Res. Plant Dis > Volume 26(1); 2020 > Article
Sang and Lee: Molecular Mechanisms of Succinate Dehydrogenase Inhibitor Resistance in Phytopathogenic Fungi

ABSTRACT

The succinate dehydrogenase inhibitor (SDHI) is a class of fungicides, which is widely and rapidly used to manage fungal pathogens in the agriculture field. Currently, fungicide resistance to SDHIs has been developed in many different plant pathogenic fungi, causing diseases on crops, fruits, vegetables, and turf. Understanding the molecular mechanisms of fungicide resistance is important for effective prevention and resistance management strategies. Two different mechanisms have currently been known in SDHI resistance. The SDHI target genes, SdhB, SdhC, and SdhD, mutation(s) confer resistance to SDHIs. In addition, overexpression of ABC transporters is involved in reduced sensitivity to SDHI fungicides. In this review, the current status of SDHI resistance mechanisms in phytopathogenic fungi is discussed.

Introduction

The current broad-spectrum fungicides for control of fungal diseases include sterol demethylation inhibitors (DMIs), quinone-outside inhibitors (QoIs), and succinate dehydrogenase inhibitors (SDHIs). DMIs and QoIs have been used at least 3-4 decades, and resistance to DMIs and QoIs has been reported in many pathogenic fungi. SDHIs are relatively new fungicide classes than DMIs and QoIs and have been rapidly adopted by the fungicide market in the agricultural field. However, repeated applications of SDHIs have led to develop resistance to SDHIs in economically important fungal pathogens, such as Botrytis cinerea and Zymoseptoria tritici. The recent review paper of SDHI resistance was written by Sierotzki and Scalliet (2013), which described the mode of action of SDHIs and different aspects of SDHI resistance. Although the Fungicide Resistance Action Committee reports the status of SDHI resistance every year, the lists of reported fungal pathogens with SDHI resistance are not all included. This review describes the current knowledge of SDHI resistance and the resistance mechanisms in plant pathogenic fungi.

SDHI Fungicides

The mode of action of SDHIs is the inhibition of fungal respiration by blocking the ubiquinone-binding (Qp) site. The Qp pocket is structurally defined by the interface between the succinate dehydrogenase (SDH) enzymes (succinate ubiquinone oxidoreductase [EC 1.3.5.1]), SdhB, SdhC, and SdhD subunits (Avenot and Michailides, 2010; Sierotzki and Scalliet, 2013). The first generation of SDHIs is carboxin and oxycarboxin and has been applied to control basidiomycete plant pathogens (e.g., Rhizoctonia sp. and rusts) (Avenot and Michailides, 2010; Von Schmeling and Kulka, 1966). The newer generation SDHIs such as boscalid, penthiopyrad, fluopyram, and fluxapyroxad are the broader-spectrum fungicides against fungal pathogens of various crops, fruits, vegetables and turf (Avenot and Michailides, 2010; Sierotzki and Scalliet, 2013). Currently, 23 different compounds (benodanil, flutolanil, mepronil, isofetamid, fluopyram, fenfuram, carboxin, oxycarboxin, thifluzamide, benzovindiflupyr, bixafen, fluindapyr, fluxapyroxad, furametpyr, inpyrfluxam, isopyrazam, penflufen, penthiopyrad, sedaxane, isoflucypram, pydiflumetofen, boscalid, and pyraziflumid) in the 11 difference chemical group of SDHIs have been listed in Fungicide Resistance Action Committee (2020). Chemical group of fungicides such as penthiopyrad and bixafen have exerted high selection pressure to fungal pathogens on different plant hosts, but some SDHIs like fluopryam displays higher activity against pathogens on broad leaved than graminaceous hosts (Sierotzki and Scalliet, 2013). The main molecular mechanism of SDHI resistance in fungi is the mutation(s) in the SDHI target genes, SdhB, SdhC, and SdhD, resulting in a decreased in binding affinity for SDHI fungicides. Also, overexpression of efflux transporter(s) in fungal species causes a reduced intracellular accumulation of SDHI fungicides, which confers reduced sensitivity to SDHI fungicides (Fig. 1).

Mechanisms of SDHI Resistance: Mutations in the SDHI Target Genes (SdhB, SdhC, and SdhD)

Resistance in Alternaria alternata and A. solani.

In Alternaria species, field resistance of A. alternata and A. solani to SDHIs have been mainly reported and mutations in the SDHI target genes (SdhB, SdhC, and SdhD) in the field resistant isolates were detected (Avenot et al., 2019; Bauske et al., 2018; Fan et al., 2015; Gudmestad et al., 2013; Yang et al., 2015). SDHI fungicides have been applied to pistachio and peach orchards to control Alternaria late blight and Alternaria brown spot caused by A. alternata, respectively. The first report of SDHI resistance in A. alternata was from pistachio orchards after only 2 years of use of the boscalid-containing product Pristine (Avenot and Michailides, 2007). A mutation (H277Y or H277R) in SdhB found in A. alternata field strains from pistachio was correlated with boscalid resistance (Avenot et al., 2008). Following the first mutation detection, Avenot et al. (2009) found various mutations in SdhB (H277Y/R/L, P230A/R/I/F/ D, and N235D/T/E/G), SdhC (H133R, H134R, and S135R), and SdhD (D123E and H133P/R) from the SDHI fungicide resistant alternata field isolates (Avenot et al., 2009, 2014, 2019). In peach orchards, A. alternata SDHI-resistant isolates harbored mutations in SdhB (H277Y/R/L), SdhC (G79R and H134R), and SdhD (A47T and D123E). The sensitivity assay of the resistant isolates revealed that mutations in SdhB (H277Y/R) and SdhC (H134R) were consistently correlated with the phenotype exhibiting the high level of resistance to boscalid. Mutations SdhC (H134R) and SdhD (D123E) were associated with high resistance to penthiopyrad and the isolates containing SdhB (H277L) or SdhC (H134R) showed the highest resistance level to boscalid, fluopyram, penthiopyrad, and fluxapyroxad among the strains from peach orchards (Yang et al., 2015). The study of fitness of A. alternata field isolates indicated that genotypes of SdhB (H277Y) and SdhC (H134R) do not suffer the fitness penalties on growth, spore production, osmotic and oxidative sensitivity, and pathogenicity but the SdhD (D123E) genotype displayed hypersensitive to oxidative stress and lower production of spores (Fan et al., 2015).
Resistance of A. solani to boscaild was reported from various potato production regions (Florida, Idaho, Minnesota, Nebraska, North Dakota, Texas, and Wisconsin) in the United States in 2010 and 2011 (Gudmestad et al., 2013). The same research group investigated the sequences of SdhB, SdhC, and SdhD of boscalid resistant A. solani isolates and detected the mutations in SdhB (H278Y/R), SdhC (H134R), and SdhD (D123E and H133R) (Mallik et al., 2014). Bauske et al. (2018) described the temporal and spatial distribution of these Sdh gene mutations. The SdhB (H278Y/R) were the most prevalent distributed mutations from 2010 to 2011 in the sampled states, but the SdhC (H134R) was the most prevalent mutation from 2013 to 2015. The strains with SdhB (H278Y/R) were highly collected in North Dakota, Minnesota, and Wisconsin, but the strains with SdhC (H134R) were prevalently distributed in Colorado, Texas, North Dakota, and Minnesota (Bauske et al., 2018). In addition, the parasitic fitness study of A. solani strains revealed that the five Sdh gene mutations do not confer fitness penalties, and only the SDHI-resistant strain containing the D123E mutation exhibited more aggressiveness on tomato leaves than the sensitive strain (Bauske and Gudmestad, 2018). Interestingly, the strains containing the D123E mutation were highly resistant to boscalid but sensitive to fluopyram (Bauske et al., 2018; Mallik et al., 2014), which supports that a lack of cross-resistance between boscalid and fluopryam in other studies (Fairchild et al., 2013; Gudmestad et al., 2013; Mallik et al., 2014; Miles et al., 2014).

Resistance in Botrytis cinerea.

Gray mold caused by Botrytis cinerea is the devastating disease on more than 230 host plants including economically important fruits, such as apples, grapes, and strawberries (Jarvis, 1977). The SDHI resistance in B. cinerea has been mostly reported in apple orchards, vineyard, and strawberry farms (Kim and Xiao, 2010; Leroch et al., 2011; Leroux et al., 2010; Veloukas et al., 2011). Also, B. cinerea isolates exhibiting resistance to multiple fungicides including boasclid were reported from kiwifruits (Bardas et al., 2010). The molecular mechanism of SDHI resistance in the B. cinerea field isolates was investigated; mutations (SdhB: N230I, H272Y/R/L, and P25F) in the isolates from strawberry farms (Veloukas et al., 2011), mutations (SdhB: P225L, N230I, and H272Y/R/L) in isolates from the vineyards (Leroux et al., 2010) and mutations in the isolates from apple orchards (Yin et al., 2011) were discovered in the B. cinerea field resistant isolates. Since the initial detection of mutations in Sdh genes of B. cinerea, the SdhB (P225F/H/L/T), SdhB (N230I), and SdhB (H272Y/L/R) mutation mutants exhibiting resistance to SDHIs have been found in China, Greece, Italy, Spain, and the United States (Amiri et al., 2014; De Miccolis Angelini et al., 2014; Fan et al., 2015; Fernández-Ortuño et al., 2017; Grabke and Stammler, 2015; Hu et al., 2016; Li et al., 2014; Veloukas et al., 2013). In the study of Veloukas et al. (2013), the sensitivity of B. cinerea strains harboring five different mutations in SdhB were assayed to eight SDHI fungicides (boscalid, isopyrazam, fenfuram, carboxin, fluopyram, bixafen, fluxapyroxad, and benodanil). The mutation SdhB (P225F) conferred resistance to all eight fungicides, but mutation SdhB (N230I) conferred moderate resistance to boscalid, fluopyram, fluxapyroxad and low resistance to isopyrazam, bixafen, fenfuram, benodanil, and carboxin. The strains with different mutations of SdhB (H272L/R/Y) in the same codon exhibited different patterns of sensitivity to SDHI fungicides. Especially, the SdhB (H272Y) mutants showing resistance to bosclid and low resistance to isopyrazam, biafen, fenfuram, and carboxin displayed increased sensitivity to benodanil and fluopyram. Velouskas et al. (2013) suggested that the benzamide derivatives benodanil and fluopyram might bind better in the Q-pocket of strains containing a tyrosine at the codon 272.

Resistance in Zymoseptoria tritici.

Septoria tritici blotch (STB), caused by Zymoseptoria tritici (synonym. Mycosphaerella graminicola, Septoria tritici), is an economically important wheat disease worldwide (Eyal et al., 1987). SDHI fungicides have been applied to wheat fields for controlling STB several years, but the fungal populations resistant to SDHIs have been detected in Europe. The SDHI-resistant strains collected from Europe contained several mutations in SdhB (N225T and T268I) and SdhC (T79N, W80S, N86S, H152R, and V166M). The microtitre and curative greenhouse tests of mutants indicated that the SdhC (H152R) mutants showed the highest resistance levels to all SDHIs tested (fluxapyroxad, fluopyram, isopyrazam, bixafen, benzovindiflupyr, and penthiopyrad) and lower efficacy to SDHIs than other mutants (Rehfus et al., 2018). Yamashita and Fraaije (2018) investigated cross-resistance of lab mutants and field strains of Z. tritici to SDHIs. The lab mutants harboring SdhC (A84V) exhibited resistance both fluopyram and isofetamid. Interestingly, the field resistant strains showed the similar phenotype as the lab mutants but did not contain any mutations in SdhB, SdhC, and SdhD. They also found these field resistant strains in Europe and New Zealand before applications of SDHIs widely. This study is the first report of non-target site SDHI resistance (Yamashita and Fraaije, 2018).

Resistance in other phytopathogenic fungi.

Due to wide applications of SDHIs to various hosts, many other fungal pathogens have developed resistance to SDHIs. In cucurbits, the SDHI resistance mechanisms of three different plant pathogens (Corynespora cassicola, Podosphaera xanthii, and Didymella bryoniae) have been reported (Avenot et al., 2012; Miyamoto et al., 2010a, 2010b). Resistance of Corynespora cassicola, the causal agent of corynespora leaf spot, to boscalid was firstly reported in Japan, and mutations in SdhB (H278Y/R) and SdhC (S73P) were detected by sequencing analysis of Sdh genes (Miyamoto et al., 2009, 2010a). Cucumber powdery mildew fungus (Podosphaera xanthii) showing resistance to boscalid also contained an amino acid substitution (histidine to tyrosine) in a third cysteine-rich center in SdhB (homologous to H272 in B. cinerea) (Miyamoto et al., 2010b). Two mutations (SdhB-H277Y and H277R) were found in the field SDHI-resistant isolates of Didymella bryoniae, causing gummy stem blight of cucurbits, in the United States (Avenot et al., 2012).
Recently, mechanisms of SDHI resistance have been reported in Pyrenophora teres (the causal agent of barley net blotch), Clarireedia homoeocarpa (the causal agent of dollar spot) and Blumeriella jaapii (the causal agent of cherry leaf spot) (Outwater et al., 2019; Popko et al., 2018; Rehfus et al., 2016). Several mutations (SdhB: H277Y; SdhC: N75S, G79R, H134R, and S135R; SdhD: D124N/E, H134R, and D145G) were associated with SDHI resistance in Pyrenophora teres (Rehfus et al., 2016), and a single mutation (SdhB: H260R) was correlated with boscalid resistance in Michigan populations of Blumeriella jaapii (Outwater et al., 2019). In Clarireedia homoeocarpa (previously Sclerotinia homoeocarpa), three different mutations (SdhB: H267Y, SdhC: G91R, and SdhC: G150R) were detected in the resistant isolates collected from golf courses in the United States and Japan. The involvement of three mutations in SDHI resistance was genetically confirmed through the fungal transformation system (Popko et al., 2018). The Fungicide Resistance Action Committee also listed the reported SDHI resistance and mutations in the Sdh genes in phytopathogenic fungi including Botrytis elliptica, Sclerotinia sclerotiorum, Stemphylium vesicarium, and Venturia inaequalis (Fungicide Resistance Action Committee, 2015). The fungal species and Sdh gene mutations described in this study are listed in Table 1.

Mechanisms of SDHI Resistance: Overexpression of Efflux Pump Transporters

During monitoring and mechanism studies of fungicide resistance in C. homoeocarpa, the field isolates exhibiting reduced sensitivity to propiconazole, iprodione, boscalid and flurprimidol were found (Popko et al., 2012; Sang et al., 2015, 2018). These multidrug-resistant isolates overexpressed two ABC efflux transporters (ShatrD and ShPDR1), which were involved in reduced sensitivity to various fungicides including SDHIs (Fig. 1). A mutation (M853T) in the transcription factor ShXDR1 in these resistant isolates conferred overexpression of CYP450s and ABC transporters, resulting in multidrug resistance. This is the first study of SDHI resistance mechanism by efflux pump transporters (Sang et al., 2018) (Table 1). In B. cinerea, the multidrug-resistant strains overexpressing efflux transporters were prevalent in vineyards of Germany (Kretschmer et al., 2009). There were three types of multidrug-resistant strains, which are MDR1 type strains (overexpression of ABC transporters atrB), MDR2 type strains (overexpression of MFS transporters MFS2) and MDR3 type strains (overexpressing both transporters) (Kretschmer et al., 2009; Leroch et al., 2011). The MDR1 type strains were not significantly associated with reduced sensitivity to boscalid, and the MDR 2 and 3 types showed slightly reduced sensitivity to boscalid (Kretschmer et al., 2009). The differences of SDHI resistance by multidrug resistance mechanisms between the ABC transporters in C. homoeocarpa and B. cinerea might be that each transporter has different substrate specificity.

Conclusion

This diversity of target gene mutations and multidrug resistance mechanisms makes resistance management difficult. Since each mutation has a different effect on cross-resistance patterns to SDHIs, the rapid detection of mutation(s) in the fungal populations is necessary to manage SDHI resistance. Currently, allele-specific real-time PCR assay has been developed for the quantitative detection of different SDHI-resistant genotypes (De Miccolis Angelini et al., 2014). Also, several SdhB mutations in B. cinerea were accurately and rapidly detected using high resolution melting analysis (Samaras et al., 2016). Together with such molecular characterization and rapid detection of SDHI mutations, use of a limited number of fungicides and strategic applications of chemical rotation and combination based on mode of action are required to prolong the field efficacy of SDHIs.

Acknowledgments

This work was supported by two grants from the Rural Development Administration of Korea (PJ01483603) and National Research Foundation of Korea (2020R1C1C1010108).

NOTES

Conflicts of Interest

No potential conflict of interest relevant to this article was reported

Fig. 1
Molecular mechanisms of succinate dehydrogenase inhibitor (SDHI) resistance in plant pathogenic fungi. (A) Mutation(s) in the SdhB, SdhC, and SdhD results in a decreased in binding affinity for SDHI fungicides. (B) Overexpression of efflux transporters causes a reduced intracellular accumulation of SDHI fungicides. The illustration was created using a web app, BioRender (http:// www.biorender.com).
RPD-26-001-f1.jpg
Table 1
SDHI resistance and molecular mechanisms reported in phytopathogenic fungi
Species Host Resistance mechanism Reference
Alternaria alternata Pistachio SdhB: H277Y/R/L, P230A/R/I/F/D, N235D/T/E/G Avenot et al. (2008)
SdhC: H133R, H134R, S135R Avenot et al. (2009)
SdhD: D123E, H133P/R Avenot et al. (2014)
Avenot et al. (2019)
Alternaria alternata Peach SdhB: H277Y/R/L Yang et al. (2015)
SdhC: G79R, H134R Fan et al. (2015)
SdhD: A47T, D123E
Alternaria solani Potato SdhB: H278Y/R Mallik et al. (2014)
SdhC: H134R
SdhD: D123E, H133R
Botrytis cinerea Apple SdhB: H272Y/L/R Yin et al. (2011)
Botrytis cinerea Grape SdhB: P225L, N230I, H272Y/R/L Leroux et al. (2010)
SdhD: H132R
Botrytis cinerea Strawberry SdhB: P225F/H/L/T Amiri et al. (2014)
SdhB: N230I Hu et al. (2016)
SdhB: H272Y/L/R Fernández-Ortuño et al. (2017)
Veloukas et al. (2011)
Botrytis elliptica Lily SdhB: 272Y/R Fungicide Resistance Action Committee (2015)
Blumeriella jaapii Cherry SdhB: H260R Outwater et al. (2019)
Clarireedia homoeocarpa Turf SdhB: H267Y Popko et al. (2018)
SdhC: G91R Sang et al. (2015)
SdhC: G150R Sang et al. (2018)
Overexpression of ABC transporters, ShPDR1 andShatrD
Corynespora cassiicola Cucurbits SdhB: H278Y/R Miyamoto et al. (2010a)
SdhC: S73P
SdhD: S89P, G109V
Didymella bryoniae Cucurbits SdhB: H277R/Y Avenot et al. (2012)
Podosphaera xanthii Cucurbits SdhB: H to Y (homologous to H272 in B. cinerea) Miyamoto et al. (2010b)
Pyrenophora teres Barley SdhB: H277Y Rehfus et al. (2016)
SdhC: N75S, G79R, H134R, S135R
SdhD: D124N/E, H134R, D145G
Sclerotinia sclerotiorum Oilseed rape SdhB: H273Y Fungicide Resistance Action Committee (2015)
SdhC: H146R
SdhD: H132R
Stemphylium vesicarium Asparagus SdhB: P225L Fungicide Resistance Action Committee (2015)
SdhB: H272Y/R
Venturia inaequalis Apple SdhC: H151R Fungicide Resistance Action Committee (2015)
Zymoseptoria tritici Wheat SdhB: N225T, T268I; SdhC: T79N, W80S, N86S, V166M, H152R Rehfus et al. (2018)
Alternaria alternata Pistachio SdhB: H277Y/R/L, P230A/R/I/F/D, N235D/T/E/G Avenot et al. (2008)
SdhC: H133R, H134R, S135R Avenot et al. (2009)
SdhD: D123E, H133P/R Avenot et al. (2014)
Avenot et al. (2019)
Alternaria alternata Peach SdhB: H277Y/R/L Yang et al. (2015)
SdhC: G79R, H134R Fan et al. (2015)
SdhD: A47T, D123E
Alternaria solani Potato SdhB: H278Y/R Mallik et al. (2014)
SdhC: H134R
SdhD: D123E, H133R
Botrytis cinerea Apple SdhB: H272Y/L/R Yin et al. (2011)
Botrytis cinerea Grape SdhB: P225L, N230I, H272Y/R/L Leroux et al. (2010)
SdhD: H132R
Botrytis cinerea Strawberry SdhB: P225F/H/L/T Amiri et al. (2014)
SdhB: N230I Hu et al. (2016)
SdhB: H272Y/L/R Fernández-Ortuño et al. (2017)
Veloukas et al. (2011)
Botrytis elliptica Lily SdhB: 272Y/R Fungicide Resistance Action Committee (2015)
Blumeriella jaapii Cherry SdhB: H260R Outwater et al. (2019)
Clarireedia homoeocarpa Turf SdhB: H267Y Popko et al. (2018)
SdhC: G91R Sang et al. (2015)
SdhC: G150R Sang et al. (2018)
Overexpression of ABC transporters, ShPDR1 andShatrD
Corynespora cassiicola Cucurbits SdhB: H278Y/R Miyamoto et al. (2010a)
SdhC: S73P
SdhD: S89P, G109V
Didymella bryoniae Cucurbits SdhB: H277R/Y Avenot et al. (2012)
Podosphaera xanthii Cucurbits SdhB: H to Y (homologous to H272 in B. cinerea) Miyamoto et al. (2010b)
Pyrenophora teres Barley SdhB: H277Y Rehfus et al. (2016)
SdhC: N75S, G79R, H134R, S135R
SdhD: D124N/E, H134R, D145G
Sclerotinia sclerotiorum Oilseed rape SdhB: H273Y Fungicide Resistance Action Committee (2015)
SdhC: H146R
SdhD: H132R
Stemphylium vesicarium Asparagus SdhB: P225L Fungicide Resistance Action Committee (2015)
SdhB: H272Y/R
Venturia inaequalis Apple SdhC: H151R Fungicide Resistance Action Committee (2015)
Zymoseptoria tritici Wheat SdhB: N225T, T268I; SdhC: T79N, W80S, N86S, V166M, H152R Rehfus et al. (2018)

SDHI, succinate dehydrogenase inhibitor.

References

Amiri, A., Heath, S. M. and Peres, N. A. 2014. Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinereafrom strawberry. Plant Dis. 98: 532-539.
crossref pmid
Avenot, H., Sellam, A. and Michailides, T. 2009. Characterization of mutations in the membrane-anchored subunits AaSDHC and AaSDHD of succinate dehydrogenase from Alternaria alternataisolates conferring field resistance to the fungicide boscalid. Plant Pathol. 58: 1134-1143.
crossref
Avenot, H. F., den Biggelaar, H., Morgan, D. P., Moral, J., Joosten, M. and Michailides, T. J. 2014. Sensitivities of baseline isolates and boscalid-resistant mutants of Alternaria alternatafrom pistachio to fluopyram, penthiopyrad, and fluxapyroxad. Plant Dis. 98: 197-205.
crossref pmid
Avenot, H. F., Luna, M. and Michailides, T. J. 2019. Phenotypic and molecular characterization of resistance to the SDHI fungicide fluopyram in populations of Alternaria alternatafrom pistachio orchards in California. Crop Prot. 124: 104838
crossref
Avenot, H. F. and Michailides, T. J. 2007. Resistance to boscalid fungicide in Alternaria alternataisolates from pistachio in California. Plant Dis. 91: 1345-1350.
crossref pmid
Avenot, H. F. and Michailides, T. J. 2010. Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot. 29: 643-651.
crossref
Avenot, H. F., Sellam, A., Karaoglanidis, G. and Michailides, T. J. 2008. Characterization of mutations in the iron-sulphur subunit of succinate dehydrogenase correlating with boscalid resistance in Alternaria alternatafrom California pistachio. Phytopathology. 98: 736-742.
crossref pmid
Avenot, H. F., Thomas, A., Gitaitis, R. D., Langston, D. B. and Stevenson, K. L. 2012. Molecular characterization of boscalidand penthiopyrad-resistant isolates of Didymella bryoniaeand assessment of their sensitivity to fluopyram. Pest Manag. Sci. 68: 645-651.
crossref pmid
Bardas, G. A., Veloukas, T., Koutita, O. and Karaoglanidis, G. S. 2010. Multiple resistance of Botrytis cinereafrom kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Manag. Sci. 66: 967-973.
crossref pmid
Bauske, M. J. and Gudmestad, N. C. 2018. Parasitic fitness of fungicide-resistant and -sensitive isolates of Alternaria solani . Plant Dis. 102: 666-673.
crossref pmid
Bauske, M. J., Mallik, I., Yellareddygari, S. K. and Gudmestad, N. C. 2018. Spatial and temporal distribution of mutations conferring QoI and SDHI resistance in Alternaria solaniacross the United States. Plant Dis. 102: 349-358.
crossref pmid
De Miccolis Angelini, R. M., Masiello, M., Rotolo, C., Pollastro, S. and Faretra, F. 2014. Molecular characterisation and detection of resistance to succinate dehydrogenase inhibitor fungicides in Botryotinia fuckeliana(Botrytis cinerea). Pest Manag. Sci. 70: 1884-1893.
crossref pmid
Eyal, Z., Scharen, A. L., Prescott, J. M.Van Ginkel, M. 1987. The Septoria Diseases of Wheat: Concepts and Methods of Disease Management. CIMMYT, Mexico. p. 51.
Fairchild, K. L., Miles, T. D. and Wharton, P. S. 2013. Assessing fungicide resistance in populations of Alternariain Idaho potato fields. Crop Prot. 49: 31-39.
crossref
Fan, Z., Yang, J.-H., Fan, F., Luo, C.-X. and Schnabel, G. 2015. Fitness and competitive ability of Alternaria alternatafield isolates with resistance to SDHI, QoI, and MBC fungicides. Plant Dis. 99: 1744-1750.
crossref pmid
Fernández-Ortuño, D., Pérez-García, A., Chamorro, M., la Peña, E., de Vicente, A. and Torés, J. A. 2017. Resistance to the SDHI fungicides boscalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinereafrom commercial strawberry fields in Spain. Plant Dis. 101: 1306-1313.
crossref pmid
Fungicide Resistance Action Committee. 2015 List of species of resistant to SDHIs. URL https://www.frac.info/docs/default-source/working-groups/sdhi-references/list-of-species-resistant-to-sdhis-april-2015.pdf?.sfvrsn=2d144a9a_2 . [26 March 2020].
Fungicide Resistance Action Committee. 2020 FRAC Code List 2020: fungal control agents sorted by cross resistance pattern and mode of action (including FRAC Code numbering). URL https://www.frac.info/docs/default-source/publications/frac-code-list/frac-code-list-2020-final.pdf?.sfvrsn=8301499a_2 . [26 March 2020].
Grabke, A. and Stammler, G. 2015. A Botrytis cinereapopulation from a single strawberry field in Germany has a complex fungicide resistance pattern. Plant Dis. 99: 1078-1086.
crossref pmid
Gudmestad, N. C., Arabiat, S., Miller, J. S. and Pasche, J. S. 2013. Prevalence and impact of SDHI fungicide resistance in Alternaria solani . Plant Dis. 97: 952-960.
crossref pmid
Hu, M.-J., Fernández-Ortuño, D. and Schnabel, G. 2016. Monitoring resistance to SDHI fungicides in Botrytis cinereafrom strawberry fields. Plant Dis. 100: 959-965.
crossref pmid
Jarvis, W. R. 1977. Botryotiniaand BotrytisSpecies: Taxonomy, Physiology and Pathogenicity. Monograph No. 15. Research Branch, Canada Department of Agriculture, Ottawa, Canada. p. 195.
Kim, Y. K. and Xiao, C. L. 2010. Resistance to pyraclostrobin and boscalid in populations of Botrytis cinereafrom stored apples in Washington State. Plant Dis. 94: 604-612.
crossref pmid
Kretschmer, M., Leroch, M., Mosbach, A., Walker, A. S., Fillinger, S., Mernke, D. and et al. 2009. Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea . PLoS Pathog. 5: e1000696.
crossref
Leroch, M., Kretschmer, M. and Hahn, M. 2011. Fungicide resistance phenotypes of Botrytis cinereaisolates from commercial vineyards in South West Germany. J. Phytopathol. 159: 63-65.
crossref
Leroux, P., Gredt, M., Leroch, M. and Walker, A.-S. 2010. Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Appl. Environ. Microbiol. 76: 6615-6630.
crossref pmid pmc
Li, X., Fernández-Ortuño, D., Chen, S., Grabke, A., Luo, C.-X., Bridges, W. C. and et al. 2014. Location-specific fungicide resistance profiles and evidence for stepwise accumulation of resistance in Botrytis cinerea . Plant Dis. 98: 1066-1074.
crossref pmid
Mallik, I., Arabiat, S., Pasche, J. S., Bolton, M. D., Patel, J. S. and Gudmestad, N. C. 2014. Molecular characterization and detection of mutations associated with resistance to succinate dehydrogenase-inhibiting fungicides in. Alternaria solani. Phytopathology. 104: 40-49.
crossref
Miles, T. D., Miles, L. A., Fairchild, K. L. and Wharton, P. S. 2014. Screening and characterization of resistance to succinate dehydrogenase inhibitors in Alternaria solani . Plant Pathol. 63: 155-164.
crossref
Miyamoto, T., Ishii, H., Seko, T., Kobori, S. and Tomita, Y. 2009. Occurrence of Corynespora cassiicolaisolates resistant to boscalid on cucumber in Ibaraki Prefecture, Japan. Plant Pathol. 58: 1144-1151.
crossref
Miyamoto, T., Ishii, H., Stammler, G., Koch, A., Ogawara, T., Tomita, Y. and et al. 2010a. Distribution and molecular characterization of Corynespora cassiicolaisolates resistant to boscalid. Plant Pathol. 59: 873-881.
crossref
Miyamoto, T., Ishii, H. and Tomita, Y. 2010b. 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. J. Gen. Plant Pathol. 76: 261-267.
crossref
Outwater, C. A., Proffer, T. J., Rothwell, N. L., Peng, J. and Sundin, G. W. 2019. Boscalid resistance in Blumeriella jaapii: distribution, effect on field efficacy, and molecular characterization. Plant Dis. 103: 1112-1118.
crossref pmid
Popko, J. T., Ok, C.-H., Campbell-Nelson, K. and Jung, G. 2012. The association between in vitro propiconazole sensitivity and field efficacy of five New England Sclerotinia homoeocarpapopulations. Plant Dis. 96: 552-561.
crossref pmid
Popko, J. T., Sang, H., Lee, J., Yamada, T., Hoshino, Y. and Jung, G. 2018. Resistance of Sclerotinia homoeocarpafield isolates to succinate dehydrogenase inhibitor fungicides. Plant Dis. 102: 2625-2631.
crossref pmid
Rehfus, A., Miessner, S., Achenbach, J., Strobel, D., Bryson, R. and Stammler, G. 2016. Emergence of succinate dehydrogenase inhibitor resistance of Pyrenophora teresin Europe. Pest Manag. Sci. 72: 1977-1988.
crossref pmid
Rehfus, A., Strobel, D., Bryson, R. and Stammler, G. 2018. Mutations in sdhgenes in field isolates of Zymoseptoria triticiand impact on the sensitivity to various succinate dehydrogenase inhibitors. Plant Pathol. 67: 175-180.
crossref
Samaras, A., Madesis, P. and Karaoglanidis, G. S. 2016. Detection of sdhB gene mutations in SDHI-resistant isolates of Botrytis cinereausing high resolution melting (HRM) analysis. Front. Microbiol. 7: 1815
pmid pmc
Sang, H., Hulvey, J. P., Green, R., Xu, H., Im, J., Chang, T. and et al. 2018. A xenobiotic detoxification pathway through transcriptional regulation in filamentous fungi. mBio. 9: e00457-18.
crossref pmid pmc
Sang, H., Hulvey, J., Popko, J. T., Lopes, J., Swaminathan, A., Chang, T. and et al. 2015. A pleiotropic drug resistance transporter is involved in reduced sensitivity to multiple fungicide classes in Sclerotinia homoeocarpa(F.TBennett). Mol. Plant Pathol. 16: 251-261.
crossref pmid
Sierotzki, H. and Scalliet, G. 2013. A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology. 103: 880-887.
crossref pmid
Veloukas, T., Leroch, M., Hahn, M. and Karaoglanidis, G. S. 2011. Detection and molecular characterization of boscalid-resistant Botrytis cinereaisolates from strawberry. Plant Dis. 95: 1302-1307.
crossref pmid
Veloukas, T., Markoglou, A. N. and Karaoglanidis, G. S. 2013. Differential effect of SdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea . Plant Dis. 97: 118-122.
crossref pmid
Von Schmeling, B. and Kulka, M. 1966. Systemic fungicidal activity of 1,4-oxathiin derivatives. Science. 152: 659-660.
crossref pmid
Yamashita, M. and Fraaije, B. 2018. Non-target site SDHI resistance is present as standing genetic variation in field populations of Zymoseptoria tritici . Pest Manag. Sci. 74: 672-681.
crossref pmid
Yang, J. H., Brannen, P. M. and Schnabel, G. 2015. Resistance in Alternaria alternatato SDHI fungicides causes rare disease outbreak in peach orchards. Plant Dis. 99: 65-70.
crossref pmid
Yin, Y. N., Kim, Y. K. and Xiao, C. L. 2011. Molecular characterization of boscalid resistance in field isolates of Botrytis cinereafrom apple. Phytopathology. 101: 986-995.
crossref pmid
TOOLS
METRICS Graph View
  • 3 Crossref
  •  0 Scopus
  • 689 View
  • 41 Download
Related articles


ABOUT
BROWSE ARTICLES
EDITORIAL POLICY
FOR CONTRIBUTORS
Editorial Office
Rm,904 (New Bldg.) The Korean Science & Technology Center 22, Teheran-ro 7-gil, Gangnam-gu, Seoul 06130, Korea
Tel: +82-2-557-9360    Fax: +82-2-557-9361    E-mail: paper@kspp.org                

Copyright © 2021 by The Korean Society of Plant Pathology.

Developed in M2PI

Close layer
prev next