Fluid dynamic simulations at the interface of the blue-green sharpshooter functional foregut and grapevine xylem sap with implications for transmission of Xylella fastidiosa

Authors: MARCUS, IAN - Drexel University; WHITE, DANIEL - University Of California; Backus, Elaine; WALKER, SHARON - Drexel University; ROPER, M. CAROLINE - University Of California

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/7/2022
Publication Date: 3/22/2022
Citation: Marcus, I.M., White, D., Backus, E.A., Walker, S.L., Roper, M. 2022. Fluid dynamic simulations at the interface of the blue-green sharpshooter functional foregut and grapevine xylem sap with implications for transmission of Xylella fastidiosa. PLoS ONE. 17(3). Article e0265762. https://doi.org/10.1371/journal.pone.0265762.
DOI: https://doi.org/10.1371/journal.pone.0265762

Interpretive Summary: Xylella fastidiosa is a multi-continental, xylem-dwelling bacterium that causes economically severe crop diseases such as Pierce’s disease of grapevine, citrus variegated chlorosis, olive quick decline syndrome, and leaf scorches of oleander, almond, and coffee. Xylella fastidiosa is transmitted by sharpshooter leafhoppers and adult spittlebug vectors. Pierce’s disease (PD) of grapevines costs the state of California and its grape growers an estimated $166 million per year in lost production, vine replacements, and vector control. The bacterium forms biofilms in plant xylem and the functional foregut of the vector. These biofilms serve as sources of inoculum for insect acquisition and subsequent inoculation to a healthy plant. In this study, mathematical simulations were performed to explain two-way propulsion of xylem sap by the vector’s sucking pump, through tube-like grapevine xylem and an anatomically accurate model of the functional foregut of the blue-green sharpshooter, Graphocephala atropunctata. The analysis supports a model of how fluid movements and velocities influence X. fastidiosa transmission during fluid flow inward (ingestion, powering acquisition of the bacteria) and outward (egestion, powering inoculation). Results from this study will greatly aid development of novel grapevine resistance traits via electropenetrographic monitoring of vector acquisition and inoculation behaviors.

Technical Abstract: Xylella fastidiosa is a multi-continental, lethal, plant pathogenic bacterium that is transmitted by sharpshooter leafhoppers (Insecta: Hemiptera: Cicadellidae: Cicadellinae) and adult spittlebugs (Hemiptera: Aphrophoridae). The bacterium forms biofilms in plant xylem and the functional foregut of the insect. These biofilms serve as sources of inoculum for insect acquisition and subsequent inoculation to a healthy plant. In this study, 3D fluid dynamic simulations were performed for bidirectional cibarial propulsion of xylem sap through tube-like grapevine xylem and an anatomically accurate model of the functional foregut of the blue-green sharpshooter, Graphocephala atropunctata. The analysis supports a model of how fluid dynamics influence X. fastidiosa transmission. The model supports the hypothesis that X. fastidiosa inoculation is mostly driven by detachment of bacteria from the foregut due to high-velocity egestion (outward fluid flow from the stylets). Acquisition occurs by fluid dynamics during both egestion and ingestion (fluid uptake through the stylets and swallowing). These simulation results are supported by previously reported X. fastidiosa colonization patterns in the functional foregut and sharpshooter stylet probing behaviors. The model indicates that xylem vessel diameter influences drag forces imposed on xylem wall-adherent bacteria; thus, vessel diameter may be an important component of the complex transmission process. Results from this study are directly applicable to development of novel grapevine resistance traits via electropenetrographic monitoring of vector acquisition and inoculation behaviors.