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Transciptomic Analysis of Larval Fat Body of Plutella xylostella under Low Temperature

저온조건에서 배추좀나방(Plutella xylostella) 지방체 유전자 발현 변화

  • 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 : 2019.10.31
  • Accepted : 2019.11.12
  • Published : 2019.12.31

Abstract

BACKGROUND: Temperature is known to be the main factor affecting development, growth and reproduction of organisms and also a physical factor directly related to insect survival. Insects as ectothermal species should be responsive to climate changes for their survival and develop various survival strategies under the unfavorable temperature such as low temperature. The purpose of this study is to identify genes contributing to adaptation of low temperature. METHODS AND RESULTS: To identify genes contributing to adaptation of low temperature, the transcriptomic data were obtained from fat body in Plutella xyostella larvae via next generation sequencing. We identified structural proteins, heat shock proteins, antioxidant enzymes, detoxification proteins, and cryoprotectant mobilization and biosynthesis-related proteins. Genes encoding chitinase, cuticular protein, Hsp23, chytochrome protein, Glutathione S transferase, and phospholipase 2 were up-regulated under low temperature. Proteins related to energy metabolism such as UDP-glycosy ltransferase, trehalase and trehalose transporter were down-regulated. CONCLUSION: When insect pests were exposed to low temperature, changes in gene expression of fat body could provide some hints for understanding temperature adaptation strategies.

온도는 곤충의 발달, 성장, 생식에 중요한 요인이며, 또한 곤충의 생존에 직접적 관련있는 물리적 요인이다. 변온동물인 곤충은 생존을 위해 기후변화에 반응을 해야 하며, 저온과 같은 취약한 환경하에서도 다양한 생존전략을 발달시켜야 한다. 본 연구는 저온에 대한 적응에 기여하는 유전자를 동정하기 위해 배추좀나방 유충의 지방체를 저온과 상온에 노출시켜 전사체 분석을 수행하였다. 저온전사체에서는 chitinase, 표피단백질, Hsp23, chytochrome, Glutathione S transferase, phospholipase 2 유전자의 발현이 증가된 반면, 에너지 대사에 관여하는 UDP-당전이효소, trehalase, trehalose transporter는 오히려 발현이 감소하였다. 저온에 곤충이 노출되었을 때, 대사중심인 지방체의 유전자 발현의 변화가 곤충의 온도 적응을 이해하는 단서를 제공할 수 있을 것으로 기대된다.

Keywords

References

  1. Ahmad, S. A., & Hopkins, T. L. (1993). ${\beta}$-glucosylation of plant phenolics by phenol ${\beta}$-glucosyltransferase in larval tissues of the tobacco hornworm, Manduca sexta (L.). Insect Biochemistry and Molecular Biology, 23(5), 581-589. https://doi.org/10.1016/0965-1748(93)90031-M
  2. Balabanidou, V., Grigoraki, L., & Vontas, J. (2018). Insect cuticle: a critical determinant of insecticide resistance. Current Opinion in Insect Science 27, 68-74. https://doi.org/10.1016/j.cois.2018.03.001
  3. Barbehenn, R. V. (2002). Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. Journal of Chemical Ecology, 28(7), 1329-1347. https://doi.org/10.1023/A:1016288201110
  4. Bauerfeind, S. S., & Fischer, K. (2014). Simulating climate change: temperature extremes but not means diminish performance in a widespread butterfly. Population Ecology, 56(1), 239-250. https://doi.org/10.1007/s10144-013-0409-y
  5. Berge, J., Feyereisen, R., & Amichot, M. (1998). Cytochrome P450 monooxygenases and insecticide resistance in insects. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 353(1376), 1701-1705. https://doi.org/10.1098/rstb.1998.0321
  6. Bettencourt, B. R., Hogan, C. C., Nimali, M., & Drohan, B. W. (2008). Inducible and constitutive heat shock gene expression responds to modification of Hsp70 copy number in Drosophila melanogaster but does not compensate for loss of thermotolerance in Hsp70 null flies. BMC biology, 6(1). https://doi.org/10.1186/1741-7007-6-5.
  7. 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, Nature Cell Biology, 2, 645-652. https://doi.org/10.1038/35023595
  8. Bull, D. L., & Whitten, C. J. (1972). Factors influencing organophosphorus insecticide resistance in tobacco budworms. Journal of Agricultural and Food Chemistry, 20(3), 561-564. https://doi.org/10.1021/jf60181a061
  9. Chen, S., Fleischer, S. J., Tobin, P. C., & Saunders, M. C. (2011). Projecting insect voltinism under high and low greenhouse gas emission conditions. Environmental Entomology, 40(3), 505-515. https://doi.org/10.1603/EN10099
  10. Cho, J. M., Kim, K. J., Kim, S. M., Han, D. S., & Hur, J. H. (2001). Diamondback moth (Plutella xylostella L.) resistance to organophosphorus and carbamate insecticides in Kangwon alpine vegetable croplands. The Korean Journal of Pesticide Science, 5(1), 30-35.
  11. Clark, M. S., & Worland, M. R. (2008). How insects survive the cold: molecular mechanisms-a review. Journal of Comparative Physiology B, 178(8), 917-933. https://doi.org/10.1007/s00360-008-0286-4
  12. Colinet, H., Lee, S. F., & Hoffmann, A. (2010). Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. The FEBS journal, 277(1), 174-185. https://doi.org/10.1111/j.1742-4658.2009.07470.x
  13. Danielson, P. B., Foster, J. L. M., McMahill, M. M., Smith, M. K., & Fogleman, J. C. (1998). Induction by alkaloids and phenobarbital of Family 4 Cytochrome P450s in Drosophila: evidence for involvement in host plant utilization. Molecular and General Genetics MGG, 259(1), 54-59. https://doi.org/10.1007/s004380050788
  14. David, J. P., Boyer, S., Mesneau, A., Ball, A., Ranson, H., & Dauphin-Villemant, C. (2006). Involvement of cytochrome P450 monooxygenases in the response of mosquito larvae to dietary plant xenobiotics. Insect Biochemistry and Molecular Biology, 36(5), 410-420. https://doi.org/10.1016/j.ibmb.2006.02.004
  15. Drobnis, E. Z., Crowe, L. M., Berger, T., Anchordoguy, T. J., Overstreet, J. W., & Crowe, J. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. Journal of Experimental Zoology, 265(4), 432-437. https://doi.org/10.1002/jez.1402650413
  16. Feyereisen, R. (1999). Insect P450 enzymes. Annual Review of Entomology, 44(1), 507-533. https://doi.org/10.1146/annurev.ento.44.1.507
  17. Garcia-Reina, A., Rodriguez-Garcia, M. J., Ramis, G., & Galian, J. (2017). Real-time cell analysis and heat shock protein gene expression in the TcA Tribolium castaneum cell line in response to environmental stress conditions. Insect Science, 24(3), 358-370. https://doi.org/10.1111/1744-7917.12306
  18. Gosden, R. (2011). Cryopreservation: a cold look at technology for fertility preservation. Fertility and Sterility, 96(2), 264-268. https://doi.org/10.1016/j.fertnstert.2011.06.029
  19. Goto, S. G., & Kimura, M. T. (1998). Heat-and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila . Journal of Insect Physiology, 44(12), 1233-1239. https://doi.org/10.1016/S0022-1910(98)00101-2
  20. Haslbeck, M., Walke, S., Stromer, T., Ehrnsperger, M., White, H. E., Chen, S., Saibil, H. R., & Buchner, J. (1999). Hsp26: a temperature-regulated chaperone. The EMBO Journal, 18(23), 6744-6751. https://doi.org/10.1093/emboj/18.23.6744
  21. Haubert, D., Haggblom, M. M., Scheu, S., & Ruess, L. (2008). Effects of temperature and life stage on the fatty acid composition of Collembola. European Journal of Soil Biology, 44(2), 213-219. https://doi.org/10.1016/j.ejsobi.2007.09.003
  22. Hayakawa, H., Tsutsui, H., & Goto, C. (1988). A survey of overwintering of the diamondback moth, Plutella xylostella Linne, in the Tokachi district of Hokkaido. Annual Report of the Society of Plant Protection of North Japan, 39, 227-228.
  23. Hazel, J. R. (1995). Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?. Annual Review of Physiology, 57(1), 19-42. https://doi.org/10.1146/annurev.ph.57.030195.000315
  24. Hazel, J. R., & Williams, E. E. (1990). The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progress in Lipid Research, 29(3), 167-227. https://doi.org/10.1016/0163-7827(90)90002-3
  25. Hopkins, T. L., & Kramer, K. J. (1992). Insect cuticle sclerotization, Annual Review of Entomology, 37(1), 273-302. https://doi.org/10.1146/annurev.en.37.010192.001421
  26. Irshad, M., & Chaudhuri, P. S. (2002). Oxidant-antioxidant system: role and significance in human body. Indian Journal of Experimental Biology, 40(11), 1233-1239.
  27. Jee, H. (2016). Size dependent classification of heat shock proteins. Journal of Exercise Rehabilitation, 12(4), 255-259. https://doi.org/10.12965/jer.1632642.321
  28. Kern, C., Wolf, C., Bender, F., Berger, M., Noack, S., Schmalz, S., & Ilg, T. (2012). Trehalose-6-phosphate synthase from the cat flea Ctenocephalides felis and Drosophila melanogaster: gene identification, cloning, heterologous functional expression and identification of inhibitors by high throughput screening. Insect Molecular Biology, 21(4), 456-471. https://doi.org/10.1111/j.1365-2583.2012.01151.x
  29. Kim, M. H., & Lee, S. C. (1991). Bionomics of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) in southern region of Korea. Korean Journal of Applied Entomology, 30(3), 169-173.
  30. Kim, Y. H., Lee, J. H., & Lee, S. H. (2011). Determination of organophosphate and carbamate resistance allele frequency in diamondback moth populations by quantitative sequencing and inhibition tests. Journal of Asia-Pacific Entomology, 14(1), 29-33. https://doi.org/10.1016/j.aspen.2010.11.007
  31. Kim, Y., Kim, K., & Kim, N. (1999). Genetic difference between two field populations of Plutella xylostella (Linnee) based on four polymorphic allozymes. Journal of Asia-Pacific Entomology, 2(1), 1-5. https://doi.org/10.1016/S1226-8615(08)60024-2
  32. King, A. M., & MacRae, T. H. (2015). Insect heat shock proteins during stress and diapause. Annual Review of Entomology, 60, 59-75. https://doi.org/10.1146/annurev-ento-011613-162107
  33. Kostal, V., Simek, P., Zahradnickova, H., Cimlova, J., & Stetina, T. (2012). Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism. Proceedings of the National Academy of Sciences of the United States of America, 109(9), 3270-3274. https://doi.org/10.1073/pnas.1119986109
  34. 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. The FASEB Journal, 24(10), 3633-3642. https://doi.org/10.1096/fj.10-156992
  35. Krobitsch, S., Brandau, S., Hoyer, C., Schmetz, C., Hubel, A., & Clos, J. (1998). Leishmania donovani heat shock protein 100 characterization and function in amastigote stage differentiation. Journal of Biological Chemistry, 273(11), 6488-6494. https://doi.org/10.1074/jbc.273.11.6488
  36. Kvist, J., Wheat, C. W., Kallioniemi, E., Saastamoinen, M., Hanski, I., & Frilander, M. J. (2013). Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Molecular Ecology, 22(3), 602-619. https://doi.org/10.1111/j.1365-294X.2012.05521.x
  37. Le Goff, G., Boundy, S., Daborn, P. J., Yen, J. L., Sofr, L., Lind, R., & Ffrench-Constant R. H. (2003). Microarray analysis of cytochrome P450 mediated insecticide resistance in Drosophila. Insect Biochemistry and Molecular Biology, 33(7), 701-708. https://doi.org/10.1016/S0965-1748(03)00064-X
  38. 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), Korean Journal of Applied Entomology, 32(3), 323-329.
  39. Li X., Schuler M. A., & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52, 231-253. https://doi.org/10.1146/annurev.ento.51.110104.151104
  40. Li, J., Qian, X., & Sha, B. (2009). Heat shock protein 40: Structural studies and their functional implications. Protein & Peptide Letters, 16(6), 606-612. https://doi.org/10.2174/092986609788490159
  41. Li, N. G. (2016). Strong tolerance to freezing is a major survival strategy in insects inhabiting central Yakutia (Sakha Republic, Russia), the coldest region on earth. Cryobiology, 73(2), 221-225. https://doi.org/10.1016/j.cryobiol.2016.07.007
  42. Mackenzie, P. I., Owens, I. S., Burchell, B., Bock, K. W., Bairoch, A., Belanger, A., Fournel-Gigleux, S., Green, M., Hum, D. W., Iyanagi, T., Lancet, D,. Louisot, P., Magdalou, J., Chowdhury, J. R., Ritter, J. K., Schachter, H., Tephly, T. R., Tipton, K. F., & Debert, D. W. (1997). The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics, 7(4), 255-269. https://doi.org/10.1097/00008571-199708000-00001
  43. Meech, R., & Mackenzie, P. I. (1997). Structure and function of uridine diphosphate glucuronosyltransferases. Clinical and Experimental Pharmacology and Physiology, 24(12), 907-915. https://doi.org/10.1111/j.1440-1681.1997.tb02718.x
  44. Merzendorfer, H., & Zimoch, L. (2003). Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. Journal of Experimental Biology, 206(24), 4393-4412. https://doi.org/10.1242/jeb.00709
  45. Michaud, M. R., & Denlinger, D. L. (2004). Molecular modalities of insect cold survival: current understanding and future trends. International Congress Series, 1275, 32-46. https://doi.org/10.1016/j.ics.2004.08.059
  46. Mizokami, H., & Yoshitama, K. (2009). Sequestration and metabolism of host-plant flavonoids by the Pale Grass Blue, Pseudozizeeria maha (Lepidoptera: Lycaenidae). Entomological Science, 12(2), 171-176. https://doi.org/10.1111/j.1479-8298.2009.00322.x
  47. Morton, R. A. (1992). Evolution of Drosophila insecticide resistance, Genome, 36(1), 1-7. https://doi.org/10.1139/g93-001
  48. Neven, L. G. (2000). Physiological responses of insects to heat. Postharvest Biology and Technology, 21(1), 103-111. https://doi.org/10.1016/S0925-5214(00)00169-1
  49. Oppenoorth, F. J. (1984). Biochemistry of insecticide resistance. Pesticide Biochemistry and Physiology, 22(2), 187-193. https://doi.org/10.1016/0048-3575(84)90088-9
  50. Ortelli, F., Rossiter, L. C., Vontas, J., Ranson, H., & Hemingway, J. (2003). Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochemical Journal, 373(3), 957-963. https://doi.org/10.1042/bj20030169
  51. Palter, K.B., Watanabe, M., Stinson, L., Mahowald, A.P., & Craig, E.A. (1986), Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Molecular Cell Biology, 6, 1187-1203. https://doi.org/10.1128/MCB.6.4.1187
  52. Park, Y. J., & Kim, Y. G (2013). RNA interference of glycerol biosynthesis suppresses rapid cold hardening of the beet armyworm, Spodoptera exigua . Journal of Experimental Biology, 4196-4203.
  53. Park, Y. J., & Kim, Y. G. (2014). A specific glycerol kinase induces rapid cold hardening of the diamondback moth, Plutella xylostella . Journal of Insect Physiology, 67, 56-63. https://doi.org/10.1016/j.jinsphys.2014.06.010
  54. Petersen, R. A., Niamsup, H., Berenbaum, M. R., & Schuler, M. A. (2003). Transcriptional response elements in the promoter of CYP6B1, an insect P450 gene regulated by plant chemicals. Biochimica et Biophysica Acta (BBA)-General Subjects, 1619(3), 269-282. https://doi.org/10.1016/S0304-4165(02)00486-5
  55. Rausell, C., Llorca, J., & Dolores Real, M. (1997). Separation by FPLC chromatofocusing of UDP-glucosyltransferases from three developmental stages of Drosophila melanogaster . Archives of Insect Biochemistry and Physiology, 34(3), 347-358. https://doi.org/10.1002/(SICI)1520-6327(1997)34:3<347::AID-ARCH8>3.0.CO;2-R
  56. Real, M. D., Ferre, J., & Chapa, F. J. (1991). UDP-glucosyltransferase activity toward exogenous substrates in Drosophila melanogaster. Analytic Biochemistry, 194(2), 349-352. https://doi.org/10.1016/0003-2697(91)90239-P
  57. Sable, M. G., & Rana, D. K. (2016). Impact of global warming on insect behavior - A review. Agricultural Reviews, 37(1), 81-84.
  58. Scott, J.G. (1999). Cytochrome P450 and insecticide resistance. Insect Biochemistry and Molecular Biology, 29(9), 757-777. https://doi.org/10.1016/S0965-1748(99)00038-7
  59. Sformo, T., Walters, K., Jeannet, K., Wowk, B., Fahy, G. M., Barnes, B. M., & Duman, J. G. (2010). Deep supercooling, vitrification and limited survival to-100 C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. Journal of Experimental Biology, 213(3), 502-509. https://doi.org/10.1242/jeb.035758
  60. Sinclair, B.J., Addo-Bediako, A., & Chown, S.L. (2003). Climatic variability and the evolution of insect freeze tolerance. Biological Reviews, 78(2), 181-195. https://doi.org/10.1017/S1464793102006024
  61. Sorensen, J. G., Nielsen, M. M., Kruhoffer, M., Justesen, J., & Loeschcke, V. (2005). Full genome gene expression analysis of the heat stress response in Drosophila melanogaster . Cell Stress & Chaperones, 10(4), 312-328. https://doi.org/10.1379/CSC-128R1.1
  62. Stetina, T., Kostal, V., & Korbelova, J. (2015). The role of inducible Hsp70, and other heat shock proteins, in adaptive complex of cold tolerance of the fruit fly (Drosophila melanogaster). PLoS One, 10(6), e0128976. https://doi.org/10.1371/journal.pone.0128976
  63. Talekar, N. S., & Shelton, A. M. (1993). Biology, ecology, and management of the diamondback moth. Annual Review of Entomology, 38(1), 275-301. https://doi.org/10.1146/annurev.en.38.010193.001423
  64. Thompson, S. N. (2003). Trehalose- the insect 'blood' sugar. Advances in Insect Physiology, 31, 205-285. https://doi.org/10.1016/S0065-2806(03)31004-5
  65. Toxopeus, J., & Sinclair, B. J. (2018). Mechanisms underlying insect freeze tolerance. Biological Reviews, 93(4), 1891-1914. https://doi.org/10.1111/brv.12425
  66. Wang, Q., Hasan, G., Pikielny, C.W. (1999). Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster , the antennae. The Journal of Biological Chemistry, 274, 10309-10315. https://doi.org/10.1074/jbc.274.15.10309
  67. Watson, G. S., Watson, J. A., & Cribb, B. W. (2017). Diversity of cuticular micro- and nanostructures on insects: properties, functions, and potential applications. Annual Review of Entomology, 62, 185-205. https://doi.org/10.1146/annurev-ento-031616-035020
  68. Wei, S. H., Clark, A. G., & Syvanen, M. (2001). Identification and cloning of a key insecticide-metabolizing glutathione S transferase (MdGST-6A) from a hyper insecticide-resistant strain of the housefly Musca domestica. Insect Biochemistry and Molecular Biology, 31(12), 1145-1153. https://doi.org/10.1016/S0965-1748(01)00059-5
  69. Weisenburger, D. D. (1993). Human health effects of agrichemical use. Human Pathology, 24(6), 571-576. https://doi.org/10.1016/0046-8177(93)90234-8
  70. Wen, Z., Pan L., Berenbaum, M. R., & Schuler, M. A. (2003). Metabolism of linear and angular furanocoumarins by Papilio polyxenes CYP6B1 co-expressed with NADPH cytochrome P450 reductase. Insect Biochemistry and Molecular Biology, 33(9), 937-947. https://doi.org/10.1016/S0965-1748(03)00100-0
  71. Wilson, T. G. (2001). Resistance of Drosophila to Toxins. Annual Review of Entomology, 46(1), 545-571. https://doi.org/10.1146/annurev.ento.46.1.545
  72. Xiong, K. C., Wang, J., Li, J. H., Deng, Y. Q., Pu, P., Fan, H., & Liu, Y. H. (2016). RNA interference of a trehalose-6-phosphate synthase gene reveals its roles during larval-pupal metamorphosis in Bactrocera minax (Diptera: Tephritidae). Journal of Insect Physiology, 91-92, 84-92. https://doi.org/10.1016/j.jinsphys.2016.07.003
  73. Yamamura, K., & Kiritani, K. (1998). A simple method to estimate the potential increase in the number of generations under global warming in temperate zones. Applied Entomology and Zoology, 33(2), 289-298. https://doi.org/10.1303/aez.33.289
  74. 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
  75. Zuo, D., Subjeck, J., & Wang, X. Y. (2016). Unfolding the role of large heat shock proteins: New insights and therapeutic implications. Frontiers in Immunology, 7, 75.