A conserved odorant receptor tuned to phenylacetaldehyde in Athetis lepigone

Yiping Fan, Guirong Wang, Yang Liu

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New Plant Protection ›› 2024, Vol. 1 ›› Issue (1) : 10. DOI: 10.1002/npp2.10
ORIGINAL PAPER

A conserved odorant receptor tuned to phenylacetaldehyde in Athetis lepigone

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Abstract

Insects carry out various behaviors, including searching for food, mates, and oviposition sites using their sensitive olfactory systems. Odorantreceptors (ORs) play critical roles during odor detection. In this study, we identified an OR (AlepOR14) in Athetis lepigone, which is clustered with a conserved HarmOR42- lineage in Lepidoptera. We cloned this OR gene and investigated its expression levels using real-time quantitative PCR. Our results indicated that the expression of AlepOR14 is biased toward antennae, with levels significantly higher in female antennae than in male antennae. Functional analysis using the Xenopus oocytes expression and voltage-clamp recording system demonstrated thatAlepOR14 robustly and sensitively responds to the critical floral scent volatile phenylacetaldehyde (PAA). In behavioral experiments, female adults are attracted by PAA. Our findings improve our general understanding of the relationship between moths and their host plants, and provide an idea for exploiting attractants of A. lepigone for biological control.

Keywords

Athetis lepigone / conserved lineage / odorant receptor / phenylacetaldehyde / Xenopus oocytes

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Yiping Fan, Guirong Wang, Yang Liu. A conserved odorant receptor tuned to phenylacetaldehyde in Athetis lepigone. New Plant Protection, 2024, 1(1): 10 https://doi.org/10.1002/npp2.10

References

[1.]
Bruce T. J. A., Wadhams L. J., & Woodcock C. M. (2005). Insect host location: A volatile situation. Trends in Plant Science, 10(6), 269-274. https://doi.org/10.1016/j.tplants.2005.04.003
[2.]
de Bruyne M., & Baker T. C. (2008). Odor detection in insects: Volatile codes. Journal of Chemical Ecology, 34(7), 882-897. https://doi.org/10.1007/s10886-008-9485-4
[3.]
Jordan M. D., Anderson A., Begum D., Carraher C., Authier A., Marshall S. D. G., Kiely A., Gatehouse L. N., Greenwood D. R., Christie D. L., Kralicek A. V., Trowell S. C., & Newcomb R. D. (2009). Odorant receptors from the light brown apple moth (Epiphyas postvittana) recognize important volatile compounds produced by plants. Chemical Senses, 34(5), 383-394. https://doi.org/10.1093/chemse/bjp010
[4.]
Turlings T. C. J., & Erb M. (2018). Tritrophic interactions mediated by herbivore-induced plant volatiles: Mechanisms, ecological relevance, and application potential. Annual Review of Entomology, 63(1), 433-452. https://doi.org/10.1146/annurev-ento-020117-043507
[5.]
Chapman R. F. (1982). Chemoreception: The significance of receptor numbers. Advances in Insect Physiology, 16, 247-356. https://doi.org/10.1016/S0065-2806(08)60155-1
[6.]
Leal W. S. (2013). Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58(1), 373-391. https://doi.org/10.1146/annurev-ento-120811-153635
[7.]
Robertson H. M. (2019). Molecular evolution of the major arthropod chemoreceptor gene families. Annual Review of Entomology, 64(1), 227-242. https://doi.org/10.1146/annurev-ento-020117-043322
[8.]
Suh E., Bohbot J. D., & Zwiebel L. J. (2014). Peripheral olfactory signaling in insects. Current Opinion in Insect Science, 6, 86-92. https://doi.org/10.1016/j.cois.2014.10.006
[9.]
Hallem E. A., Ho M. G., & Carlson J. R. (2004). The molecular basis of odor coding in the Drosophila antenna. Cell, 117(7), 965-979. https://doi.org/10.1016/j.cell.2004.05.012
[10.]
Leal W. S., Chen A. M., Ishida Y., Chiang V. P., Erickson M. L., Morgan T. I., & Tsuruda J. M. (2005). Kinetics and molecular properties of pheromone binding and release. Proceedings of the National Academy of Sciences, 102(15), 5386-5391. https://doi.org/10.1073/pnas.0501447102
[11.]
Clyne P. J., Warr C. G., Freeman M. R., Lessing D., Kim J. H., & Carlson J. R. (1999). A novel family of divergent seven- transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron, 22(2), 327-338. https://doi.org/10.1016/S0896-6273(00)81093-4
[12.]
Vosshall L. B., Amrein H., Morozov P. S., Rzhetsky A., & Axel R. (1999). A spatial map of olfactory receptor expression in the Drosophila antenna. Cell, 96(5), 725-736. https://doi.org/10.1016/S0092-8674(00)80582-6
[13.]
Krieger J., Klink O., Mohl C., Raming K., & Breer H. (2003). A candidate olfactory receptor subtype highly conserved across different insect orders. Journal of Comparative Physiology A, 189(7), 519-526. https://doi.org/10.1007/s00359-003-0427-x
[14.]
Pitts R. J., Fox A. N., & Zwiebel L. J. (2004). A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proceedings of the National Academy of Sciences, 101(14), 5058-5063. https://doi.org/10.1073/pnas.0308146101
[15.]
Dekel A., Pitts R. J., Yakir E., & Bohbot J. D. (2016). Evolutionarily conserved odorant receptor function questions ecological context of octenol role in mosquitoes. Scientific Reports, 6(1), 37330, 37330. https://doi.org/10.1038/srep37330
[16.]
Liu W. B., Li H. M., Wang G. R., Cao H. Q., & Wang B. (2023). Conserved odorant receptor, EcorOR4, mediates attraction of mated female Eupeodes corollae to 1-Octen-3-ol. Journal of Agricultural and Food Chemistry, 71(4), 1837-1844. https://doi.org/10.1021/acs.jafc.2c06132
[17.]
Hou X. Q., Jia Z. Q., Zhang D. D., & Wang G. R. (2023). Odorant receptor orthologues from moths display conserved responses to cis-jasmone. Insect Science, 0(4), 1-14. https://doi.org/10.1111/1744-7917.13296
[18.]
Wang J. X., Wei Z. Q., Chen M. D., Yan Q., Zhang J., & Dong S. L. (2023). Conserved odorant receptors involved in nonanal-induced female attractive behavior in two Spodoptera species. Journal of Agricultural and Food Chemistry, 71(37), 13795-13804. https://doi.org/10.1021/acs.jafc.3c03265
[19.]
Guo M. B., Du L. X., Chen Q. Y., Feng Y. L., Zhang J., Zhang X. X., Tian K., Cao S., Huang T. Y., Jacquin-Joly E., Wang G. R., & Liu Y. (2021). Odorant receptors for detecting flowering plant cues are functionally conserved across moths and butterflies. Molecular Biology and Evolution, 38(4), 1413-1427. https://doi.org/10.1093/molbev/msaa300
[20.]
Kawahara A. Y., Plotkin D., Espeland M., Meusemann K., Toussaint E. F. A., Donath A., Gimnich F., Frandsen P. B., Zwick A., Reis M. D., Barber J. R., Peters R. S., Liu S. L., Zhou X., Mayer C., Podsiadlowski L., Storer C., Yack J. E., Misof B., & Breinholt J. W. (2019). Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proceedings of the National Academy of Sciences, 116(45), 22657-22663. https://doi.org/10.1073/pnas.1907847116
[21.]
Liu X. H., Shi L. F., Khashaveh A., Shan S., Lv B. B., Gu S. H., & Zhang Y. J. (2023). Loss of binding capabilities in an ecologically important odorant receptor of the fall armyworm, Spodoptera frugiperda, by a single point mutation. Journal of Agricultural and Food Chemistry, 71(35), 13003-13013. https://doi.org/10.1021/acs.jafc.3c04247
[22.]
Knauer A. C., & Schiestl F. P. (2015). Bees use honest floral signals as indicators of reward when visiting flowers. Ecology Letters, 18(2), 135-143. https://doi.org/10.1111/ele.12386
[23.]
Andersson S. (2003). Antennal responses to floral scents in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae). Chemoecology, 13(1), 13-20. https://doi.org/10.1007/s000490300001
[24.]
Fu X. W., Liu Y. Q., Li Y. H., Ali A., & Wu K. M. (2014). Does Athetis lepigone moth (Lepidoptera: Noctuidae) take a long- distance migration? Journal of Economic Entomology, 107(3), 995-1002. https://doi.org/10.1603/EC14014
[25.]
Jiang X. F., Luo L. Z., Jiang Y. Y., Zhang Y. J., Zhang L., & Wang Z. Y. (2011). Damage characteristics and outbreak causes of Athetis lepigone in China. Plant Protection, 37, 130-133. https://doi.org/10.3969/j.issn.0529-1542.2011.06.025
[26.]
Wang Z. Y., Shi J., & Dong J. B. (2012). Reason analysis on Proxenus lepigone outbreak of summer corn region in the Yellow River, Huai and Hai Rivers Plain and the countermeasures suggested. Maize Science, 20(1), 132-134. https://doi.org/10.13597/j.cnki.maize.science.2012.01.002
[27.]
Zhang Y. N., Ma J. F., Sun L., Dong Z. P., Li Z. Q., Zhu X. Y., Wang Y., Wang L., Deng D. G., & Li J. B. (2016). Molecular identification and sex distribution of two chemosensory receptor families in Athetis lepigone by antennal transcriptome analysis. Journal of Asia-Pacific Entomology, 19(3), 571-580. https://doi.org/10.1016/j.aspen.2016.05.009
[28.]
Yan Q., Zheng M. Y., Xu J. W., Ma J. F., Chen Y., Dong Z. P., Liu L., Dong S. L., & Zhang Y. N. (2018). Female sex pheromone of Athetis lepigone (Lepidoptera: Noctuidae): Identification and field evaluation. Journal of Applied Entomology, 142(1-2), 125-130. https://doi.org/10.1111/jen.12413
[29.]
Zhang Y. N., Du L. X., Xu J. W., Wang B., Zhang X. Q., Yan Q., & Wang G. R. (2019). Functional characterization of four sex pheromone receptors in the newly discovered maize pest Athetis lepigone. Journal of Insect Physiology, 113, 59-66. https://doi.org/10.1016/j.jinsphys.2018.08.009
[30.]
Du L. X., Zhao X. C., Liang X. Z., Gao X. W., Liu Y., & Wang G. R. (2018). Identification of candidate chemosensory genes in Mythimna separata by transcriptomic analysis. BMC Genomics, 19(1), 518, 518. https://doi.org/10.1186/s12864-018-4898-0
[31.]
Liu Y., Gu S. H., Zhang Y. J., Guo Y. Y., & Wang G. R. (2012). Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One, 7(10), e48260. https://doi.org/10.1371/journal.pone.0048260
[32.]
Zhang J., Wang B., Dong S. L., Cao D., Dong J., Walker W., Liu Y., & Wang G. R. (2015). Antennal transcriptome analysis and comparison of chemosensory gene families in two closely related Noctuidae moths, Helicoverpa armigera and H. assulta. PLoS One, 10(2), e0117054. https://doi.org/10.1371/journal.pone.0117054
[33.]
Walker W. B., Roy A., Anderson P., Schlyter F., Hansson B. S., & Larsson M. C. (2019). Transcriptome analysis of gene families involved in chemosensory function in Spodoptera littoralis (Lepidoptera: Noctuidae). BMC Genomics, 20(1), 428. https://doi.org/10.1186/s12864-019-5815-x
[34.]
de Fouchier A., Walker W. B., Montagné N., Steiner C., Binyameen M., Schlyter F., Chertemps T., Maria A., François M. C., Monsempes C., Anderson P., Hansson B. S., Larsson M. C., & Jacquin-Joly E. (2017). Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nature Communications, 8(1), 15709. https://doi.org/10.1038/ncomms15709
[35.]
Cheng J. J., Gui J. W., Yao X. M., Zhao H., Zhou Y. J., & Du Y. J. (2023). Functional identification of olfactory receptors of Cnaphalocrocis medinalis (Lepidoptera: Crambidae) for plant odor. Insects, 14(12), 930. https://doi.org/10.3390/insects14120930
[36.]
Li G. C., Nuo S. M., Wang Z. Q., Yang A. J., & Liu N. Y. (2021). Identification and expression profiling of chemosensory membrane protein genes in Achelura yunnanensis (Lepidoptera: Zygaenidae). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 40, 100876. https://doi.org/10.1016/j.cbd.2021.100876
[37.]
Wang Z. Q., Wu C., Li G. C., Nuo S. M., Yin N. N., & Liu N. Y. (2021). Transcriptome analysis and characterization of chemosensory genes in the forest pest, Dioryctria abietella (Lepidoptera: Pyralidae). Frontiers in Ecology and Evolution, 9, 748199. https://doi.org/10.3389/fevo.2021.748199
[38.]
Liu Y. P., Zhang S., Liu Y., & Wang G. R. (2022). Odorant receptor PxylOR11 mediates repellency of Plutella xylostella to aromatic volatiles. Frontiers in Physiology, 13, 938555. https://doi.org/10.3389/fphys.2022.938555
[39.]
Zhang X.X., Wang X., Zhao S. W., Fang K., Wang Z., Liu J. N., Xi J. H., Wang S., & Zhang J. H. (2023). Response of odorant receptors with phenylacetaldehyde and the effects on the behavior of the Rice Water Weevil (Lissorhoptrus oryzophilus). Journal of Agricultural and Food Chemistry, 71(17), 6541-6551. https://doi.org/10.1021/acs.jafc.2c07963
[40.]
Fan H., Jin Y. J., Li J. Q., & Chen H. J. (2004). Advances on plant volatile semiochemicals attracting herbivorous insects. Journal of Beijing Forestry University, 26(3), 76-81. https://lib.cqvip.com/Qikan/Article/Detail?id=10408439
[41.]
Hern A., & Dorn S. (1999). Sexual dimorphism in the olfactory orientation of adult Cydia pomonella in response to α-farnesene. Entomologia Experimentalis et Applicata, 92(1), 63-72. https://doi.org/10.1046/j.1570-7458.1999.00525.x
[42.]
Wenda-Piesik A., Piesik D., & Buszewski B. (2017). Do mated Tribolium confusum adults respond to blends of odors? Polish Journal of Environmental Studies, 26(1), 447-452. https://doi.org/10.15244/pjoes/64308
[43.]
Landolt P., Jang E., Carvalho L., & Pogue M. (2011). Attraction of pest moths (Lepidoptera: Noctuidae, Crambidae) to floral lures on the island of Hawaii. Proceedings of the Hawaiian Entomological Society, 43, 49-58. https://api.semanticscholar.orgCorpusID:86655431
[44.]
Meagher R. L. (2001). Collection of soybean looper and other noctuids in phenylacetaldehyde-baited field traps. Florida Entomologist, 84(1), 154-155. https://doi.org/10.2307/3496678
[45.]
Eby C., Gardiner M. G. T., Gries R., Judd G. J. R., Khaskin G., & Gries G. (2013). Phenylacetaldehyde attracts male and female apple clearwing moths, Synanthedon myopaeformis, to inflorescences of showy milkweed, Asclepias speciosa. Entomologia Experimentalis et Applicata, 147(1), 82-92. https://doi.org/10.1111/eea.12045
[46.]
Landolt P. J., Tóth M., Meagher R. L., & Szarukán I. (2013). Interaction of acetic acid and phenylacetaldehyde as attractants for trapping pest species of moths (Lepidoptera: Noctuidae). Pest Management Science, 69(2), 245-249. https://doi.org/10.1002/ps.3381
[47.]
Hejazi M., Movahedi M. F., Askari O., & Higbee B. S. (2016). Novel chemo-attractants for trapping tomato leafminer moth (Lepidoptera: Gelechiidae). Journal of Economic Entomology, 109(5), 2074-2081. https://doi.org/10.1093/jee/tow195
[48.]
Deng J. Y., Wei H. Y., Huang Y. P., & Du J. W. (2004). Enhancement of attraction to sex pheromones of Spodoptera exigua by volatile compounds produced by host plants. Journal of Chemical Ecology, 30(10), 2037-2045. https://doi.org/10.1023/B:JOEC.0000045593.62422.73
[49.]
Shen Y. L., Gao Y., & Du Y. J. (2009). The synergism of plant volatile compounds and sex pheromones of the tobacco cutworm moth. Spodoptera litura (Lepidoptera: Noctuidae). Acta Entomologica Sinica, 52(12), 1290-1297. https://doi.org/10.16380/j.kcxb.2009.12.007
Funding
National Key Research and Development Program of China(2022YFD1400800); Innovation Program of Chinese Academy of Agricultural Sciences(CAAS-CSCB-202302); National Natural Science Foundation of China(32072509); National Natural Science Foundation of China(32272540)
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