Plant water stress and vector feeding preference mediate transmission efficiency of a plant pathogen

Authors: DEL CID, CELIA - University Of California; Krugner, Rodrigo; ZEILINGER, ADAM - University Of California; DAUGHERTY, MATT - University Of California; ALMEIDA, RODRIGO - University Of California

Submitted to: Environmental Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/10/2018
Publication Date: 9/22/2018
Citation: Del Cid, C., Krugner, R., Zeilinger, A.R., Daugherty, M., Almeida, R.P. 2018. Plant water stress and vector feeding preference mediate transmission efficiency of a plant pathogen. Environmental Entomology. 47(6):1471-1478. https://doi.org/10.1093/ee/nvy136.
DOI: https://doi.org/10.1093/ee/nvy136

Interpretive Summary: Xylella fastidiosa is a bacterium that causes Pierce’s disease of grapevines, which can severely damage plants and shorten the productive life of the vineyard. X. fastidiosa is transmitted from plant to plant by several species of leafhoppers, including the glassy-winged sharpshooter, a relatively recent invader of California. Understanding of the factors controlling the spread of bacteria by insect vectors is critically important to management efforts. Irrigation is the most significant input in California agriculture, and future climate projection models predict reduced water availability to farmland. Therefore, knowledge of the effects of plant water stress caused by either natural drought periods or controlled deficit irrigation on the spread of bacteria is key to develop disease management strategies. In laboratory experiments, vectors transmitted X. fastidiosa to grapevines in conditions ranging from well-watered to severely water-stressed. In no-choice tests, acquisition of X. fastidiosa by vectors increased significantly as xylem sap tension (water stress) increased in source plants, while inoculation of bacteria to plants by vectors was not affected by water status of recipient vines. However, when vectors were presented with a choice of a healthy well-watered versus an infected water-stressed grapevine, a significant reduction in transmission of bacteria to the healthy plant occurred as water stress levels increased. Further, a host-vector epidemic model indicated a non-linear relationship between water stress and pathogen spread: moderate water stress enhances pathogen spread but extreme water stress produces equivalent spread as in a well-watered scenario. Thus, host plant conditions and vector host preference interacted to determine transmission efficiency of this plant pathogen.

Technical Abstract: Insect-transmitted plant pathogens are complex biological systems because pathogen spread and disease are the outcome of insect-plant-pathogen interactions where abiotic stresses influence each component as well as how they relate to each other. To assess how water stress impacts pathogen spread of a vector-borne plant pathogen, the grapevine-sharpshooter leafhopper- Xylella fastidiosa pathosystem was used. This system is unique in that all organisms are directly impacted by water stress, but the outcome of the interactions among them in relation to pathogen dissemination is unknown. Two sets of experiments were conducted to determine the impact of plant water stress on the vector transmission of the bacterium X. fastidiosa. In the first set of experiments, vectors acquired or inoculated X. fastidiosa to grapevines over a range of water stress levels. Pathogen acquisition efficiency increased as water stress increased in source plants, while inoculation efficiency was not affected by water status of recipient vines. Thus, under no choice conditions, water stress caused an increase in transmission of the pathogen. However, when vectors were presented with a choice of a healthy well-watered versus an infected water-stressed grapevine, transmission efficiency declined when water stress levels increased. Further, a host-vector epidemic model was used to investigate the effects of water stress on the spread of X. fastidiosa based on the experimental results. Combined data and model results indicate a non-linear relationship between water stress and pathogen spread: moderate water stress enhances pathogen spread but extreme water stress produces equivalent spread as in a well-watered scenario. Thus, both host plant condition and vector host preference interacted to determine transmission efficiency of this plant pathogen.