Green leaf volatiles (GLVs) are short-chain oxylipins that are emitted from plants in response to stress. Previous studies have shown that oral secretions (OS) of the tobacco hornworm Manduca sexta, introduced into plant wounds during feeding, catalyze the re-arrangement of GLVs from Z-3- to E-2-isomers. This change in the volatile signal however is bittersweet for the insect as it can be used by their natural enemies, as a prey location cue. Here we show that (3Z):(2E)-hexenal isomerase (Hi-1) in M. sexta's OS catalyzes the conversion of the GLV Z-3-hexenal to E-2-hexenal. Hi-1 mutants that were raised on a GLV-free diet showed developmental disorders, indicating that Hi-1 also metabolizes other substrates important for the insect's development. Phylogenetic analysis placed Hi-1 within the GMCβ-subfamily and showed that Hi-1 homologs from other lepidopterans could catalyze similar reactions. Our results indicate that Hi-1 not only modulates the plant's GLV-bouquet but also functions in insect development.

Department of Ecology and Evolutionary Biology Cornell University Ithaca NY US

Department of Entomology National Taiwan University Taipei Taiwan

Department of Evolutionary Neuroethology Max Planck Institute for Chemical Ecology Jena Germany

Department of Insect Symbiosis Max Planck Institute for Chemical Ecology Jena Germany

EXTEMIT K Faculty of Forestry and Wood Sciences Czech University of Life Sciences 16500 Prague Czech Republic

Green Life Sciences Research Cluster Department of Plant Physiology Swammerdam Institute for Life Sciences University of Amsterdam Amsterdam Netherlands

Laboratory for Mass Spectrometry of Biomolecules Swammerdam Institute for Life Sciences University of Amsterdam Amsterdam Netherlands

Terrestrial Ecology Unit Department of Biology Faculty of Sciences Ghent University Ghent Belgium

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Kessler A, Baldwin IT. Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev. Plant Biol. 2002;53:299–328. doi: 10.1146/annurev.arplant.53.100301.135207. PubMed DOI

Clavijo McCormick A, Unsicker SB, Gershenzon J. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 2012;17:303–310. doi: 10.1016/j.tplants.2012.03.012. PubMed DOI

Erb M, Reymond P. Molecular interactions between plants and insect Herbivores. Annu. Rev. Plant Biol. 2019;70:527–557. doi: 10.1146/annurev-arplant-050718-095910. PubMed DOI

Jones, A. C., Felton, G. W. & Tumlinson, J. H. The dual function of elicitors and effectors from insects: reviewing the ‘arms race’ against plant defenses. Plant Mol. Biol.109, 427–445(2021). PubMed

Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW. Cues from chewing insects — the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr. Opin. Plant Biol. 2015;26:80–86. doi: 10.1016/j.pbi.2015.05.029. PubMed DOI

Felton GW, Tumlinson JH. Plant–insect dialogs: complex interactions at the plant–insect interface. Curr. Opin. Plant Biol. 2008;11:457–463. doi: 10.1016/j.pbi.2008.07.001. PubMed DOI

Erb M. Volatiles as inducers and suppressors of plant defense and immunity—origins, specificity, perception and signaling. Curr. Opin. Plant Biol. 2018;44:117–121. doi: 10.1016/j.pbi.2018.03.008. PubMed DOI

Bouwmeester H, Schuurink RC, Bleeker PM, Schiestl F. The role of volatiles in plant communication. Plant J. 2019;100:892–907. doi: 10.1111/tpj.14496. PubMed DOI PMC

Dudareva N, Klempien A, Muhlemann JK, Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. N. Phytologist. 2013;198:16–32. doi: 10.1111/nph.12145. PubMed DOI

Dicke M, Baldwin IT. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci. 2010;15:167–175. doi: 10.1016/j.tplants.2009.12.002. PubMed DOI

Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D. Timing of induced volatile emissions in maize seedlings. Planta. 1998;207:146–152. doi: 10.1007/s004250050466. DOI

Ameye M, et al. Green leaf volatile production by plants: a meta-analysis. N. Phytologist. 2018;220:666–683. doi: 10.1111/nph.14671. PubMed DOI

D’Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 2007;49:194–207. doi: 10.1111/j.1365-313X.2006.02946.x. PubMed DOI

Engelberth J. Green leaf volatiles: airborne signals that protect against biotic and abiotic stresses. Biol. Life Sci. Forum. 2021;4:101.

Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC. Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 2013;14:17781–17811. doi: 10.3390/ijms140917781. PubMed DOI PMC

Matsui K. Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant Biol. 2006;9:274–280. doi: 10.1016/j.pbi.2006.03.002. PubMed DOI

Farag MA, et al. (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta. 2005;220:900–909. doi: 10.1007/s00425-004-1404-5. PubMed DOI

Sufang Z, Jianing W, Zhen Z, Le K. Rhythms of volatiles release from healthy and insect-damaged Phaseolus vulgaris. Plant Signal Behav. 2013;8:25759. doi: 10.4161/psb.25759. PubMed DOI PMC

Shiojiri K, et al. Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc. Natl Acad. Sci. USA. 2006;103:16672–16676. doi: 10.1073/pnas.0607780103. PubMed DOI PMC

Savchenko T, Pearse IS, Ignatia L, Karban R, Dehesh K. Insect herbivores selectively suppress the HPL branch of the oxylipin pathway in host plants. Plant J. 2013;73:653–662. doi: 10.1111/tpj.12064. PubMed DOI

Takai H, et al. Silkworms suppress the release of green leaf volatiles by mulberry leaves with an enzyme from their spinnerets. Sci. Rep. 2018;8:11942. doi: 10.1038/s41598-018-30328-6. PubMed DOI PMC

Jones, A. C., Cofer, T. M., Engelberth, J. & Tumlinson, J. H. Herbivorous caterpillars and the green leaf volatile (GLV) quandary. J. Chem. Ecol.10.1007/s10886-021-01330-6 (2021). PubMed

Lin PA, et al. Silencing the alarm: an insect salivary enzyme closes plant stomata and inhibits volatile release. N. Phytol. 2021;230:793–803. doi: 10.1111/nph.17214. PubMed DOI PMC

Jones AC, et al. Herbivorous caterpillars can utilize three mechanisms to alter green leaf volatile emission. Environ. Entomol. 2019;48:419–425. doi: 10.1093/ee/nvy191. PubMed DOI

Allmann S, Halitschke R, Schuurink RC, Baldwin IT. Oxylipin channelling in Nicotiana attenuata: lipoxygenase 2 supplies substrates for green leaf volatile production. Plant, Cell Environ. 2010;33:2028–2040. doi: 10.1111/j.1365-3040.2010.02203.x. PubMed DOI

Allmann S, et al. Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. Elife. 2013;2:e00421. doi: 10.7554/eLife.00421. PubMed DOI PMC

Allmann S, Baldwin IT. Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science. 2010;329:1075–1078. doi: 10.1126/science.1191634. PubMed DOI

Kunishima M, et al. Identification of (Z)-3:(E)-2-hexenal isomerases essential to the production of the leaf aldehyde in plants. J. Biol. Chem. 2016;291:14023–14033. doi: 10.1074/jbc.M116.726687. PubMed DOI PMC

Spyropoulou EA, et al. Identification and Characterization of (3Z):(2E)-Hexenal Isomerases from Cucumber. Front Plant Sci. 2017;8:1342. doi: 10.3389/fpls.2017.01342. PubMed DOI PMC

Gershman A, et al. De novo genome assembly of the tobacco hornworm moth (Manduca sexta) G3 (Bethesda) 2021;11:jkaa047. doi: 10.1093/g3journal/jkaa047. PubMed DOI PMC

Sun W, et al. Expansion of the silkworm GMC oxidoreductase genes is associated with immunity. Insect Biochem Mol. Biol. 2012;42:935–945. doi: 10.1016/j.ibmb.2012.09.006. PubMed DOI

Kirsch R, et al. Host plant shifts affect a major defense enzyme in Chrysomela lapponica. Proc. Natl Acad. Sci. USA. 2011;108:4897–4901. doi: 10.1073/pnas.1013846108. PubMed DOI PMC

Michalski C, Mohagheghi H, Nimtz M, Pasteels J, Ober D. Salicyl alcohol oxidase of the chemical defense secretion of two chrysomelid leaf beetles. Molecular and functional characterization of two new members of the glucose-methanol-choline oxidoreductase gene family. J. Biol. Chem. 2008;283:19219–19228. doi: 10.1074/jbc.M802236200. PubMed DOI

Rahfeld P, et al. Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve. Proc. Biol. Sci. 2014;281:20140842. PubMed PMC

Lu F, et al. SilkDB 3.0: visualizing and exploring multiple levels of data for silkworm. Nucleic Acids Res. 2019;48:D749–D755. PubMed PMC

De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH. Herbivore-infested plants selectively attract parasitoids. Nature. 1998;393:570–573. doi: 10.1038/31219. DOI

Turlings TCJ, Erb M. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 2018;63:433–452. doi: 10.1146/annurev-ento-020117-043507. PubMed DOI

Arce CM, Besomi G, Glauser G, Turlings TCJ. Caterpillar-induced volatile emissions in cotton: the relative importance of damage and insect-derived factors. Front. Plant Sci. 2021;12:709858. doi: 10.3389/fpls.2021.709858. PubMed DOI PMC

Gaquerel E, Weinhold A, Baldwin IT. Molecular interactions between the specialist herbivore manduca sexta (Lepidoptera, Sphigidae) and its natural Host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the Plant’s elicited volatile emissions. Plant Physiol. 2009;149:1408–1423. doi: 10.1104/pp.108.130799. PubMed DOI PMC

Frey M, et al. An herbivore elicitor activates the gene for indole emission in maize. Proc. Natl Acad. Sci. 2000;97:14801–14806. doi: 10.1073/pnas.260499897. PubMed DOI PMC

De Lange ES, et al. Spodoptera frugiperda caterpillars suppress Herbivore-induced volatile emissions in Maize. J. Chem. Ecol. 2020;46:344–360. doi: 10.1007/s10886-020-01153-x. PubMed DOI

Sützl L, Foley G, Gillam EMJ, Bodén M, Haltrich D. The GMC superfamily of oxidoreductases revisited: analysis and evolution of fungal GMC oxidoreductases. Biotechnol. Biofuels. 2019;12:118. doi: 10.1186/s13068-019-1457-0. PubMed DOI PMC

Wongnate T, Chaiyen P. The substrate oxidation mechanism of pyranose 2-oxidase and other related enzymes in the glucose–methanol–choline superfamily. FEBS J. 2013;280:3009–3027. doi: 10.1111/febs.12280. PubMed DOI

Yamashita M, et al. Separation of the two reactions, oxidation and isomerization, catalyzed by Streptomyces cholesterol oxidase. Protein Eng., Des. Selection. 1998;11:1075–1081. doi: 10.1093/protein/11.11.1075. PubMed DOI

Stadtman TC, Cherkes A, Anfinsen CB. Studies on the microbiological degradation of cholesterol. J. Biol. Chem. 1954;206:511–523. doi: 10.1016/S0021-9258(19)50819-5. PubMed DOI

Bubliy OA, Imasheva AG, Loeschcke V. Half-sib analysis of three morphological traits in Drosophila melanogaster under poor nutrition. Hereditas. 2000;133:59–63. doi: 10.1111/j.1601-5223.2000.00059.x. PubMed DOI

Dadd RH. Insect nutrition: current developments and metabolic implications. Annu Rev. Entomol. 1973;18:381–420. doi: 10.1146/annurev.en.18.010173.002121. PubMed DOI

Levinson HZ, Navon A. Ascorbic acid and unsaturated fatty acids in the nutrition of the Egyptian cotton leafworm, Prodenia litura. J. Insect Physiol. 1969;15:591–595. doi: 10.1016/0022-1910(69)90257-1. DOI

Rosenthal GA, Dahlman DL. Non-protein amino acid-insect interactions—II. Effects of canaline-urea cycle amino acids on growth and development of the tobacco hornworm, Manduca Sexta L. (Sphingidae) Comp. Biochem. Physiol. Part A: Physiol. 1975;52:105–108. doi: 10.1016/S0300-9629(75)80138-1. PubMed DOI

Nohara C, et al. Ingestion of radioactively contaminated diets for two generations in the pale grass blue butterfly. BMC Evolut. Biol. 2014;14:193. doi: 10.1186/s12862-014-0193-0. PubMed DOI PMC

Geer BW, Vovis GF. The effects of choline and related compounds on the growth and development of Drosophila melanogaster. J. Exp. Zool. 1965;158:223–236. doi: 10.1002/jez.1401580209. PubMed DOI

Iida K, Cavener DR. Glucose dehydrogenase is required for normal sperm storage and utilization in female Drosophila melanogaster. J. Exp. Biol. 2004;207:675–681. doi: 10.1242/jeb.00816. PubMed DOI

Li Z, et al. Ectopic expression of ecdysone oxidase impairs tissue degeneration in Bombyx mori. Proc. R. Soc. B: Biol. Sci. 2015;282:20150513. doi: 10.1098/rspb.2015.0513. PubMed DOI PMC

Wybouw N, et al. Convergent evolution of cytochrome P450s underlies independent origins of keto-carotenoid pigmentation in animals. Proc. R. Soc. B: Biol. Sci. 2019;286:20191039. doi: 10.1098/rspb.2019.1039. PubMed DOI PMC

Jensen NB, et al. Convergent evolution in biosynthesis of cyanogenic defence compounds in plants and insects. Nat. Commun. 2011;2:273. doi: 10.1038/ncomms1271. PubMed DOI PMC

Phillips DR, Matthew JA, Reynolds J, Fenwick GR. Partial purification and properties of a cis−3: trans−2-enal isomerase from cucumber fruit. Phytochemistry. 1979;18:401–404. doi: 10.1016/S0031-9422(00)81874-9. DOI

Noordermeer MA, Veldink GA, Vliegenthart JFG. Alfalfa contains substantial 9-hydroperoxide lyase activity and a 3Z: 2E-enal isomerase. Febs Lett. 1999;443:201–204. doi: 10.1016/S0014-5793(98)01706-2. PubMed DOI

Takamura H, Gardner HW. Oxygenation of (3Z)-alkenal to (2E)-4-hydroxy-2-alkenal in soybean seed (Glycine max L) Biochimica Et. Biophysica Acta-Lipids Lipid Metab. 1996;1303:83–91. doi: 10.1016/0005-2760(96)00076-8. PubMed DOI

Chen C, et al. Characterization of a new (Z)-3:(E)-2-hexenal isomerase from tea (Camellia sinensis) involved in the conversion of (Z)-3-hexenal to (E)-2-hexenal. Food Chem. 2022;383:132463. doi: 10.1016/j.foodchem.2022.132463. PubMed DOI

Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics. 2017;33:3387–3395. doi: 10.1093/bioinformatics/btx431. PubMed DOI

Almagro Armenteros JJ, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 2019;37:420–423. doi: 10.1038/s41587-019-0036-z. PubMed DOI

Bendtsen JD, Jensen LJ, Blom N, von Heijne G, Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng., Des. Selection. 2004;17:349–356. doi: 10.1093/protein/gzh037. PubMed DOI

Bendtsen JD, Kiemer L, Fausbøll A, Brunak S. Non-classical protein secretion in bacteria. BMC Microbiol. 2005;5:58. doi: 10.1186/1471-2180-5-58. PubMed DOI PMC

Zhang Y, et al. Comparative proteome analysis of multi-layer cocoon of the silkworm, Bombyx mori. PLoS One. 2015;10:e0123403. doi: 10.1371/journal.pone.0123403. PubMed DOI PMC

Huang HJ, et al. Identification of salivary proteins in the whitefly Bemisia tabaci by transcriptomic and LC-MS/MS analyses. Insect Sci. 2021;28:1369–1381. doi: 10.1111/1744-7917.12856. PubMed DOI

Farkaš R, et al. Apocrine secretion in Drosophila salivary glands: subcellular origin, dynamics, and identification of secretory proteins. PLOS ONE. 2014;9:e94383. doi: 10.1371/journal.pone.0094383. PubMed DOI PMC

Farkaš R. Apocrine secretion: new insights into an old phenomenon. Biochimica et. Biophysica Acta (BBA) - Gen. Subj. 2015;1850:1740–1750. doi: 10.1016/j.bbagen.2015.05.003. PubMed DOI

Aumüller G, Wilhelm B, Seitz J. Apocrine secretion — fact or artifact. Ann. Anat. - Anatomischer Anz. 1999;181:437–446. doi: 10.1016/S0940-9602(99)80020-X. PubMed DOI

Bassett AR, Liu J-L. CRISPR/Cas9 and genome editing in Drosophila. J. Genet. Genomics. 2014;41:7–19. doi: 10.1016/j.jgg.2013.12.004. PubMed DOI

Hospital F. Selection in backcross programmes. Philos. Trans. R. Soc. B: Biol. Sci. 2005;360:1503–1511. doi: 10.1098/rstb.2005.1670. PubMed DOI PMC

Meldau S, Wu J, Baldwin IT. Silencing two herbivory-activated MAP kinases, SIPK and WIPK, does not increase Nicotiana attenuata’s susceptibility to herbivores in the glasshouse and in nature. N. Phytologist. 2009;181:161–173. doi: 10.1111/j.1469-8137.2008.02645.x. PubMed DOI

Kessler A, Baldwin IT. Defensive function of herbivore-induced plant volatile emissions in nature. Science. 2001;291:2141–2144. doi: 10.1126/science.291.5511.2141. PubMed DOI

Zipfel C. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 2009;12:414–420. doi: 10.1016/j.pbi.2009.06.003. PubMed DOI

Yoshinaga N, et al. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc. Natl Acad. Sci. USA. 2008;105:18058–18063. doi: 10.1073/pnas.0809623105. PubMed DOI PMC

Lievers R, Kuperus P, Groot AT. DNA methylation patterns in the tobacco budworm, Chloridea virescens. Insect Biochem. Mol. Biol. 2020;121:103370. doi: 10.1016/j.ibmb.2020.103370. PubMed DOI

Chang Y, et al. Snellenius manilae bracovirus suppresses the host immune system by regulating extracellular adenosine levels in Spodoptera litura. Sci. Rep. 2020;10:2096. doi: 10.1038/s41598-020-58375-y. PubMed DOI PMC

Lin YH, et al. Adenosine receptor modulates permissiveness of baculovirus (Budded Virus) infection via regulation of energy metabolism in bombyx mori. Front Immunol. 2020;11:763. doi: 10.3389/fimmu.2020.00763. PubMed DOI PMC

Roda A, Halitschke R, Steppuhn A, Baldwin IT. Individual variability in herbivore-specific elicitors from the plant’s perspective. Mol. Ecol. 2004;13:2421–2433. doi: 10.1111/j.1365-294X.2004.02260.x. PubMed DOI

Schägger H, von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 1987;166:368–379. doi: 10.1016/0003-2697(87)90587-2. PubMed DOI

Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 1996;68:850–858. doi: 10.1021/ac950914h. PubMed DOI

Pauchet Y, et al. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol. Biol. 2010;19:61–75. doi: 10.1111/j.1365-2583.2009.00936.x. PubMed DOI

Kanost MR, et al. Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta. Insect Biochem. Mol. Biol. 2016;76:118–147. doi: 10.1016/j.ibmb.2016.07.005. PubMed DOI PMC

Dhonukshe P, et al. Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development. 2010;137:3245–3255. doi: 10.1242/dev.052456. PubMed DOI

Karimi M, De Meyer B, Hilson P. Modular cloning in plant cells. Trends Plant Sci. 2005;10:103–105. doi: 10.1016/j.tplants.2005.01.008. PubMed DOI

Voinnet O, Rivas S, Mestre P, Baulcombe D. Retracted: An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003;33:949–956. doi: 10.1046/j.1365-313X.2003.01676.x. PubMed DOI

Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 2006;1:641–646. doi: 10.1038/nprot.2006.97. PubMed DOI

Fielder S, Rowan DD. The synthesis of 3,4-2H2-3Z-hexenal and 6,6,6-2H3-3Z-hexenal. J. Label. Compd. Radiopharmaceuticals. 1995;36:465–470. doi: 10.1002/jlcr.2580360510. DOI

Fandino RA, et al. Mutagenesis of odorant coreceptor Orco fully disrupts foraging but not oviposition behaviors in the hawkmoth Manduca sexta. Proc. Natl Acad. Sci. USA. 2019;116:15677–15685. doi: 10.1073/pnas.1902089116. PubMed DOI PMC

Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 2014;42:W401–W407. doi: 10.1093/nar/gku410. PubMed DOI PMC

Labun K, Montague TG, Gagnon JA, Thyme SB, Valen E. CHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering. Nucleic Acids Res. 2016;44:W272–W276. doi: 10.1093/nar/gkw398. PubMed DOI PMC

Labun K, et al. CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing. Nucleic Acids Res. 2019;47:W171–W174. doi: 10.1093/nar/gkz365. PubMed DOI PMC

Kessler A, Baldwin IT. MANDUCA QUINQUEMACULATA’S OPTIMIZATION OF INTRA-PLANT OVIPOSITION TO PREDATION, FOOD QUALITY, AND THERMAL CONSTRAINTS. Ecology. 2002;83:2346–2354. doi: 10.1890/0012-9658(2002)083[2346:MQSOOI]2.0.CO;2. DOI

Chandler CH, Chari S, Dworkin I. Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends Genet. 2013;29:358–366. doi: 10.1016/j.tig.2013.01.009. PubMed DOI PMC

Cheng T, et al. Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. Nat. Ecol. Evolution. 2017;1:1747–1756. doi: 10.1038/s41559-017-0314-4. PubMed DOI

Fritz ML, et al. Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices. Mol. Ecol. 2018;27:167–181. doi: 10.1111/mec.14430. PubMed DOI

Eddy SR. Accelerated profile HMM searches. PLOS Computational Biol. 2011;7:e1002195. doi: 10.1371/journal.pcbi.1002195. PubMed DOI PMC

Shen J, et al. Complete genome of Pieris rapae, a resilient alien, a cabbage pest, and a source of anti-cancer proteins. F1000Res. 2016;5:2631. doi: 10.12688/f1000research.9765.1. PubMed DOI PMC

Zhan S, Merlin C, Boore JL, Reppert SM. The monarch butterfly genome yields insights into long-distance migration. Cell. 2011;147:1171–1185. doi: 10.1016/j.cell.2011.09.052. PubMed DOI PMC

Iida K, Cox-Foster DL, Yang X, Ko W-Y, Cavener DR. Expansion and evolution of insect GMC oxidoreductases. BMC Evolut. Biol. 2007;7:75. doi: 10.1186/1471-2148-7-75. PubMed DOI PMC

Kirsch R, et al. To be or not to be convergent in salicin-based defence in chrysomeline leaf beetle larvae: evidence from Phratora vitellinae salicyl alcohol oxidase. Proc. Biol. Sci. 2011;278:3225–3232. PubMed PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Minh BQ, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC

Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC