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The downside of metabolic diversity: Postingestive rearrangements by specialized insects
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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9214519/ https://www.ncbi.nlm.nih.gov/pubmed/35666864 http://dx.doi.org/10.1073/pnas.2122808119 |
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author | Heiling, Sven Li, Jiancai Halitschke, Rayko Paetz, Christian Baldwin, Ian T. |
author_facet | Heiling, Sven Li, Jiancai Halitschke, Rayko Paetz, Christian Baldwin, Ian T. |
author_sort | Heiling, Sven |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9214519 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-92145192022-06-23 The downside of metabolic diversity: Postingestive rearrangements by specialized insects Heiling, Sven Li, Jiancai Halitschke, Rayko Paetz, Christian Baldwin, Ian T. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2022-06-06 2022-06-14 /pmc/articles/PMC9214519/ /pubmed/35666864 http://dx.doi.org/10.1073/pnas.2122808119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Heiling, Sven Li, Jiancai Halitschke, Rayko Paetz, Christian Baldwin, Ian T. The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title | The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title_full | The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title_fullStr | The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title_full_unstemmed | The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title_short | The downside of metabolic diversity: Postingestive rearrangements by specialized insects |
title_sort | downside of metabolic diversity: postingestive rearrangements by specialized insects |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9214519/ https://www.ncbi.nlm.nih.gov/pubmed/35666864 http://dx.doi.org/10.1073/pnas.2122808119 |
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