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Biochemical Adaptation of the Oriental Tobacco Budworm, Helicoverpa assulta, to Host-plant Defensive Compounds

기주식물 방어물질에 대한 담배나방의 생화학적 적응

  • Ahn, Seung-Joon (Department of Biochemistry, Molecular Biology, Entomology & Plant Pathology, Mississippi State University)
  • 안승준 (미국 미시시피주립대학교)
  • Received : 2022.01.29
  • Accepted : 2022.02.14
  • Published : 2022.03.01

Abstract

Plant secondary metabolites play an important role in insect-plant interactions. Herbivorous insects have various strategies to cope with the plant defensive compounds. Polyphagous insects feed on a wide variety of plant species, and their detoxification mechanisms are more complex since they tend to respond to a large array of different plant-derived chemicals. Alternatively, oligophagous insects specialize on only a few related plant species and may be expected to have a more efficient form of adaptation. This adaptation could involve either the production of large quantities of enzymes to detoxify their defensive compounds or the sequestration of the compounds or their metabolites. The oriental tobacco budworm, Helicoverpa assulta, is a specialist herbivore, feeding on a few plants of Solanaceae, such as tobacco and hot pepper. Understanding its host-plant adaptation not provides an important insight on physiology, ecology and evolution of specialist herbivores, but also gives a clue to develop management strategies of the pest species such as H. assulta. This paper briefly reviews the specialist, H. assulta, focusing on its host range, larval associations with the host plants, and detoxification mechanisms to nicotine and capsaicin, two characteristic defensive compounds derived from its two major host plants, tobacco and hot pepper, respectively. It summarizes the relevant research over the last half century and provides a future perspective on this subject.

식물의 이차대사산물은 곤충-식물 상호관계에서 중요한 역할을 한다. 식식성 곤충은 식물의 방어물질에 대처하는 다양한 전략을 가지고 있다. 광식성 곤충은 넓은 범위의 다양한 식물들을 섭식하고 그 해독 기작도 보다 복잡한데, 이는 많은 종류의 식물유래 화합물에 반응하는 경향이 있기 때문으로 보인다. 이와는 달리 협식성 곤충은 몇몇 유사한 식물에 국한되어 살아가며 보다 효율적인 적응 방식을 지니고 있을 것으로 여겨진다. 이러한 협식성 곤충의 적응은 식물의 방어물질에 대한 해독효소를 다량 생산하거나 방어물질 또는 그 대사산물을 격리하는 전략을 마련하였기 때문으로 보인다. 담배나방은 담배와 고추 등 주로 가지과의 몇몇 식물만을 가해하는 협식성 곤충이다. 담배나방의 기주식물 적응성을 이해한다면, 이 해충에 의한 작물의 피해를 줄이는 방법을 개발하는데 도움을 줄 수 있을 뿐만 아니라, 담배나방과 같은 협식성 곤충의 생리, 생태, 진화를 연구하는 데에도 중요한 단서를 제공할 것이다. 본 종설에서는 담배나방의 기주식물 범위, 유충과 기주식물의 상호작용, 그리고 기주식물에서 특이적으로 나오는 니코틴과 캡사이신에 대한 곤충의 반응과 해독 메카니즘을 중심으로, 지난 반세기 동안의 연구결과를 요약하고 앞으로의 전망을 제시하고자 한다.

Keywords

Acknowledgement

The author would like to express special appreciation to the late Prof. Kyung Saeng Boo for his dedication to the development of insect physiology and chemical ecology in Korea. This manuscript is based upon work supported by the National Institute of Food and Agriculture, USDA, Hatch-Multistate project (MIS-311360) and by the Mississippi Agricultural and Forestry Experiment Station (MAFES) Special Research Initiative (SRI) grant.

References

  1. Ahn, S.-J., Badenes-Perez, F.R., Heckel, D.G., 2011a. A host-plant specialist, Helicoverpa assulta, is more tolerant to capsaicin from Capsicum annuum than other noctuid species. J. Insect Physiol. 57, 1212-1219. doi:10.1016/j.jinsphys.2011.05.015
  2. Ahn, S.-J., Badenes-Perez, F.R., Reichelt, M., Svatos, A., Schneider, B., Gershenzon, J., Heckel, D.G., 2011b. Metabolic detoxification of capsaicin by UDP-glycosyltransferase in three Helicoverpa species. Arch. Insect Biochem. Physiol. 78, 104-118. doi:10.1002/arch.20444
  3. Ahn, S.-J., Choi, M.-Y., Boo, K.S., 2002. Mating effect on sex pheromone production of the oriental tobacco budworm, Helicoverpa assulta. J. Asia-Pacific Entomol. 5, 43-48. doi: 10.1016/S1226-8615(08)60131-4
  4. Ahn, S.-J., Vogel, H., Heckel, D.G., 2012. Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochem. Mol. Biol. 42, 133-147. doi:10.1016/j.ibmb.2011.11.006
  5. Ali, J.G., Agrawal, A.A., 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293-302. doi:10.1016/j.tplants.2012.02.006
  6. An, C.H., 1976. Study on the ecological characteristics of oriental tobacco budworm. Study Tob. Leaves 3, 15-20.
  7. Bernays, E., Graham, M., 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886-892. doi:10.2307/1941237
  8. Bonaventure, G., VanDoorn, A., Baldwin, I.T., 2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci. 16, 294-299. doi:10.1016/j.tplants.2011.01.006
  9. Boo, K.S., Park, K.C., Hall, D.R., Cork, A., Berg, B.G., Mustaparta, H., 1995. (Z)-9-tetradecenal: a potent inhibitor of pheromone-mediated communication in the oriental tobacco budworm moth, Helicoverpa assulta. J. Comp. Physiol. A 177, 695-699. doi:10.1007/BF00187628
  10. Boo, K.S., Shin, H.C., Han, M.W., Lee, M.H., 1990. Initiation and termination of pupal diapause in the oriental tobacco budworm (Heliothis assulta). Korean J. Appl. Entomol. 29, 277-285.
  11. Boo, K.S., Yang, J.P., 1998. Olfactory response of Trichogramma chilonis to Capsicum annuum. J. Asia-Pacific Entomol. 1, 123-129. doi:10.1016/S1226-8615(08)60014-X
  12. Boo, K.S., Yang, J.P., 2000. Kairomones used by Trichogramma chilonis to find Helicoverpa assulta eggs. J. Chem. Ecol. 26, 359-375. doi:10.1023/A:1005453220792
  13. Brattsten, L.B., 1988. Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. J. Chem. Ecol. 14, 1919-1939. doi:10.1007/BF01013486
  14. Brattsten, L.B., 1992. Metabolic defenses against plant allelochemicals, Vol II: Ecological and evolutionary processes, in: Rosenthal, G.A., Berenbaum, M.R. (Eds.), Herbivores: Their interactions with secondary plant metabolites. Academic Press, pp. 175-242.
  15. CAB International, 2020. Distribution map of Helicoverpa assulta (Oriental tobacco budworm) [WWW Document]. https://www.cabi.org/isc/datasheet/26758 (accessed on 28 January, 2022).
  16. Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., Julius, D., 1997. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389, 816-824. doi:10.1038/39807
  17. 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. doi:10.1371/JOURNAL.PONE.0179243
  18. Cheng, Q., Gu, S., Liu, Z., Wang, C.-Z., Li, X., 2017. Expressional divergence of the fatty acid-amino acid conjugate-hydrolyzing aminoacylase 1 (L-ACY-1) in Helicoverpa armigera and Helicoverpa assulta. Sci. Rep. 7, 8721. doi:10.1038/s41598-017-09185-2
  19. Cho, J.R., Boo, K.S., 1988. Behavior and circadian rhythm of emergence, copulation and oviposition in the oriental tobacco budworm, Heliothis assulta Guenee. Korean J. Appl. Entomol. 27, 103-110.
  20. Cho, K.H., Boo, K.S., 1990. Change in protein and carbohydrate contents in diapausing and non-diapausing pupae of the oriental tobacco budworm, Heliothis assulta Guenee. Korean J. Appl. Entomol. 29, 286-293.
  21. Choi, K.M., Cho, E.H., So, J.S., Hwang, C.Y., 1975. Studies on the seasonal occurrences of the tobacco budworm, Heliothis assulta H. (Lepidoptera: Noctuidae), and the parasitism ratio of Trichogramma spp. on the eggs. Korean J. Plant Prot. 14, 137-140.
  22. Choi, K.S., Boo, K.S., 1989a. Food attractancy of the oriental tobacco budworm, Heliothis assulta, larvae. Korean J. Appl. Entomol. 28, 88-92.
  23. Choi, K.S., Boo, K.S., 1989b. Effects of extracts from some selected wild plant species on larval development and adult oviposition in Heliothis assulta. Korean J. Appl. Entomol. 28, 113-119.
  24. Choi, M.Y., Han, K.S., Boo, K.S., Jurenka, R.A., 2002. Pheromone biosynthetic pathways in the moths Helicoverpa zea and Helicoverpa assulta. Insect Biochem. Mol. Biol. 32, 1353-1359. doi:10.1016/S0965-1748(02)00055-3
  25. Choi, M.Y., Tanaka, M., Kataoka, H., Boo, K.S., Tatsuki, S., 1998a. Isolation and identification of the cDNA encoding the pheromone biosynthesis activating neuropeptide and additional neuropeptides in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochem. Mol. Biol. 28, 759-766. doi:10.1016/S0965-1748(98)00065-4
  26. Choi, M.Y., Tatsuki, S., Boo, K.S., 1998b. Regulation of sex pheromone biosynthesis in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Insect Physiol. 44, 653-658. doi:10.1016/S0022-1910(98)00029-8
  27. Chung, C.S., Hyun, J.S., 1980. The effects of temperatures on the development of oriental tobacco budmoth, Heliothis assulta Guenee, and control effects of Thuricide HP®. Korean J. Plant Prot. 19, 57-65.
  28. Cork, A., Boo, K.S., Dunkelblum, E., Hall, D.R., Jee-Rajunga, K., Kehat, M., Kong Jie, E., Park, K.C., Tepgidagarn, P., Xun, L., 1992. Female sex pheromone of oriental tobacco budworm, Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae): Identification and field testing. J. Chem. Ecol. 18, 403-418. doi:10.1007/BF00994240
  29. Cowles, R.S., Keller, J.E., Miller, J.R., 1989. Pungent spices, ground red pepper, and synthetic capsaicin as onion fly ovipositional deterrents. J. Chem. Ecol. 15, 719-730. doi:10.1007/BF01014714
  30. Cunningham, J.P., Zalucki, M.P., 2014. Understanding Heliothine (Lepidoptera: Heliothinae) pests: What is a host plant. J. Econ. Entomol. 107, 881-896. doi:10.1603/EC14036
  31. Despres, L., David, J.P., Gallet, C., 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298-307. doi:10.1016/j.tree.2007.02.010
  32. Dong, J.-F., Zhang, J.-H., Wang, C.-Z., 2002. Effects of plant allelochemicals on nutritional utilization and detoxication enzyme activities in two Helicoverpa species. Acta Entomol. Sin. 45, 296-300. https://doi.org/10.3321/j.issn:0454-6296.2002.03.003
  33. Ehrlich, P.R., Raven, P.H., 1964. Butterflies and plants: A study in coevolution. Evolution. 18, 586-608. doi:10.1079/IVP2001184
  34. Eichenseer, H., Mathews, M.C., Bi, J.L., Murphy, J.B., Felton, G.W., 1999. Salivary glucose oxidase: Multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42, 99-109. doi:10.1002/(SICI)1520-6327(199909)42:1<99::AID-ARCH10>3.0.CO;2-B
  35. Eichenseer, H., Mathews, M.C., Powell, J.S., Felton, G.W., 2010. Survey of a salivary effector in caterpillars: Glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36, 885-897. doi:10.1007/s10886-010-9830-2
  36. Feyereisen, R., 2012. Insect CYP genes and P450 enzymes, in: Insect Molecular Biology and Biochemistry. Elsevier, pp. 236-316. doi:10.1016/B978-0-12-384747-8.10008-X
  37. Fitt, G.P., 1989. The ecology of Heliothis species in relation to agroecosystems. Annu. Rev. Entomol. 34, 17-53. doi:10.1146/annurev.en.34.010189.000313
  38. Han, M.-W., Lee, J.-H., Lee, M.-H., 1993. Effect of temperature on development of oriental tobacco budworm, Helicoverpa assulta Guenee. Korean J. Appl. Entomol. 32, 236-244.
  39. Han, M.-W., Lee, J.-H., Son, J.-S., 1994. Intra- and inter-plant distribution of Helicoverpa assulta (Lepioprera: Noctuidae) eggs in red pepper and tobacco fields. Korean J. Appl. Entomol. 33, 6-11.
  40. Heckel, D.G., 2018. Insect detoxification and sequestration strategies, in: Annual Plant Reviews Online. John Wiley & Sons, Ltd, Chichester, UK, pp. 77-114. doi:10.1002/9781119312994.apr0507
  41. Hori, M., Nakamura, H., Fujii, Y., Suzuki, Y., Matsuda, K., 2011. Chemicals affecting the feeding preference of the Solanaceaefeeding lady beetle Henosepilachna vigintioctomaculata (Coleoptera: Coccinellidae). J. Appl. Entomol. 135, 121-131. doi:10.1111/j.1439-0418.2010.01519.x
  42. Hwang, C.Y., Choi, K.M., Park, J.S., 1987. Studies on bionomics of the oriental tobacco budworm, Heliothis assulta Guenee. Res. Rep. RDA 29, 95-113.
  43. Jadhav, D.R., Armes, N.J., 1996. Comparative status of insecticide resistance in the Helicoverpa and Heliothis species (Lepidoptera: Noctuidae) of south India. Bull. Entomol. Res. 86, 525-531. doi:10.1017/S0007485300039316
  44. Jallow, M.F.A., Paul Cunningham, J., Zalucki, M.P., 2004. Intraspecific variation for host plant use in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae): Implications for management. Crop Prot. 23, 955-964. doi:10.1016/j.cropro.2004.02.008
  45. Jordt, S.E., Julius, D., 2002. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108, 421-430. doi:10.1016/S0092-8674(02)00637-2
  46. Jung, J.K., Boo, K.S., 1992. Lipid and carbohydrate contents in the adult hemolymph during flight of the oriental tobacco budworm (Helicoverpa assulta (Guenee)). Korean J. Appl. Entomol. 31, 329-337.
  47. Kamimura, M., Tatsuki, S., 1993. Diel rhythms of calling behavior and pheromone production of oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Chem. Ecol. 19, 2953-2963. doi:10.1007/BF00980595
  48. Kamimura, M., Tatsuki, S., 1994. Effects of photoperiodic changes on calling behavior and pheromone production in the Oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J. Insect Physiol. 40, 731-734. doi:10.1016/0022-1910(94)90101-5
  49. Ketterman, A.J., Saisawang, C., Wongsantichon, J., 2011. Insect glutathione transferases. Drug Metab. Rev. 43, 253-265. doi:10.3109/03602532.2011.552911
  50. Kirkpatrick, T.H., 1961. Comparative morphological studies of Heliothis species (Lepidoptera: Noctuidae) in Queensland. Queensl. J. Agric. Sci. 18, 179-194.
  51. Koh, Y.H., Park, K.C., Boo, K.S., 1995. Antennal sensilla in adult Helicoverpa assulta (Lepidoptera: Noctuidae): Morphology, distribution, and ultrastructure. Ann. Entomol. Soc. Am. 88, 519-530. doi:10.1093/aesa/88.4.519
  52. Kumar, P., Pandit, S.S., Steppuhn, A., Baldwin, I.T., 2014. Natural history-driven, plant-mediated RNAi-based study reveals CYP-6B46's role in a nicotine-mediated antipredator herbivore defense. Proc. Natl. Acad. Sci. U. S. A. 111, 1245-1252. doi:10.1073/pnas.1600609113
  53. Lee, D.W., Kim, S.S., Shin, S.W., Kim, W.T., Boo, K.S., 2006. Molecular characterization of two acetylcholinesterase genes from the oriental tobacco budworm, Helicoverpa assulta (Guenee). Biochim. Biophys. Acta 1760, 125-133. doi:10.1016/J.BBAGEN.2005.10.009
  54. Lee, J.H., Boo, K.S., 1993a. Comparative effects of nicotine and diazinon on larval mortality and activity of cytochrome P-450 monooxygenases in Helicoverpa assulta and Spodoptera exigua. Korean J. Appl. Entomol. 32, 225-235.
  55. Lee, J.H., Boo, K.S., 1993b. Activity of mixed function oxidase in a few insect species in relation to their food source. Korean J. Appl. Entomol. 32, 291-299.
  56. Lee, J.-H., Han, M.-W., 1998. Survival and development of overwintering pupae of the oriental tobacco budworm, Helicoverpa assulta, from different locality. Korean J. Appl. Entomol. 37, 127-135.
  57. Lim, H.-J., Kang, T.J., Kim, H.H., Yang, C.Y., Kim, I., Kim, D.H., Ahn, S.-J., 2016. Effect of a non-host plant Phaseolus vulgaris on larval performance and oviposition of the oriental tobacco budworm Helicoverpa assulta (Lepidoptera: Noctuidae). Entomol. Res. 46, 170-175. doi:10.1111/1748-5967.12158
  58. Liu, Y.-L., Guo, H., Huang, L.-Q., Pelosi, P., Wang, C.-Z., 2014. Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. J. Exp. Biol. 217, 1821-1826. doi:10.1242/jeb.102020
  59. Madhumathy, A.P., Aivazi, A.A., Vijayan, V.A., 2007. Larvicidal efficacy of Capsicum annum against Anopheles stephensi and Culex quinquefasciatus. J. Vector Borne Dis. 44, 223-226.
  60. Maliszewska, J., Tegowska, E., 2012. Capsaicin as an organophosphate synergist against Colorado potato beetle (Leptinotarsa decemlineata Say). J. Plant Prot. Res. 52, 28-34. doi:10.2478/v10045-012-0005-8
  61. Matthews, M., 1999. Heliothine moths of Australia. A guide to pest bollworms and related noctuid groups. CSIRO Publishing, Collingwood, Australia.
  62. Mazourek, M., Pujar, A., Borovsky, Y., Paran, I., Mueller, L., Jahn, M.M., 2009. A dynamic interface for capsaicinoid systems biology. Plant Physiol. 150, 1806-1821. doi:10.1104/pp.109.136549
  63. McIndoo, N.E., 1916. Effects of nicotine as an insecticide. J. Agric. Res. Dep. Agric. 7, 89-122.
  64. Ming, Q.-L., Yan, Y.-H., Wang, C.-Z., 2007. Mechanisms of premating isolation between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae). J. Insect Physiol. 53, 170-178. doi:10.1016/J.JINSPHYS.2006.11.007
  65. Mitter, C., Poole, R.W., Matthews, M., 1993. Biosystematics of the Heliothinae (Lepidoptera: Noctuidae). Annu. Rev. Entomol. 38, 207-225. doi:10.1146/annurev.en.38.010193.001231
  66. Musser, R.O., Hum-Musser, S.M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J.B., Felton, G.W., 2002. Caterpillar saliva beats plant defences. Nature 416, 599-600. doi:10.1038/416599a
  67. Park, K.C., Boo, K.S., Cork, A., Hall, D.R., 2002. Monitoring Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae) with synthetic sex pheromone and small scale disruption trial with controlledrelease PVC resin formulation. Chem. Pharm. Bull. 34, 19-22.
  68. Park, K.C., Boo, K.S., Hall, D.R., Cork, A., 1994. Biological activity of female sex pheromone of the oriental tobacco budworm, Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae). Korean J. Appl. Entomol. 33, 26-32.
  69. Park, K.C., Cork, A., Boo, K.S., 1996. Intrapopulational changes in sex pheromone composition during scotophase in oriental tobacco budworm, Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae). J. Chem. Ecol. 22, 1201-1210. doi:10.1007/BF02027955
  70. Park, S.S., Boo, K.S., 1988. Structure of sensilla on the antenna and mouthparts of the oriental tobacco budworm (Heliothis assulta Guenee) larvae. Korean J. Appl. Entomol. 27, 94-102.
  71. Pearce, S.L., Clarke, D.F., East, P.D., Elfekih, S., Gordon, K.H.J., Jermiin, L.S., McGaughran, A., Oakeshott, J.G., Papanikolaou, A., Perera, O.P., Rane, R. V., Richards, S., Tay, W.T., Walsh, T.K., Anderson, A., Anderson, C.J., Asgari, S., Board, P.G., Bretschneider, A., Campbell, P.M., Chertemps, T., Christeller, J.T., Coppin, C.W., Downes, S.J., Duan, G., Farnsworth, C.A., Good, R.T., Han, L.B., Han, Y.C., Hatje, K., Horne, I., Huang, Y.P., Hughes, D.S.T., Jacquin-Joly, E., James, W., Jhangiani, S., Kollmar, M., Kuwar, S.S., Li, S., Liu, N.Y., Maibeche, M.T., Miller, J.R., Montagne, N., Perry, T., Qu, J., Song, S. V., Sutton, G.G., Vogel, H., Walenz, B.P., Xu, W., Zhang, H.J., Zou, Z., Batterham, P., Edwards, O.R., Feyereisen, R., Gibbs, R.A., Heckel, D.G., McGrath, A., Robin, C., Scherer, S.E., Worley, K.C., Wu, Y.D., 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, 63. doi:10.1186/s12915-017-0402-6
  72. Schoonhoven, L.M., van Loon, J.J.A., Dicke, M., 2005. Insectplant biology, Second. ed. Oxford University Press, New York.
  73. Slansky, F., 1990. Insect nutritional ecology as a basis for studying host plant resistance. Florida Entomol. 73, 359-378. doi:10.2307/3495455
  74. Snyder, M.J., Walding, J.K., Feyereisen, R., 1994. Metabolic fate of the allelochemical nicotine in the tobacco hornworm Manduca sexta. Insect Biochem. Mol. Biol. 24, 837-846. doi:10.1016/0965-1748(94)90112-0
  75. Sun, L., Hou, W., Zhang, J., Dang, Y., Yang, Q., Zhao, X., Ma, Y., Tang, Q., 2021. Plant metabolites drive different responses in caterpillars of two closely related Helicoverpa species. Front. Physiol. 12, 662978. doi:10.3389/fphys.2021.662978
  76. Sun, Y.-L., Huang, L.-Q., Pelosi, P., Wang, C.-Z., 2012. Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species. PLoS ONE 7, e30040. doi:10.1371/journal.pone.0030040
  77. Tang, D., Wang, C., Luo, L., Qin, J., 2000. Comparative study on the responses of maxillary sensilla styloconica of cotton bollworm Helicoverpa armigera and Oriental tobacco budworm H. assulta larvae to phytochemicals. Sci. China Ser. C Life Sci. 43, 606-612. doi:10.1007/BF02882281
  78. Tang, Q.-B., Jiang, J.-W., Yan, Y.-H., van Loon, J.J.A., Wang, C.-Z., 2006. Genetic analysis of larval host-plant preference in two sibling species of Helicoverpa. Entomol. Exp. Appl. 118, 221-228. doi:10.1111/j.1570-7458.2006.00387.x
  79. Tewksbury, J.J., Nabhan, G.P., 2001. Seed dispersal: Directed deterrence by capsaicin in chillies. Nature 412, 403-404. doi:10.1038/35086653
  80. Tian, K., Zhu, J., Li, M., Qiu, X., 2019. Capsaicin is efficiently transformed by multiple cytochrome P450s from Capsicum fruit-feeding Helicoverpa armigera. Pestic. Biochem. Physiol. 156, 145-151. doi:10.1016/j.pestbp.2019.02.015
  81. Tomizawa, M., Casida, J.E., 2005. Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45, 247-268. doi:10.1146/annurev.pharmtox.45.120403.095930
  82. Wang, C., Dong, J., 2001. Interspecific hybridization of Helicoverpa armigera and H. assulta (Lepidoptera: Noctuidae). Chinese Sci. Bull. 46, 489-491. doi:10.1007/BF03187264
  83. Wang, C., Dong, J., Tang, D., Zhang, J., Li, W., Qin, J., 2004. Host selection of Helicoverpa armigera and H. assulta and its inheritance. Prog. Nat. Sci. 14, 880-884. doi:10.1080/10020070412331344491
  84. Wang, H.-L., Zhao, C.-H., Wang, C.-Z., 2005. Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochem. Mol. Biol. 35, 575-583. doi:10.1016/J.IBMB.2005.01.018
  85. Wang, K.-Y., Zhang, Y., Wang, H.-Y., Xia, X.-M., Liu, T.-X., 2008. Biology and life table studies of the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae), influenced by different larval diets. Insect Sci. 15, 569-576. doi:10.1111/j.1744-7917.2008.00247.x
  86. Wang, Y., Ma, Y., Zhou, D.-S., Gao, S.-X., Zhao, X.-C., Tang, Q.-B., Wang, C.-Z., van Loon, J.J.A., 2017. Higher plasticity in feeding preference of a generalist than a specialist: Experiments with two closely related Helicoverpa species. Sci. Rep. 7, 17876. doi:10.1038/s41598-017-18244-7
  87. Weissenberg, M., Klein, M., Meisner, J., Ascher, K.R.S., 1986. Larval growth inhibition of the spiny bollworm, Earias insulana, by some steroidal secondary plant compounds. Entomol. Exp. Appl. 42, 213-217. doi:10.1111/j.1570-7458.1986.tb01024.x
  88. Wu, K.J., Gong, P.Y., Ruan, Y.M., 2006. Is tomato plant the host of the oriental tobacco budworm, Helicoverpa assulta (Guenee)? Acta Entomol. Sin. 49, 421-427. https://doi.org/10.3321/j.issn:0454-6296.2006.03.012
  89. Xie, L., Jiang, M., Zhang, X., 1998. Effect of temperature and humidity on laboratory population of Helicoverpa assulta. Acta Entomol. Sin. 41, 61-69.
  90. Xu, G., Qin, J., 1994. Extraction and characterization of midgut proteases from Heliothis armigera and H. assulta (Lepidoptera: Noctuidae) and their inhibition by tannic acid. J. Econ. Entomol. 87, 334-338. doi:10.1093/jee/87.2.334
  91. Xu, G., Qin, J.-D., 1987. Responses of two Heliothis species to plant secondary substances: the influence of host secondary substances on larval growth and food utilization. Acta Entomol. Sin. 30, 359-366.
  92. Xu, M., Guo, H., Hou, C., Wu, H., Huang, L.-Q., Wang, C.-Z., 2016. Olfactory perception and behavioral effects of sex pheromone gland components in Helicoverpa armigera and Helicoverpa assulta. Sci. Rep. 6, 22998. doi:10.1038/srep22998
  93. Yang, C.-Y., Jen, H.-Y., Cho, M.-R., Kim, D.-S., and Yiem, M.-S., 2004. Seasonal occurrence of oriental tobacco budworm (Lepidoptera: Noctuidae) male and cohemical control at red pepper fields. Korean J. Appl. Entomol. 43, 49-54.
  94. Yang, L., Wang, X., Bai, S., Li, Xin, Gu, S., Wang, C.-Z., Li, Xianchun, 2017. Expressional divergence of insect GOX genes: From specialist to generalist glucose oxidase. J. Insect Physiol. 100, 21-27. doi:10.1016/j.jinsphys.2017.05.003
  95. Yoshinaga, N., Aboshi, T., Abe, H., Nishida, R., Alborn, H.T., Tumlinson, J.H., Mori, N., 2008. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc. Natl. Acad. Sci. U. S. A. 105, 18058-18063. doi:10.1073/pnas.0809623105
  96. Zalucki, M.P., Daglish, G., Firempong, S., Twine, P., 1986. The biology and ecology of Heliothis armigera (Hubner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia - What do we know. Aust. J. Zool. 34, 779-814. https://doi.org/10.1071/ZO9860779
  97. Zhang, D.-D., Zhu, K.Y., Wang, C.-Z., 2010. Sequencing and characterization of six cDNAs putatively encoding three pairs of pheromone receptors in two sibling species, Helicoverpa armigera and Helicoverpa assulta. J. Insect Physiol. 56, 586-593. doi:10.1016/J.JINSPHYS.2009.12.002
  98. Zhang, Y., Wang, K.Y., Wang, G., Guo, Q.L., Fan, K., Yuan, X.L., Wu, C.Z., 2006. Preference and adaptability of oriental tobacco budworm, Helicoverpa assulta, to three food plants. Chinese Bull. Entomol. 43, 781-784. https://doi.org/10.3969/j.issn.0452-8255.2006.06.008
  99. Zhou, D.-S., Wang, C.-Z., van Loon, J.J.A., 2022. Habituation to a deterrent plant alkaloid develops faster in the specialist herbivore Helicoverpa assulta than in its generalist congener Helicoverpa armigera and coincides with taste neuron desensitisation. Insects 13, 21. doi:10.3390/insects13010021
  100. Zhu, J., Tian, K., Reilly, C.A., Qiu, X., 2020. Capsaicinoid metabolism by the generalist Helicoverpa armigera and specialist H. assulta: Species and tissue differences. Pestic. Biochem. Physiol. 163, 164-174. doi:10.1016/J.PESTBP.2019.11.013
  101. Zong, N., Wang, C.-Z., 2004. Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chinese Sci. Bull. 49, 1596-1601. doi:10.1360/03wc0185
  102. Zong, N., Wang, C.-Z., 2007. Larval feeding induced defensive responses in tobacco: Comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226, 215-224. doi:10.1007/s00425-006-0459-x