Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L.

Dimitra Papantoniou,Fredd Vergara,Alexander Weinhold,David I Pattison,Bekzod Khakimov,Teresa Quijano,Ainhoa Martínez-Medina,Søren Bak,Nicole M Van Dam

doi:10.3390/metabo11110731

Abstract

Root mutualistic microbes can modulate the production of plant secondary metabolites affecting plant–herbivore interactions. Still, the main mechanisms underlying the impact of root mutualists on herbivore performance remain ambiguous. In particular, little is known about how changes in the plant metabolome induced by root mutualists affect the insect metabolome and post-larval development. By using bioassays with tomato plants (Solanum lycopersicum), we analyzed the impact of the arbuscular mycorrhizal fungus Rhizophagus irregularis and the growth-promoting fungus Trichoderma harzianum on the plant interaction with the specialist insect herbivore Manduca sexta. We found that root colonization by the mutualistic microbes impaired insect development, including metamorphosis. By using untargeted metabolomics, we found that root colonization by the mutualistic microbes altered the secondary metabolism of tomato shoots, leading to enhanced levels of steroidal glycoalkaloids. Untargeted metabolomics further revealed that root colonization by the mutualists affected the metabolome of the herbivore, leading to an enhanced accumulation of steroidal glycoalkaloids and altered patterns of fatty acid amides and carnitine-derived metabolites. Our results indicate that the changes in the shoot metabolome triggered by root mutualistic microbes can cascade up altering the metabolome of the insects feeding on the colonized plants, thus affecting the insect development.

Highlights

Plants are a nutritious food source for insect species that belong to a wide range of taxonomic groups
By using tomato (Solanum lycopersicum) and the specialist chewing insect Manduca sexta as a model system, we found that root colonization by Rhizophagus irregularis or Trichoderma harzianum negatively affected the metamorphosis success of larvae that fed on the leaves of root-colonized plants
−6.93 −6.26 −6.73 p-Value p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001 p < 0.0001. Root mutualistic microbes such as mycorrhiza and Trichoderma fungi can modulate the production of plant secondary metabolites and affect the performance of the herbivores feeding on the colonized plants [37,43]

Summary

Introduction

Plants are a nutritious food source for insect species that belong to a wide range of taxonomic groups. To defend themselves against phytophagous insects, plants can produce a large range of metabolites that have repellent, anti-nutritive, or toxic effects on herbivores [1]. They are secondary plant metabolites, such as alkaloids, benzoxazinoids, glucosinolates, terpenoids, phenolics, non-protein amino acids and cyanogenic glucosides [2,3]. Plants produce a number of defense proteins that reduce the digestibility of plants, such as protein inhibitors, α-amylase inhibitors, and polyphenol oxidases [4] These metabolites can be produced constitutively or are induced upon herbivore damage. Anti-herbivore metabolites that are affecting basic processes, such as molting, are less easy for insect herbivores to adapt to, and can affect specialists

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Results

Conclusion