Non-linear dynamics of vector transmission of a plant pathogen: a test of theory and application to disease management

Authors: ZEILINGER, ADAM - University Of California; Wallis, Christopher; BEAL, DYLAN - University Of California; SICARD, ANNE - University Of California; WALKER, M. ANDREW - University Of California; ALMEIDA, RODRIGO - University Of California

Submitted to: Ecosphere
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/17/2020
Publication Date: 5/16/2021
Citation: Zeilinger, A.R., Wallis, C.M., Beal, D., Sicard, A., Walker, M., Almeida, R.P. 2021. Non-linear dynamics of vector transmission of a plant pathogen: a test of theory and application to disease management. Ecosphere. 12(5):e03505. https://doi.org/10.1002/ecs2.3505.
DOI: https://doi.org/10.1002/ecs2.3505

Interpretive Summary: Understanding the dynamics of vector feeding preference, host resistance, and transmission over the course of disease progression are key to decoding the epidemiology of vector-borne plant pathogens such as as Xylella fastidiosa. Therefore, susceptible and PdR1-resistant grapevines were inoculated with Xylella fastidiosa and exposed to blue-green sharpshooter vectors to evaluate factors potentially important in pathogen spread including symptom severity, bacteria titers, grapevine chemistry, and sharpshooter vector attraction, leaving, acquisition, and transmission rates. Vector feeding preference was observed to change over the course of infection, but preference alone did not predict pathogen transmission. The pathogen latent or asymptomatic period was identified as the most likely time when transmission to new hosts occurs. Because tolerant grapevines rarely become symptomatic, such plants could be considered very important reservoirs of Xylella fastidiosa. However, induced host resistance was observed to eventually develop in tolerant grapevines, leading to greatly reduced titers and mitigating the role of such plants as reservoirs for long-term spread. These results increase scientific knowledge about the epidemiology of vector-borne plant pathogens such as Xylella fastidiosa when tolerant hosts are present.

Technical Abstract: Host resistance 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 some ecological conditions, enhance spread of pathogens and spillover to more susceptible populations or cultivars. The host selection behavior of vectors based on infection status appears to be key in driving epidemic risk from tolerant hosts. At the same time, 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 feeding preference and transmission are lacking. Such tests are critical to inform future developments of theory. Here how vector feeding preference affects transmission was tested from hybrid grapevine cultivars providing defense against the pathogenic bacterium Xylella fastidiosa, conferred by the PdR1 gene. A range of epidemiologically relevant parameters in a series of vector transmission experiments was measured and show that 1) vector feeding preference changes over the course of disease progression, 2) vector feeding preference is clearly important but does not predict transmission alone, and 3) duration of the incubation period, in which plant hosts are infectious but asymptomatic, is likely when most vector transmission occurs. The results suggest, consistent with theory, that the PdR1 gene may lengthen the incubation period, increasing X. fastidiosa transmission, but induced resistance conferred by the gene may ultimately reduce spread over the long-term. Vector feeding preference, host resistance, and transmission are clearly dynamic, changing over the course of disease progression, in X. fastidiosa pathosystems and likely other systems. Understanding these dynamics is critical for broader insights into the epidemiology of vector-borne plant pathogens.