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Research article - Peer-reviewed, 2021

Stage-specific expression of an odorant receptor underlies olfactory behavioral plasticity in Spodoptera littoralis larvae

Revadi, Santosh, V; Giannuzzi, Vito Antonio; Rossi, Valeria; Hunger, Gert Martin; Conchou, Lucie; Rondoni, Gabriele; Conti, Eric; Anderson, Peter; Walker, William B.; Jacquin-Joly, Emmanuelle; Koutroumpa, Fotini; Becher, Paul G.

Abstract

Background: The detection of environmental cues and signals via the sensory system directs behavioral choices in diverse organisms. Insect larvae rely on input from the chemosensory system, mainly olfaction, for locating food sources. In several lepidopteran species, foraging behavior and food preferences change across larval instars; however, the molecular mechanisms underlying such behavioral plasticity during larval development are not fully understood. Here, we hypothesize that expression patterns of odorant receptors (ORs) change during development, as a possible mechanism influencing instar-specific olfactory-guided behavior and food preferences.Results: We investigated the expression patterns of ORs in larvae of the cotton leafworm Spodoptera littoralis between the first and fourth instar and revealed that some of the ORs show instar-specific expression. We functionally characterized one OR expressed in the first instar, SlitOR40, as responding to the plant volatile, beta-caryophyllene and its isomer alpha-humulene. In agreement with the proposed hypothesis, we showed that first but not fourth instar larvae responded behaviorally to beta-caryophyllene and alpha-humulene. Moreover, knocking out this odorant receptor via CRISPR-Cas9, we confirmed that instar-specific responses towards its cognate ligands rely on the expression of SlitOR40.Conclusion: Our results provide evidence that larvae of S. littoralis change their peripheral olfactory system during development. Furthermore, our data demonstrate an unprecedented instar-specific behavioral plasticity mediated by an OR, and knocking out this OR disrupts larval behavioral plasticity. The ecological relevance of such behavioral plasticity for S. littoralis remains to be elucidated, but our results demonstrate an olfactory mechanism underlying this plasticity in foraging behavior during larval development.

Keywords

alpha-Humulene; beta-Caryophyllene; CRISPR-Cas9; Electrophysiology; Larval transcriptome; Modulation; Odorant receptor; Olfactometer

Published in

BMC Biology
2021, volume: 19, number: 1, article number: 231
Publisher: BMC

Authors' information

Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Giannuzzi, Vito Antonio (Giannuzzi, Vito Antonio )
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Giannuzzi, Vito Antonio
University of Perugia
Rossi, Valeria
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Rossi, Valeria
University of Perugia
Hunger, Martin
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Conchou, Lucie
AGRIODOR
Rondoni, Gabriele
University of Perugia
Conti, Eric
University of Perugia
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Walker, William B. (Walker, William B.)
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Walker, William
United States Department of Agriculture (USDA)
Jacquin-Joly, Emmanuelle
Universite Paris-Est-Creteil-Val-de-Marne (UPEC)
Koutroumpa, Fotini
Universite Paris-Est-Creteil-Val-de-Marne (UPEC)
Swedish University of Agricultural Sciences, Department of Plant Protection Biology

UKÄ Subject classification

Biochemistry and Molecular Biology
Behavioral Sciences Biology

Publication Identifiers

DOI: https://doi.org/10.1186/s12915-021-01159-1

URI (permanent link to this page)

https://res.slu.se/id/publ/114308