Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f.sp.tritici

Abstract

Background: Costs of adaptation play an important role in host-parasite coevolution. For parasites, evolving the ability to circumvent host resistance may trade off with subsequent growth or transmission. Such costs of virulence (sensu plant pathology) limit the spread of all-infectious genotypes and thus facilitate the maintenance of genetic polymorphism in both host and parasite. We investigated costs of three virulence factors in Puccinia striiformis f.sp.tritici, a fungal pathogen of wheat (Triticum aestivum).

Results: In pairwise competition experiments, we compared the fitness of near-isogenic genotypes that differed by a single virulence factor. Two virulence factors (vir4, vir6) imposed substantial fitness costs in the absence of the corresponding resistance genes. In contrast, the vir9 virulence factor conferred a strong competitive advantage to several isolates, and this for different host cultivars and growing seasons. In part, the experimentally derived fitness costs and benefits are consistent with frequency changes of these virulence factors in the French pathogen population.

Conclusion: Our results illustrate the variation in the evolutionary trajectories of virulence mutations and the potential role of compensatory mutations. Anticipation of such variable evolutionary outcomes represents a major challenge for plant breeding strategies. More generally, we believe that agro-patho-systems can provide valuable insight in (co)evolutionary processes in host-parasite systems.

Figure 1

Competitive success of vir9 isolates in the climate chamber experiment. Mean (± S.E.) frequencies of vir9 isolates relative to avir9 isolates over the course of 5 pathogen generations in pairwise competition experiments. Two A vir/vir pairs (A, B) were competed on two host cultivars (Thésée, Récital). Each point represents the mean and S.E. calculated over 2 independent replicates.

Figure 2

Competitive success of virulent isolates in field experiments. Mean (± S.E.) frequencies of vir9 (a), vir4 and vir6 (b) isolates relative to their corresponding avirulent (Avir) isolates, as determined in pairwise competition experiments. Competing pairs (A-J) of virulent (vir) and avirulent (Avir) isolates (i1–i16) were started at an initial 50:50 ratio and the relative frequency of the vir isolate measured at the end of the growing season. Each point represents the means and S.E. calculated over 2 years and 2 host cultivars. For all 10 pairs, final frequencies were significantly different from the initial 50:50 ratio (t₇ > 3.49; p < 0.0101).

Figure 3

Time series of aggressiveness of vir9 isolates. Infection types on Clement seedlings of 33 isolates carrying the vir9 gene and collected from French populations during two epidemic periods between 1989 and 1997. Large values of infection type indicate high levels of sporulation and thus high aggressiveness. Each point represents the mean of two independent measurements. Four isolates (i5–i8) were used in the field competition experiments.