Submitted to: Annals of the Entomological Society of America
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/17/2009
Publication Date: 8/28/2009
Publication URL: http://www.bioone.org/toc/essa/102/5
Citation: Backus, E.A., Holmes,, W., Schreiber,, F., Reardon,, B., Walker,, G. 2009. Sharpshooter X-wave: Correlation of an Electrical Penetration Graph (EPG) Waveform With Xylem Penetration Supports a Hypothesized Mechanism For Xylella Fastidiosa Inoculation. Annals of the Entomological Society of America. 102(5):847-867. Interpretive Summary: Xylem fluid-ingesting leafhoppers, called sharpshooters, are among the most economically damaging agricultural pests because they are vectors of plant pathogens such as Xylella fastidiosa, the bacterium that causes Pierce’s Disease (PD). Development of host plant resistance to PD is hindered by lack of understanding of the mechanism of sharpshooter inoculation of X. fastidiosa, and by absence of a rapid, objective means of measuring occurrence of inoculation on putatively resistant varieties. The present study is a crucial step towards identification and measurement of X. fastidiosa inoculation. Electrical Penetration Graph (EPG) monitoring of insect feeding was used to identify the X wave of the smoke tree sharpshooter, Homalodisca liturata (Hemiptera: Cicadellidae: Cicadellinae), a vector of X. fastidiosa that is closely related to the glassy-winged sharpshooter, H. vitripennis. The complex components of the X wave represent salivation, tasting, ingestion, and probably egestion by sharpshooters when stylet tips are inside a plant xylem cell. It is proposed that egestion and salivation behaviors, represented in EPG by the X wave, control inoculation of X. fastidiosa. Therefore, characterization of the sharpshooter X wave makes possible the future use of EPG for comparisons among crop cultivars for resistance to inoculation by the vector.
Technical Abstract: Electrical Penetration Graph (EPG) monitoring is the most rigorous means of observation and quantification of feeding by piercing-sucking arthropods. Previous EPG studies with aphids and leafhoppers have demonstrated that the X waveform identifies when the insect is ingesting from its preferred plant vascular cell. Previous studies have identified X waves strictly for ingestion from phloem sieve elements. This paper presents the first direct evidence of an X wave identifying ingestion from a xylem tracheary element by a xylem-ingesting leafhopper, the smoke tree sharpshooter, Homalodisca liturata (Hemiptera: Cicadellidae: Cicadellinae). We document consistent association of the sharpshooter X wave with salivary sheath termini in xylem, especially lignified secondary xylem cells, and absence of the X wave in the rare instances of ingestion from a non-xylem cell. The X wave is a complex, multi-component waveform composed of X wave-specific variants of waveform types B1w (representing salivation), B1s (associated behavior is unknown, but suspected to represent precibarial valve movement for tasting), C1 (a new waveform type that may represent egestion) and C2 (a new designation for the waveform type representing ingestion/ cibarial pumping). It is proposed that the sharpshooter X wave represents a suite of behaviors that function to: 1) physically seal stylet tips into the cell via sheath salivation, 2) repeatedly taste then eject (egest) chemical constituents of the cell to determine acceptability, and 3) mechanically test the strength of the stylet seal via trial cibarial pumping (ingestion). It is further hypothesized that the X wave is associated with vector behaviors that control inoculation of the Pierce’s Disease bacterium, Xylella fastidiosa. Characterization of the sharpshooter X wave makes possible the future use of EPG for comparisons among crop cultivars for host plant resistance, without time-consuming histology of salivary sheaths.