflower in South Africa. Plant Disease, 81: 111. doi: 10.1094/PDIS.1997.81.1.111C Go to original source... Go to PubMed...
  65. Virányi F. (1992): Downy mildew of sunflower. In: Chaube H.S., Singh U.S., Mukhopadhyay A.N., Kumar J. (eds): Plant Diseases of International Importance. Vol. 2. Eaglewood Cliffs, Prentice Hall: 328-344.
  66. Virányi F. (2018): CABI invasive species compendium. Datasheet Plasmopara halstedii (downy mildew of sunflower). Available at https://www.cabi.org/isc/datasheet/41911 (accessed Jan 20, 2019).
  67. Virányi F., Spring O. (2011): Advances in sunflower downy mildew research. European Journal of Plant Pathology, 129: 207-220. Go to original source...
  68. Virányi F., Gulya T.J., Tourvielle D.L. (2015): Recent changes in the pathogenic variability of Plasmopara halstedii (sunflower downy mildew) populations in different countries. Helia, 38: 149-162. Go to original source...
  69. Vranceanu V., Stoenescu F. (1970): Immunity to sunflower downy mildew due to a single dominant gene. Problème Agricole, 22: 34-40.
  70. Weldekidan T. (1986): Ethiopian Journal of Agricultural Sciences, 8: 95-101. Go to original source...
  71. Yang S.M, Wei S.E., Ge C.F., Liang K.Z., Wang L. (1988): Diseases of cultivated sunflower in Liaoning province, People's Republic of China. Plant Disease, 72: 546. doi: 10.1094/PD-72-0546A Go to original source...
  72. Yoshida K., Burbano H.A., Krause J., Thines M., Weigel D., Kamoun S. (2014): Mining herbaria for plant pathogen genomes: Back to the future. PLoS Pathogens, 10: e1004028. doi: 10.1371/journal.ppat.1004028 Go to original source... Go to PubMed...
  73. Young P.A., Morris H.E. (1927): Plasmopara downy mildew of cultivated sunflowers. American Journal of Botany, 14: 551-553. Go to original source...
  74. Zazzerini A. (1983): Peronospora disease (Plasmopara helianthi Novot.) of sunflower: Physiologic races of the parasite and methods of identifying infected material. Informatore Fitopatologico, 33: 117-119.
  75. Zimmer D.E. (1974): Physiological specialization between races of Plasmopara halstedii in America and Europe. Phytopathology, 64: 1465-1467. Go to original source...
  76. Zimmer D.E., Hoes J.A. (1978): Diseases. In: Carter J.F. (ed.): Sunflower Science and Technology. Madison, American Society of Agronomy: 225-262. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.