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

Authors: REVADI, SANTOSH - Swedish University Of Agricultural Sciences; GIANUZZI, VITO-ANTONIO - Swedish University Of Agricultural Sciences; ROSSI, VALERIA - Swedish University Of Agricultural Sciences; HUNGER, GERT - Swedish University Of Agricultural Sciences; CONCHOU, LUCIE - Agriodor; RONDONI, GABRIELE - University Of Perugia; CONTI, ERIC - University Of Perugia; ANDERSON, PETER - Swedish University Of Agricultural Sciences; Walker, William; JACQUIN-JOLY, EMMANUELLE - Inrae; KOUTROUMPA, FOTINI - Inrae; BECHER, PAUL - Swedish University Of Agricultural Sciences

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/9/2021
Publication Date: 10/28/2021
Citation: Revadi, S.V., Gianuzzi, V., Rossi, V., Hunger, G.M., Conchou, L., Rondoni, G., Conti, E., Anderson, P., Walker III, W.B., Jacquin-Joly, E., Koutroumpa, F., Becher, P.G. 2021. Stage-specific expression of an odorant receptor underlies olfactory behavioral plasticity in Spodoptera littoralis larvae. BMC Biology. 19. Article 231. https://doi.org/10.1186/s12915-021-01159-1.
DOI: https://doi.org/10.1186/s12915-021-01159-1

Interpretive Summary: The Egyptian cotton leafworm is a polyphagous insect pest to numerous and varied agricultural crops across Europe, the Middle East and Africa. In recent decades, it has emerged as a model moth species for chemical ecology research. However, knowledge gaps remain, especially as it relates to the olfactory system and olfactory-based behaviors in the leafworm caterpillar, which is the life-stage that directly damages crop plants. Characterization of odorant receptors expressed in the olfactory system of the leafworm caterpillar revealed developmental regulation of gene expression. Some odorant receptors are expressed throughout all stages of caterpillar development, while others are expressed only during late or early stages of development. Differential expression of odorant receptors is hypothesized to serve as a genetic mechanism underlying different behaviors exhibited by the leafworm caterpillar throughout its pre-adult development. This knowledge establishes a foundation for future research on Egyptian cotton leafworm and other lepidopteran species involving practical measures to manipulate caterpillar behavior using odorants, aimed at reducing infestations and damage to crop plants

Technical Abstract: Insect larvae rely on sensory input, mainly olfaction for locating food sources. In several lepidopteran species, foraging behavior and food preferences change across larval instars. 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. 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 of these ORs, SlitOR40 as responding to plant the volatile, ß-caryophyllene and its isomer a-humulene. In agreement with the proposed hypothesis, we showed that first but not fourth instar larvae responded behaviorally to ß-caryophyllene and a-humulene. Moreover, knocking-out this odorant receptor via CRISPR-Cas9, we confirmed that instar specific responses towards its cognate ligands rely on expression of SlitOR40. Our results provide evidence that larvae of S. littoralis change their peripheral olfactory system during development. Furthermore, our data demonstrate an unprecedented instar-specific behavioural 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