Spreading and global pathogenic diversity of sunflower downy mildew – Review

https://doi.org/10.17221/32/2019-PPSCitation:Spring O. (2019): Spreading and global pathogenic diversity of sunflower downy mildew – Review. Plant Protect. Sci., 55: 149-158.
download PDF

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.

References:
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.
 
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-  https://doi.org/10.1094/PDIS-10-17-1609-PDN
 
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.
 
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.
 
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.
 
CMI (1988): Distribution Maps of Plant Diseases No. 286. 5th Ed. Wallingford, CAB International.
 
Cohen Yigal, Sackston W. E. (1974): Seed infection and latent infection of sunflowers by Plasmopara halstedii. Canadian Journal of Botany, 52, 231-238  https://doi.org/10.1139/b74-027
 
Constantinescu O., Thines M. (2010): Plasmopara halstedii is absent from Australia and New Zealand. Polish Botanical Journal, 55: 293–298.
 
Delanoe D. (1972): Biologie et epidemiologie du mildiou du tornesol. Cetiom Informations Techniques, 26: 1–61.
 
Delmotte François, Giresse Xavier, Richard-Cervera Sylvie, M’Baya Jessica, Vear Felicity, Tourvieille Jeanne, Walser Pascal, Labrouhe Denis Tourvieille de (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  https://doi.org/10.1016/j.meegid.2008.02.012
 
Drábková Trojanová Z., Sedlářová M., Pospíchalová R., Lebeda A. (2018): Pathogenic variability of Plasmopara halstedii infecting sunflower in the Czech Republic. Plant Pathology, 67, 136-144  https://doi.org/10.1111/ppa.12722
 
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.
 
Farlow W.G., Seymour A.B. (1890): A Provisional Host-index of the Fungi of the USA. Cambridge, Library of Harvard.
 
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.
 
Fucikovsky-Zak L. (1976): Enfermedades y Plagas del Girasol en Mexico. Chapingo, Escuela Nacional de Agricultura, Colegio de Postgraduados.
 
Gascuel Quentin, Martinez Yves, Boniface Marie-Claude, Vear Felicity, Pichon Magalie, Godiard Laurence (2015): The sunflower downy mildew pathogen Plasmopara halstedii. Molecular Plant Pathology, 16, 109-122  https://doi.org/10.1111/mpp.12164
 
Gascuel Quentin, Bordat Amandine, Sallet Erika, Pouilly Nicolas, Carrere Sébastien, Roux Fabrice, Vincourt Patrick, Godiard Laurence, Gijzen Mark (2016): Effector Polymorphisms of the Sunflower Downy Mildew Pathogen Plasmopara halstedii and Their Use to Identify Pathotypes from Field Isolates. PLOS ONE, 11, e0148513-  https://doi.org/10.1371/journal.pone.0148513
 
Gindrat D., Frei P., Pellet D. (1997): Le mildiou du tournesol en Suisse. Revue Suisse d’Agriculture, 30: 62–66.
 
Gomez-Menor J. (1936): Review of Applied Mycology. Kew, Commonwealth Mycological Institute.
 
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.
 
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.
 
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 2nd International Downy Mildew Symposium, July 2–6, 2007, Olomouc, Czech Republic: 121–134.
 
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.
 
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.
 
Gulya T. J., Sackston W. E., Viranyi F., Masirevic S., Rashid K. Y. (1991): New Races of the Sunflower Downy Mildew Pathogen (Plasmopara halstedii) in Europe and North and South America. Journal of Phytopathology, 132, 303-311  https://doi.org/10.1111/j.1439-0434.1991.tb00125.x
 
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.
 
Henry A.W., Gilbert H.C. (1924): Important fungous diseases of the common sunflower. Minnesota Studies in Plant Science, 5: 285–305.
 
Hübner Sariel, Bercovich Natalia, Todesco Marco, Mandel Jennifer R., Odenheimer Jens, Ziegler Emanuel, Lee Joon S., Baute Gregory J., Owens Gregory L., Grassa Christopher J., Ebert Daniel P., Ostevik Katherine L., Moyers Brook T., Yakimowski Sarah, Masalia Rishi R., Gao Lexuan, Ćalić Irina, Bowers John E., Kane Nolan C., Swanevelder Dirk Z. H., Kubach Timo, Muños Stephane, Langlade Nicolas B., Burke John M., Rieseberg Loren H. (2019): Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nature Plants, 5, 54-62  https://doi.org/10.1038/s41477-018-0329-0
 
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  https://doi.org/10.1111/j.1365-3059.2006.01500.x
 
Karel G. (1958): A Preliminary List of Plant Diseases in Turkey. Ankara, Ministry of Agriculture.
 
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.
 
Kucmierz J. (1976): Plasmopara helianthi Novot., a new fungus species for Poland. Fragmenta Floristica et Geobotanica, 22: 373–375.
 
Leppik E.E. (1962): Distribution of downy mildew and some other seedborne pathogens on sunflower. FAO Plant Protection Bulletin, 10: 126–129.
 
Leppik E.E. (1966): Origin and specialization of Plasmopara halstedii complex on Compositae. FAO Plant Protection Bulletin, 14: 72–76.
 
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.
 
Masirevic S. (1992): Races of downy mildew (Plasmopara halstedii) on sunflower present in our region and in the world. Zbornik Radova, 20: 405–408.
 
Mayee C.D., Patil M.A. (1986): Downy mildew of sunflower. Indian Phytopathology, 39: 314.
 
McTaggart Alistair R., Shuey Louise S., McKenna Stephen G., Davis Richard I., Shivas Roger G. (2015): Plasmopara sphagneticolae sp. nov. (Peronosporales) on Sphagneticola (Asteraceae) in Australia. Australasian Plant Pathology, 44, 81-85  https://doi.org/10.1007/s13313-014-0323-6
 
Melero-Vara J. M. (1982): Control of Sunflower Downy Mildew with Metalaxyl. Plant Disease, 66, 132-  https://doi.org/10.1094/PD-66-132
 
Mikhailova L.S. (1988): Nauchno-Tekhnicheskii Byulleten’ Vsesoyuznogo Nauchno-Issledovatel’skogo Instituta Maslichnykh Kul’tur No. 2: 3–4.
 
Novotelnova N.S. (1966): Downy Mildew of Sunflower. Moscow, Leningrad, Nauka.
 
Pontis R., Feldman J., Klinger A. (1959): Downy Mildew of Sunflower in Argentina. Plant Disease Report No. 43. Beltsville, USDA Plant Industry Station.
 
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)
 
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.
 
Sackston W.E. (1957): Dieseases of sunflower in Uruguay. The Plant Disease Reporter, 41: 885–889.
 
Sackston W. E. (1992): On a Treadmill: Breeding Sunflowers for Resistance to Disease. Annual Review of Phytopathology, 30, 529-551  https://doi.org/10.1146/annurev.py.30.090192.002525
 
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.
 
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.
 
Michaela Sedlářová, Romana Pospíchalová, Zuzana Drábková Trojanová, Tomáš Bartůšek, Lucie Slobodianová, Aleš Lebeda (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  https://doi.org/10.17221/7/2016-PPS
 
Sharma Rahul, Xia Xiaojuan, Cano Liliana M., Evangelisti Edouard, Kemen Eric, Judelson Howard, Oome Stan, Sambles Christine, van den Hoogen D. Johan, Kitner Miloslav, Klein Joël, Meijer Harold J. G., Spring Otmar, Win Joe, Zipper Reinhard, Bode Helge B., Govers Francine, Kamoun Sophien, Schornack Sebastian, Studholme David J., Van den Ackerveken Guido, Thines Marco (2015): Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. BMC Genomics, 16, -  https://doi.org/10.1186/s12864-015-1904-7
 
Shin H.D. (1991): Occurrence of sunflower downy mildew in Korea. Korean Journal of Plant Pathology, 7: 192–194.
 
Spring O. (2000): Homothallic sexual reproduction in Plasmopara halstedii, the downy mildew of sunflower. Helia, 23: 19–26.
 
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.
 
Spring Otmar, Zipper Reinhard (2006): Evidence for asexual genetic recombination in sunflower downy mildew, Plasmopara halstedii. Mycological Research, 110, 657-663  https://doi.org/10.1016/j.mycres.2006.03.009
 
Spring Otmar, Zipper Reinhard, Gijzen Mark (2016): Asexual Recombinants of Plasmopara halstedii Pathotypes from Dual Infection of Sunflower. PLOS ONE, 11, e0167015-  https://doi.org/10.1371/journal.pone.0167015
 
Otmar Spring, Reinhard Zipper (2018): New highly aggressive pathotype 354 of Plasmopara halstedii in German sunflower fields. Plant Protection Science, 54, 83-86  https://doi.org/10.17221/99/2017-PPS
 
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.
 
Spring Otmar, Gomez-Zeledon Javier, Hadziabdic Denita, Trigiano Robert N., Thines Marco, Lebeda Aleš (2019): Biological Characteristics and Assessment of Virulence Diversity in Pathosystems of Economically Important Biotrophic Oomycetes. Critical Reviews in Plant Sciences, 37, 439-495  https://doi.org/10.1080/07352689.2018.1530848
 
Thanassoulopoulos C. C. (1992): First Report of Downy Mildew of Sunflower in Greece. Plant Disease, 76, 539B-  https://doi.org/10.1094/PD-76-0539B
 
Tourvieille D., Lafon S., Walser P., Raulic I. (2000): A new race of Plasmopara halstedii, pathogen of sunflower downy mildew. Oleagineux, 12: 85–93.
 
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.
 
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.
 
Trojanová Z., Sedlářová 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  https://doi.org/10.1111/ppa.12593
 
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, 111-111  https://doi.org/10.1094/PDIS.1997.81.1.111C
 
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.
 
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).
 
Viranyi Ferenc, Spring Otmar (2011): Advances in sunflower downy mildew research. European Journal of Plant Pathology, 129, 207-220  https://doi.org/10.1007/s10658-010-9683-0
 
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.
 
Vranceanu V., Stoenescu F. (1970): Immunity to sunflower downy mildew due to a single dominant gene. Problème Agricole, 22: 34–40.
 
Weldekidan T. (1986): Ethiopian Journal of Agricultural Sciences, 8: 95–101. https://doi.org/10.1016/S0388-0001(86)80009-2
 
Yang S. M. (1988): Diseases of Cultivated Sunflower in Liaoning Province, People's Republic of China. Plant Disease, 72, 546-  https://doi.org/10.1094/PD-72-0546A
 
Yoshida Kentaro, Burbano Hernán A., Krause Johannes, Thines Marco, Weigel Detlef, Kamoun Sophien, Heitman Joseph (2014): Mining Herbaria for Plant Pathogen Genomes: Back to the Future. PLoS Pathogens, 10, e1004028-  https://doi.org/10.1371/journal.ppat.1004028
 
Young P. A., Morris H. E. (1927): PLASMOPARA DOWNY MILDEW OF CULTIVATED SUNFLOWERS. American Journal of Botany, 14, 551-552  https://doi.org/10.1002/j.1537-2197.1927.tb04866.x
 
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.
 
Zimmer D. E. (1974): Physiological Specialization Between Races of Plasmopara halstedii in America and Europe. Phytopathology, 64, 1465-  https://doi.org/10.1094/Phyto-64-1465
 
Zimmer D.E., Hoes J.A. (1978): Diseases. In: Carter J.F. (ed.): Sunflower Science and Technology. Madison, American Society of Agronomy: 225–262.
 
download PDF

© 2019 Czech Academy of Agricultural Sciences