[en] Odorant receptors (ORs) are essential for plant-insect interactions. However, despite the global impacts of Lepidoptera (moths and butterflies) as major herbivores and pollinators, little functional data are available about Lepidoptera ORs involved in plant-volatile detection. Here, we initially characterized the plant-volatile-sensing function(s) of 44 ORs from the cotton bollworm Helicoverpa armigera, and subsequently conducted a large-scale comparative analysis that establishes how most orthologous ORs have functionally diverged among closely related species whereas some rare ORs are functionally conserved. Specifically, our systematic analysis of H. armigera ORs cataloged the wide functional scope of the H. armigera OR repertoire, and also showed that HarmOR42 and its Spodoptera littoralis ortholog are functionally conserved. Pursuing this, we characterized the HarmOR42-orthologous ORs from 11 species across the Glossata suborder and confirmed the HarmOR42 orthologs form a unique OR lineage that has undergone strong purifying selection in Glossata species and whose members are tuned with strong specificity to phenylacetaldehyde, a floral scent component common to most angiosperms. In vivo studies via HarmOR42 knockout support that HarmOR42-related ORs are essential for host-detection by sensing phenylacetaldehyde. Our work also supports that these ORs coevolved with the tube-like proboscis, and has maintained functional stability throughout the long-term coexistence of Lepidoptera with angiosperms. Thus, beyond providing a rich empirical resource for delineating the precise functions of H. armigera ORs, our results enable a comparative analysis of insect ORs that have apparently facilitated and currently sustain the intimate adaptations and ecological interactions among nectar feeding insects and flowering plants.
Disciplines :
Entomology & pest control
Author, co-author :
Guo, Mengbo ✱; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; Guangdong Laboratory for Lingnan Modern Agriculture (Shenzhen Branch), Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Du, Lixiao ✱; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Chen, Qiuyan; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Feng, Yilu; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Jin; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Xiaxuan; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Tian, Ke; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Cao, Song; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Huang, Tianyu ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Jacquin-Joly, Emmanuelle; INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université de Paris, Institute of Ecology and Environmental Sciences of Paris, Versailles, France
Wang, Guirong ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; Guangdong Laboratory for Lingnan Modern Agriculture (Shenzhen Branch), Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Liu, Yang ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Odorant Receptors for Detecting Flowering Plant Cues Are Functionally Conserved across Moths and Butterflies.
Publication date :
13 April 2021
Journal title :
Molecular Biology and Evolution
ISSN :
0737-4038
eISSN :
1537-1719
Publisher :
Oxford University Press, United States
Volume :
38
Issue :
4
Pages :
1413 - 1427
Peer reviewed :
Peer Reviewed verified by ORBi
Funding text :
We thank Dr Peter C. Gregg (University of New England) for providing valuable suggestions for setting up two-choice olfactometer system; Dr Yidong Wu and Dr Huidong Wang (Nanjing Agricultural University) for offering advices about gene knock-out by using CRISPR-Cas9 system; Dr Hu Li and Dr Xin Zhou (China Agricultural University) and Dr Fangluan Gao (Fujian Agriculture and Forestry University) for providing valuable suggestions for selection pressure analysis; Ms Chunyan Wang for giving assistance insect rearing. This work was funded by National Natural Science Foundation of China (31725023, 31621064, 31861133019 to G.W., and 31672095 to Y.L.), Shenzhen Science and Technology Program (Grant No. KQTD20180411143628272), and the French National Research Agency (ANR-16-CE21-0002-01 to E.J.-J.) and with the support of the International Associated Laboratory for Plant Protection INRA-CAAS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article.
Anderson AR, Wanner KW, Trowell SC, Warr CG, Jaquin-Joly E, Zagatti P, Robertson H, Newcomb RD. 2009. Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem Mol Biol. 39(3):189-197.
Anderson P, Hilker M, Hansson BS, Bombosch S, Klein B, Schildknecht H. 1993. Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): a behavioural and electrophysiological evaluation. J Insect Physiol. 39(2):129-137.
Auer TO, Khallaf MA, Silbering AF, Zappia G, Ellis K, Álvarez-Ocaña R, Arguello JR, Hansson BS, Jefferis GSXE, Caron SJC, et al. 2020. Olfactory receptor and circuit evolution promote host specialization. Nature 579(7799):402-408.
Benton R, Sachse S, Michnick SW, Vosshall LB. 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4(2):e20.
Bruce TJ, Wadhams LJ, Woodcock CM. 2005. Insect host location: a volatile situation. Trends Plant Sci. 10(6):269-274.
Cao D, Liu Y, Wei J, Liao X, Walker WB, Li J, Wang G. 2014. Identification of candidate olfactory genes in Chilo suppressalis by antennal transcriptome analysis. Int J Biol Sci. 10(8):846-860.
Cao S, Liu Y, Guo M, Wang G. 2016. A conserved odorant receptor tuned to floral volatiles in three Heliothinae species. PLoS One 11(5):e0155029.
Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR. 2010. Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464(7285):66-71.
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. Sci Rep. 6(1):srep18742.
Chang H, Liu Y, Ai D, Jiang X, Dong S, Wang G. 2017. A pheromone antagonist regulates optimal mating time in the moth Helicoverpa armigera. Curr Biol. 27(11):1610-1615.
Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22(2):327-338.
Cork A. 2016. Insect attractant compositions. London: University of Greenwich.
Cui W-C, Wang B, Guo M-B, Liu Y, Jacquin-Joly E, Yan S-C, Wang G-R. 2018. A receptor-neuron correlate for the detection of attractive plant volatiles in Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochem Mol Biol. 97:31-39.
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 pestmoths of the genus Spodoptera. Front Ecol Evol. 3(95):e49.
de Fouchier A, Walker WB, Montagné N, Steiner C, Binyameen M, Schlyter F, Chertemps T, Maria A, François M-C, Monsempes C, et al. 2017. Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nat Commun. 8(1):15709.
Degenhardt J, Gershenzon J. 2000. Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4,8-dimethyl-1,3,7-nonatriene biosynthesis. Planta 210(5):815-822.
Del Socorro AP, Gregg PC, Alter D, Moore CJ. 2010. Development of a synthetic plant volatile-based attracticide for female noctuid moths. I. Potential sources of volatiles attractive to Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Aust J Entomol. 49(1):10-20.
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(84):48-62.
Engsontia P, Sangket U, Chotigeat W, Satasook C. 2014. Molecular evolution of the odorant and gustatory receptor genes in lepidopteran insects: implications for their adaptation and speciation. J Mol Evol. 79(1-2):21-39.
Eyun SI, Soh HY, Posavi M, Munro JB, Hughes DST, Murali SC, Qu J, Dugan S, Lee SL, Chao H, et al. 2017. Evolutionary history of chemosensory-related gene families across the Arthropoda. Mol Biol Evol. 34(8):1838-1862.
Fleischer J, Pregitzer P, Breer H, Krieger J. 2018. Access to the odor world: olfactory receptors and their role for signal transduction in insects. Cell Mol Life Sci. 75(3):485-508.
Gao Q, Chess A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60(1):31-39.
Guo H, Lackus N, Köllner TG, Li R, Bing J, Wang Y, Baldwin IT, Xu S. 2020. Evolution of a novel and adaptive floral scent in wild tobacco. Mol Biol Evol. 37(4):1090-1099.
Guo M, Chen Q, Liu Y, Wang G, Han Z. 2018. Chemoreception of mouthparts: sensilla morphology and discovery of chemosensory genes in proboscis and labial palps of adult Helicoverpa armigera (Lepidoptera: Noctuidae). Front Physiol. 9:e970.
Hallem EA, Carlson JR. 2006. Coding of odors by a receptor repertoire. Cell 125(1):143-160.
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:e49.
Jacquin-Joly E, Legeai F, Montagné N, Monsempes C, François M-C, Poulain J, Gavory F, Walker WB 3rd, Hansson BS, Larsson MC. 2012. Candidate chemosensory genes in female antennae of the noctuid moth Spodoptera littoralis. Int J Biol Sci. 8(7):1036-1050.
Jones CM, Parry H, Tay WT, Reynolds DR, Chapman JW. 2019. Movement ecology of pest Helicoverpa: implications for ongoing spread. Annu Rev Entomol. 64(1):277-295.
Joseph RM, Carlson JR. 2015. Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet. 31(12):683-695.
Kawahara AY, Plotkin D, Espeland M, Meusemann K, Toussaint EFA, Donath A, Gimnich F, Frandsen PB, Zwick A, Dos Reis M, et al. 2019. Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proc Natl Acad Sci U S A. 116(45):22657-22663.
Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, et al. 2010. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci U S A. 107(27):12168-12173.
Knauer AC, Schiestl FP. 2015. Bees use honest floral signals as indicators of reward when visiting flowers. Ecol Lett. 18(2):135-143.
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B. 2006. Diversity and distribution of floral scent. Bot Rev. 72(1):1-120.
Koenig C, Hirsh A, Bucks S, Klinner C, Vogel H, Shukla A, Mansfield JH, Morton B, Hansson BS, Grosse-Wilde E. 2015. A reference gene set for chemosensory receptor genes of Manduca sexta. Insect Biochem Mol Biol. 66:51-63.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 35(6):1547-1549.
Kurtovic A, Widmer A, Dickson BJ. 2007. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446(7135):542-546.
Larsson MC, Domingos AI, Jones WD, Chiappe M, Amrein H, Vosshall LB. 2004. Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction. Neuron 43(5):703-714.
Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, Kavanaugh MP, Wanner KW. 2012. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci U S A. 109(35):14081-14086.
Li G, Du J, Li Y, Wu J. 2015. Identification of putative olfactory genes from the oriental fruit moth Grapholita molesta via an antennal transcriptome analysis. PLoS One 10(11):e0142193.
Liu N, Xu W, Papanicolaou A, Dong S, Anderson A. 2014. Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics 15(1):e597.
Liu Y, Gu S, Zhang Y, Guo Y, Wang G. 2012. Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One 7(10):e48260.
Liu Y, Liu C, Lin K, Wang G. 2013. Functional specificity of sex pheromone receptors in the cotton bollworm Helicoverpa armigera. PLoS One 8(4):e62094.
Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E. 2014. Evolution of insect olfactory receptors. eLife 3:e02115.
Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T. 2008. Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur J Neurosci. 28(5):893-902.
Mitter C, Davis DR, Cummings MP. 2017. Phylogeny and evolution of Lepidoptera. Annu Rev Entomol. 62(1):265-283.
Montagné N, Chertemps T, Brigaud I, François A, François M-C, de Fouchier A, Lucas P, Larsson MC, Jacquin-Joly E. 2012. Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur J Neurosci. 36(5):2588-2596.
Nakagawa T, Sakurai T, Nishioka T, Touhara K. 2005. Insect sexpheromone signals mediated by specific combinations of olfactory receptors. Science 307(5715):1638-1642.
Nei M, Niimura Y, Nozawa M. 2008. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet. 9(12):951-963.
Pearce SL, Clarke DF, East PD, Elfekih S, Gordon KHJ, Jermiin LS, McGaughran A, Oakeshott JG, Papanikolaou A, Perera OP, et al. 2017. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol. 15(1):63.
Poivet E, Gallot A, Montagne 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(4):e60263.
Robertson HM. 2019. Molecular evolution of the major arthropod chemoreceptor gene families. Annu Rev Entomol. 64(1):227-242.
Roe AD, Weller SJ Baixeras J, Brown J, Cummings MP, Davis D, Kawahara AY Parr C, Regier JC, Rubinoff D. 2009. Evolutionary framework for Lepidoptera model systems. In: Goldsmith MR, Marec F, editors. Molecular biology and genetics of the Lepidoptera. Boca Raton (FL): CRC Press. p. 1-24.
Schiestl FP. 2010. The evolution of floral scent and insect chemical communication. Ecol Lett. 13(5):643-656.
Schoonhoven LM, van Loon JJA, Dicke M, editors. 2005. Host-plant selection: how to find a host plant. In: Insect-plant biology. Oxford: Oxford University Press. p. 135-168.
Schuman MC, Baldwin IT. 2016. The layers of plant responses to insect herbivores. Annu Rev Entomol. 61(1):373-394.
Slone JD, Pask GM, Ferguson ST, Millar JG, Berger SL, Reinberg D, Liebig J, Ray A, Zwiebel LJ. 2017. Functional characterization of odorant receptors in the ponerine ant, Harpegnathos saltator. Proc Natl Acad Sci U S A. 114(32):8586-8591.
Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, et al. 2012. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151(6):1345-1357.
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(11): 881-890.
Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ. 2006. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci U S A. 103(21):8287-8292.
Turlings TCJ, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol. 63(1):433-452.
Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725-736.
Wang G, Carey AF, Carlson JR, Zwiebel LJ. 2010. Molecular basis of odor coding in themalaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A. 107(9):4418-4423.
Wang H, Shi Y, Wang L, Liu S, Wu S, Yang Y, Feyereisen R, Wu Y. 2018. CYP6AE gene cluster knockout in Helicoverpa armigera reveals role in detoxification of phytochemicals and insecticides. Nat Commun. 9(1):4820.
Whitfield EC, Lobos E, Cork A, Hall DR. 2019. Comparison of different trap designs for capture of noctuid moths (Lepidoptera: Noctuidae) with pheromone and floral odor attractants. J Econ Entomol. 112(5):2199-2206.
Wicher D, Morinaga S, Halty-deLeon L, Funk N, Hansson B, Touhara K, Stengl M. 2017. Identification and characterization of the bombykal receptor in the hawkmoth Manduca sexta. J Exp Biol. 220(Pt 10):1781-1786.
Xu H, Turlings TCJ. 2018. Plant volatiles as mate-finding cues for insects. Trends Plant Sci. 23(2):100-111.
Yang B, Ozaki K, Ishikawa Y, Matsuo T. 2015. Identification of candidate odorant receptors in Asian corn borer Ostrinia furnacalis. PLoS One 10(3):e0121261.
Yang K, Huang LQ, Ning C, Wang CZ. 2017. Two single-point mutations shift the ligand selectivity of a pheromone receptor between two closely related moth species. eLife 6:e29100.
Yang Z. 2007. PAMl 4: phylogenetic analysis bymaximum likelihood. Mol Biol Evol. 24(8):1586-1591.
Yuvaraj JK, Corcoran JA, Andersson MN, Newcomb RD, Anderbrant O, Löfstedt C. 2017. Characterization of odorant receptors from a nonditrysianmoth, Eriocrania semipurpurella sheds light on the origin of sex pheromone receptors in Lepidoptera. Mol Biol Evol. 34(11):2733-2746.
Zhang J, Wang B, Dong S, Cao D, Dong J, Walker WB, Liu Y, Wang G. 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.
Zhou X, Slone JD, Rokas A, Berger SL, Liebig J, Ray A, Reinberg D, Zwiebel LJ. 2012. Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet. 8(8):e1002930.
