Patterns of thermal adaptation in a globally distributed plant pathogen: Local diversity and plasticity reveal two‐tier dynamics

Abstract

Plant pathogen populations inhabit patchy environments with contrasting, variable thermal conditions. We investigated the diversity of thermal responses in populations sampled over contrasting spatiotemporal scales, to improve our understanding of their dynamics of adaptation to local conditions. Samples of natural populations of the wheat pathogen Zymoseptoria tritici were collected from sites within the Euro‐Mediterranean region subject to a broad range of climatic conditions. We tested for local adaptation, by accounting for the diversity of responses at the individual and population levels on the basis of key thermal performance curve parameters and “thermotype” (groups of individuals with similar thermal responses) composition. The characterization of phenotypic responses and genotypic structure revealed the following: (i) a high degree of individual plasticity and variation in sensitivity to temperature conditions across spatiotemporal scales and populations; and (ii) geographic variation in thermal response among populations, with major alterations due to seasonal patterns over the wheat‐growing season. The seasonal shifts in functional composition suggest that populations are locally structured by selection, contributing to adaptation patterns. Further studies combining selection experiments and modeling are required to determine how functional group selection drives population dynamics and adaptive potential in response to thermal heterogeneity.

Success and failure of invasive races of plant pathogens: The case of Puccinia striiformis f. sp. tritici in France

“…The two types of invasive isolates are thus expected to be quite competitive in terms of latency period compared to local isolates. Moreover, we found a negative correlation between P max and TPB 80 , as in Boixel et al (2022) considering populations of Zymoseptoria tritici , the causal agent of Septoria tritici blotch.…”

“…We considered a fixed minimal temperature of 0°C, an optimal temperature between 18 and 22°C, a maximal temperature between 24 and 30°C and a maximal performance (inverse of latency period) between 0.10 and 0.15 per day. We computed 80% thermal performance breadth (TPB 80 ), corresponding to the temperature range over which performance exceeds 80% of P max (Boixel et al, 2022). For each isolate × cultivar, we chose the 10 curves that best fitted the experimental points.…”

Diversity of thermal aptitude of Middle Eastern and Mediterranean Puccinia striiformis f. sp. tritici isolates from different altitude zones

“…In addition, another type of adaptation, temporal adaptation, was suggested for the British Pst population during the 2014 and 2015 growing seasons. Isolates from a particular genetic group were able to infect wheat throughout the growing season, whereas isolates from other genetic groups were identified only late in the spring and into the summer (Bueno-Sancho et al, 2017).…”

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

“…The recent discovery of chlamydospores in Z. tritici (Sardinha-Francisco et al 2019) adds a new element to the pathogen life cycle that can also contribute to the effective population size and maintenance of genetic diversity by enabling the buildup of a chlamydospore bank in soils planted to wheat and long-term persistence of the pathogen between crop rotations. The population genetics and population genomics of Z. tritici has been well characterized by using transect sampling to obtain well annotated collections of strains coming from naturally infected wheat fields distributed around the world (McDonald and Mundt 2016;Boixel et al 2022), enabling comparisons of population structure across different geographical scales. In some cases, the same field site was sampled over several years (Zhan et al 2001;El Chartouni et al 2012;Morais et al 2019;Oggenfuss et al 2021), enabling comparisons of population structure over time.…”

“…The population genetics and population genomics of Z. tritici has been well characterized by using transect sampling to obtain well annotated collections of strains coming from naturally infected wheat fields distributed around the world (McDonald and Mundt 2016; Boixel et al 2022), enabling comparisons of population structure across different geographical scales. In some cases, the same field site was sampled over several years (Zhan et al 2001; El Chartouni et al 2012; Morais et al 2019; Oggenfuss et al 2021), enabling comparisons of population structure over time.…”