Adaptation of a plant pathogen to partial host resistance: selection for greater aggressiveness in grapevine downy mildew

Abstract

An understanding of the evolution of pathogen quantitative traits in response to host selective pressures is essential for the development of durable management strategies for resistant crops. However, we still lack experimental data on the effects of partial host resistance on multiple phenotypic traits (aggressiveness) and evolutionary strategies in pathogens. We performed a cross‐inoculation experiment with four grapevine hosts and 103 isolates of grapevine downy mildew (Plasmopara viticola) sampled from susceptible and partially resistant grapevine varieties. We analysed the neutral and adaptive genetic differentiation of five quantitative traits relating to pathogen transmission. Isolates from resistant hosts were more aggressive than isolates from susceptible hosts, as they had a shorter latency period and higher levels of spore production. This pattern of adaptation contrasted with the lack of neutral genetic differentiation, providing evidence for directional selection. No specificity for a particular host variety was detected. Adapted isolates had traits that were advantageous on all resistant varieties. There was no fitness cost associated with this genetic adaptation, but several trade‐offs between pathogen traits were observed. These results should improve the accuracy of prediction of fitness trajectories for this biotrophic pathogen, an essential element for the modelling of durable deployment strategies for resistant varieties.

The genetic background modulates the intensity of Rpv3‐dependent downy mildew resistance in grapevine

“…First, Rpv3 ‐dependent ETI was ineffective in recognizing some pathovariants that have occasionally emerged in European populations of P. viticola over the past decades (Peressotti et al., ). Second, P. viticola collected from partially sporulating ETI lesions had higher aggressiveness, in particular a shorter latency period, than isolates sporulating on leaves of susceptible varieties (Delmas et al., ). Enhancing the efficacy of ETI by the introgression of an R gene into an optimal background is important to reduce pathogen propagation from resistant varieties, in order to have greater durability and lower likelihood for the pathogen to adapt.…”

Aggressiveness profiling of the coffee pathogen Colletotrichum kahawae

“…The IDI_10dai is a quantitative trait that is easier to measure (only one time point) and, due to its high correlation with AUDPC, can be considered a highly efficient aggressiveness trait that could be applied in future studies. The latent period is also one of the most used aggressiveness quantitative traits in the literature, and provides important information regarding isolate adaptation, as isolates with shorter latent period have a selective advantage in the field, by quickly releasing the conidia into the environment (Pariaud et al ., ; Frézal et al ., ; Delmas et al ., ). The latent period is sometimes considered identical to the incubation period (Luo & TeBeest, ).…”

“…A quantitative adaptation to the host is theoretically expected to be slower than the acquisition of new qualitative virulence factors (Pariaud et al ., ). Therefore, it is necessary to gather empirical knowledge on the nature of pathogen aggressiveness, as well as its genetic and environmental determinants, and on the ability of pathogens to respond to the selective pressures imposed by host quantitative resistance (Pariaud et al ., ; Delmas et al ., ). In this study, similar to that described in other plant pathogen interaction studies (Boedo et al ., ; Pariaud et al ., ; Purahong et al ., ), ‘aggressiveness’ will be considered as the quantitative measurement of the level of disease reached over time.…”

“…For several plant pathogen species, aggressiveness is a polygenic quantitative trait, influenced not only by the host genotype but also by the environment (e.g. temperature and humidity; Boedo et al ., ; Delmas et al ., ), and therefore it is considered to be shaped by natural selection resulting in different adaptive patterns according to the environment (Pariaud et al ., , ; Boedo et al ., ; Delmas et al ., ). A quantitative adaptation to the host is theoretically expected to be slower than the acquisition of new qualitative virulence factors (Pariaud et al ., ).…”

Potato resistance to quarantine diseases

“…Количественные аспекты взаимодействия грибов и оомицетов с растени ями, характеризующие эрозию частичной устойчивости растенияхозяина и увеличение агрессивности патогена, отражены в обзорах (Pariaud et al, 2009;Mundt, 2014). В работе (Delmas et al, 2016) изучено влияние частичной устойчивости хозяина на фенотипические признаки, особенно на агрессивность, возбудителя милдью (Plas mopara viticola) винограда. Показано, что изоляты этого патогена, выделенные из устойчивых хозяев, были более агрессивны (имели более короткий латентный период и более интенсивное спорообразование) по сравнению с изолятами, выделенными из восприимчивых образцов.…”