ATP Hydrolyzing Salivary Enzymes of Caterpillars Suppress Plant Defenses

Shuang Wu,Michelle Peiffer,Gary W Felton,Dawn S Luthe,Mark F Feldlaufer

doi:10.1371/journal.pone.0041947

Shuang Wu, Michelle Peiffer + Show 3 more

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https://doi.org/10.1371/journal.pone.0041947

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Journal: PloS one	Publication Date: Jul 25, 2012
Citations: 116	License type: CC BY 4.0

Affiliation: Southwest University, Pennsylvania State University

Abstract

The oral secretions of herbivores are important recognition cues that can be used by plants to mediate induced defenses. In this study, a degradation of adenosine-5′-triphosphate (ATP) in tomato leaves was detected after treatment with Helicoverpa zea saliva. Correspondingly, a high level of ATPase activity in saliva was detected and three ATP hydrolyzing enzymes: apyrase, ATP synthase and ATPase 13A1 were identified in salivary glands. To determine the functions of these proteins in mediating defenses, they were cloned from H. zea and expressed in Escherichia coli. By applying the purified expressed apyrase, ATP synthase or ATPase 13A1 to wounded tomato leaves, it was determined that these ATP hydrolyzing enzymes suppressed the defensive genes regulated by the jasmonic acid and ethylene pathways in tomato plant. Suppression of glandular trichome production was also observed after treatment. Blood-feeding arthropods employ 5′-nucleotidase family of apyrases to circumvent host responses and the H. zea apyrase, is also a member of this family. The comparatively high degree of sequence similarity of the H. zea salivary apyrase with mosquito apyrases suggests a broader evolutionary role for salivary apyrases than previously envisioned.

Highlights

The oral secretions of herbivores have been reported to be important cues in mediating inducible plant responses [1,2,3,4,5,6,7,8,9,10,11,12]
Saliva depletes foliar levels of ATP Based on the importance of extracellular ATP (eATP) in plant physiological responses, H. zea saliva was assayed for ATP hydrolysis activity
It was noted that the ATP synthase and ATPase 13A1 proteins were highly conserved among insect species

Summary

Introduction

The oral secretions of herbivores have been reported to be important cues in mediating inducible plant responses [1,2,3,4,5,6,7,8,9,10,11,12]. Plants generate inducible defense responses according to the overall effect of elicitors and effectors from caterpillar oral secretions. It was reported that H. zea salivary glucose oxidase has opposing effects on tomato Solanum lycopersicum. It elicits both rapid and delayedinduced defenses in tomato plants [10]. Saliva contains scores of proteins many of which have no known function [10]

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