How large and diverse are field populations of fungal plant pathogens? The case of Zymoseptoria tritici

Abstract

Pathogen populations differ in the amount of genetic diversity they contain. Populations carrying higher genetic diversity are thought to have a greater evolutionary potential than populations carrying less diversity. We used published studies to estimate the range of values associated with two critical components of genetic diversity, the number of unique pathogen genotypes and the number of spores produced during an epidemic, for the septoria tritici blotch pathogen Zymoseptoria tritici. We found that wheat fields experiencing typical levels of infection are likely to carry between 3.1 and 14.0 million pathogen genotypes per hectare and produce at least 2.1–9.9 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 × 10−10 substitutions per site per cell division, we estimate that between 27 and 126 million pathogen spores carrying adaptive mutations to counteract fungicides and resistant cultivars will be produced per hectare during a growing season. This suggests that most of the adaptive mutations that have been observed in Z. tritici populations can emerge through local selection from standing genetic variation that already exists within each field. The consequences of these findings for disease management strategies are discussed.

The impact of wheat cultivar mixtures on virulence dynamics in Zymoseptoria tritici populations persists after interseason sexual reproduction

“…An understanding of the interactions between these factors will clearly require modelling approaches, but also further experimental fungal biology studies in semicontrolled conditions (e.g., Orellana‐Torrejon et al, 2022b) to characterize the abovementioned mechanisms in greater detail. The potential impact of resistance deployment strategies, including cultivar mixtures—which may be beneficial, but also detrimental over the years—remain to be fully assessed considering both the size and the genetic diversity of a pathogen population (McDonald & Linde, 2002; McDonald et al, 2022). Our conclusions were drawn at field scale, but it should clearly be borne in mind that the impact of mixtures is diluted at greater spatial scales when considering inoculum exchanges between fields planted with different cultivars (e.g., Fabre et al, 2015).…”

Modelling quantitative fungicide resistance and breakdown of resistant cultivars: designing integrated disease management strategies for Septoria of winter wheat

“…The value for the mutation proportion we use is based on estimates for the total number of spores generated in a growing season and the number of spores per season carrying adaptive mutations for fungicides and resistant cultivars ( McDonald et al, 2022 ). See Appendix 2.…”

“…McDonald et al (2022 ) estimate that wheat fields typically produce 2.3 to 10.5 trillion pycnidiospores per hectare, of which between 28 and 130 million spores carry adaptive mutations to counteract fungicides and/or resistant cultivars. This allows us to produce an estimate for the proportion of offspring which carry a mutation by dividing the average number of spores carrying mutations by the average total number of spores: …”

A thousand-genome panel retraces the global spread and climatic adaptation of a major crop pathogen

“…The timing and shared geographic origin of the pathogen and domesticated wheat strongly suggests coevolution between the two species. The pathogen harbors extensive standing variation from individual infected leaves to large agricultural regions 12,13 . As a consequence, the pathogen showed rapid responses across all major wheat-producing areas to overcome host resistance and gain tolerance to fungicides in less than a decade 10 .…”