Metabolomic analysis reveals reliance on secondary plant metabolites to facilitate carnivory in the Cape sundew, Drosera capensis.

Drosera capensis carnivorous plant metabolomics plant–insect interactions secondary plant metabolites

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
26 08 2021
Historique:
received: 24 03 2021
accepted: 01 06 2021
pubmed: 3 6 2021
medline: 28 9 2021
entrez: 2 6 2021
Statut: ppublish

Résumé

Secondary metabolites are integral to multiple key plant processes (growth regulation, pollinator attraction and interactions with conspecifics, competitors and symbionts) yet their role in plant adaptation remains an underexplored area of research. Carnivorous plants use secondary metabolites to acquire nutrients from prey, but the extent of the role of secondary metabolites in plant carnivory is not known. We aimed to determine the extent of the role of secondary metabolites in facilitating carnivory of the Cape sundew, Drosera capensis. We conducted metabolomic analysis of 72 plants in a time-series experiment before and after simulated prey capture. We used ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS) and the retention time index to identify compounds in the leaf trap tissue that changed up to 72 h following simulated prey capture. We identified associated metabolic pathways, and cross-compared these compounds with metabolites previously known to be involved in carnivorous plants across taxa. For the first time in a carnivorous plant, we have profiled the whole-leaf metabolome response to prey capture. Reliance on secondary plant metabolites was higher than previously thought - 2383 out of 3257 compounds in fed leaves had statistically significant concentration changes in comparison with unfed controls. Of these, ~34 compounds are also associated with carnivory in other species; 11 are unique to Nepenthales. At least 20 compounds had 10-fold changes in concentration, 12 of which had 30-fold changes and are typically associated with defence or attraction in non-carnivorous plants. Secondary plant metabolites are utilized in plant carnivory to an extent greater than previously thought - we found a whole-metabolome response to prey capture. Plant carnivory, at the metabolic level, likely evolved from at least two distinct functions: attraction and defence. Findings of this study support the hypothesis that secondary metabolites play an important role in plant diversification and adaptation to new environments.

Sections du résumé

BACKGROUND AND AIMS
Secondary metabolites are integral to multiple key plant processes (growth regulation, pollinator attraction and interactions with conspecifics, competitors and symbionts) yet their role in plant adaptation remains an underexplored area of research. Carnivorous plants use secondary metabolites to acquire nutrients from prey, but the extent of the role of secondary metabolites in plant carnivory is not known. We aimed to determine the extent of the role of secondary metabolites in facilitating carnivory of the Cape sundew, Drosera capensis.
METHODS
We conducted metabolomic analysis of 72 plants in a time-series experiment before and after simulated prey capture. We used ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS) and the retention time index to identify compounds in the leaf trap tissue that changed up to 72 h following simulated prey capture. We identified associated metabolic pathways, and cross-compared these compounds with metabolites previously known to be involved in carnivorous plants across taxa.
KEY RESULTS
For the first time in a carnivorous plant, we have profiled the whole-leaf metabolome response to prey capture. Reliance on secondary plant metabolites was higher than previously thought - 2383 out of 3257 compounds in fed leaves had statistically significant concentration changes in comparison with unfed controls. Of these, ~34 compounds are also associated with carnivory in other species; 11 are unique to Nepenthales. At least 20 compounds had 10-fold changes in concentration, 12 of which had 30-fold changes and are typically associated with defence or attraction in non-carnivorous plants.
CONCLUSIONS
Secondary plant metabolites are utilized in plant carnivory to an extent greater than previously thought - we found a whole-metabolome response to prey capture. Plant carnivory, at the metabolic level, likely evolved from at least two distinct functions: attraction and defence. Findings of this study support the hypothesis that secondary metabolites play an important role in plant diversification and adaptation to new environments.

Identifiants

pubmed: 34077503
pii: 6291309
doi: 10.1093/aob/mcab065
pmc: PMC8389465
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

301-314

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the Annals of Botany Company.

Auteurs

Christopher R Hatcher (CR)

Loughborough University, Loughborough, UK.
Agri-Tech Centre, Pershore College, Part of WCG, Pershore, UK.

Ulf Sommer (U)

Biocrates Life Sciences AG, Innsbruck, Austria.

Liam M Heaney (LM)

Agri-Tech Centre, Pershore College, Part of WCG, Pershore, UK.

Jonathan Millett (J)

Agri-Tech Centre, Pershore College, Part of WCG, Pershore, UK.

Articles similaires

Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria
Fragaria Light Plant Leaves Osmosis Stress, Physiological
Risk Assessment Plant Leaves Isomerism Humans Stereoisomerism

Classifications MeSH