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. 2022 Mar 22;17(3):e0265762. doi: 10.1371/journal.pone.0265762. eCollection 2022.

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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Hemiptera* / microbiology
  • Hydrodynamics
  • Insect Vectors / microbiology
  • Plant Diseases / microbiology
  • Vitis* / microbiology
  • Xylella*
  • Xylem

Supplementary concepts

  • Xylella fastidiosa

Grants and funding

DW - 1631776 funded by United States National Science Foundation - https://www.nsf.gov/ No, The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. CMR - 2019-67014-29358 funded by United States Department of Agriculture National Institute of Food and Agriculture www.usda.gov No, The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.