Higher fitness and competitive advantage of Pyricularia oryzae Triticum lineage resistant to QoI fungicides

Abstract

Background Quinone outside inhibitor (QoI) fungicides have not been effective in controlling the wheat blast disease [Pyricularia oryzae Triticum lineage (PoTl)] in Brazil. The first report of resistance of PoTl to QoIs in this country occurred in 2015. This study aimed to test hypotheses about the changes in fitness parameters and competitive advantage of the QoI‐resistant (R) PoTl isolate group compared to the sensitive (S) isolate group. Mycelial growth on PDA medium and in vivo conidial production, incubation period and disease severity were analyzed as fitness parameters. The competitive ability was measured on wheat leaves and heads inoculated with mixtures of R:S isolates at the following proportions: 0S:100R, 20S:80R, 50S:50R, 80S:20R, 100S:0R, and 0S:0R. Results The QoI‐R isolate group had significantly higher fitness than the sensitive isolate group, considering both in vitro and in vivo parameters. The highest in vivo conidial production on wheat leaves and the highest leaf and head disease severity were detected when resistant strains were predominant in the isolate's mixtures (20S:80R or 0S:100R proportions), in the absence of fungicide pressure. Conidia harvested from wheat blast lesions on leaves inoculated with 20S:80R and 0S:100R mixtures were resistant to QoIs in vitro assays based on discriminatory doses of the fungicide. Conclusion Therefore, QoI resistance facilitated a higher fitness and a competitive advantage in PoTl, which contrasts with the evolutionary theory that associates a fitness cost to fungicide resistance. We discuss the evolutionary and ecological implications of the higher fitness as found in the fungicide‐resistant adapted populations of the wheat blast pathogen. © 2022 Society of Chemical Industry.

Temporal dynamics of wheat blast caused by Pyricularia oryzae Triticum lineage throughout the successive wheat cycles

“…Similar to what was observed for P.oryzae Triticum on wheat, the PoTl inoculum and blast symptoms also spread from leaves to heads, following a vertical movement (Gongora-Canul et al, 2020). In our study, the time between inoculation and the rst conidia emergency on wheat leaves (latent period) was shorter for PoTl isolate 12.1.146 than that of the PoTl isolate Py6038 in all infection cycles (Fig.3C), which was consistent with the previous report in P. oryzae on rice, where the latent period of the isolates ranged from 5 to 7 days on rice leaves (D' Avila et al, 2022).Secondly, in all infection cycles, the period in days between inoculation and the rst symptom on wheat leaves and heads (incubation period) was shorter for PoTl isolate 12.1.146 than that of the PoTl isolate Py6038 (Fig.3Aand Fig.3B), which was consistent with previous report in PoTl isolates, where the incubation period of the isolates ranged from 2.54 to 2.95 days and wheat leaves, and from 2.88 to 3.16 days on wheat heads(Dorigan et al, 2022). The wheat blast severity from both 12.1.146 and Py6038 isolates increased over time on wheat leaves and heads.…”

“…Even though the wheat blast has been reported in Brazil for more than 30 years, there are still unanswered questions about the pathogen´s ecology and disease epidemiology; in this study, we assessed the effect of successive infection cycles of the 12.1146 and Py6038 PoTl isolates on the temporal development of blast on wheat leaves and heads (Dorigan et al, 2022). Knowledge about the biology and epidemiology of the PoTl isolate may lead us to understand better and to develop integrated disease management strategies against PoTl that cause blast in wheat elds in Brazil.…”

Target and non‐target site mechanisms of fungicide resistance and their implications for the management of crop pathogens

“…Similar to what was observed for Z. tritici, Pyricularia oryzae pathotype Triticum isolates carrying the G143A mutation in the cyt b gene also show greater virulence and competitive advantage than sensitive wildtype isolates (Table 2). 187 These results contrast with the evolutionary idea that fungicide resistance can come with fitness costs. 10 Conversely, many plant pathogens with fungicide resistance are associated with a fitness cost and/or absence of fitness cost.…”

Aerobiology of the Wheat Blast Pathogen: Inoculum Monitoring and Detection of Fungicide Resistance Alleles

“…Despite the seasonal fluctuations detected in the prevalence of the cytb allele for QoI resistance in the PoTl airborne inoculum, it was clear from our study that QoI-R strains were prompt to reemerge and dominate the wheat blast fungal population along the cropping season. This ability for re-emergence has been attributed to an inherited competitive advantage associated with the PoTl QoI-R strains [51] although a competitive disadvantage has been reported for the cytb G143A allele carried by QoI-R strains from fungal species, such as Zymoseptoria tritici, and the sister species P. oryzae Lolium lineage [52,53].…”