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Sustainable and efficient control of sunflower downy mildew by means of genetic resistance: a review

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Abstract

The breeding of sunflower (Helianthus annuus L.) for resistance to downy mildew (caused by the oomycete Plasmopara halstedii Farl. Berl. & de Toni) is reviewed in this work under the scope of its sustainability and efficiency. When sunflower turned into an oilseed crop, resistance to the disease was included in its initial breeding strategies. Subsequent development of genomic tools allowed a significant expansion of the knowledge on the diversity of its genetic resistance and its application to the genetic control of the disease. Simultaneously to genetic improvements, and as a consequence of the close interaction between the pathogen and its host plant, an enormous variety of pathotypes has been described in all the sunflower-growing areas worldwide. Thus, the genetic control of sunflower downy mildew is an active research field subjected to continuous evolution and challenge. In practice, genetic resistance constitutes the base tier of Integrated Pest Management against sunflower downy mildew. The second tier is composed of elements related to crop management: rotation, removal of volunteer plants, sowing date, tillage. Biological control alternatives and resistance inducers could also provide additional restraint. Finally, the top tier includes chemical treatments that should only be used when necessary and if the more basal Integrated Pest Management elements fail to keep pathogen populations under the economic threshold.

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References

  • Ahmed S, Tourvieille de Labrouhe D, Delmotte F (2012) Emerging virulence arising from hybridisation facilitated by multiple introductions of the sunflower downy mildew pathogen Plasmopara halstedii. Fungal Genet Biol 49:847–855

    Article  CAS  Google Scholar 

  • Albourie JM, Tourvieille J, Tourvieille de Labrouhe D (1998) Resistance to metalaxyl in isolates of the sunflower pathogen Plasmopara halstedii. Eur J Plant Pathol 104:235–242

    Article  CAS  Google Scholar 

  • As-sadi F, Carrere S, Gascuel Q, Hourlier T, Rengel D, Le Paslier MC, Bordat A, Boniface MC, Brunel D, Gouzy J, Godiard L, Vincourt P (2011) Transcriptomic analysis of the interaction between Helianthus annuus and its obligate parasite Plasmopara halstedii shows single nucleotide polymorphisms in CRN sequences. BMC Genomics 12:498. http://www.biomedcentral.com/1471-2164/12/498

  • Bachlava E, Radwan OE, Abratti G, Tang S, Gao W, Heesacker AF, Bazzalo ME, Zambelli A, Leon AJ, Knapp SJ (2011) Downy mildew (Pl8 and Pl14) and rust (RAdv) resistance genes reside in close proximity to tandemly duplicated clusters of non-TIR-like NBS-LRR-encoding genes on sunflower chromosomes 1 and 13. Theor Appl Genet 122:1211–1221

    Article  Google Scholar 

  • Badouin H, Gouzy J et al (2017) The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546(1):148. https://doi.org/10.1038/nature22380

    Article  CAS  Google Scholar 

  • Baldini M, Danuso F, Turi M, Sandra M, Raranciuc S (2008) Main factors influencing downy mildew (Plasmopara halstedii) infection in high-oleic sunflower hybrids in northern Italy. Crop Prot 27:590–599

    Article  Google Scholar 

  • Bán R, Kovács A, Perczel M, Körösi K, Turóczi G (2014) First report on the increased distribution of pathotype 704 of Plasmopara halstedii in Hungary. Plant Dis 98(6):844. https://doi.org/10.1094/PDIS-09-13-0920-PDN

    Article  Google Scholar 

  • Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58:649–662

    Article  CAS  Google Scholar 

  • Bazzalo ME, Huguet N, Romano MC, Bock F, Piubello S, Quiroz F, Erreguerrena I, Zuil S, Bertero A (2016) History and present state of downy mildew in Argentina. In: International sunflower association (ed) proceedings of the 19th international sunflower conference. Edirne, Turkey, May 29-June 3 2016. International Sunflower Association, Paris, France, vol. 2, pp 800–804

  • Bert PF, Tourvieille de Labrouhe D, Philippon J, Mouzeyar S, Jouan I, Nicolas P, Vear F (2001) Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 103:992–997

    Article  CAS  Google Scholar 

  • Bertero de Romano A, Romano C, Bulos M, Altieri E, Sala C (2010) A new gene for resistance to downy mildew in sunflower. In: International sunflower association (ed) proceedings of the international symposium “Sunflower breeding on resistance to diseases”. Krasnodar, Russia, June 23–24 2010. All-Russia Research Institute of Oil Crops by V. S. Pustovoit (VNIIMK), Krasnodar, Russia, pp 141–146

  • Bouzidi MF, Badaoui S, Cambon F, Vear F, De Labrouhe DT, Nicolas P, Mouzeyar S (2002) Molecular analysis of a major locus for resistance to downy mildew in sunflower with specific PCR-based markers. Theor Appl Genet 104:592–600

    Article  CAS  Google Scholar 

  • Carson ML (1981) New race of Plasmopara halstedii virulent on resistant sunflowers in South Dakota. Plan Dis 65:842–843

    Article  Google Scholar 

  • Cohen Y (1994) 3-Aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiol Mol Plant Pathol 44:273–288

    Article  CAS  Google Scholar 

  • Cohen Y, Coffey MD (1986) Systemic fungicides and the control of oomycetes. Annu Rev Phytopathol 24:311–338

    Article  CAS  Google Scholar 

  • Covarelli L, Tosi L (2006) Presence of sunflower downy mildew in an integrated weed control field trial. Phytopathol 154:281–285

    Article  Google Scholar 

  • Davidse LC, van den Berg-Velthuis GCM, Mantel BC, Jespers ABK (1991) Phenylamides and Phytophthora. In: Lucas JA, Shattock RC, Shaw DS, Cooke LR (eds) Phytophthora. British Mycological Society, Cambridge, pp 349–360

    Google Scholar 

  • 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. Infect Genet Evol 8:534–540

    Article  CAS  Google Scholar 

  • Diaz de la Guardia M, Garcia-Baudin C, Montes-Agusti F, Romero-Munoz F (1981) “Pemir”, variedad española de girasol con resistencia al mildiu. An Inst Nac Invest Agrar 15:13–22

    Google Scholar 

  • Drabkova Trojanova Z, Sedlarova M, Pospıchalova R, Lebeda A (2018) Pathogenic variability of Plasmopara halstedii infecting sunflower in the Czech Republic. Plant Pathol 67:136–144. https://doi.org/10.1111/ppa.12722

    Article  CAS  Google Scholar 

  • Dußle CM, Hahn V, Knapp SJ, Bauer E (2004) PlArg from Helianthus argophyllus is unlinked to other known downy mildew resistance genes in sunflower. Theor Appl Genet 109:1083–1086

    Article  Google Scholar 

  • Enns H, Dorrell DG, Hoes HA, Chubb WO (1970) Sunflower research – a progress report. In: International sunflower association (ed) proceedings of the 4th international sunflower conference. Memphis TN, USA, June 23–25 1970. International Sunflower Association, Paris, France, pp 162–167

  • Er Y, Özer N, Katırcıoğlu YZ (2021) In vivo anti-mildew activity of essential oils against downy mildew of sunflower caused by Plasmopara halstedii. Eur J Plant Pathol 161:619–627. https://doi.org/10.1007/s10658-021-02347-z

    Article  CAS  Google Scholar 

  • Fages J, Lux B (1991) Identification of bacteria isolated from roots of sunflower cultivated in a French soil. Can J Microbiol 37:971–974

    Article  Google Scholar 

  • FAOSTAT, 2020. https://www.fao.org/faostat/es/#data/QCL. Last accessed Oct. 19, 2021

  • Fernández-Martínez JM, Domínguez Giménez J (1978) Estudios genéticos de la resistencia al mildiu en girasol (Helianthus annuus L.) Ann INIA Ser Prod Veg 8:105–111.

  • Fick GN, Miller JF (1997) Sunflower Breeding. In: Schneiter AA (ed) Sunflower technology and production. CSSA, SSSA publishers, Madison WI, ASA, pp 395–439

    Google Scholar 

  • Fick GN, Zimmer DE (1974) RHA 271, RHA 273, and RHA 274: sunflower parental lines for producing downy mildew resistant hybrids. Farm Res ND Agric Exp Stn Fargo 32(2):7–9

    Google Scholar 

  • Fick GN, Zimmer DE (1975) Linkage tests among genes for six qualitative characters in sunflowers. Crop Sci 15:777–779

    Article  Google Scholar 

  • Fick GN, Kinman ML, Zimmer DE (1975) Registration of RHA-273 and RHA-274 sunflower parental lines. Crop Sci 15:106

    Article  Google Scholar 

  • Franchel J, Bouzidi MF, Bronner G, Vear F, Nicolas P, Mouzeyar S (2013) Positional cloning of a candidate gene for resistance to the sunflower downy mildew, Plasmopara halstedii race 300. Theor Appl Genet 126:359–367. https://doi.org/10.1007/s00122-012-1984-6

    Article  Google Scholar 

  • Fuchs A (1988) Implications of steroisomerism in agricultural fungicides. In: Ariëns EJ, van Rensen JJS, Welling W (eds) Stereoselectivity of pesticides: biological and chemical problems. Elsevier science Publishers, Amsterdam, pp 203–209

    Google Scholar 

  • García G, Gulya TJ (1991) Sunflower downy mildew race distribution in North Dakota and Minnesota. In: National sunflower association (ed) Proceedings of the 13th sunflower research workshop, Fargo ND, USA, Jan 10–11 1991. National Sunflower Association, Bismarck ND, USA, pp 3–5

  • Gascuel Q, Martinez Y, Boniface MC, Vear F, Pichon M, Godiard L (2015) The sunflower downy mildew pathogen Plasmopara halstedii. Mol Plant Pathol 16(2):109–122. https://doi.org/10.1111/mpp.12164

    Article  Google Scholar 

  • Gedil MA, Slabaugh MB, Berry S, Johnson R, Michelmore R, Miller J, Gulya T, Knapp SJ (2001) Candidate disease resistance genes in sunflower cloned using conserved nucleotide-binding site motifs: genetic mapping and linkage to the downy mildew resistance gene Pl1. Genome 44(2):205–212

    Article  CAS  Google Scholar 

  • Giresse X, Tourvieille de Labrouhe D, Richard-Cervera S, Delmotte F (2007) Twelve polymorphic expressed sequence tags-derived markers for Plasmopara halstedii, the causal agent of sunflower downy mildew. Mol Ecol Notes 7:1363–1365. https://doi.org/10.1111/j.1471-8286.2007.01887.x

    Article  CAS  Google Scholar 

  • Goossen PG, Sackston WE (1968) Transmission, and biology of sunflower downy mildew. Can J Bot 46:5–10

    Article  Google Scholar 

  • Görlach J, Volrath S, KnaufBeiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643

    Google Scholar 

  • Guatimosim E, Pinto HJ, Pereira OL, Fuga CAG, Vieira BS, Barreto RW (2015) Pathogenic mycobiota of the weeds Bidens pilosa and Bidens subalternans. Trop Plant Pathol 40:298–317. https://doi.org/10.1007/s40858-015-0040-x

    Article  Google Scholar 

  • Gulya TJ, Urs RR (1985) A new race of sunflower downy mildew. Phytopathol 75:1339

    Google Scholar 

  • Gulya TJ, Sackston WE, Viranyi F, Masirevic S, Rashid KY (1991) New races of the sunflower downy mildew pathogen (Plasmopara halstedii) in Europe and North and South America. J Phytopathol 132:303–311

    Article  Google Scholar 

  • Gulya TJ, Rashid KY, Marisevic S (1997) Sunflower diseases. In: Schneiter AA (ed) Sunflower technology and production. CSSA, SSSA publishers, Madison WI, ASA, pp 263–379

    Google Scholar 

  • Gulya TJ, de Labrouhe DT, Masirevic S, Penaud A, Rashid K, Viranyi F (1998) Proposal for standardized nomenclature and identification of races of Plasmopara halstedii (sunflower downy mildew). In: Gulya T, Vear F (eds) Proceedings of the ISA symposium III Sunflower downy mildew. Fargo, ND, USA, Jan 13–14 1998. International Sunflower Association, Paris, France, pp 130–136

  • Gulya TJ, Draper M, Harbour J, Holen C, Knodel J, Lamey A, Mason P (1999) Metalaxyl resistance in sunflower downy mildew in North America. In: National sunflower association (ed) Proceedings of the 21st Sunflower research workshop. Fargo ND, USA, Jan 12–13 1999. National Sunflower Association, Bismarck ND, USA, pp 2–7

  • Hebbar P, Berge O, Heulin T, Singh SP (1991) Bacterial antagonists of sunflower (Helianthus annuus L.) fungal pathogens. Plant Soil 133:131–140

    Article  Google Scholar 

  • Hulke BS, Miller JF, Gulya TJ, Vick BA (2010) Registration of the oilseed sunflower genetic stocks HA 458, HA 459, and HA 460 possessing genes for resistance to downy mildew. J Plant Regist 4:93–97

    Article  Google Scholar 

  • Humann RM, Johnson KD et al (2019) Evaluation of oxathiapiprolin for the management of sunflower downy mildew. Plant Dis 103(10):2498–2504

    Article  CAS  Google Scholar 

  • Iliescu H (1980) La lutte contre le mildiou du tournesol par des traîtements chimiques. In: Servicio de publicaciones agrarias (ed) Resúmenes de la IX Conferencia internacional del girasol Vol. I, Torremolinos, Malaga, Spain, June 8–13 1980. Vol. I. Jomagar, Madrid, Spain, pp 152–161

  • Intelmann F, Spring O (2002) Analysis of total DNA by minisatellite and simple sequence repeat primers for the use of population studies in Plasmopara halstedii. Can J Microbiol 48:555–559

    Article  CAS  Google Scholar 

  • Jaber LR (2015) Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. Biocontrol 60:103–112

    Article  Google Scholar 

  • Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45

    Article  Google Scholar 

  • Jan CC, Tan AS, Gulya TJ (1991) Genetics of downy mildew race 2 resistance derived from two wild Helianthus annuus accessions. In: National sunflower association (ed) Proceedings of the 13th Sunflower research workshop. Fargo ND, USA, Jan 10–11 1991. National Sunflower Association, Bismarck ND, USA, p 125

  • Kandel H, Endres G, Buetow R (2020) Sunflower production guide. North Dakota State University Extension, Fargo ND, USA. www.ndsu.edu/extension

  • Kinman ML (1970) New Developments in the USDA and State Experiment Station Sunflower Breeding Programs. In: International sunflower association (ed) Proceedings of the 4th International sunflower conference. Memphis TN, USA, June 23–25 1970. International Sunflower Association, Paris, France, pp 181–183

  • Kogel KH, Beckhove U, Dreschers J, Münch S, Romme Y (1994) Acquired resistance in barley. Plant Physiol 106:1269–1277

    Article  CAS  Google Scholar 

  • Körösi K, Lázár N, Virányi F (2009) Resistance to downy mildew in sunflower induced by chemical activators. Acta Phytopathologica 44:1–9

    Google Scholar 

  • Körösi K, Bán R, Barna B, Virányi F (2011) Biochemical and molecular changes in downy mildew-infected sunflower triggered by resistance inducers. J Phytopathol 159:471–478. https://doi.org/10.1111/j.1439-0434.2011.01787.x

    Article  CAS  Google Scholar 

  • Lawson WR, Goulter KC, Henry RJ, Kong GA, Kochman JK (1998) Marker-assisted selection for two rust resistance genes in sunflower. Mol Breed 4:227–234

    Article  CAS  Google Scholar 

  • Leclercq P (1969) Une sterilite male cytoplasmique chez Ie tournesol. Ann Amelior Plant 19:99–106

    Google Scholar 

  • Leclercq P, Cauderon Y, Dauge M (1970) Selection pour la resistance au mildiou du tournesol à partir d’hybrides topinambour x tournesol. Ann Amelior Plant 20(3):363–373

    Google Scholar 

  • Limpert E, Müller K (1994) Designation of pathotypes of plant-pathogens. J Phytopathol 140(4):346–358. https://doi.org/10.1111/j.1439-0434.1994.tb00617.x

    Article  Google Scholar 

  • Liu Z, Gulya TJ, Seiler GJ, Vick BA, Jan CC (2012) Molecular mapping of the Pl16 downy mildew resistance gene from HA-R4 to facilitate marker-assisted selection in sunflower. Theor Appl Genet 125:121–131

    Article  CAS  Google Scholar 

  • Liu Z, Zhang L, Ma GJ, Seiler GJ, Jan CC, Qi LL (2019) Molecular mapping of the downy mildew and rust resistance genes in a sunflower germplasm line TX16R. Mol Breed 39:19

    Article  Google Scholar 

  • Ljubich A, Gulya TJ, Miller JF (1988) A new race of sunflower downy mildew in North America. Phytopathol 78:1580

    Google Scholar 

  • Ma GJ, Markell SG, Song QJ, Qi LL (2017) Genotyping-by-sequencing targeting of a novel downy mildew resistance gene Pl20 from wild Helianthus argophyllus in sunflower (Helianthus annuus L.). Theor Appl Genet 130:1519–1529

    Article  CAS  Google Scholar 

  • Martín-Sanz A, Rueda S, García-Carneros AB, Molinero-Ruiz L (2020) First report of a new highly virulent pathotype of sunflower downy mildew (Plasmopara halstedii) overcoming the Pl8 resistance gene in Europe. Plant Dis 104(2):597. https://doi.org/10.1094/PDIS-07-19-1425-PDN

    Article  Google Scholar 

  • Melero-Vara JM, García-Baudín C, López-Herrera CJ, Jiménez-Díaz RM (1982) Control of sunflower downy mildew with metalaxyl. Plant Dis 66:132–135

    Article  CAS  Google Scholar 

  • Menzler-Hokkanen I (2006) Socioeconomic significance of biological control. In: Eilenberg G, Menzler-Hokkanen I (eds) An ecological and societal approach to biological control. Springer, Dordrecht, pp 13–25

    Chapter  Google Scholar 

  • Miller JF (1986) Registration of five nonoilseed sunflower restorer germplasm lines. Crop Sci 26:1265

    Google Scholar 

  • Miller JF (1992) Update on inheritance of sunflower characteristics. In: International sunflower association (ed) Proc 13th Int Sunf Conf, Pisa, Italy, Sept 7–11, 1992. International Sunflower Association, Paris, France, pp 905–945

  • Miller JF, Gulya TJ (1984) Sources and inheritance of resistance to race 3 downy mildew in sunflower. Helia 7:17–20

    Google Scholar 

  • Miller JF, Gulya TJ (1987) Inheritance of resistance to race 3 downy mildew in sunflower. Crop Sci 27:210–212

    Article  Google Scholar 

  • Miller JF, Gulya TJ (1991) Inheritance of resistance to race 4 of downy mildew derived from interspecific crosses in sunflower. Crop Sci 31:40–43

    Article  Google Scholar 

  • Miranda-Fuentes P, Garcia-Carneros AB, Montilla-Carmona AM, Molinero-Ruiz L (2020) Evidence of soil-located competition as the cause of the reduction of sunflower verticillium wilt by entomopathogenic fungi. Plant Pathol 69:1492–1503

    Article  CAS  Google Scholar 

  • Miranda-Fuentes P, García-Carneros A, Molinero-Ruiz L (2021) Updated characterization of races of Plasmopara halstedii and entomopathogenic fungi as endophytes of sunflower plants in axenic culture. Agronomy 11:268. https://doi.org/10.3390/agronomy11020268

    Article  CAS  Google Scholar 

  • Molinero-Ruiz L (2019) Recent advances on the characterization and control of sunflower soilborne pathogens under climate change conditions. OCL 26(1):2. https://doi.org/10.1051/ocl/2018046

    Article  Google Scholar 

  • Molinero-Ruiz L, García-de-Tejada JA (2021) Genes y productos en el control del mildiu de girasol. In: Asociación española del girasol (ed) Presentaciones de la XXXI reunión anual de AEG, Sanlúcar de Barrameda, España, Nov 25 2021

  • Molinero-Ruiz ML, Melero-Vara JM, Dominguez J (2002) Inheritance of resistance to race 330 of Plasmopara halstedii in three sunflower (Helianthus annuus L.) lines. Plant Breed 121 (1):61–65. https://doi.org/10.1046/j.1439-0523.2002.00654.x

  • Molinero-Ruiz ML, Melero-Vara JM, Dominguez J (2003a) Inheritance of resistance to two races of sunflower downy mildew (Plasmopara halstedii) in two Helianthus annuus L. lines. Euphytica 131:47–51. https://doi.org/10.1023/A:1023063726185

    Article  CAS  Google Scholar 

  • Molinero-Ruiz ML, Melero-Vara JM, Gulya TJ, Dominguez J (2003b) First report of resistance to metalaxyl in downy mildew of sunflower caused by Plasmopara halstedii in Spain. Plant Dis 87:749

    Article  CAS  Google Scholar 

  • Molinero-Ruiz ML, Cordón-Torres MM, Martínez-Aguilar J, Melero-Vara JM, Domínguez J (2008) Resistance to metalaxyl and to metalaxyl-M in populations of Plasmopara halstedii causing downy mildew in sunflower. Can J Plant Pathol 30:97–105

    Article  CAS  Google Scholar 

  • Molinero-Ruiz L, Delavault P, Pérez-Vich B, Pacureanu-Joita M, Bulos M, Altieri E, Dominguez J (2015) History of the race structure of Orobanche cumana and the breeding of sunflower for resistance to the parasitic weed: a review. Spanish J Agri Res 13 (4): e10R01, https://doi.org/10.5424/sjar/2015134-8080

  • Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1993) Histopathological studies of resistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii). J Phytopathol 139:289–297

    Article  Google Scholar 

  • Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1994) Effect of host-race combination on resistance of sunflower, Helianthus annuus L., to downy mildew Plasmopara halstedii. J Phytopathol 141:249–258

    Article  Google Scholar 

  • Mouzeyar S, Roeckel-Crevet P, Gentzbittel L, Philippon J, Tourvieille D, Vear F, Nicolas P (1995) RFLP and RAPD mapping of the sunflower Pl1 locus for resistance to Plasmopara halstedii race 1. Theor Appl Gent 91:733–737

    Article  CAS  Google Scholar 

  • Mulpuri S, Liu Z, Feng J, Gulya TJ, Jan CC (2009) Inheritance and molecular mapping of a downy mildew resistance gene, Pl13 in cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 119:795–803

    Article  CAS  Google Scholar 

  • Panchenco Y (1966) Sunflower production and breeding in the USSR. In: International sunflower association (ed) Proceedings of the 2nd International sunflower conference, Morden, Manitoba, Canada, August 17–18, 1966. International Sunflower Association, Paris, France, pp 15–29

  • Pasteris RJ, Hanagan MA et al (2016) Discovery of oxathiapiprolin, a new oomycete fungicide that targets an oxysterol binding protein. Bioorg Med Chem 24:354–361

    Article  CAS  Google Scholar 

  • Pecrix Y, Penouilh-Suzette C, Muños S, Vear F, Godiard L (2018) Ten broad spectrum resistances to downy mildew physically mapped on the sunflower genome. Front Plant Sci 9:1780. https://doi.org/10.3389/fpls.2018.01780

    Article  Google Scholar 

  • Pecrix Y, Buendia L, Penouilh-Suzette C, Maréchaux M, Legrand L, Bouchez O, Rengel D, Gouzy J, Cottret L, Vear F, Godiard L (2019) Sunflower resistance to multiple downy mildew pathotypes revealed by recognition of conserved effectors of the oomycete Plasmopara halstedii. Plant J. https://doi.org/10.1111/tpj.14157

    Article  Google Scholar 

  • Pustovoit GV (1966) Distant (interspecific) hybridization of sunflowers in the USSR. In: International sunflower association (ed) Proceedings of the 2nd International sunflower conference, Morden, Manitoba, Canada, august 17–18, 1966. International Sunflower Association, Paris, France, pp 82–95

  • Putt ED (1978) History and present world status. In: Carter JF (ed) Sunflower science and technology. ASA, Madison WI, pp 4–29

  • Qi L, Ma G (2020) Marker-assisted gene pyramiding and the reliability of using SNP markers located in the recombination suppressed regions of sunflower (Helianthus annuus L.). Genes 11:10. https://doi.org/10.3390/genes11010010

  • Qi LL, Long YM, Jan CC, Ma GJ, Gulya TJ (2015) Pl17 is a novel gene independent of known downy mildew resistance genes in the cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 128:757–767

    Article  CAS  Google Scholar 

  • Qi LL, Foley ME, Cai XW, Gulya TJ (2016) Genetics and mapping of a novel downy mildew resistance gene, Pl18, introgressed from wild Helianthus argophyllus into cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 129(4):741–752. https://doi.org/10.1007/s00122-015-2662-2

  • Qi LL, Ma GJ, Li X, Seiler GJ (2019) Diversification of the downy mildew resistance gene pool by introgression of a new gene, Pl35, from wild Helianthus argophyllus into oilseed and confection sunflowers (Helianthus annuus L.) Theor Appl Genet 132(9):2553–2565. https://doi.org/10.1007/s00122-019-03370-9

  • Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBSLRR disease resistance proteins in sunflower. Mol Genet Genomics 280:111–125

    Article  CAS  Google Scholar 

  • Radwan O, Bouzidi MF, Mouzeyar S (2011) Molecular characterization of two types of resistance in sunflower to Plasmopara halstedii, the causal agent of downy mildew. Phytopathol 101:970–979

    Article  CAS  Google Scholar 

  • Rahim M, Jan CC, Gulya TJ (2002) Inheritance of resistance to sunflower downy mildew races 1, 2 and 3 in cultivated sunflower. Plant Breed 121:57–60

    Article  Google Scholar 

  • Roeckel-Drevet P, Gagne G, Mouzeyar S, Gentzbittel L, Philippon J, Nicolas P, De Labrouhe DT, Vear F (1996) Colocation of downy mildew (Plasmopara halstedii) resistance genes in sunflower (Helianthus annuus L.). Euphytica 91:225–228

    Article  CAS  Google Scholar 

  • Roeckel-Drevet P, Tourvieille J, Gulya TJ, Charmet G, Nicolas P, Tourvieille de Labrouhe D (2003) Molecular variability of sunflower downy mildew, Plasmopara halstedii, from different continents. Can J Microbiol 49:492–502

    Article  CAS  Google Scholar 

  • Sackston WE (1992a) On a treadmill: breeding sunflowers for resistance to disease. Annu Rev Phytopathol 30:529–551

    Article  CAS  Google Scholar 

  • Sackston WE (1992b) Cotyledon limited infection (CLI) and leaf disk immersion (LDI) inoculation of sunflower by downy mildew (Plasmopara halstedii). In: International sunflower association (ed) Proc 13th Int Sunf Conf, Pisa, Italy, Sept 7–11, 1992. International Sunflower Association, Paris, France, pp 840–848

  • Sackston WE (1993) Biological control of downy mildew of sunflower. Phytopathol 83:247

    Google Scholar 

  • Sedlářová M, Pospíchalová R, Drábková Trojanová Z, Bartůšek 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 Protect Sci 52(3):182–187. https://doi.org/10.17221/7/2016-PPS

    Article  Google Scholar 

  • Seiler GJ (1991) Registration of 13 downy mildew tolerant interspecific sunflower germplasm lines derived from wild annual species. Crop Sci 31:1714–1716

    Article  Google Scholar 

  • Seiler GJ, Qi LL, Marek LF (2017) Utilization of sunflower crop wild relatives for cultivated sunflower improvement. Crop Sci 57:1083–1011

    Article  Google Scholar 

  • Semelczi-Kovacs A (1975) Acclimatization and dissemination of the sunflower in Europe. Acta Ethnogr Acad Sci Hung 24:47–88

    Google Scholar 

  • Spring O, Zipper R (2006) Evidence for asexual genetic recombination in sunflower downy mildew, Plasmopara halstedii. Mycol Res 110:657–663

    Article  CAS  Google Scholar 

  • Spring O, Gomez-Zeledon J, Hadziabdic D, Trigiano RN, Thines M, Lebeda A (2018) Biological characteristics and assessment of virulence diversity in pathosystems of economically important biotrophic oomycetes. Crit Rev Plant Sci 37(6):439–495. https://doi.org/10.1080/07352689.2018.1530848

    Article  CAS  Google Scholar 

  • Sudisha J, Niranjana SR, Sukanya SL, Girijamba R, Lakshmi Devi N, Shekar Shetty H (2010) Relative efficacy of strobilurin formulations in the control of downy mildew of sunflower. J Pest Sci 83:461–470. https://doi.org/10.1007/s10340-010-0316-3

    Article  Google Scholar 

  • Sukul P, Spiteller M (2000) Metalaxyl: persistence, degradation, metabolism and analytical methods. Rev Envir Contam Toxicol 164:1–26

    CAS  Google Scholar 

  • Talukder ZI, Ma G, Hulke BS, Jan CC, Qi L (2019) Linkage mapping and genome-wide association studies of the Rf gene cluster in sunflower (Helianthus annuus L.) and their distribution in world sunflower collections. Front Genet 10:216. https://doi.org/10.3389/fgene.2019.00216

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

    Article  CAS  Google Scholar 

  • Tosi L, Beccari L (2007) A new race, 704, of Plasmopara helianthi pathogen of sunflower downy mildew in Italy. Plant Dis 91(4):463. https://doi.org/10.1094/PDIS-91-4-0463B

    Article  CAS  Google Scholar 

  • Tosi L, Giovannetti M, Zazzerini A, Sbrana C (1993) Interactions between Plasmopara halstedii and arbuscular mycorrhizal fungi in sunflower seedlings susceptible and resistant to downy mildew. Phytopathol Medit 32:106–114

    Google Scholar 

  • Tourvieille de Labrouhe D, Lafon S, Walser P, Raulic I (2000) Une nouvelle race de Plasmopara halstedii, agent du mildiou du tournesol. OCL 7(5):404–405. https://doi.org/10.1051/ocl.2000.0404

    Article  Google Scholar 

  • Tourvieille de Labrouhe D, Walser P, Serre F, Roche S, Vear F (2008) Relations between spring rainfall and infection of sunflower by Plasmopara halstedii (downy mildew). In: International sunflower Association (ed) Proceedings of the 17th International sunflower conference. Córdoba, Spain, June 8–12 2008. International Sunflower Association, Paris, France, pp 97–102

  • 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: International sunflower association (ed) Proceedings of the 18th International sunflower conference. Mar del Plata, Argentina, February 26-March 1 2012. International Sunflower Association, Paris, France, pp 322–327

  • Vear F (1974) Studies on resistance to downy mildew in sunflowers (Helianthus annuus L.). In: Vranceanu A (ed) Proceedings of the 6th International sunflower conference, Bucharest, Romania, July 22–24, 1974. International Sunflower Association, Paris, France, pp 297–302

  • Vear F (2016) Changes in sunflower breeding over the last fifty years. OCL 23(2):D202. https://doi.org/10.1051/ocl/2016006

    Article  Google Scholar 

  • Vear F, Leclercq P (1971) Deux nouveaux gènes de résistance au mildiou du tournesol. Ann Amélior Plantes 21(3):251–255

    Google Scholar 

  • Vear F, Philippon J (1978) Réaction de certains génotypes de tournesol résistants au mildiou (Plasmopara helianthi) au test de résistance sur la plantule. Ann Amélior Plantes 28(3):327–332

    Google Scholar 

  • Vear F, Gentzbittel L, Philippon J, Mouzeyar S, Mestries E, Roeckel-Drevet P, Tourvieille de Labroube D, Nicolas P (1997) The genetics of resistance to five races of downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 95:584–589

    Article  Google Scholar 

  • Vear F, Seriveys H, Petit A, Serre F, Boudon JP, Roche S, Walser P, de Labrouhe DT (2008) Origins of major genes for downy mildew resistance in sunflower. In: Velasco L (ed) Proceedings of 17th International Sunflower Conference, Cordoba, Spain, june 8–12 2008. Junta de Andalucía, Consejería de Agricultura y Pesca, Sevilla, Spain, pp 125–130

  • Vega FE (2018) The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110:4–30

    Article  Google Scholar 

  • Vincourt P, As-Sadi F, Bordat A, Langlade NB, Gouzy J, Pouilly N, Lippi Y, Serre F, Godiard L, De Labrouhe DT, Vear F (2012) Consensus mapping of major resistance genes and independent QTL for quantitative resistance to sunflower downy mildew. Theor Appl Genet 125:909–920

    Article  Google Scholar 

  • Virányi F, Gulya TJ (1995) Inter-isolate variation for virulence in Plasmopara halstedii (sunflower downy mildew) from Hungary. Plant Pathol 44:619–624

    Article  Google Scholar 

  • Virányi F, Gulya TJ, Labrouhe de Tourvieille D (2015) Recent changes in the pathogenic variability of Plasmopara halstedii (sunflower downy mildew) populations from different continents. Helia 38(63):149–162. https://doi.org/10.1515/helia-2015-0009

    Article  Google Scholar 

  • Vrânceanu V (1970) Advances in sunflower breeding in Romania. In: International sunflower association (ed) Proceedings of the 4th International sunflower conference, Memphis TN, USA, june 23–25 1970. International Sunflower Association, Paris, France, pp 136–148

  • Vrânceanu A, Stoenescu F (1970) Immunity to sunflower downy mildew due to a single dominant gene. Probl Agric 2:34–40

    Google Scholar 

  • Vrânceanu A, Pirvu N, Iliescu H (1978) A new race of the fungus Plasmopara halstedii Novot. identified in Romania. In: International sunflower association (ed), Proceedings of the 8th International sunflower conference, July 23–27 1978, Minneapolis MN, USA, pp 328–333

  • Vrânceanu A, Pirvu N, Stoenescu FM (1981) New sunflower downy mildew resistance genes and their management. Helia 4:23–27

    Google Scholar 

  • Wiggins TE, Jager BJ (1993) Mode of action of the new methoxyacrylate antifungal agent ICIA5504. Biochem Soc Trans 22:68S

    Article  Google Scholar 

  • Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring MJ, Soper J, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry S, Leon A, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387

    Article  CAS  Google Scholar 

  • Zhang M, Liu Z, Jan CC (2016) Molecular mapping of a rust resistance gene R14 in cultivated sunflower line PH3. Mol Breed 36:32

    Article  Google Scholar 

  • Zhang ZW, Ma GJ, Zhao J, Markell SG, Qi LL (2017) Discovery and introgression of the wild sunflower-derived novel downy mildew resistance gene Pl19 in confection sunflower (Helianthus annuus L.). Theor Appl Genet 130:29–39

    Article  CAS  Google Scholar 

  • Zimmer DE (1974) Physiological specialization between races of Plasmopara halstedii in America and Europe. Phytopathol 64:1465–1467

    Article  Google Scholar 

  • Zimmer DE (1975) Some biotic and climatic factors influencing sporadic occurrence of sunflower downy mildew. Phytopathol 65:751–754

    Article  Google Scholar 

  • Zimmer DE, Kinman ML (1972) Downy mildew resistance in cultivated sunflower and its inheritance. Crop Sci 12:749–751

    Article  Google Scholar 

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    L. Molinero-Ruiz

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Molinero-Ruiz, L. Sustainable and efficient control of sunflower downy mildew by means of genetic resistance: a review. Theor Appl Genet 135, 3757–3771 (2022). https://doi.org/10.1007/s00122-022-04038-7

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