Mutations in sdh genes in field isolates of Zymoseptoria tritici and impact on the sensitivity to various succinate dehydrogenase inhibitors

Abstract

Zymoseptoria tritici is the causal agent of septoria tritici blotch (STB), a foliar wheat disease important worldwide. Succinate dehydrogenase inhibitors (SDHIs) have been used in cereals for effective control of STB for several years, but resistance towards SDHIs has been reported in several phytopathogenic fungi. Resistance mechanisms are target-site mutations in the genes coding for subunits B, C and D of the succinate dehydrogenase (SDH) enzyme. Previous monitoring data in Europe indicated the presence of single isolates of Z. tritici with reduced SDHI sensitivity. These isolates carried mutations leading to amino acid exchanges: C-T79N, C-W80S in 2012; C-N86S in 2013; B-N225T and C-T79N in 2014; and C-V166M, B-T268I, C-N86S, C-T79N and C-H152R in 2015. The current study provides results from microtitre and greenhouse experiments to give an insight into the impact of different mutations in field isolates on various SDHIs. In microtitre tests, the highest EC 50 values for all tested SDHIs were obtained with mutants carrying C-H152R. Curative greenhouse tests with various SDHIs confirmed the findings of microtitre tests that isolates with C-H152R are, in general, controlled with lower efficacy than isolates carrying B-T268I, C-T79N and C-N86S. SDHI-resistant isolates of Z. tritici found in the field were shown to have cross-resistance towards all SDHIs tested. So far, SDHI-resistant isolates of Z. tritici have been found in low frequencies in Europe. Therefore, FRAC recommendations for resistance management in cereals, including a limited number of applications, alternation and combination with other MOAs, should be followed to prolong SDHI field efficacy.

Non‐target site SDHI resistance is present as standing genetic variation in field populations of Zymoseptoria tritici

“…The detection of strains highly resistant to fluopyram, and in particular isofetamid, in multiple locations as early as 2003 (Table ), before the widespread introduction of a newer generation of SDHIs into the cereal market in 2010, indicates pre‐existing non‐target site resistance. We have also seen that European Z. tritici populations have developed acquired resistance only through a range of different Sdh target‐site mutations since 2012 . In addition, strains with altered efflux pump activity, including MgMFS1 ‐overexpressing strains have recently spread in Europe as a response to selection by QoI, azole and SDHI fungicides.…”

“…For cross‐resistance studies, reference strain IPO323‐derived laboratory mutants and field isolates, for which the Sdh genotypes had been analysed previously,, , were tested. For additional field population monitoring studies, sampling and isolation of Z. tritici strains from infected wheat leaves were performed as described previously .…”

“…Furthermore, the new SDHI isofetamid had a sensitivity profile similar to that of fluopyram when a B‐H272Y mutant of B. cinerea was tested , . Low levels of SDHI resistance in Z. tritici strains carrying Sdh mutations C‐T79 N and C‐W80S were reported in 2012, followed by C‐N86S (2013), B‐N225 T (2014) and B‐T268I (2015) . High levels of resistance due to strains carrying Sdh mutation C‐H152R were recently reported in Ireland and the UK , , .…”

Antifungal activity of metyltetraprole against the existing QoI‐resistant isolates of various plant pathogenic fungi

“…In the case of QoIs, it has been reported that the orthologous amino acid mutations result in similar resistance profiles across different organisms with respect to the strength of resistance; the G143A mutation causes very high level of resistance (the resistance factor RF, [EC 50 of the resistant mutant]/[EC 50 of the wild type], is always greater than 100) to all commercial QoIs in any known cases of more than 20 pathogen species . However, recently some cases of different resistance profiles within the orthologous mutations of different pathogen species were reported in cases of resistance against succinate dehydrogenase inhibitor (SDHI), another important agricultural fungicide class . Considering the unique behavior of metyltetraprole in the G143A mutants of Z. tritici as well as in the F129L mutants of P. teres , its consistency in orthologous mutations in different species should be investigated.…”

Pyridachlometyl has a novel anti‐tubulin mode of action which could be useful in anti‐resistance management

“…In recent years, only three classes of fungicides, DMI (sterol C14 demethylation inhibitor in ergosterol biosynthesis), QoI (Qo site of complex III inhibitor in the respiratory chain), and SDHI (succinate dehydrogenase inhibitor in the respiratory chain), have accounted for approximately 60% of the global fungicide market because of their high efficacy and the broad spectrum of these three chemical classes. Frequent usage of these three classes of fungicides has led to the development of resistance in crop pathogens, such as Zymoseptoria tritici , Erysiphe necator , Podosphaera xanthii , Microdochium spp., and Cercospora beticola . As a result, agrochemical research and development seek new chemical classes of fungicides to respond to the needs of crop growers .…”