Plant defense against a pathogen drives nonlinear transmission dynamics through both vector preference and acquisition

Abstract

Host defense against vector-borne plant pathogens is a critical component of integrated disease management. However, theory predicts that traits that confer tolerance or partial resistance can, under certain ecological conditions, enhance the spread of pathogens and spillover to more susceptible populations or cultivars. A key component driving such epidemic risk appears to be variation in host-selection behavior of vectors based on infection status of the host. While recent theory has further emphasized the importance of infection-induced host-selection behavior by insect vectors for plant disease epidemiology, experimental tests on the relationship between vector host-selection preference and transmission are lacking. We test how host plant defense -conferred by the PdR1 gene complex-mediates vector host-selection preference and transmission of the pathogenic bacterium Xylella fastidiosa among grapevine cultivars. We confirmed that PdR1 confers resistance against X. fastidiosa by reducing both pathogen population size and disease severity. We found that vector transmission rates to new hosts exhibited unimodal dynamics over the course of infection when both susceptible and resistant were infected and acted as sources of the pathogen. Transmission from susceptible plants initially increased and then declined as insect vectors avoided severely diseased plants. While transmission from PdR1resistant plants also initially increased and then declined as well, this was not due to avoidance by vectors, although the exact mechanism remains unclear. We show that (1) vector preference changes over the course of disease progression, (2) vector preference is clearly important but a poor predictor of transmission, and (3) the post-latent incubation period-in which plant hosts are infectious but asymptomatic-is likely a key period for vector transmission of X. fastidiosa. Our results suggest that, consistent with theory, defensive traits lengthen the duration of the incubation period, increasing X. fastidiosa transmission. However, defensive traits may over the long-term ultimately reduce spread possibly through induced resistance. Vector host-selection preference, host resistance, and transmission are clearly dynamic, changing over the course of disease progression. Understanding these dynamics is critical for broader insights into the epidemiology of vector-borne plant pathogens, theory development, and deploying disease-resistant cultivars in an effective and sustainable manner.