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

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 flow during 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.

Xylella fastidiosa inoculation behaviors (EPG X wave) are performed differently by blue-green sharpshooters based on infection status of prior probing host

“…In our results, T3 and T4 insects from basil generally performed fewer than 30 X waves in 10 h, each of relatively short event duration. During each X wave, they took up/tasted/tested then egested out fluid (Marcus et al 2022) before accepting the xylem cell and progressing into sustained ingestion. Thus, insects that probed only basil pre-EPG (T3 and T4) rapidly accepted a xylem cell and progressed into sustained ingestion.…”

“…As first hypothesized by Backus (2016), this waveform probably represents the most important behavior for inoculation of Xf , due to the large volume of fluid egested (Dugravot et al 2008, Cornara et al 2020). Hereafter, XC1 is also called ‘foregut and xylem clearing’ because it is thought to dislodge and clear obstructions (especially microbes) in both the functional foregut and the xylem (Marcus et al 2022). XNC: XB1 and XC1, combined, thus all types of egestion (Backus et al 2021b).…”

“…EPG history and principles have recently been reviewed (Backus et al 2019, 2021a, Backus and Shih 2021). In brief, principles of EPG are based on the electrical properties of fluid movements/dynamics through the stylets and functional foregut of hemipterans (Marcus et al 2022). Voltage equilibria that are cyclically established-then-broken produce stereotypical waveforms that indicate volume, velocity, and direction of fluid flow (Dugravot et al 2008, Backus 2016).…”

“…XB1 alternates with XC1, which represents discharging egestion or high-volume, eruptive ‘spitting’ (Dugravot et al 2008). Fluid dynamics through the precibarium during discharging egestion are 14x more powerful than those during ingestion (Marcus et al 2022). The above X wave behaviors serve two purposes: i) to taste/test chemical constituents in the plant fluid to find/test/accept a xylem cell, but also ii) to scrub off contaminating microbes that can reduce functionality of the precibarium (Ruschioni et al 2019), thus inoculating Xf (Backus 2016, Cornara et al 2020).…”

An overview of the most threating diseases that affect worldwide citriculture: Main features, diagnose, and current control strategies

“…CVC vectors are insects that feed on citrus xylem vessels (Almeida et al, 2005), such as the leafhoppers of the Cicadellidae family, which include Bucephalogonia xanthophis and Macugonalia leucomelas that are more efficient at transmitting the pathogen. However, the transmission can also occur through spittlebugs (Aphrophoridae) (Lopes & Krugner, 2016;Marcus et al, 2022).…”