Helicoverpa zea gut‐associated bacteria indirectly induce defenses in tomato by triggering a salivary elicitor(s)

Abstract

Insect gut-associated microbes modulating plant defenses have been observed in beetles and piercing-sucking insects, but the role of caterpillar-associated bacteria in regulating plant induced defenses has not been adequately examined. We identified bacteria from the regurgitant of field-collected Helicoverpa zea larvae using 16S ribosomal RNA (rRNA) gene sequencing and matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry. A combination of biochemical, molecular, and confocal electron microscopy methods were used to determine the role of caterpillar-associated bacteria in mediating defenses in Solanum lycopersicum (tomato). Laboratory-reared H. zea inoculated with one of the bacteria identified in field-collected H. zea, Enterobacter ludwigii, induced expression of the tomato defense-related enzyme polyphenol oxidase and genes regulated by jasmonic acid (JA), whereas the salicylic acid (SA)-responsive pathogenesis-related gene was suppressed. Additionally, saliva and its main component glucose oxidase from inoculated caterpillars played an important role in elevating tomato anti-herbivore defenses. However, there were only low detectable amounts of regurgitant or bacteria on H. zea-damaged tomato leaves. Our results suggest that H. zea gut-associated bacteria indirectly mediate plant-insect interactions by triggering salivary elicitors. These findings provide a proof of concept that introducing gut bacteria to a herbivore may provide a novel approach to pest management through indirect induction of plant resistance.

Parasitic wasp‐associated symbiont affects plant‐mediated species interactions between herbivores

“…Alternatively, PDV genes might be exclusively expressed in the caterpillar body in the presence of the venom as found during in vitro experiments in the closely related host-parasitoid system Pieris rapae -C. rubecula in which the venom is suggested to assist uncoating of viral particles (Zhang et al 2004). In particular, it will be interesting to investigate if PDV genes are expressed in a tissue-specific manner in P. brassicae caterpillars parasitised by C. glomerata and whether the venom facilitates this process (Bitra et al 2011). In conclusion, our work shows that not only symbionts associated with herbivorous insects can impact plant responses to herbivory (Chung et al 2013;Su et al 2015;Wang et al 2017), but symbionts of carnivorous insects can also play an important role. This finding adds an extralayer of complexity to the ecology of plant-insect interactions suggesting that consideration of the third-trophic level should be extended to the associated symbionts as well to fully understand how plants cope with herbivores.…”

“…; Wang et al . ), but symbionts of carnivorous insects can also play an important role. This finding adds an extra‐layer of complexity to the ecology of plant‐insect interactions suggesting that consideration of the third‐trophic level should be extended to the associated symbionts as well to fully understand how plants cope with herbivores.…”

The controversies of silicon's role in plant biology

“…This is in line with predictions that phloem‐feeding insects cause only minor tissue damage and induce defense signaling pathways resembling those activated against biotrophic and hemibiotrophic pathogens (Walling, ; Kusnierczyk et al ., ). Recent evidence indicates that herbivore‐associated endosymbionts (Wang et al ., ) and the constituents of oral secretions, saliva, eggs (i.e. oviposition fluids) and frass, notably effectors, play an important role in manipulating direct and indirect plant defenses (Hilfiker et al ., ), dramatically reshaping plant transcriptomes, proteomes and metabolomes (Wu & Baldwin, ).…”

Promises and challenges in insect–plant interactions

“…Among genes identified and annotated, many herbivore proteins are predicted for secretion in aphids. Salivary GOX has been shown to elicit JA-regulated defences in tomato (Tian et al, 2012;Wang et al, 2017). Current technology of targeted silencing of herbivore genes is inefficient and new approaches that target multiple putative effector genes are needed.…”

“…For example, the parasitoid Microplitis croceipes (Cresson) suppressed protein synthesis in the labial glands of its host Heliothis virescens (Fabricius) and, thus, affected the expression of key effectors such as glucose oxidase (GOX). Salivary GOX has been shown to elicit JA-regulated defences in tomato (Tian et al, 2012;Wang et al, 2017).…”