Salivary Glucose Oxidase from Caterpillars Mediates the Induction of Rapid and Delayed-Induced Defenses in the Tomato Plant

Donglan Tian,Dawn S Luthe,Eric Haubruge,Frederic Francis,John Tooker,Michelle Peiffer,Erica Shoemaker,Gary W Felton,Gustavo Bonaventure

doi:10.1371/journal.pone.0036168

Donglan Tian, Dawn S Luthe + Show 7 more

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https://doi.org/10.1371/journal.pone.0036168

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Abstract

Caterpillars produce oral secretions that may serve as cues to elicit plant defenses, but in other cases these secretions have been shown to suppress plant defenses. Ongoing work in our laboratory has focused on the salivary secretions of the tomato fruitworm, Helicoverpa zea. In previous studies we have shown that saliva and its principal component glucose oxidase acts as an effector by suppressing defenses in tobacco. In this current study, we report that saliva elicits a burst of jasmonic acid (JA) and the induction of late responding defense genes such as proteinase inhibitor 2 (Pin2). Transcripts encoding early response genes associated with the JA pathway were not affected by saliva. We also observed a delayed response to saliva with increased densities of Type VI glandular trichomes in newly emerged leaves. Proteomic analysis of saliva revealed glucose oxidase (GOX) was the most abundant protein identified and we confirmed that it plays a primary role in the induction of defenses in tomato. These results suggest that the recognition of GOX in tomato may represent a case for effector-triggered immunity. Examination of saliva from other caterpillar species indicates that saliva from the noctuids Spodoptera exigua and Heliothis virescens also induced Pin2 transcripts.

Highlights

The ability of many plant species to mount induced defenses to herbivores has been documented in what is becoming a voluminous literature [1],[2]
Of the 33 proteins that were identified (Table S1), glucose oxidase (GOX) was by far the most abundant protein accounting for 34% of the identified proteins (Fig. 1)
We found that saliva did not affect the expression of lipoxygenase D (LoxD), allene oxide synthase (Aos), allene oxide cyclase (Aoc), 12-oxophytodienoate reductase (Opr3), or prosystemin (Psy) at 2, 4, or 8 h post wounding (Fig. 5)

Summary

Introduction

The ability of many plant species to mount induced defenses to herbivores has been documented in what is becoming a voluminous literature [1],[2]. The expression of many of these proteins is regulated by the octadecanoid pathway [18],[19],[20]. In addition to these proteins, the role of glandular trichomes in resistance to insect feeding is being explored [21]. Glandular type VI trichomes in tomato are a formidable defense against some herbivores. The production of these trichomes is dependent upon jasmonic acid signaling [22],[23]. The glandular trichomes can be induced by wounding or application of methyl jasmonate [24]

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