Dataset Information

The downside of metabolic diversity: Postingestive rearrangements by specialized insects

ABSTRACT: Deploying toxins in complex mixtures is thought to be advantageous and is observed during antagonistic interactions in nature. Toxin mixtures are widely utilized in medicine and pest control, as they are thought to slow the evolution of detoxification counterresponses in the targeted organisms. Here we show that caterpillars rearrange key constituents of two distinct plant defense pathways to postingestively disable the defensive properties of both pathways. Specifically, phenolic esters of quinic acid, chlorogenic acids (CAs), potent herbivore and ultraviolet (UV) defenses, are reesterified to decorate particular sugars of 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) and prevent their respective anti–herbivore defense functions. This was discovered through the employment of comparative metabolomics of the leaves of Nicotiana attenuata and the frass of this native tobacco’s specialist herbivore, Manduca sexta larvae. Feeding caterpillars on leaves of transgenic plants abrogated in each of the two pathways, separately and together, revealed that one of the fully characterized frass conjugates, caffeoylated HGL-DTG, originated from ingested CA and HGL-DTGs and that both had negative effects on the defensive function of the other compound class, as revealed by rates of larval mass gain. This negative defensive synergy was further explored in 183 N. attenuata natural accessions, which revealed a strong negative covariance between the two defense pathways. Further mapping analyses in a biparental recombinant inbred line (RIL) population imputed quantitative trait loci (QTLs) for the two pathways at distinct genomic locations. The postingestive repurposing of defense metabolism constituents reveals a downside of deploying toxins in mixtures, a downside which plants in nature have evolved to counter.

INSTRUMENT(S): Liquid Chromatography MS - positive - reverse phase

SUBMITTER: Sven Heiling

PROVIDER: MTBLS3676 | MetaboLights | 2022-12-04

REPOSITORIES: MetaboLights

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The downside of metabolic diversity: Postingestive rearrangements by specialized insects.

Heiling Sven S Li Jiancai J Halitschke Rayko R Paetz Christian C Baldwin Ian T IT

Proceedings of the National Academy of Sciences of the United States of America 20220606 24

Deploying toxins in complex mixtures is thought to be advantageous and is observed during antagonistic interactions in nature. Toxin mixtures are widely utilized in medicine and pest control, as they are thought to slow the evolution of detoxification counterresponses in the targeted organisms. Here we show that caterpillars rearrange key constituents of two distinct plant defense pathways to postingestively disable the defensive properties of both pathways. Specifically, phenolic esters of quin ...[more]

PMID: 35666864

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			Action	DRS
	MTBLS3676	Other
	FILES	Other
	a_MTBLS3676_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
	files-all.json	Other
	i_Investigation.txt	Txt