Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths.
Spodoptera
Xenopus oocytes
pheromone
pheromone receptor
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
Apr 2023
Apr 2023
Historique:
revised:
24
06
2022
received:
25
05
2022
accepted:
08
07
2022
medline:
4
4
2023
pubmed:
7
8
2022
entrez:
6
8
2022
Statut:
ppublish
Résumé
Moths possess an extremely sensitive and diverse sex pheromone processing system, in which pheromone receptors (PRs) are essential to ensure communication between mating partners. Functional properties of some PRs are conserved among species, which is important for reproduction. However, functional differentiation has occurred in some homologous PR genes, which may drive species divergence. Here, using genome analysis, 17 PR genes were identified from Spodoptera frugiperda, S. exigua, and S. litura, which belong to 6 homologous groups (odorant receptor [OR]6, 11, 13, 16, 56, and 62); of which 6 PR genes (OR6, OR11, OR13, OR16, OR56, and OR62) were identified in S. frugiperda and S. exigua, and 5 PR genes were identified in S. litura, excluding OR62. Using heterologous expression in Xenopus oocytes, we characterized the functions of PR orthologs including OR6, OR56, and OR62, which have not been clarified in previous studies. OR6 orthologs were specifically tuned to (Z,E)-9,12-tetradecadienyl acetate (Z9,E12-14:OAc), and OR62 orthologs were robustly tuned to Z7-12:OAc in S. frugiperda and S. exigua. The optimal ligand for OR56 was Z7-12:OAc in S. frugiperda, but responses were minimal in S. exigua and S. litura. In addition, SfruOR6 was male antennae-specific, whereas SfruOR56 and SfruOR62 were male antennae-biased. Our study further clarified the functional properties of PRs in 3 Spodoptera moth species, providing a comprehensive understanding of the mechanisms of intraspecific communication and interspecific isolation in Spodoptera.
Identifiants
pubmed: 35932282
doi: 10.1111/1744-7917.13098
doi:
Substances chimiques
Sex Attractants
0
Receptors, Pheromone
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
305-320Subventions
Organisme : National Natural Science Foundation of China
ID : 31725023
Organisme : National Natural Science Foundation of China
ID : 31911530234
Organisme : National Natural Science Foundation of China
ID : 32072509
Organisme : National Key Research and Development Program of China
ID : 2021YFD1400703
Organisme : Shenzhen Science and Technology Program
ID : KQTD20180411143628272
Organisme : Central Public-interest Scientific Institution Basal Research Fund
ID : CAAS-ZDRW202108
Organisme : Projects subsidized by Special Funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District
ID : PT202101-02
Organisme : Agricultural Science and Technology Innovation Program
Informations de copyright
© 2022 Institute of Zoology, Chinese Academy of Sciences.
Références
Ando, T. & Yamakawa, R. (2011) Analyses of lepidopteran sex pheromones by mass spectrometry. TrAC Trends in Analytical Chemistry, 30, 990-1002.
Andrade, R., Rodriguez, C. & Oehlschlager, A.C. (2000) Optimization of a pheromone lure for Spodoptera frugiperda (Smith) in Central America. Journal of the Brazilian Chemical Society, 11, 609-613.
Baker, T.C., Ochieng, S.A., Cosse, A.A., Lee, S.G., Todd, J.L., Quero, C. et al. (2004) A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. Journal of Comparative Physiology A Neuroethology, Sensory, Neural, and Behavioral Physiology, 190, 155-165.
Batista-Pereira, L.G., Stein, K., De Paula, A.F., Moreira, J.A., Cruz, I., Figueiredo, M.L.C. et al. (2006) Isolation, identification, synthesis, and field evaluation of the sex pheromone of the Brazilian population of Spodoptera frugiperda. Journal of Chemical Ecology, 32, 1085-1099.
Cao, S., Liu, Y., Wang, B. & Wang, G. (2021) A single point mutation causes one-way alteration of pheromone receptor function in two Heliothis species. iScience, 24, 102981.
Cao, S., Liu, Y. & Wang, G. (2020) Research progress of pheromone receptors in moths. Acta Entomological Sinica, 63, 1546-1568.
Chang, H., Guo, M., Wang, B., Liu, Y., Dong, S. & Wang, G. (2016) Sensillar expression and responses of olfactory receptors reveal different peripheral coding in two Helicoverpa species using the same pheromone components. Scientific Reports, 6, 18742.
Cheng, T., Wu, J., Wu, Y., Chilukuri, R.V., Huang, L., Yamamoto, K. et al. (2017) Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. Nature Ecology & Evolution, 1, 1747-1756.
De Fouchier, A., Sun, X., Monsempes, C., Mirabeau, O., Jacquin-Joly, E. & Montagné, N. (2015) Evolution of two receptors detecting the same pheromone compound in crop pest moths of the genus Spodoptera. Frontiers in Ecology and Evolution, 3, 1-11.
Deshmukh, S., Kalleshwaraswamy, C.M., Asokan, R., Swamy, H.M.M., Maruthi, M.S., Pavithra, H.B. et al. (2018) First report of the fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Management in Horticultural Ecosystems, 24, 23-29.
Dong, S. & Du, J. (2002) Chemical identification and fields tests of sex pheromone of beet armyworm Spodoptera exigua. Acta Phytophylacica Sinica, 29, 19-24.
Du, L.X., Liu, Y., Zhang, J., Gao, X.W., Wang, B. & Wang, G.R. (2018) Identification and characterization of chemosensory genes in the antennal transcriptome of Spodoptera exigua. Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics, 27, 54-65.
Dumas, P., Barbut, J., Le Ru, B., Silvain, J.F., Clamens, A.L., D'alencon, E. et al. (2015a) Phylogenetic molecular species delimitations unravel potential new species in the pest genus Spodoptera Guenee, 1852 (Lepidoptera, Noctuidae). PLoS ONE, 10, e0122407.
Dumas, P., Legeai, F., Lemaitre, C., Scaon, E., Orsucci, M., Labadie, K. et al. (2015b) Spodoptera frugiperda (Lepidoptera: Noctuidae) host-plant variants two host strains or two distinct species? Genetica, 143, 305-316.
EI-Sayed, A. (2020) The pherobase: database of pheromones and semiochemicals. Available from: https://www.pherobase.com/database/genus/genus-Spodoptera.php (Accessed on 2 September 2021)
Fleischer, J. & Krieger, J. (2018) Insect pheromone receptors - key elements in sensing intraspecific chemical signals. Frontiers in Cellular Neuroscience, 12, 1-14.
Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L. & Postlethwait, J. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531-1545.
Goergen, G., Kumar, P.L., Sankung, S.B., Togola, A. & Tamo, M. (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new Alien invasive pest in west and central Africa. PLoS ONE, 11, e0165632.
Goldstein, P.Z. (2017) Diversity and significance of Lepidoptera: a phylogenetic perspective. Insect Biodiversity: Science and Society, 1, 463-495.
Gouin, A., Bretaudeau, A., Nam, K., Gimenez, S., Aury, J.M., Duvic, B. et al. (2017) Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. Scientific Reports, 7, 11816.
Grosse-Wilde, E., Gohl, T., Bouche, E., Breer, H. & Krieger, J. (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. European Journal of Neuroscience, 25, 2364-2373.
Guo, H., Gong, X.L., Li, G.C., Mo, B.T., Jiang, N.J., Huang, L.Q. et al. (2022) Functional analysis of pheromone receptor repertoire in the fall armyworm, Spodoptera frugiperda. Pest Management Science, 78, 2052-2064.
Guo, J.M., Liu, X.L., Liu, S.R., Wei, Z.Q., Han, W.K., Guo, Y. et al. (2020) Functional characterization of sex pheromone receptors in the fall armyworm (Spodoptera frugiperda). Insects, 11, 1-14.
Jiang, N.J., Mo, B.T., Guo, H., Yang, J., Tang, R. & Wang, C.Z. (2021) Revisiting the sex pheromone of the fall armyworm Spodoptera frugiperda, a new invasive pest in south China. Insect Science, 29, 865-878.
Jiang, Y., Liu, J., Xie, M., Li, Y., Yang, J., Zhang, J. et al. (2019) Observation on law of diffusion of Spodoptera frugiperda in China in 2019. Plant Protection, 45, 10-19.
Jung, C.R., Park, Y.J. & Boo, K.S. (2003) Optimal sex pheromone composition for monitoring Spodoptera exigua (Lepidoptera: Noctuidae) in Korea. Journal of Asia-Pacific Entomology, 6, 175-182.
Kaissling, K.E. (1986) Chemo-electrical transduction in insect olfactory receptors. Annual Review of Neuroscience, 9, 121-145.
Kergoat, G.J., Goldstein, P.Z., Le Ru, B., Meagher Jr, R.L., Zilli, A., Mitchell, A. et al. (2021) A novel reference dated phylogeny for the genus Spodoptera Guenee (Lepidoptera: Noctuidae: Noctuinae): new insights into the evolution of a pest-rich genus. Molecular Phylogenetics and Evolution, 161, 107161.
Kergoat, G.J., Prowell, D.P., Le Ru, B.P., Mitchell, A., Dumas, P., Clamens, A.L. et al. (2012) Disentangling dispersal, vicariance and adaptive radiation patterns: a case study using armyworms in the pest genus Spodoptera (Lepidoptera: Noctuidae). Molecular Phylogenetics and Evolution, 65, 855-870.
Koutroumpa, F.A., Monsempes, C., François, M.-C., Severac, D., Montagné, N., Meslin, C. et al. (2021) Description of chemosensory genes in unexplored tissues of the moth Spodoptera littoralis. Frontiers in Ecology and Evolution, 9, 1-23.
Krieger, J., Grosse-Wilde, E., Gohl, T., Dewer, Y.M., Raming, K. & Breer, H. (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proceedings of the National Academy of Sciences USA, 101, 11845-11850.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.
Leal, W.S. (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58, 373-391.
Legeai, F., Malpel, S., Montagne, N., Monsempes, C., Cousserans, F., Merlin, C. et al. (2011) An expressed sequence tag collection from the male antennae of the Noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genomics, 12, 1-18.
Li, R.T., Ning, C., Huang, L.Q., Dong, J.F., Li, X. & Wang, C.Z. (2017) Expressional divergences of two desaturase genes determine the opposite ratios of two sex pheromone components in Helicoverpa armigera and Helicoverpa assulta. Insect Biochemistry and Molecular Biology, 90, 90-100.
Li, Z., Ni, J.D., Huang, J. & Montell, C. (2014) Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genetics, 10, e1004600.
Liu, C., Liu, Y., Walker, W.B., Dong, S. & Wang, G. (2013a) Identification and functional characterization of sex pheromone receptors in beet armyworm Spodoptera exigua (Hübner). Insect Biochemistry and Molecular Biology, 43, 747-754.
Liu, Y., Liu, C., Lin, K. & Wang, G. (2013b) Functional specificity of sex pheromone receptors in the cotton bollworm Helicoverpa armigera. PLoS ONE, 8, e62094.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, Calif.), 25, 402-408.
Llopis Gimenez, A., Carrasco Oltra, T., Jacquin Joly, E., Herrero, S. & Crava, C.M. (2020) Coupling transcriptomics and behaviour to unveil the olfactory system of Spodoptera exigua larvae. Journal of Chemical Ecology, 46, 1017-1031.
Mitchell, E.R., Baumhover, A.H. & Jacobson, M. (1976) Reduction of mating potential of male Heliothis spp. and Spodoptera frugiperda in field plots treated with Disruptants. Environmental Entomology, 5, 484-486.
Mitchell, E.R., Copeland, W.W., Sparks, A.N. & Sekul, A.A. (1974) Fall armyworm: disruption of pheromone communication with synthetic acetates. Environmental Entomology, 3, 778-780.
Montagne, N., Chertemps, T., Brigaud, I., Francois, A., Francois, M.C., De Fouchier, A. et al. (2012) Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. European Journal of Neuroscience, 36, 2588-2596.
Montezano, D.G., Specht, A., Sosa-Gómez, D.R., Roque-Specht, V.F., Sousa-Silva, J.C., Paula-Moraes, S.V. et al. (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, 26, 286-300.
N akagawa, T., Sakurai, T., Nishioka, T. & Touhara, K. (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science, 307, 1638-1642.
Nagoshi, R.N., Goergen, G., Plessis, H.D., Van Den Berg, J. & Meagher Jr, R. (2019) Genetic comparisons of fall armyworm populations from 11 countries spanning sub-Saharan Africa provide insights into strain composition and migratory behaviors. Scientific Reports, 9, 8311.
Nagoshi, R.N., Koffi, D., Agboka, K., Tounou, K.A., Banerjee, R., Jurat-Fuentes, J.L. et al. (2017) Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE, 12, e0181982.
Nei, M., Gu, X. & Sitnikova, T. (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Sciences USA, 94, 7799-7806.
Nei, M. & Rooney, A.P. (2005) Concerted and birth-and-death evolution of multigene families. Annual Review of Genetics, 39, 121-152.
Pashley, D.P. (1986) Host-associated genetic differentiation in fall armyworm (Lepidoptera: Noctuidae): a sibling species complex? Annals of the Entomological Society of America, 79, 894-904.
Pashlfy, D.P., Hammond, A.M. & Hardy, T.N. (1992) Reproductive isolating mechanisms in Fall Armyworm host strains (Lepidoptera: Noctuidae). Annals of the Entomological Society of America, 85, 400-405.
Rogers, M.E., Krieger, J. & Vogt, R.G. (2001) Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. Journal of Neurobiology, 49, 47-61.
Pogue, M.G. (2002) A world revision of the genus Spodoptera Guenée (Lepidoptera: Noctuidae). Memoirs of the American Entomological Society, 43, 1-202.
Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L.B. & Touhara, K. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature, 452, 1002-1006.
Saveer, A.M., Becher, P.G., Birgersson, G.R., Hansson, B.S., Witzgall, P. & Bengtsson, M. (2014) Mate recognition and reproductive isolation in the sibling species Spodoptera littoralis and Spodoptera litura. Frontiers in Ecology and Evolution, 2, 1-7.
Sun, X., Hu, C., Jia, H., Wu, Q., Shen, X., Zhao, S. et al. (2019) Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. Journal of Integrative Agriculture, 20, 664-672.
Tamaki, Y., Noguchi, H. & Yushima, T. (1973) Sex pheromone of Spodoptera litura (F.) (Lepidoptera: Noctuidae): Isolation, identification, and synthesis. Applied Entomology and Zoology, 8, 200-203.
Vasquez, G.M., Fischer, P., Grozinger, C.M. & Gould, F. (2011) Differential expression of odorant receptor genes involved in the sexual isolation of two Heliothis moths. Insect Molecular Biology, 20, 115-124.
Wan, J., Huang, C., Li, C., Zhou, H., Ren, Y., Li, Z. et al. (2021) Biology, invasion and management of the agricultural invader: Fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Integrative Agriculture, 20, 646-663.
Wang, G., Vásquez, G.M., Schal, C., Zwiebel, L.J. & Gould, F. (2011) Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Molecular Biology, 20, 125-133.
Wicher, D., Schafer, R., Bauernfeind, R., Stensmyr, M.C., Heller, R., Heinemann, S.H. et al. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature, 452, 1007-1011.
Wu, Q.L., Jiang, Y.Y., Liu, J., Hu, G. & Wu, K.M. (2021) Trajectory modeling revealed a southwest-northeast migration corridor for fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) emerging from the North China Plain. Insect Science, 28, 649-661.
Xiao, H., Ye, X., Xu, H., Mei, Y., Yang, Y., Chen, X. et al. (2020) The genetic adaptations of fall armyworm Spodoptera frugiperda facilitated its rapid global dispersal and invasion. Molecular Ecology Resources, 20, 1050-1068.
Yan, Q., Liu, X.L., Wang, Y.L., Tang, X.Q., Shen, Z.J., Dong, S.L. et al. (2019) Two sympatric Spodoptera species could mutually recognize sex pheromone components for behavioral isolation. Frontier in Physiology, 10, 1256.
Zhang, D.D. & Löfstedt, C. (2015) Moth pheromone receptors: gene sequences, function, and evolution. Frontiers in Ecology and Evolution, 3, 1-10.
Zhang, D., Xiao, Y., Xu, P., Yang, X., Wu, Q. & Wu, K. (2021) Insecticide resistance monitoring for the invasive populations of fall armyworm, Spodoptera frugiperda in China. Journal of Integrative Agriculture, 20, 783-791.
Zhang, J., Yan, S., Liu, Y., Jacquin-Joly, E., Dong, S. & Wang, G. (2015) Identification and functional characterization of sex pheromone receptors in the common cutworm (Spodoptera litura). Chemical Senses, 40, 7-16.
Zhang, L., Liu, B., Jiang, Y., Liu, J., Wu, K. & Xiao, Y. (2019) Molecular characterization analysis of fall armyworm populations in China. Plant Protection, 45, 20-27.
Zhang, L., Liu, B., Zheng, W., Liu, C., Zhang, D., Zhao, S. et al. (2020a) Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Molecular Ecology Resources, 20, 1682-1696.
Zhou, Y., Wu, Q., Zhang, H. & Wu, K. (2021) Spread of invasive migratory pest Spodoptera frugiperda and management practices throughout China. Journal of Integrative Agriculture, 20, 637-645.
Zuo, Y.Y., Shi, Y., Zhang, F., Guan, F., Zhang, J.P., Feyereisen, R., et al. (2021) Genome mapping coupled with CRISPR gene editing reveals a P450 gene confers avermectin resistance in the beet armyworm. PLoS Genetics, 17(7), e1009680.