Deorphanizing an odorant receptor tuned to palm tree volatile esters in the Asian palm weevil sheds light on the mechanisms of palm tree selection.

Deorphanization odorant receptor palm esters palm weevil sustainable palm agriculture synergistic effect

Journal

Insect biochemistry and molecular biology
ISSN: 1879-0240
Titre abrégé: Insect Biochem Mol Biol
Pays: England
ID NLM: 9207282

Informations de publication

Date de publication:
02 May 2024
Historique:
received: 24 01 2024
revised: 06 04 2024
accepted: 28 04 2024
medline: 5 5 2024
pubmed: 5 5 2024
entrez: 4 5 2024
Statut: aheadofprint

Résumé

The Asian palm weevil, Rhynchophorus ferrugineus, is a tremendously important agricultural pest primarily adapted to palm trees and causes severe destruction, threatening sustainable palm cultivation worldwide. The host plant selection of this weevil is mainly attributed to the functional specialization of odorant receptors (ORs) that detect palm-derived volatiles. Yet, ligands are known for only two ORs of R. ferrugineus, and we still lack information on the mechanisms of palm tree detection. This study identified a highly expressed antennal R. ferrugineus OR, RferOR2, thanks to newly generated transcriptomic data. The phylogenetic analysis revealed that RferOR2 belongs to the major coleopteran OR group 2A and is closely related to a sister clade containing an R. ferrugineus OR (RferOR41) tuned to the non-host plant volatile and antagonist, α-pinene. Functional characterization of RferOR2 via heterologous expression in Drosophila olfactory neurons revealed that this receptor is tuned to several ecologically relevant palm-emitted odors, most notably ethyl and methyl ester compounds, but not to any of the pheromone compounds tested, including the R. ferrugineus aggregation pheromone. We did not evidence any differential expression of RferOR2 in the antennae of both sexes, suggesting males and females detect these compounds equally. Next, we used the newly identified RferOR2 ligands to demonstrate that including synthetic palm ester volatiles as single compounds and in combinations in pheromone-based mass trapping has a synergistic attractiveness effect to R. ferrugineus aggregation pheromone, resulting in significantly increased weevil catches. Our study identified a key OR from a palm weevil species tuned to several ecologically relevant palm volatiles and represents a significant step forward in understanding the chemosensory mechanisms of host detection in palm weevils. Our study also defines RferOR2 as an essential model for exploring the molecular basis of host detection in other palm weevil species. Finally, our work showed that insect OR deorphanization could aid in identifying novel behaviorally active volatiles that can interfere with weevil host-searching behavior in sustainable pest management applications.

Identifiants

pubmed: 38704126
pii: S0965-1748(24)00060-2
doi: 10.1016/j.ibmb.2024.104129
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104129

Informations de copyright

Copyright © 2024. Published by Elsevier Ltd.

Déclaration de conflit d'intérêts

Declaration of Competing Interest BA, NM, EJJ, and AP are inventors of palm ester combinations in the field trap experiment and may have a financial interest in patent applications related to R. ferrugineus pest management. BA, NM, EJJ, KP, KC, and AP have interests in filing patent applications related to R. ferrugineus RferOR2-biosensor for pest management applications. The remaining authors declare that they have no competing financial interests.

Auteurs

Binu Antony (B)

King Saud University, Chair of Date Palm Research, Center for Chemical Ecology and Functional Genomics, Department of Plant Protection, College of Food and Agricultural Sciences, Riyadh 11451, Saudi Arabia. Electronic address: bantony@ksu.edu.sa.

Nicolas Montagné (N)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, 78000 Versailles, France.

Arthur Comte (A)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, 78000 Versailles, France.

Sara Mfarrej (S)

King Abdullah University of Science and Technology (KAUST), Bioscience Programme, BESE Division, Thuwal, Jeddah 23955-6900, Saudi Arabia.

Jernej Jakše (J)

University of Ljubljana, Biotechnical Faculty, Agronomy Department, SI-1000 Ljubljana, Slovenia.

Rémi Capoduro (R)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, 78000 Versailles, France.

Rajan Shelke (R)

Don Bosco College of Agriculture, Agricultural Entomology Department, Sulcorna, Goa 403705, India.

Khasim Cali (K)

The University of Manchester, Department of Chemical Engineering, Manchester, M13 9PL, UK.

Mohammed Ali AlSaleh (MA)

King Saud University, Chair of Date Palm Research, Center for Chemical Ecology and Functional Genomics, Department of Plant Protection, College of Food and Agricultural Sciences, Riyadh 11451, Saudi Arabia.

Krishna Persaud (K)

The University of Manchester, Department of Chemical Engineering, Manchester, M13 9PL, UK.

Arnab Pain (A)

King Abdullah University of Science and Technology (KAUST), Bioscience Programme, BESE Division, Thuwal, Jeddah 23955-6900, Saudi Arabia.

Emmanuelle Jacquin-Joly (E)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, 78000 Versailles, France.

Classifications MeSH