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Analysis of Gene Expression in Larval Fat Body of Plutella Xylostella Under High Temperature

고온에서 배추좀나방 유충 지방체의 유전자 발현 변화 분석

  • Kim, Kwang Ho (Crop Protection Division, Department of Agro-food Safety and Crop Protection, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lee, Dae-Weon (Department of Life Sciences, School of Chemistry and Life Sciences, Kyungsung University)
  • 김광호 (농촌진흥청 국립농업과학원 농산물안전성부 작물보호과) ;
  • 이대원 (경성대학교 화학생명과학부 생명과학전공)
  • Received : 2018.11.22
  • Accepted : 2018.12.21
  • Published : 2018.12.31

Abstract

BACKGROUND: Insects are ectothermic organisms in terrestrial ecosystems and play various roles such as controlling plant biomass and maintaining species diversity. Because insects are ectothermic, their physiological responses are very sensitive to environmental temperature which determines survival and distribution of insect population and that affects climate change. This study aimed to identification of genes contributing to fitness under high temperature. METHODS AND RESULTS: To identify genes contributing to fitness under high temperature, the transcriptomes of fat body in Plutella xyostella larva have been analyzed via next generation sequencing. From the fat body transcriptomes, structure-related proteins, heat shock proteins, antioxidant enzymes and detoxification proteins were identified. Genes encoding proteins such as structural proteins (cuticular proteins, chitin synthase and actin), stress-related protein (cytochrome P450), heat shock protein and antioxidant enzyme (catalase) were up-regulated at high temperature. In contrast expression of glutathione S transferase was down-regulated. CONCLUSION: Identifications of temperature-specific up- or down-regulated genes can be useful for detecting temperature adaptation and understanding physiological responses in insect pests.

곤충은 변온동물로 육지생태계에서 주로 서식하면서, 식물의 생체량 조절, 종다양성 유지에 중요한 역할을 한다. 주변온도는 변온동물인 곤충의 생리적 반응속도, 뿐만 아니라 생존과 분포를 결정하며, 기후변화에 영향을 준다. 본 연구는 높은 온도에서 곤충의 적응성에 관련있는 유전자를 전사체를 이용하여 동정하였다. 고온에서 사육된 배추좀나방 유충의 지방체로부터 차세대 염기서열 분석법을 이용하여 전사체를 확보하였다. 대사중심인 지방체에서 구조단백질, 열충격단백질, 항산화단백질, 해독효소 들이 동정되었다. 이들 중에서 표피단백질(표피단백질, 키틴합성효소, 엑틴, 카이틴 합성), 스트레스관련단백질(시토크롬 P450), 열충격단백질, 한산화단백질은 발현이 증가되었으나, glutathione S transferase 발현은 오히려 감소되었다. 이상의 결과는 기후변화의 주요인인 온난화에 대한 해충의 생리적 대응과 온도적응을 이해하는데 필요한 기초자료를 제시한다.

Keywords

References

  1. Abdollahi, M., Ranjbar, A., Shadnia, S., Nikfar, S., & Rezaie, A. (2004). Pesticides and oxidative stress: a review, Med. Sci. Monitor 10, Ra141-147.
  2. Angilletta, M. J., Steury, T. D., & Sears, M. W. (2004). Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle, Integr. Comp. Biol. 44, 498-509. https://doi.org/10.1093/icb/44.6.498
  3. Arrigo, A.-P. (1987). Cellular localization of HSP23 during Drosophila development and following subsequent heat shock, Dev. Biol. 122, 39-48. https://doi.org/10.1016/0012-1606(87)90330-7
  4. Bagchi, R., Gallery, R. E., Gripenberg, S., Gurr, S. J., Narayan, L., Addis, C. E., Freckleton, R. P., & Lewis, O. T. (2014). Pathogens and insect herbivores drive rain forest plant diversity and composition, Nature 506, 85-88. https://doi.org/10.1038/nature12911
  5. Balabanidou, V., Grigoraki, L., & Vontas, J. (2018). Insect cuticle: a critical determinant of insecticide resistance, Curr. Opin. Insect Sci. 27, 68-74. https://doi.org/10.1016/j.cois.2018.03.001
  6. Balabanidou, V., Kampouraki, A., MacLean, M., Blomquist, G. J., Tittiger, C., Juarez, M. P., Mijailovsky, S. J., Chalepakis, G., Anthousi, A., Lynd, A., Antoine, S., Hemingway, J., Ranson, H., Lycett, G. J., & Vontas, J. (2016). Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae, Proc. Nat'l Acad. Sci. USA. 113, 9268-9273. https://doi.org/10.1073/pnas.1608295113
  7. Barrett, R. D., Paccard, A., Healy, T. M., Bergek, S., Schulte, P. M., Schluter, D., & Rogers, S. M. (2011). Rapid evolution of cold tolerance in stickleback, Proc. Biol. Sci. 278, 233-238. https://doi.org/10.1098/rspb.2010.0923
  8. Bauerfeind, S. S., & Fischer, K. (2014). Simulating climate change: Temperature extremes but not means diminish performance in a widespread butterfly, Popul. Ecol. 56, 239-520. https://doi.org/10.1007/s10144-013-0409-y
  9. Bruey, J. M., Ducasse, C., Bonniaud, P., Ravagnan, L,, Susin, S. A., Diaz-Latoud, C., Gurbuxani, S., Arrigo, A. P., Kroemer, G., Solary, E., & Garrido, C. (2000). Hsp27 negatively regulates cell death by interacting with cytochrome c, Nat. Cell Biol. 2, 645-652. https://doi.org/10.1038/35023595
  10. Casique-Arroyo, G., Martinez-Gallardo, N., de la Vara, L. G., & Delano-Frier, J. P. (2014). Betacyanin biosynthetic genes and enzymes are differentially induced by (a)biotic stress in Amaranthus hypochondriacus, PLOS ONE 6, e99012.
  11. Chowdary, T. K., Raman, B., Ramakrishna, T., & Rao, C. M. (2004). Mammalian Hsp22 is a heat-inducible small heat-shock protein with chaperone-like activity, Biochem. J. 381, 379-387. https://doi.org/10.1042/BJ20031958
  12. Chown, S. L., Hoffmann, A. A., Kristensen, T. N., Angilletta, M. J., Stenseth, N. C., & Pertoldi, C. (2010). Adapting to climate change: a perspective from evolutionary physiology, Climate Res. 43, 3-15. https://doi.org/10.3354/cr00879
  13. Chown, S. L., Terblanche, J. S., & Simpson, S. J. (2006). Physiological diversity in insects: ecological and evolutionary contexts, Adv. Insect Physiol. 33, 50-152.
  14. Dennis, D., & Weisenburger, M. D. (1993). Human health effects of agrichemical use, Human Pathol. 24, 571-576. https://doi.org/10.1016/0046-8177(93)90234-8
  15. Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C., & Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude, Proc. Natl. Acad. Sci. USA. 105, 6668-6672. https://doi.org/10.1073/pnas.0709472105
  16. Ehrnsperger, M., Graber, S., Gaestel, M., & Buchner, J. (1997). Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation, EMBO J. 16, 221-229. https://doi.org/10.1093/emboj/16.2.221
  17. Enayati, A. A., Ranson, H., & Hemingway, J. (2005). Insect glutathione transferases and insecticide resistance, Insect Mol. Biol. 14, 3-8. https://doi.org/10.1111/j.1365-2583.2004.00529.x
  18. Goto, S., & Kimura, M. (1998). Heat- and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila, J. Insect Physiol. 44, 1233-1239. https://doi.org/10.1016/S0022-1910(98)00101-2
  19. Grazyna, C., Hanna, C., Adam A., & Magdalena, B. M. (2017). Natural antioxidants in milk and dairy products, Int. J. Dairy Technol. 70, 165-178. https://doi.org/10.1111/1471-0307.12359
  20. Guittard, E., Blais, C., Maria, A., Parvy, J. P., Parishna, S., Lumb, C., Lafont, R., Daborn, P. J., & Dauphin-Villemant, C. (2011). CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis, Dev. Biol. 349, 35-45. https://doi.org/10.1016/j.ydbio.2010.09.023
  21. Gutierrez, E. D., Wiggins, D., Fielding, B., & Gould, A. P. (2007). Specialized hepatocyte-like cells regulate Drosophila lipid metabolism, Nature 445, 275-280. https://doi.org/10.1038/nature05382
  22. Habig, W. H., Pabst, M. J., & Jakoby, W. B., (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation, J. Biol. Chem. 249, 7130-7139.
  23. Haslbeck, M., Walke, S., Stromer, T., Ehrnsperger, M., White, H. E., Chen, S., Saibil, H. R., & Buchner, J. (1999). Hsp26: a temperature-regulated chaperone, EMBO J. 18, 6744-6751. https://doi.org/10.1093/emboj/18.23.6744
  24. Hillebrand, H., Borer, E. T., Bracken, M. E. S., Cardinale, B. J., Cebrian, J., Cleland, E. E., Elser, J. J., Gruner, D. S., Harpole, W. S., Ngai, J. T., Sandin, S., Seabloom, E. W., Shurin, J. B., Smith, J. E., & Smith, M. D. (2009). Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems, Ecology Lett. 12, 516-527. https://doi.org/10.1111/j.1461-0248.2009.01304.x
  25. Hopkins, T. L., & Kramer, K. J. (1992). Insect cuticle sclerotization, Annu. Rev. Entomol. 37, 273-302. https://doi.org/10.1146/annurev.en.37.010192.001421
  26. Kaplanoglu, E., Chapman, P., & Scott, Donly, C. (2017). Overexpression of a cytochrome P450 and a UDP glycosyltransferase is associated with imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata, Sci. Rep. 7, 1762. https://doi.org/10.1038/s41598-017-01961-4
  27. Kim, E., Choi, B., Park, Y., Cha, O., Jung, C., Lee, D., Kim, K., & Kim, Y. (2014). Overwintering conditions of the Diamondback moth and genetic variation of overwintering populations, Kor. J. Appl. Entomol. 53, 353-363.
  28. Kim, S. M., Hur, J. H., Han, D. S., Cho, J. M., & Kim, K. J., 2001. Diamondback moth (Plutella xylostella L.) resistance to organophosphorus and carbamate insecticides in Kangwon alpine vegetable croplands, Kor. Soc. Pestic. Sci. 5, 24-30.
  29. Kim, T. M., Underwood, N., & Inouye, B. D., 2013. Insect herbivores change the outcome of plant competition through both inter- and intraspecific processes, Ecology 94, 1753-1763. https://doi.org/10.1890/12-1261.1
  30. Kriehuber, T., Rattei, T., Weinmaier, T., Bepperling, A., Haslbeck, M., & Buchner, J. (2010). Independent evolution of the core domain and its flanking sequences in small heat shock proteins, FASEB J. 24, 3633-3642. https://doi.org/10.1096/fj.10-156992
  31. Lavoie, J. N., Gingras-Breton, G., Tanguay, R. M., & Landry, J. (1993). Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization, J. Biol. Chem. 268, 3420-3429.
  32. Leal, M., & Gunderson, A. R. (2012). Rapid change in the thermal tolerance of a tropical lizard, Am Nat. 180, 815-822. https://doi.org/10.1086/668077
  33. Lee, S. C., Cho, Y. S., Kim, D. I. (1993). Comparative study of toxicological methods and field resistance to insecticides in diamondback moth (Lepidoptera: Plutellidae), Kor. J. Appl. Entomol. 32, 323-329.
  34. Lee, S. H., Kang, J. S., Min, J. S., Yoon, K. S., Strycharz, J. P., Johnson, R., Mittapalli, O., Margam, V. M., Sun, W., Li, H. M., Xie, J., Wu, J., Kirkness, E. F., Berenbaum, M. R., Pittendrigh, B. R., & Clark, J. M. (2010). Decreased detoxification genes and genome size make the human body louse an efficient model to study xenobiotic metabolism, Insect Mol. Biol. 19, 599-615. https://doi.org/10.1111/j.1365-2583.2010.01024.x
  35. Lemoine, N. P., & Burkepile, D. E. (2012). Temperatureinduced mismatches between consumption and metabolism reduce consumer fitness, Ecology 93, 2483-2489. https://doi.org/10.1890/12-0375.1
  36. Lemoine, N. P., Drews, W. A., Burkepile, D. E., & Parker, J. D. (2013). Increased temperature alters feeding behavior of a generalist herbivore, Oikos 122, 1669-1678. https://doi.org/10.1111/j.1600-0706.2013.00457.x
  37. Li, X., Schuler, M. A., & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics, Annu. Rev. Entomol. 52,231-253. https://doi.org/10.1146/annurev.ento.51.110104.151104
  38. Li, X., Zhu, B., Gao, X., & Liang, P. (2017). Over-expression of UDP-glycosyltransferase gene UGT2B17 is involved in chlorantraniliprole resistance in Plutella xylostella (L.), Pest Manag. Sci. 73, 1402-1409. https://doi.org/10.1002/ps.4469
  39. Lindmark-Mansson, H., & Akesson, B. (2000). Antioxidative factors in milk, Br. J. Nutr. 84, 103-110. https://doi.org/10.1017/S0007114500002324
  40. Lumjuan, N., McCarroll, L., Prapanthadara, L. A., Hemingway, J., & Ranson, H. (2005). Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti, Insect Biochem. Mol. Biol. 35,861-871. https://doi.org/10.1016/j.ibmb.2005.03.008
  41. Maibeche-Coisne, M. L., Monti-Dedieu, S., Aragon, S., & Dayphin-Villemant, C. (2000). A new cytochrome P450 from Drosophila melanogaster, CYP4G15, expressed in the nervous system, Biochem. Biophys. Res. Commun. 273, 1132-1137. https://doi.org/10.1006/bbrc.2000.3058
  42. Mannervik, B. (1985). The isoenzymes of glutathione transferase, Adv. Enzymol. Relat, Areas Mol. Biol. 57, 357-417.
  43. Metcalf, D. B., Asner, G. P., Martin, R. E., Espejo, J. E. S., Huasco, W. H., Amezquita, F. F. F., Carranza-Jimenez, L., Cabrera, D. F. G., Baca, L. D., Sinca, F., Quispe, L. P. H,, Taype, I. A., Mora, L. E., Davila, A. R., Solorzano, M. M., Vilca, B. L. P., Roman, J. M. L., Bustios, P. C. G., Revilla, N. S., Tupayachi, R., Girardin, C. A. J., Doughty, C. E., & Malhi, Y. (2014). Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 17, 324-332. https://doi.org/10.1111/ele.12233
  44. O'Connor, M. I. (2009). Warming strengthens an herbivore- plant interaction, Ecology 90, 388-398. https://doi.org/10.1890/08-0034.1
  45. O'Connor, M. I., Piehler, M. F., Leech, D. M., Anton, A., & Bruno, J. F. (2009). Warming and resource availability shift food web structure and metabolism, PLOS Biol. 7, e1000178. https://doi.org/10.1371/journal.pbio.1000178
  46. Pan, Y., Tian, F., Wei, X., Wu, Y., Gao, X., Xi, J., & Shang, Q. (2018). Thiamethoxam resistance in Aphis gossypii Glover relies on multiple UDP-glucuronosyltransferases, Front. Physiol. 9, 322. https://doi.org/10.3389/fphys.2018.00322
  47. Pavlidi, N., Vontas, J., & Van Leeuwen, T. (2018). The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors, Curr. Opin. Insect Sci. 27, 97-102. https://doi.org/10.1016/j.cois.2018.04.007
  48. Peyser, R. D., Lanno, S. M., Shimshak, S. J., & Coolon, J. D. (2017). Analysis of cytochrome P450 contribution to evolved plant toxin resistance in Drosophila sechellia, Insect Mol. Biol. 26, 715-720. https://doi.org/10.1111/imb.12329
  49. Rewitz, K. F., & Gilbert, L. I. (2008). Daphnia Halloween genes that encode cytochrome P450s mediating the synthesis of the arthropod molting hormone: evolutionary implications, BMC Evol. Biol. 8, 60. https://doi.org/10.1186/1471-2148-8-60
  50. Riveron, J. M., Yunta, C., Ibrahim, S. S., Djouaka, R., Irving, H., Menze, B. D., Ismail, H. M., Hemingway, J., Ranson, H., Albert, A., & Wondji, C. S. (2014). A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector, Genome Biol. 2014, 15.
  51. Sable, M. G., & Rana, D. K. (2016). Impact of global warming on insect behavior - A review, Agricultural Rev. 37, 81-84.
  52. Strode, C., Wondji, C. S., David, J. P., Hawkes, N. J., Lumjuan, N., Nelson, D. R., Drane, D. R., Karunaratne, S. H., Hemingway, J., Black, W. C., & Ranson, H. (2008). Genomic analysis of detoxification genes in the mosquito Aedes aegypti, Insect Biochem. Mol. Biol. 38, 113-123. https://doi.org/10.1016/j.ibmb.2007.09.007
  53. Sunday, J. M., Bates, A. E., & Dulvy, N. K. (2012). Thermal tolerance and the global redistribution of animals, Nat. Clim. Chang. 2, 686-690. https://doi.org/10.1038/nclimate1539
  54. Sunday, J. M., Bates, A. E., Kearney, M. R., Colwell, R. K., Dulvy, N. K., Longino, J. T., & Huey, R. B. (2014). Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation, Proc. Natl. Acad. Sci. USA. 111, 5610-5615. https://doi.org/10.1073/pnas.1316145111
  55. Talekar, N., & Shelton, A. (1993). Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38, 275-301. https://doi.org/10.1146/annurev.en.38.010193.001423
  56. Taylor, R. P., & Benjamin, I. J. (2005). Small heat shock proteins: a new classification scheme in mammals, J. Mol. Cell. Cardiol. 38, 433-444. https://doi.org/10.1016/j.yjmcc.2004.12.014
  57. Thomas, J. H. (2007). Rapid birth-death evolution specific to xenobiotic cytochrome P450 genes in vertebrates, PLOS Genet. 3, e67. https://doi.org/10.1371/journal.pgen.0030067
  58. Tissieres, A., Mitchell, H. K., & Tracy, U. M. (1974). Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs, J. Mol. Biol. 84, 389-398. https://doi.org/10.1016/0022-2836(74)90447-1
  59. Vucic-Pestic, O., Ehnes, R. B., Rall, B. C., & Brose, U. (2011). Warming up the system: higher predator feeding rates but lower energetic efficiencies, Global Change Biol. 17, 1301-1310. https://doi.org/10.1111/j.1365-2486.2010.02329.x
  60. Watson, G. S., Watson, J. A., & Cribb, B. W. (2017). Diversity of cuticular micro- and nanostructures on insects: properties, functions, and potential applications, Annu. Rev. Entomol. 62, 185-205. https://doi.org/10.1146/annurev-ento-031616-035020
  61. Wilding, C. S., Weetman, D., Rippon, E. J., Steen, K., Mawejje, H. D., Barsukov, I., & Donnelly, M. J. (2015). Parallel evolution or purifying selection, not introgression, explains similarity in the pyrethroid detoxification linked GSTE4 of Anopheles gambiae and An. Arabiensis, Mol. Genet. Genomics 290, 201-215. https://doi.org/10.1007/s00438-014-0910-9
  62. Xu, Z.-B., Zou, X.-P., Zhang, N., Feng, Q.-L., & Zheng, S.-C. (2015). Detoxification of insecticides, allelochemicals and heavy metals by glutathione S-transferase SlGSTE1 in the gut of Spodoptera litura, Insect Sci. 22, 503-511. https://doi.org/10.1111/1744-7917.12142
  63. Yamamoto, K., Nagaoka, S., Banno, Y., & Aso, Y. (2009). Biochemical properties of an omega-class glutathione S-transferase of the silkmoth, Bombyx mori, Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 461-467. https://doi.org/10.1016/j.cbpc.2008.10.108
  64. Yamamoto, K., & Yamada, N. (2016). Identification of a diazinon metabolizing glutathione S-transferase in the silkworm, Bombyx mori, Sci. Rep. 6.
  65. Zhang, X., Wu, M., Yao, H., Yang, Y., Cui, M., Tu, Z., Stallones, L., & Xiang, H. (2016). Pesticide poisoning and neurobehavioral function among farm workers in Jiangsu, People's Republic of China, Cortex 74, 396-404. https://doi.org/10.1016/j.cortex.2015.09.006