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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Project description:Soybean is one of the main sources of oil worldwide, and the cotton bollworm [Helicoverpa armigera (Hübner)] is one of the common herbivores seriously affecting soybean production. After being attacked by herbivores, multiple signaling patheways will be triggered in plants, which induces the production of toxic, repellent, or anti-digestive compounds. Genetic engineering and breeding of resistant plant lines are the most effective and environmentally friendly approaches to control herbivores and improve the performance of plants. This study focuses on founding changes genes and proteins in soybean defense response induced by H. armigera. Illumina Solexa sequencing platform and iTRAQ were used for the comparative analysis of transcriptome and proteome profiles in the leaves of Tianlong 2 (a cultivated soybean susceptible to herbivores) and ED059 (a wild soybean resistant to herbivores) in response to infestation by H. armigera. Transcriptome data show that 2073 differentially expressed genes (DEGs) were uniquely expressed in ED059 compared with those in Tianlong 2 after 24 h of H. armigera treatment. Based on gene ontology classification of these 2073 DEGs, we identified 233 DEGs corresponded to various signaling pathways, including protein kinases, transcriptional factors, hormone biosynthesis and signal transduction pathways. In addition, a large number of genes related to antinutritive or toxic proteins were special induced in ED059. By combining the gene expression at the transcriptomic and proteomic levels, results reveal that no significantly high correlation was detected between the expression of mRNAs and proteins. Functional analysis of three candidate genes was accomplished by Agrobacterium-mediated transformation in Arabidopsis thaliana, and a MYB transcription factor 109 (MYB109) was identified with herbivore defense function in ED059. This study provides insights into the identification of the potential genes and proteins involved in herbivore defense, and a possible understanding of the herbivore defense mechanism in a wild soybean by combining analysis of transcriptome and proteome data. Moreover, a novel gene associated with herbivore resistance function was identified and validated.

Dataset Information

The downside of metabolic diversity: Postingestive rearrangements by specialized insects

Publications

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

Similar Datasets

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