Introduction and General Information

The FRAC SDHI Working Group is responsible for common resistance management recommendations for the SDHI fungicides (benodanil, benzovindiflupyr, bixafen, boscalid, carboxin, fenfuram, fluopyram, flutolanil, fluxapyroxad, furametpyr, isofetamid, isopyrazam, mepronil, oxycarboxin, penflufen, penthiopyrad, sedaxane and thifluzamide).

The above-mentioned fungicides are in general cross-resistant and have been grouped under the FRAC Code No. 7 in the revised FRAC Code List.

Code Target site of action Group name Chemical group Common name Comments
7 Complex II;
succinate-
dehydro-
genase
SDHI (Succinate dehydro-
genase inhibitors
Phenyl-benzamides Benodanil
Flutolanil
Mepronil
Resistance
known for
several fungal
species in field
populations and
lab mutants.
Target site
mutations in sdh
gene, e.g. H/Y
(or H/L) at 257* or
P225L**.

Medium-high risk.
Resistance
management
required
phenyl-oxo-ethyl
thiophene amide
Isofetamid
Pyridinyl-ethyl-
benzamide
Fluopyram
Furan-carboxamides Fenfuram
Oxathiin-
carboxamides
Carboxin
Oxycarboxin
Thiazole-
carboxamides
Thifluzamide
Pyrazole-
carboxamides
Benzovindiflupyr
Bixafen
Fluxapyroxad
Furametpyr
Isopyrazam
Penflufen
Penthiopyrad
Sedaxane
Pyridine-
carboxamides
Boscalid

* Ustilago maydis, homolog to 267 in Zymoseptoria tritici and 272 in Botrytis cinerea.
** B. cinerea

SDHI fungicides were discovered more than 40 years ago. Due to the limited disease and application spectrum of the “first generation” carboxamides, resistance under commercial conditions remained limited to a few crop/pathosystems (primarily Basidiomycetes), e.g.Puccinia horiana, chrysanthemum rust, and Ustilago nuda, loose smut in barley.

In addition to these “first generation” molecules,  SDHIs with increased spectrum and potency were launched starting in 2003 and new ones continue to be launched today.  These modern generation SDHIs are rapidly achieving market share in many crops and new SDHIs are currently in development. 

The target enzyme of SDH inhibitors is succinate dehydrogenase (SDH, so-called complex II in the mitochondrial respiration chain), which is a functional part of the tricarboxylic cycle and linked to the mitochondrial electron transport chain (Keon et al., 1991). SDH consists of four subunits (A, B, C and D) and the binding site of  the SDHIs (the ubiquinone binding site) is formed by the subunits B, C and D.  Target site mutations conferring reduced sensitivity can develop in all three subunits.

Mutations conferring resistance


Mutations conferring reduced sensitivity were (and continue to be) identified in a number of pathogens both from field monitoring as well as laboratory mutagenesis studies. Field populations most intensively studied to date include Botrytis cinerea isolated from a number of crops (Yin et al. 2011, Veloukas et al. 2011), cucurbit diseases (McGrath 2008, Miazzi & McGrath 2008, Stevenson et al. 2008, Miyamoto et al. 2009, Ishi et al. 2011, Avenot et al. 2012),  or Alternaria species on different crops  (Avenot et al. 2008 and Avenot et al. 2009, Gudmestad et al. 2013). The market introduction of new SDHIs and more scientific studies will most likely change our current understanding of resistance in these field populations.

Work with isolates from both field and lab studies suggests that cross-resistance patterns between SDHIs for different target site mutations are complex. Different target site mutations confer varying degrees of insensitivity between the different SDHIs. This suggests the effect of these target site mutations on field performance of specific SDHIs may vary if they were to spread in field populations. The various degrees of reduced sensitivity to different target site mutations may be explained by structural differences between classes of SDHIs and how they interact with the target site of a specific pathogen (Scalliet et al. 2012). Additionally, the magnitude of the effect conferred by a specific target site mutation can vary from species to species. In other words, the reduction in sensitivity conferred by specific target site mutations may vary between pathogen species, SDHI used and geographic location of the isolates (Sierotzki and Scalliet 2013).  

Current Resistance Status (2014)


In pathogens where isolates with reduced sensitivity were detected under field conditions, the current resistance status of the population is shifting as disease pattern/severity  and product usage across multiple modes of action changes from year to year.  Monitoring at the regional level in specific crop/pathosystems is crucial to understand the resistance status at any given time.  As mentioned above, it is also important to understand how the different members of the SDHI group will respond to specific target site mutations within that species and the frequency of those mutations in the field population when deciding on specific product usage.  

Isolates with reduced sensitivity were identified in field populations of Alternaria alternata on nut crops in the US (Avenot et al., 2008 and 2009), A. solani on potatoes in the US (Gudemstad et al., 2013), Botrytis cinerea from apple (Yin et al., 2011), kiwi (Bardas et al., 2010), and strawberry (Veloukas et al. 2011 and 2013), Corynespora cassicola on cucurbits in Japan (Miyamoto et al., 2009 and Ishii et al., 2011), Didymella bryoniae on cucurbits in the US (Avenot et al., 2012), and Podosphaeria xanthii in the US (Miazzi and McGrath 2008) and Japan (Miyamoto et al, 2010 and 2011).  Reduced field efficacy of certain SDHIs was reported for all of these species. 

In addition, field isolates with target site mutations conferring reduced sensitivity were identified during routine monitoring in Europe in B. cinerea in grapes, Venturia ineaqualis in apples, Pyrenophora teres in barley, Mycospharella graminicola in wheat and Sclerotinia sclerotiorum on oilseed rape.  Many of the identified mutations have low to moderate resistance factors for commercially available SDHIs and the frequency of the resistant mutations remains low in the population.  Reports on field performance of the SDHIs remained good in 2014 (MInutes of the 2014 SDHI Meeting, Recommendations for 2015).  These early monitoring reports of isolates with reduced sensitivity emphasize the need to abide by resistance management guidelines to prolong the life of the SDHIs.  


References


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

Avenot H, Sellam A, Michailides T. 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 pathology 2009; 58(6): 1134-1143.

Avenot HF, Thomas A, Gitaitis RD, Langston Jr. DB, Stevenson KL Molecular characterization of boscalid‐and penthiopyrad‐resistant isolates of Didymella bryoniae and assessment of their sensitivity to fluopyram. Pest management science 2012 ; 68(4) : 645-651.

Bardas GA, Veloukas T, Koutita O, Karaoglanidis GS. Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest management science 2010; 66(9): 967-973.

Gudmestad NC, Arabiat S, Miller JS, Pasche JS. Prevalence and Impact of SDHI Fungicide Resistance in Alternaria solani. Plant Disease 2013; 97: 952-960.

Ishii H, Miyamoto T, Ushio S, Kakishima M. Lack of cross‐resistance to a novel succinate dehydrogenase inhibitor, fluopyram, in highly boscalid‐resistant isolates of Corynespora cassiicola and Podosphaera xanthii.  Pest management science 2011; 67(4): 474-482.

Keon JPR, White GA, Hargreaves JA. Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis. Current Genetics 1991; 19: 475-481.

McGrath MT. Fungicide sensitivity in Podosphaera xanthii and efficacy for cucurbit powdery mildew in NY, USA, in 2003-2006. Journal of Plant Pathology 2008; 90:90.

Miazzi M, McGrath MT. Sensitivity of Podosphaera xanthii to registered fungicides and experimentals in GA and NY, USA, in 2007.  Journal of Plant Pathology 2008; 90:2.

Miyamoto, T., Ishii, H., Seko, T., Kobori, S., & Tomita, Y. (2009). Occurrence of Corynespora cassiicola isolates resistant to boscalid on cucumber in Ibaraki Prefecture, Japan. Plant Pathology, 58(6), 1144-1151.

Miyamoto T, Ishii H, Tomita Y. Occurrence of boscalid resistance in cucumber powdery mildew in Japan and molecular characterization of the iron–sulfur protein of succinate dehydrogenase of the causal fungus. Journal of General Plant Pathology 2010: 76(4): 261-267.

Scalliet G, Bowler J, Luksch T, Kirchhofer-Allan L, Steinhauer D, Ward, K., Niklaus M, Verras A, Csukai M, Daina A, Fonné-Pfister, R. Mutagenesis and functional studies with succinate dehydrogenase inhibitors in the wheat pathogen Mycosphaerella graminicola. PloS one 2012; 7(4): e35429.

Sierotzki H, Scalliet G. A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides.Phytopathology 2013; 103(9): 880-887.

Stammler G, Brix HD, Glaettli A, Semar M, Schoefl U. Biological properties of the carboxamide boscalid including recent studies on its mode of action. In XVI International Plant Protection Congress, Glasgow, 2007. pp 40-45.

Stevenson KL, Langston DB Jr., Sanders F. Baseline sensitivity and evidence of resistance to boscalid in Didymella bryoniae. (Abstr.) Phytopathology 2008; 98: S151.

Veloukas T, Leroch M, Hahn M, Karaoglanidis GS. Detection and molecular characterization of boscalid-resistant Botrytis cinerea isolates from strawberry. Plant Disease 2011; 95(10): 1302-1307.

Veloukas T, Markoglou AN, Karaoglanidis GS. Differential effect of SdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea. Plant Disease 2013; 97 (1): 118-122.

Yin YN, Kim YK, Xiao CL. Molecular characterization of boscalid resistance in field isolates of Botrytis cinerea from apple. Phytopathology 2011; 101(8): 986-995.

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Dr. Kristin Klappach
Chair

BASF SE
Agricultural Research Station Limburgerhof
D-67114 Limburgerhof,
Germany

Tel: +49 62160- 27287 Fax: +49 62160- 6627287

E-Mail: Dr. K. Klappach