Acylsugars, Nicotine and a Protease Inhibitor Provide Variable Protection for Nicotiana benthamiana in a Natural Setting.

Nicotiana benthamiana acylsugars insects invertebrates natural setting nicotine snails specialized metabolites

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
14 Oct 2024
Historique:
revised: 05 09 2024
received: 23 05 2024
accepted: 25 09 2024
medline: 14 10 2024
pubmed: 14 10 2024
entrez: 14 10 2024
Statut: aheadofprint

Résumé

Plants produce an immense diversity of defensive specialized metabolites. However, despite extensive functional characterization, the relative importance of different defensive compounds is rarely examined in natural settings. Here, we compare the efficacy of three Nicotiana benthamiana defensive compounds, nicotine, acylsugars and a serine protease inhibitor, by growing plants with combinations of knockout mutations in a natural setting, quantifying invertebrate interactions and comparing relative plant performance. Among the three tested compounds, acylsugars had the greatest defensive capacity, affecting aphids, leafhoppers, spiders and flies. Nicotine mutants displayed increased leafhopper feeding and aphid colonization. Plants lacking both nicotine and acylsugars were more susceptible to flea beetles and thrips. By contrast, knockout of the serine protease inhibitor did not affect insect herbivory in the field. Complementary experiments under controlled laboratory conditions with caterpillars, grasshoppers and aphids confirmed results obtained in a natural setting. We conclude that the three metabolite groups collectively provide broad-spectrum protection to N. benthamiana. However, there is a gradient in their effects on the interacting invertebrates present in the field. Furthermore, we demonstrate that, even if individual metabolites do not have a measurable defensive benefit on their own, they can have an additive effect when combined with other defensive compounds.

Identifiants

pubmed: 39400373
doi: 10.1111/pce.15195
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : This research was made possible by US Department of Agriculture postdoctoral fellowship number 2022-67012-36739 to Boaz Negin, and by US Department of Agriculture award 2021-67013-33565 and a Triad Foundation award to Georg Jander.

Informations de copyright

© 2024 John Wiley & Sons Ltd.

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Auteurs

Boaz Negin (B)

Boyce Thompson Institute, Ithaca, New York, USA.

Fumin Wang (F)

Boyce Thompson Institute, Ithaca, New York, USA.

Hillary D Fischer (HD)

Boyce Thompson Institute, Ithaca, New York, USA.

Georg Jander (G)

Boyce Thompson Institute, Ithaca, New York, USA.

Classifications MeSH