Abstract
Insect chemosensation is crucial for many aspects related to food seeking, enemy avoidance, and reproduction. Different families of receptors and binding proteins interact with chemical stimuli, including odorant receptors (ORs), ionotropic receptors (IRs), gustatory receptors (GRs), odorant binding proteins (OBPs) and chemosensory proteins (CSPs). In this work, we describe the chemosensory-related gene repertoire of the worldwide pest Spodoptera exigua (Lepidoptera: Noctuidae), focusing on the transcripts expressed in larvae, which feed on many horticultural crops producing yield losses. A comprehensive de novo assembly that includes reads from chemosensory organs of larvae and adults, and other larval tissues, enabled us to annotate 200 candidate chemosensory-related genes encoding 63 ORs, 28 IRs, 38 GRs, 48 OBPs and 23 CSPs. Of them, 51 transcripts are new annotations. Fifty ORs are expressed in larval heads based on RNA-seq and reverse transcription PCR analyses. Fourteen OBPs are expressed in larval, but not in adult heads. We also observe that expression profiles of ORs are strongly and non-specifically up-regulated upon pre-exposure of larvae to single volatile organic compounds (VOCs). Finally, we develop a behavioural assay to study the attraction/repellence to VOCs in S. exigua larvae and thus identify candidate ecologically relevant odours. A single-dose assay demonstrated that 1-hexanol triggers attraction and indole repels larvae at any timepoint. This work establishes the foundation for the study of chemosensation in S. exigua larvae, allowing further studies aimed to characterize chemosensory-related genes that underlie the ecologically relevant behaviours of larvae.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allison JD, Carde RT (Eds.), 2016 Pheromone communications in Moths: Evolution, Behaviour and Application, American Entomologist. https://doi.org/10.1093/ae/tmx062
Anderson P, Sadek MM, Larsson M, Hansson BS, Thöming G (2013) Larval host plant experience modulates both mate finding and oviposition choice in a moth. Anim Behav 85:1169–1175. https://doi.org/10.1016/j.anbehav.2013.03.002
Becher PG, Guerin PM (2009) Oriented responses of grapevine moth larvae Lobesia botrana to volatiles from host plants and an artificial diet on a locomotion compensator. J Insect Physiol 55:384–393. https://doi.org/10.1016/j.jinsphys.2009.01.006
Bell RA, Joachim FG (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373. https://doi.org/10.1093/aesa/69.2.365
Carroll MJ, Berenbaum MR (2002) Behavioral responses of the parsnip webworm to host plant volatiles. J Chem Ecol 28:2191–2201. https://doi.org/10.1023/A:1021093114663
Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924. https://doi.org/10.1007/s10886-006-9117-9
Carroll MJ, Schmelz EA, Teal PEA (2008) The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J Chem Ecol 34:291–300. https://doi.org/10.1007/s10886-007-9414-y
Chang H, Liu Y, Yang T, Pelosi P, Dong S, Wang G (2015) Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Sci Rep 5:1–12. https://doi.org/10.1038/srep13093
Chang H, Ai D, Zhang J, Dong S, Liu Y, Wang G (2017) Candidate odorant binding proteins and chemosensory proteins in the larval chemosensory tissues of two closely related noctuidae moths, Helicoverpa armigera and H . assulta. PLoS One 12:e0179243. https://doi.org/10.1371/journal.pone.0179243
Cheng T, Wu J, Wu Y, Chilukuri RV, Huang L, Yamamoto K, Feng L, Li W, Chen Z, Guo H, Liu J, Li S, Wang X, Peng L, Liu D, Guo Y, Fu B, Li Z, Liu C, Chen Y, Tomar A, Hilliou F, Montagné N, Jacquin-Joly E, D’Alençon E, Seth RK, Bhatnagar RK, Jouraku A, Shiotsuki T, Kadono-Okuda K, Promboon A, Smagghe G, Arunkumar KP, Kishino H, Goldsmith MR, Feng Q, Xia Q, Mita K (2017) Genomic adaptation to polyphagy and insecticides in a major east Asian noctuid pest. Nat Ecol Evol 1:1747–1756
Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6:e1001064. https://doi.org/10.1371/journal.pgen.1001064
Davidson NM, Oshlack A (2014) Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biol 15:1–14. https://doi.org/10.1186/s13059-014-0410-6
de Fouchier A, Sun X, Caballero-Vidal G, Travaillard S, Jacquin-Joly E, Montagné N (2018) Behavioral effect of plant volatiles binding to Spodoptera littoralis larval odorant receptors. Front Behav Neurosci 12:1–8. https://doi.org/10.3389/fnbeh.2018.00264
Depetris-Chauvin A, Galagovsky D, Grosjean Y (2015) Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila. Front Ecol Evol 3. https://doi.org/10.3389/fevo.2015.00041
Di C, Ning C, Huang LQ, Wang CZ (2017) Design of larval chemical attractants based on odorant response spectra of odorant receptors in the cotton bollworm. Insect Biochem Mol Biol 84:48–62. https://doi.org/10.1016/j.ibmb.2017.03.007
Dion E, Monteiro A, Nieberding CM (2019) The role of learning on insect and spider sexual behaviors, sexual trait evolution, and speciation. Front Ecol Evol 6. https://doi.org/10.3389/fevo.2018.00225
Du L, Liu Y, Zhang J, Gao X, Wang B, Wang G (2018) Identification and characterization of chemosensory genes in the antennal transcriptome of Spodoptera exigua. Comparative Biochemistry and Physiology - Part D Identification and characterization of chemosensory genes in the antennal transcriptome of Spod Comp Biochem Physiol - Part D 27:54–65. https://doi.org/10.1016/j.cbd.2018.05.001
Dunipace L, Meister S, Mcnealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822–835. https://doi.org/10.1016/s0960-9822(01)00258-5
Dweck HKM, Ebrahim SAM, Retzke T, Grabe V, Weißflog J, Svatoš A, Hansson BS, Knaden M (2018) The olfactory logic behind fruit odor preferences in larval and adult Drosophila. Cell Rep 23:2524–2531. https://doi.org/10.1016/j.celrep.2018.04.085
Ebrahim SAM, Dweck HKM, Stökl J, Hofferberth JE, Trona F, Weniger K, Rybak J, Seki Y, Stensmyr MC, Sachse S, Hansson BS, Knaden M (2015) Drosophila avoids parasitoids by sensing their semiochemicals via a dedicated olfactory circuit. PLoS Biol 13:1–18. https://doi.org/10.1371/journal.pbio.1002318
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Forêt S, Wanner KW, Maleszka R (2007) Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochem Mol Biol 37:19–28. https://doi.org/10.1016/j.ibmb.2006.09.009
García-Robledo C, Horvitz CC (2012) Parent-offspring conflicts, “optimal bad motherhood” and the “mother knows best” principles in insect herbivores colonizing novel host plants. Ecol Evol 2:1446–1457. https://doi.org/10.1002/ece3.267
Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings TCJ, Erb M, Herrero S (2019) Can herbivore-induced volatiles protect plants by increasing the herbivores’ susceptibility to natural pathogens? Appl Environ Microbiol 85:1–10. https://doi.org/10.1128/AEM.01468-18
Gomez-Diaz C, Martin F, Garcia-Fernandez JM, Alcorta E (2018) The two main olfactory receptor families in Drosophila, ORs and IRs: a comparative approach. Front Cell Neurosci 12. https://doi.org/10.3389/fncel.2018.00253
Gouin A, Bretaudeau A, Nam K, Gimenez S, Aury J, Duvic B, Hilliou F, Durand N, Montagné N, Darboux I, Kuwar S, Chertemps T, Siaussat D, Bretschneider A, Mo Y, Ahn S, Hänniger S, Grenet AG, Neunemann D, Anderson AR, Khan SA, Dumas P, Orsucci M, Belser C, Alberti A, Noel B, Couloux A (2017) Two genomes of highly polyphagous lepidopteran pests with different host-plant ranges. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-10461-4
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Greenberg SM, Sappington TW, Legaspi BC, Liu T, Sétamou M (2006) Feeding and life history of Spodoptera exigua (Lepidoptera: Noctuidae) on different host plants. Ann Entomol Soc Am 94:566–575. https://doi.org/10.1603/0013-8746(2001)094[0566:FALHOS]2.0.CO;2
Gu SH, Zhou JJ, Gao S, Wang DH, Li XC, Guo YY, Zhang YJ (2015) Identification and comparative expression analysis of odorant binding protein genes in the tobacco cutworm Spodoptera litura. Sci Rep 5:13800. https://doi.org/10.1038/srep13800
Guo H, Cheng T, Chen Z, Jiang L, Guo Y, Liu J, Li S, Taniai K, Asaoka K, Kadono-Okuda K, Arunkumar KP, Wu J, Kishino H, Zhang H, Seth RK, Gopinathan KP, Montagné N, Jacquin-Joly E, Goldsmith MR, Xia Q, Mita K (2017) Expression map of a complete set of gustatory receptor genes in chemosensory organs of Bombyx mori. Insect Biochem Mol Biol 82:74–82. https://doi.org/10.1016/j.ibmb.2017.02.001
Haverkamp A, Hansson BS, Knaden M (2018) Combinatorial codes and labeled lines: how insects use olfactory cues to find and judge food, mates, and oviposition sites in complex environments. Front Physiol 9:1–8. https://doi.org/10.3389/fphys.2018.00049
Jin R, Liu NY, Liu Y, Dong SL (2015) A larval specific OBP able to bind the major female sex pheromone component in Spodoptera exigua (Hübner). J Integr Agric 14:1356–1366. https://doi.org/10.1016/S2095-3119(14)60849-2
Johnson BR, Atallah J, Plachetzki DC (2013) The importance of tissue specificity for RNA-seq: highlighting the errors of composite structure extractions. BMC Genomics 14:586. https://doi.org/10.1186/1471-2164-14-586
Joseph R, Carlson JR (2017) Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Physiol Behav 176:139–148. https://doi.org/10.1016/j.physbeh.2017.03.040
Koerte S, Keesey IW, Khallaf MA, Cortés Llorca L, Grosse-Wilde E, Hansson BS, Knaden M (2018) Evaluation of the DREAM technique for a high-throughput deorphanization of chemosensory receptors in Drosophila. Front Mol Neurosci 11:1–13. https://doi.org/10.3389/fnmol.2018.00366
Koh T, He Z, Gorur-shandilya S, Menuz K, Larter NK, Carlson JR (2015) The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors. Neuron 83:850–865. https://doi.org/10.1016/j.neuron.2014.07.012
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–360. https://doi.org/10.1038/nmeth.1923
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12. https://doi.org/10.1186/1471-2105-12-323
Liu C. Liu Y, Walker WB, Dong S, Wang G (2013) Identification and functional characterization of sex pheromone receptors in beet armyworm Spodoptera exigua (Hubner). Insect Biochem Mol Biol 43:747–754. https://doi.org/10.1016/j.cbpa.2013.03.016
Liu NY, Yang K, Liu Y, Xu W, Anderson A, Dong SL (2015a) Two general-odorant binding proteins in Spodoptera litura are differentially tuned to sex pheromones and plant odorants. Comp Biochem Physiol -Part A Mol Integr Physiol 180:23–31. https://doi.org/10.1016/j.cbpa.2014.11.005
Liu NY, Zhang T, Ye ZF, Li F, Dong SL (2015b) Identification and characterization of candidate chemosensory gene families from Spodoptera exigua developmental transcriptomes. Int J Biol Sci 11:1036–1048. https://doi.org/10.7150/ijbs.12020
Liu NY, Xu W, Dong SL, Zhu JY, Xu YX, Anderson A (2018) Genome-wide analysis of ionotropic receptor gene repertoire in Lepidoptera with an emphasis on its functions of Helicoverpa armigera. Insect Biochem Mol Biol 99:37–53. https://doi.org/10.1016/j.ibmb.2018.05.005
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
McCormick AC, Heyer J, Sims JW, Mescher MC, De Moraes CM (2017) Exploring the effects of plant odors, from tree species of differing host quality, on the response of Lymantria dispar males to female sex pheromones. J Chem Ecol 43:243–253. https://doi.org/10.1007/s10886-017-0825-0
Montagné N, De Fouchier A, Newcomb RD, Jacquin-Joly E (2015) Advances in the identification and characterization of olfactory receptors in insects. Prog Mol Biol Transl Sci 130:55–80. https://doi.org/10.1016/bs.pmbts.2014.11.003
Mooney AC, Robertson HM, Wanner KW (2009) Neonate silkworm (Bombyx mori) larvae are attracted to mulberry (Morus alba) leaves with conspecific feeding damage. J Chem Ecol 35:552–559. https://doi.org/10.1007/s10886-009-9639-z
Ning C, Yang K, Xu M, Huang LQ, Wang CZ (2016) Functional validation of the carbon dioxide receptor in labial palps of Helicoverpa armigera moths. Insect Biochem Mol Biol 73:12–19. https://doi.org/10.1016/j.ibmb.2016.04.002
Pelosi P, Calvello M, Ban L (2005) Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem Senses 30:i291–i292. https://doi.org/10.1093/chemse/bjh229
Piesik D, Weaver DK, Runyon JB, Buteler M, Peck GE, Morrill WL (2008) Behavioural responses of wheat stem sawflies to wheat volatiles. Agric For Entomol 10:245–253. https://doi.org/10.1111/j.1461-9563.2008.00380.x
Poivet E, Rharrabe K, Monsempes C, Glaser N, Rochat D, Renou M, Marion-Poll F, Jacquin-Joly E (2012) The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars. Nat Commun 3. https://doi.org/10.1038/ncomms2050
Poivet E, Gallot A, Montagné N, Glaser N, Legeai F, Jacquin-Joly E (2013) A comparison of the olfactory gene repertoires of adults and larvae in the noctuid moth Spodoptera littoralis. PLoS One 8:e60263. https://doi.org/10.1371/journal.pone.0060263
Ramachandran R, Norris DM (1991) Volatiles mediating plant-herbivore-natural enemy interactions: Electroantennogram responses of soybean looper, Pseudoplusia includens, and a parasitoid, Microplitis demolitor, to green leaf volatiles. J Chem Ecol 17:1665–1690. https://doi.org/10.1007/BF00984696
Rharrabe K, Jacquin-Joly E, Marion-Poll F (2014) Electrophysiological and behavioral responses of Spodoptera littoralis caterpillars to attractive and repellent plant volatiles. Front Ecol Evol 2:1–9. https://doi.org/10.3389/fevo.2014.00005
Robertson HM (2015) The insect chemoreceptor superfamily is ancient in animals. Chem Senses 40:609–614. https://doi.org/10.1093/chemse/bjv046
Robinson MD, McCarthy DJ, Smyth GK (2009) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Rytz R, Croset V, Benton R (2013) Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol 43:888–897. https://doi.org/10.1016/j.ibmb.2013.02.007
Scherer S, Stocker RF, Gerber B (2003) Olfactory learning in individually assayed Drosophila larvae. Learn Mem 10:217–225. https://doi.org/10.1101/lm.57903
Singh AK, Mullick S (2002) Leaf volatiles as attractants for neonate Helicoverpa armigera Hbn. (Lep., Noctuidae) larvae. J Appl Entomol 126:14–19. https://doi.org/10.1046/j.1439-0418.2002.00600.x
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, Wicher D, Sachse S, Knaden M, Becher PG, Seki Y, Hansson BS (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357. https://doi.org/10.1016/j.cell.2012.09.046
Sun JS, Xiao S, Carlson JR. 2018 The diverse small proteins called odorant-binding proteins Open Biol 8. https://doi.org/10.1098/rsob.180208
Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19:881–890. https://doi.org/10.1016/j.cub.2009.04.035
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. https://doi.org/10.1093/nar/gkm306
van Schooten B, Jiggins CD, Briscoe AD, Papa R (2016) Genome-wide analysis of ionotropic receptors provides insight into their evolution in Heliconius butterflies. BMC Genomics 17:1–15. https://doi.org/10.1186/s12864-016-2572-y
Vogt RG, Große-Wilde E, Zhou JJ (2015) The Lepidoptera odorant binding protein gene family: gene gain and loss within the GOBP/PBP complex of moths and butterflies. Insect Biochem Mol Biol 62:142–153. https://doi.org/10.1016/j.ibmb.2015.03.003
Von Der Weid B, Rossier D, Lindup M, Tuberosa J, Widmer A, Col JD, Kan C, Carleton A, Rodriguez I (2015) Large-scale transcriptional profiling of chemosensory neurons identifies receptor-ligand pairs in vivo. Nat Neurosci 18:1455–1463. https://doi.org/10.1038/nn.4100
Walker WB, Gonzalez F, Garczynski SF, Witzgall P (2016) The chemosensory receptors of codling moth Cydia pomonella-expression in larvae and adults. Sci Rep 6:1–15. https://doi.org/10.1038/srep23518
Walker WB, Roy A, Anderson P, Schlyter F, Hansson BS, Larsson MC (2019) Transcriptome analysis of gene families involved in chemosensory function in Spodoptera littoralis (Lepidoptera: Noctuidae). BMC Genomics 20:428. https://doi.org/10.1186/s12864-019-5815-x
Wan X, Qian K, Du Y (2015) Synthetic pheromones and plant volatiles alter the expression of chemosensory genes in Spodoptera exigua. Sci Rep 5. https://doi.org/10.1038/srep17320
Wanner KW, Robertson HM (2008) The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 17:621–629. https://doi.org/10.1111/j.1365-2583.2008.00836.x
Xu P, Wen X, Leal WS (2020) CO2 per se activates carbon dioxide receptors. Insect Bioechm Mol Biol doi 117:103284. https://doi.org/10.1016/j.ibmb.2019.103284
Zhang S, Liu H, Kong X, Wang H, Liu F, Zhang Z (2017) Identification and expression profiling of chemosensory genes in Dendrolimus punctatus Walker. Front Physiol 8:471. https://doi.org/10.3389/fphys.2017.00471
Zhang Y, Xue T, Sun L (2018) Identification of chemosensory genes based on the transcriptomic analysis of six different chemosensory organs in Spodoptera exigua. Insects Rear Tissue Coll 9:1–18. https://doi.org/10.3389/fphys.2018.00432
Zheng XL, Cong XP, Wang XP, Lei CL (2011) A review of geographic distribution, overwintering and migration in Spodoptera exigua Hübner (Lepidoptera: Noctuidae). J Entomol Res Soc 13:39–48
Zhou JJ, 2010 Odorant-binding proteins in insects, in: vitamins and hormones (Gerald Litwack, ed). 83, pp. 241–272, academic press. https://doi.org/10.1016/S0083-6729(10)83010-9
Zhu J, Ban L, Song LM, Liu Y, Pelosi P, Wang G (2016) General odorant-binding proteins and sex pheromone guide larvae of Plutella xylostella to better food. Insect Biochem Mol Biol 72:10–19. https://doi.org/10.1016/j.ibmb.2016.03.005
Zhu JY, Xu ZW, Zhang XM, Liu NY (2018) Genome-based identification and analysis of ionotropic receptors in Spodoptera litura. Naturewissenschaften 105:38. https://doi.org/10.1007/s00114-018-1563-z
Zielonka M, Gehrke P, Badeke E, Sachse S (2016) Larval sensilla of the moth Heliothis virescens respond to sex pheromone components. Insect Mol Biol 25:666–678. https://doi.org/10.1111/imb.12253
Acknowledgements
We thank Rosa María González-Martínez and Óscar Marín-Vázquez at the University of Valencia (Spain) for their excellent help with insect rearing and laboratory management. We thank Marie-Christine François, Christelle Monsempès and Gabriela Caballero-Vidal at iEES-Paris (Versailles, France) for helping in chemosensory gene annotation.
Availability of Data and Material
Raw reads and the de novo assembled transcriptome generated during the study have been deposited at NCBI under project number PRJNA634227.
Funding
This work has been supported by projects from the Spanish Ministry of Science, Innovation and Universities (No. AGL2014–57752-C2-2R and RTI2018–094350-B-C32). ALG was the recipient of a PhD grant from the Spanish Ministry of Science, Innovation and Universities (No. BES-2015-071369). CMC was supported by a Juan de la Cierva contract (No. IJCI-2017-32501).
Author information
Authors and Affiliations
Contributions
ALG participated in the design of the experiments, annotated transcripts, carried out behavioural and molecular biology experiments, analysed results and drafted the manuscript, TCO carried out the molecular biology experiments, EJJ participated in result discussion and revised the manuscript, SH participated in the design of the experiments, acquired funding, discussed the results and revised the manuscript, CC participated in the design of the experiments, analysed RNA-seq data, discussed the results and revised the manuscript.
Corresponding authors
Ethics declarations
Competing Interests
The authors declare that they have no competing interests.
Code Availability
Not applicable.
Rights and permissions
About this article
Cite this article
Llopis-Giménez, A., Carrasco-Oltra, T., Jacquin-Joly, E. et al. Coupling Transcriptomics and Behaviour to Unveil the Olfactory System of Spodoptera exigua Larvae. J Chem Ecol 46, 1017–1031 (2020). https://doi.org/10.1007/s10886-020-01224-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-020-01224-z