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

Revadi, Santosh and Giannuzzi, Vito Antonio and Giannuzzi, Vito Antonio and Rossi, Valeria and Hunger, Martin and Conchou, Lucie and Rondoni, Gabriele and Conti, Eric and Anderson, Peter and Walker, William B. and Walker, William and Jacquin-Joly, Emmanuelle and Koutroumpa, Fotini and Becher, Paul (2021). Stage-specific expression of an odorant receptor underlies olfactory behavioral plasticity in Spodoptera littoralis larvae. BMC Biology. 19 , 231
[Research article]

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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.

Authors/Creators:Revadi, Santosh and Giannuzzi, Vito Antonio and Giannuzzi, Vito Antonio and Rossi, Valeria and Hunger, Martin and Conchou, Lucie and Rondoni, Gabriele and Conti, Eric and Anderson, Peter and Walker, William B. and Walker, William and Jacquin-Joly, Emmanuelle and Koutroumpa, Fotini and Becher, Paul
Title:Stage-specific expression of an odorant receptor underlies olfactory behavioral plasticity in Spodoptera littoralis larvae
Series Name/Journal:BMC Biology
Year of publishing :2021
Volume:19
Article number:231
Number of Pages:18
Publisher:BMC
ISSN:1741-7007
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Behavioural Sciences Biology
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Biochemistry and Molecular Biology
Keywords:alpha-Humulene, beta-Caryophyllene, CRISPR-Cas9, Electrophysiology, Larval transcriptome, Modulation, Odorant receptor, Olfactometer
URN:NBN:urn:nbn:se:slu:epsilon-p-114308
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-114308
Additional ID:
Type of IDID
DOI10.1186/s12915-021-01159-1
Web of Science (WoS)000711874400001
ID Code:26095
Faculty:LTV - Fakulteten för landskapsarkitektur, trädgårds- och växtproduktionsvetenskap
Department:(LTJ, LTV) > Department of Plant Protection Biology
Deposited By: SLUpub Connector
Deposited On:12 Nov 2021 10:20
Metadata Last Modified:12 Nov 2021 10:21

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