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QoI Fungicide Resistance Mutations in Alternaria solani and Alternaria alternata are Fully Established in Potato Growing Areas in Bavaria and Dual Resistance against SDHI Fungicides is Upcoming

Umfangreiche Verbreitung von QoI-Fungizidresistenzmutationen in Alternaria solani und Alternaria alternata in bayerischen Kartoffelanbaugebieten und anfängliches Auftreten von dualen Resistenzen gegen SDHI-Fungizide

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Abstract

Alternaria leaf spots caused by Alternaria solani and Alternaria alternata are a major foliar disease of potatoes. Reduced sensitivity of A. solani and A. alternata towards Quinone outside inhibitors (QoI) fungicides has been observed in Europe. QoI-insensitive A. alternata isolates carry a G143A amino acid exchange caused by a single nucleotide polymorphism (SNP) in the cytochrome b gene. A. solani evolved a similar F129L mutation. A shift from the predominant A. solani genotype I to genotype II, which was exclusively associated with the F129L mutation, was observed in Germany after QoI approval for Alternaria control. Here, we found QoI mutations to be highly abundant in A. solani and A. alternata field isolates, collected in 2016 in Bavaria, located in southeastern Germany. The frequency of the F129L mutation, but not of A. solani genotype II, was higher than in the last available study. This might be due to that we also found the F129L mutation in genotype I, indicating QoI resistance progression through the previously unaffected genotype. In contrast to previous data, QoI mutations were present in all examined areas. An analysis of SNP diversity pointed to the region of Lower Bavaria as a hotspot for F129L mutation evolution. Reduced sensitivity of Alternaria spp. towards succinate dehydrogenase inhibitors (SDHI) fungicides is an emerging issue in Europe. We observed the presence of SDHI mutations, but only in combination with QoI mutations, indicating a further adaption to applied fungicides and a selection for dual fungicide resistance.

Zusammenfassung

Die durch Alternaria solani und Alternaria alternata verursachten Dürr- und Sprühflecken sind eine bedeutende Blattkrankheit der Kartoffel. In Europa wurde eine reduzierte Sensitivität von A. solani und A. alternata gegen Fungizide der Quinone-outside-Inhibitoren (QoI)-Wirkstoffgruppe beobachtet. QoI-insensitive A. alternata Isolate zeigen einen G143A Aminosäurenaustausch, der durch eine Punktmutation (SNP) im Cytochrom b Gen verursacht wird. A. solani entwickelte mit F129L eine ähnliche Mutation. In Deutschland wurde eine Verschiebung vom vorherrschenden A. solani Genotyp I zum Genotyp II, in dem ausschließlich die F129L-Mutation auftrat, beobachtet, nachdem QoI-Präparate für die Alternaria-Kontrolle zugelassen waren. QoI-Mutationen waren in den in dieser Arbeit untersuchten A. solani und A. alternata Feldisolaten, die im Jahr 2016 in Bayern gesammelt wurden, äußerst häufig. Im Vergleich zur letzten verfügbaren Studie nahm die Häufigkeit der F129L-Mutation insgesamt zu, nicht jedoch die Häufigkeit des A. solani Genotyps II. Da wir die F129L-Mutation auch in Genotyp I gefunden haben, könnte das auf eine zusätzliche Ausbreitung der F129L-Mutation durch den bisher nicht betroffenen Genotyp hindeuten. Zudem waren nun, im Gegensatz zu einer früheren Studie, QoI-Mutationen in allen untersuchten Gebieten nachweisbar. Eine Analyse der SNP-Diversität deutete auf die Region Niederbayern als Hotspot für die Evolution von F129L-Mutationen hin. Eine reduzierte Sensitivität von Alternaria spp. gegen Fungizide aus der Wirkstoffgruppe der Succinat-Dehydrogenase-Inhibitoren (SDHI) ist ein aufkommendes Problem in Europa. Wir konnten SDHI-Mutationen nachweisen, allerdings nur in Kombination mit QoI-Mutationen. Das könnte eine fortschreitende Anpassung an angewandte Fungizidkombinationen und eine Selektion von doppelter Fungizidresistenz andeuten.

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References

  • Avenot HF, Michailides TJ (2010) Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot 29(7):643–651

    Article  CAS  Google Scholar 

  • Avenot HF, van den Biggelaar H, Morgan DP, Moral J, Joosten M, Michailides TJ (2014) Sensitivities of baseline isolates and boscalid-resistant mutants of Alternaria alternata from pistachio to fluopyram, penthiopyrad, and fluxapyroxad. Plant Dis 98(2):197–205

    Article  CAS  Google Scholar 

  • Avenot HF, Sellam A, Karaoglanidis G, Michailides TJ (2008) Characterization of mutations in the iron-sulfur subunit of succinate dehydrogenase correlating with boscalid resistance in Alternaria alternata from California pistachio. Phytopathology 98(6):736–742

    Article  CAS  Google Scholar 

  • Avenot HF, Sellam A, Michailides TJ (2009) Characterization of mutations in the membrane-anchored subunits AaSDHC and AaSDHD of succinate dehydrogenase from Alternaria alternata isolates conferring field resistance to the fungicide boscalid. Plant Pathol 58(6):1134–1143

    Article  CAS  Google Scholar 

  • Bartlett DW, Clough JM, Godwin JR, Alison AH, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58(7):649–662

    Article  CAS  Google Scholar 

  • Dillard HR, Wicks TJ, Philip B (1993) A grower survey of diseases, invertebrate pests, and pesticide use on potatoes grown in South Australia. Aust J Exp Agric 33(5):653–661

    Article  CAS  Google Scholar 

  • Fairchild KL, Miles TD, Wharton PS (2013) Assessing fungicide resistance in populations of Alternaria in Idaho potato fields. Crop Prot 49:31–39

    Article  CAS  Google Scholar 

  • FRAC (2018a) FRAC Code List ©*2018: Fungicides sorted by mode of action (including FRAC Code numbering). Fungicide Resistance Action Committee. http://www.frac.info/docs/default-source/publications/frac-code-list/frac_code_list_2018-final.pdf?sfvrsn=6144b9a_2. Accessed 24 Mar 2018

    Google Scholar 

  • FRAC (2018b) General recommendations for use (of SBI fungicides). Fungicide Resistance Action Committee. http://www.frac.info/working-group/sbi-fungicides/general-use-recommendations. Accessed 24 Mar 2018

    Google Scholar 

  • Gisi U, Chin KM, Knapova G, Küng Färber R, Mohr U, Parisi S, Sierotzki H, Steinfeld U (2000) Recent developments in elucidating modes of resistance to phenylamide, DMI and strobilurin fungicides. Crop Prot 19(8–10):863–872

    Article  CAS  Google Scholar 

  • Gisi U, Sierotzki H, Cook A, McCaffery A (2002) Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag Sci 58(9):859–867

    Article  CAS  Google Scholar 

  • Grasso V, Palermo S, Sierotzki H, Garibaldi A, Gisi U (2006) Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Manag Sci 62(6):465–472

    Article  CAS  Google Scholar 

  • Gudmestad NC, Arabiat S, Miller JS, Pasche JS (2013) Prevalence and Impact of SDHI Fungicide Resistance in Alternaria solani. Plant Dis 97:952–960

    Article  CAS  Google Scholar 

  • Hausladen H, Leiminger JH (2007) Potato early blight in Germany (Alternaria solani—Alternaria alternata). In: Westerdijk CE, Schepers HTAM (eds) Applied Plant Research BV. PPOSpecial report, vol 12. Applied Arable and Vegetable Research, Wageningen

    Google Scholar 

  • Kim Y‑S, Dixon EW, Vincelli P, Farman ML (2003) Field Resistance to Strobilurin (QoI) Fungicides in Pyricularia grisea Caused by Mutations in the Mitochondrial Cytochrome b Gene. Phytopathology 93(7):891–900

    Article  CAS  Google Scholar 

  • Landschoot S, Carrette J, Vandecasteele M, De Baets B, Höfte M, Audenaert K, Haesaert G (2017) Boscalid-resistance in Alternaria alternata and Alternaria solani populations: An emerging problem in Europe. Crop Prot 92:49–59

    Article  Google Scholar 

  • Leiminger JH (2009) Alternaria spp. an Kartoffeln – Empirische Untersuchungen zur Epidemiologie, Schadrelevanz und integrierten Bekämpfungsstrategien. Hieronymus, München

    Google Scholar 

  • Leiminger JH, Hausladen H (2012) Early Blight Control in Potato Using Disease-Oriented Threshold Values. Plant Dis 96(1):124–130

    Article  CAS  Google Scholar 

  • Leiminger J, Bäßler E, Knappe C, Bahnweg H, Hausladen H (2015) Quantification of disease progression of Alternaria spp. on potato using real-time PCR. Eur J Plant Pathol 141(2):295–309

    Article  Google Scholar 

  • Leiminger JH, Adolf B, Hausladen H (2014) Occurrence of the F129L mutation in Alternaria solani populations in Germany in response to QoI application, and its effect on sensitivity. Plant Pathol 63(3):640–650

    Article  CAS  Google Scholar 

  • LfL (2018) The correct strategy against late blight in potatoes. Bavarian State Research Center for Agriculture. https://www.lfl.bayern.de/ips/blattfruechte/034444/index.php. Accessed 23 Mar 2018

    Google Scholar 

  • Ma Z, Felts D, Michailides TJ (2003) Resistance to azoxystrobin in Alternaria isolates from pistachio in California. Pestic Biochem Physiol 77(2):66–74

    Article  CAS  Google Scholar 

  • Mallik I, Arabiat S, Pasche JS, Bolton MD, Patel JS, Gudmestad NC (2014) Molecular Characterization and Detection of Mutations Associated with Resistance to Succinate Dehydrogenase-Inhibiting Fungicides in Alternaria solani. Phytopathology 104(1):40–49

    Article  CAS  Google Scholar 

  • Miles TD, Miles LA, Fairchild KL, Wharton PS (2014) Screening and characterization of resistance to succinate dehydrogenase inhibitors in Alternaria solani. Plant Pathol 63(1):155–164

    Article  CAS  Google Scholar 

  • Pasche JS, Gudmestad NC (2008) Prevalence, competitive fitness and impact of the F129L mutation in Alternaria solani from the United States. Crop Prot 27(3–5):427–435

    Article  CAS  Google Scholar 

  • Pasche JS, Piche LM, Gudmestad NC (2005) Effect of the F129L Mutation in Alternaria solani on Fungicides Affecting Mitochondrial Respiration. Plant Dis 89(3):269–278

    Article  CAS  Google Scholar 

  • Pasche JS, Wharam CM, Gudmestad NC (2004) Shift in sensitivity of Alternaria solani in response to QoI fungicides. Plant Dis 88(2):181–187

    Article  CAS  Google Scholar 

  • Price CL, Parker JE, Warrilow AG, Kelly DE, Kelly S (2015) Azole fungicides—understanding resistance mechanisms in agricultural fungal pathogens. Pest Manag Sci 71(8):1054–1058

    Article  CAS  Google Scholar 

  • Pscheidt JW, Stevenson WR (1986) Comparison of forecasting methods for control of potato early blight in Wisconsin. Plant Dis 70(10):915–920

    Article  Google Scholar 

  • Radtke W, Rieckmann W, Brendler F (2000) Kartoffel: Krankheiten – Schädlinge – Unkräuter. Th. Mann, Gelsenkirchen

    Google Scholar 

  • Rotem J (1994) The Genus Alternaria. APS Press, St. Paul

    Google Scholar 

  • Sierotzki H, Wullschleger J, Gisi U (2000) Point mutation in cytochrome b gene conferring resistance to strobilurin fungicides in Erysiphe graminis f.sp. tritici field isolates. Pestic Biochem Physiol 68(2):107–112

    Article  CAS  Google Scholar 

  • Stevenson WR, Loria R, Franc GD, Weingartner DP (eds) (2001) Compendium of Potato Diseases, 2nd edn. APS Press, St. Paul, Minnesota

    Google Scholar 

  • Wharton P, Fairchild K, Belcher A, Wood E (2012) First Report of In-Vitro Boscalid-Resistant Isolates of Alternaria solani Causing Early Blight of Potato in Idaho. Plant Dis 96(3):454

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the colleagues from the Bavarian State agricultural offices for collecting Alternaria diseased potato leaves.

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Correspondence to Michael Zellner.

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M. Nottensteiner, C. Absmeier and M. Zellner declare that they have no competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Nottensteiner, M., Absmeier, C. & Zellner, M. QoI Fungicide Resistance Mutations in Alternaria solani and Alternaria alternata are Fully Established in Potato Growing Areas in Bavaria and Dual Resistance against SDHI Fungicides is Upcoming. Gesunde Pflanzen 71, 155–164 (2019). https://doi.org/10.1007/s10343-019-00475-5

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