Korean Journal of Environmental Biology (환경생물)

Korean Society of Environmental Biology (한국환경생물학회)
권호 표지
DOI QR코드

DOI QR Code

Molecular characterization of juvenile hormone signaling pathway-related genes in the brackish water flea Diaphanosoma celebensis

기수산 물벼룩의 유충 호르몬(Juvenile hormone) 신호전달경로 관련 유전자의 특성 분석

  • Hayoung Cho (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Jewon Yoo (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Young-Mi Lee (Department of Biotechnology, College of Convergence Engineering, Sangmyung University)
  • 조하영 (상명대학교 융합공과대학 생명공학과) ;
  • 유제원 (상명대학교 융합공과대학 생명공학과) ;
  • 이영미 (상명대학교 융합공과대학 생명공학과)
  • Received : 2022.07.28
  • Accepted : 2022.08.29
  • Published : 2022.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

In crustaceans, molting is regulated by interactions between ecdysteroid and juvenile hormone (JH) signaling pathway-related genes. Unlike the ecdysteroid signaling pathway, little information on the role of JH signaling pathway-related genes in molting is available in zooplanktonic crustaceans. In this study, three genes (juvenile hormone acid O-methyltransferase (JHAMT), methoprene-tolerant (Met), and juvenile hormone epoxide hydrolase (JHEH)) which are involved in the synthesis, receptor-binding, and degradation of JH were identified using sequence and phylogenetic analysis in the brackish water flea, Diaphanosoma celebensis. Transcriptional changes in these genes during the molting cycle in D. celebensis were analyzed. Sequence and phylogenetic analysis revealed that these putative proteins may be functionally conserved along with those of insects and other crustaceans. In addition, the expression of the three genes was correlated with the molting cycle of D. celebensis, indicating that these genes may be involved in the synthesis and degradation of JH, resulting in normal molting. This study will provide information for a better understanding of the role of JH signaling pathway-related genes during the molting process in Cladocera.

갑각류에서 탈피는 ecdysteroid와 juvenile hormone (JH) 신호 경로에 관여하는 유전자의 상호작용에 의해 조절된다. Ecdysteroid와 달리, 탈피 과정에서 JH 신호 경로 유전자의 역할은 부유성 갑각류에서는 잘 알려져 있지 않다. 본 연구는 기수산 물벼룩(Diaphanosoma celebensis)의 JH 신호경로에서 JH 합성, 수용체, 분해 등에 관여하는 3종의 유전자(JHAMT, Met, JHEH)의 염기서열 분석과 계통 분석을 실시하였다. 또한 탈피 주기에서 이들 유전자의 mRNA 발현양상을 분석하였다. D. celebensis의 JH 관련 유전자는 잘 보존된 domain을 가지고 있었으며, 아미노산 서열 분석과 계통 분석 결과는 이들 단백질이 곤충 및 다른 갑각류의 해당 단백질과 기능적으로 유사한 특징을 나타낸다. 또한 탈피 주기에 따른 유충 호르몬( JH) 신호전달경로 관련 유전자의 발현변화 결과를 통해 이들 유전자가 JH의 합성 및 분해에 관여함으로써 D. celebensis에서 성공적인 탈피에 기여할 것임을 제시하였다. 본 연구는 지각류에서 탈피 주기에서 JH 경로 유전자의 역할을 이해하는 데 도움이 될 것이다.

Keywords

Acknowledgement

본 연구는 한국연구재단 과제(NRF-2020R1F1A1069736) 연구비 지원을 받아 수행하였다.

References

  1. Arand M, A Cronin, M Adamska and F Oesch. 2005. Epoxide hydrolases: structure, function, mechanism, and assay. Methods Enzymol. 400:569-588. https://doi.org/10.1016/S0076-6879(05)00032-7
  2. Chang ES, MJ Bruce and SL Tamone. 1993. Regulation of crustacean molting: A multi-hormonal system. Am. Zool. 33:324-329. https://doi.org/10.1093/icb/33.3.324
  3. Chen X, Q Gao, H Cheng, F Peng, C Wang and B Xu. 2021. Molecular cloning and expression pattern of the juvenile hormone epoxide hydrolase gene from the giant freshwater prawn Macrobrachium rosenbergii during larval development and the moult cycle. Aquac. Res. 52:3890-3899. https://doi.org/10.1111/are.15233
  4. Daimon T and T Shinoda. 2013. Function, diversity, and application of insect juvenile hormone epoxidases (CYP15). Biotechnol. Appl. Biochem. 60:82-91. https://doi.org/10.1002/bab.1058
  5. Defelipe LA, E Dolghih, AE Roitberg, M Nouzova, JG Mayoral, FG Noriega and AG Turjanski. 2011. Juvenile hormone synthesis: "esterify then epoxidize" or "epoxidize then esterify"? Insights from the structural characterization of juvenile hormone acid methyltransferase. Insect Biochem. Mol. Biol. 41:228-235. https://doi.org/10.1016/j.ibmb.2010.12.008
  6. Dubrovsky EB. 2005. Hormonal cross talk in insect development. Trends Endocrinol. Metab. 16:6-11. https://doi.org/10.1016/j.tem.2004.11.003
  7. Gilbert LI, NA Granger and RM Roe. 2000. The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem. Mol. Biol. 30:617-644. https://doi.org/10.1016/s0965-1748(00)00034-5
  8. Giraudo M, M Douville, G Cottin and M Houde. 2017. Transcriptomic, cellular and life-history responses of Daphnia magna chronically exposed to benzotriazoles: Endocrine-disrupting potential and molting effects. PLoS One 12:e0171763. https://doi.org/10.1371/journal.pone.0171763
  9. Guo E, Q He, S Liu, L Tian, Z Sheng, Q Peng, J Guan, M Shi, K Li and LI Gilbert. 2012. MET is required for the maximal action of 20-hydroxyecdysone during Bombyx metamorphosis. PLoS One 7:e53256. https://doi.org/10.1371/journal.pone.0053256
  10. Guo P, Y Zhang, L Zhang, H Xu, H Zhang, Z Wang, Y Jiang, D Molloy, P Zhao and Q Zia. 2021. Structural basis for juvenile hormone biosynthesis by the juvenile hormone acid methyltransferase. J. Biol. Chem. 297:101234. https://doi.org/10.1016/j.jbc.2021.101234
  11. Hui JHL, A Hayward, WG Bendena, T Takahashi and SS Tobe. 2010. Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects. Peptides 31:451-455. https://doi.org/10.1016/j.peptides.2009.10.003
  12. Hyde CJ, A Elizur and T Ventura. 2019. The crustacean ecdysone cassette: A gatekeeper for molt and metamorphosis. J. Steroid Biochem. Mol. Biol. 185:172-183. https://doi.org/10.1016/j.jsbmb.2018.08.012
  13. In S, H Cho and YM Lee. 2021. Identification of ecdysteroid pathway-related genes and their transcriptional modulation in the brackish water flea Diaphanosoma celebensis exposed to bisphenol analogs. Toxicol. Environ. Health Sci. 13:261-268. https://doi.org/10.1007/s13530-021-00103-8
  14. In S, H Cho, KW Lee, EJ Won and YM Lee. 2020. Cloning and molecular characterization of estrogen-related receptor(ERR) and vitellogenin genes in the brackish water flea Diaphanosoma celebensis exposed to bisphenol A and its structural analogues. Mar. Pollut. Bull. 154:111063. https://doi.org/10.1016/j.marpolbul.2020.111063
  15. In S, HW Yoon, JW Yoo, H Cho, RO Kim and YM Lee. 2019. Acute toxicity of bisphenol A and its structural analogues and transcriptional modulation of the ecdysone-mediated pathway in the brackish water flea Diaphanosoma celebensis. Ecotox. Environ. Safe. 179:310-317. https://doi.org/10.1016/j.ecoenv.2019.04.065
  16. Jiang M, S Lu and Y Zhang. 2017. Characterization of juvenile hormone related genes regulating cantharidin biosynthesis in Epicauta chinensis. Sci. Rep. 7:2308-2311. https://doi.org/10.1038/s41598-017-02393-w
  17. Jindra M, SR Palli and LM Riddiford. 2013. The juvenile hormone signaling pathway in insect development. Annu. Rev. Entomol. 58:181-204. https://doi.org/10.1146/annurev-ento120811-153700
  18. Kato Y, K Kobayashi, S Oda, N Tatarazako, H Watanabe and T Iguchi. 2007. Cloning and characterization of the ecdysone receptor and ultraspiracle protein from the water flea Daphnia magna. J. Endocrinol. 193:183-194. https://doi.org/10.1677/JOE-06-0228
  19. Kim BM, S Kang, RO Kim, JH Jung, KW Lee, JS Rhee and YM Lee. 2018. De novo transcriptome assembly of brackish water flea Diaphanosoma celebensis based on short-term cadmium and benzo[a]pyrene exposure experiments. Hereditas 155:36. https://doi.org/10.1186/s41065-018-0075-3
  20. Kim DH, BS Choi, HM Kang, JC Park, MS Kim, A Hagiwara and JS Lee. 2021. The genome of the marine water flea Diaphanosoma celebensis: Identification of phase I, II, and III detoxification genes and potential applications in marine molecular ecotoxicology. Comp. Biochem. Physiol. D-Genomics Proteomics 32:100787. https://doi.org/10.1016/j.cbd.2020.100787
  21. Lee KJ, RD Watson and RD Roer. 1998. Moult-inhibiting hormone mRNA levels and ecdysteroid titer during a moult cycle of the blue crab, Callinectes sapidus. Biochem. Biophys. Res. Commun. 249:624-627. https://doi.org/10.1006/bbrc.1998.9215
  22. Lee YM, H Cho, RO Kim, S In, SJ Kim and EJ Won. 2021. Validation of reference genes for quantitative real-time PCR in chemical exposed and at different age's brackish water flea Diaphanosoma celebensis. Sci. Rep. 11:23691. https://doi.org/10.1038/s41598-021-03098-x
  23. Li G, Q Sun, X Liu, J Zhang, W Dou, J Niu and J Wang. 2019. Expression dynamics of key ecdysteroid and juvenile hormone biosynthesis genes imply a coordinated regulation pattern in the molting process of a spider mite, Tetranychus urticae. Exp. Appl. Acarol. 78:361-372. https://doi.org/10.1007/s10493-019-00396-y
  24. Li M, EA Mead and JS Zhu. 2011. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc. Natl. Acad. Sci. U.S.A. 108:638-643. https://doi.org/10.1073/pnas.1013914108
  25. Li W, ZY Huang, F Liu, Z Li, L Yan, S Zhang, S Chen, B Zhong and S Su. 2013. Molecular cloning and characterization of juvenile hormone acid methyltransferase in the honey bee, Apis mellifera, and its differential expression during caste differentiation. PloS One 8:e68544. https://doi.org/10.1371/journal.pone.0068544
  26. Li YX, D Wang, WL Zhao, JY Zhang, XL Kang, YL Li and XF Zhao. 2021. Juvenile hormone induces methoprene-tolerant 1 phosphorylation to increase interaction with Taiman in Helicoverpa armigera. Insect Biochem. Mol. Biol. 130:103519. https://doi.org/10.1016/j.ibmb.2021.103519
  27. Mackert A, K Hartfelder, MMG Bitondi and ZLP Simoes. 2010. The juvenile hormone (JH) epoxide hydrolase gene in the honey bee (Apis mellifera) genome encodes a protein which has negligible participation in JH degradation. J. Insect Physiol. 56:1139-1146. https://doi.org/10.1016/j.jinsphys.2010.03.007
  28. Marcial HS and A Hagiwara. 2007. Multigenerational effects of 17β-estradiol and nonylphenol on euryhaline cladoceran Diaphanosoma celebensis. Fish. Sci. 73:324-330. https://doi.org/10.1111/j.1444-2906.2007.01338.x
  29. Martin JL and FM McMillan. 2002. SAM (dependent) I AM: The S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12:783-793. https://doi.org/10.1016/S0959-440X(02)00391-3
  30. Minakuchi C, T Namiki, M Yoshiyama and T Shinoda. 2008. RNAimediated knockdown of juvenile hormone acid O-methyltransferase gene causes precocious metamorphosis in the red flour beetle Tribolium castaneum. FEBS J. 275:2919-2931. https://doi.org/10.1111/j.1742-4658.2008.06428.x
  31. Miura K, M Oda, S Makita and Y Chinzei. 2005. Characterization of the Drosophila Methoprene-tolerant gene product: Juvenile hormone binding and ligand dependent gene regulation. FEBS J. 272:1169-1178. https://doi.org/10.1111/j.1742-4658.2005.04552.x
  32. Miyakawa H, K Toyota, I Hirakawa, Y Ogino, S Miyagawa, S Oda, N Tatarazako, T Miura, JK Colbourne and T Iguchi. 2013. A mutation in the receptor Methoprene-tolerant alters juvenile hormone response in insects and crustaceans. Nat. Commun. 4:1856. https://doi.org/10.1038/ncomms2868
  33. Miyakawa H, T Sato, Y Song, KE Tollefsen and T Iguchi. 2018. Ecdysteroid and juvenile hormone biosynthesis, receptors and their signaling in the freshwater microcrustacean Daphnia. J. Steroid Biochem. Mol. Biol. 184:62-68. https://doi.org/10.1016/j.jsbmb.2017.12.006
  34. Nakagawa Y and VC Henrich. 2009. Arthropod nuclear receptors and their role in molting. FEBS J. 276: 6128-6157. https://doi.org/10.1111/j.1742-4658.2009.07347.x
  35. Niwa R, T Niimi, N Honda, M Yoshiyama, K Itoyama, H Kataoka and T Shinoda. 2008. Juvenile hormone acid O-methyltransferase in Drosophila melanogaster. Insect Biochem. Mol. Biol. 38:714-720. https://doi.org/10.1016/j.ibmb.2008.04.003
  36. Palli SR, TR Ladd, WL Tomkins, S Shu, SB Ramaswamy, Y Tanaka, B Arif and A Retnakaran. 2000. Choristoneura fumiferana entomopoxvirus prevents metamorphosis and modulates juvenile hormone and ecdysteroid titers. Insect Biochem. Mol. Biol. 30:869. https://doi.org/10.1016/S0965-1748(00)00060-6
  37. Riddiford LM, K Hiruma, X Zhou and CA Nelson. 2003 Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem. Mol. Biol. 33:1327-1338. https://doi.org/10.1016/j.ibmb.2003.06.001
  38. Rivera-Perez C, M Nouzova, I Lamboglia and FG Noriega. 2014. Metabolic analysis reveals changes in the mevalonate and juvenile hormone synthesis pathways linked to the mosquito reproductive physiology. Insect Biochem. Mol. Biol. 51:1-9. https://doi.org/10.1016/j.ibmb.2014.05.001
  39. Shinoda T and K Itoyama. 2003. Juvenile hormone acid methyltransferase: a key regulatory enzyme for insect metamorphosis Proc. Natl. Acad. Sci. U.S.A. 100:11986-11991. https://doi.org/10.1073/pnas.2134232100
  40. Sin YW, NJ Kenny, Z Qu, KW Chan, KWS Chan, SPS Cheong, RWT Leung, TF Chan, WG Bendena, KH Chu, SS Tobe and JHL Hui. 2015. Identification of putative ecdysteroid and juvenile hormone pathway genes in the shrimp Neocaridina denticulate. Gen. Comp. Endocrinol. 214:167-176. https://doi.org/10.1016/j.ygcen.2014.07.018
  41. Wen D, C Rivera-Perez, M Abdou, Q Jia, Q He, X Liu, O Zyann, J Xu, WG Bendena, SS Tobe, FG Noriega, SR Palli, J Wang and S Li. 2015. Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet. 11:e1005038. https://doi.org/10.1371/journal.pgen.1006559
  42. Wen R, B Wang, B Wang and L Ma. 2018. Characterization and expression profiles of juvenile hormone epoxide hydrolase from Lymantria dispar (Lepidoptera: Lymantridae) and RNA interference by ingestion. J. Insect Sci. 18:13. https://doi.org/10.1093/jisesa/iey002
  43. Yamada T, C Morisseau, JE Maxwell, MA Argiriadi, DW Christianson and BD Hammock. 2000. Biochemical evidence for the involvement of tyrosine in epoxide activation during the catalytic cycle of epoxide hydrolase. J. Biol. Chem. 275:23082-23088. https://doi.org/10.1074/jbc.M001464200
  44. Zhang QR, WH Xu, FS Chen and S Li. 2005. Molecular and biochemical characterization of juvenile hormone epoxide hydrolase from the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 35:153-164. https://doi.org/10.1016/j.ibmb.2004.10.010
  45. Zhou K, N Jia, C Ju, YL Jiang, JP Yang, Y Chen, S Li, WF Li and CZ Zhou. 2014. Crystal structure of juvenile hormone epoxide hydrolase from the silkworm Bombyx mori. Proteins 82:3224-3229. https://doi.org/10.1002/prot.24676
  46. Zhu J, JM Busche and X Zhang. 2010. Identification of juvenile hormone target genes in the adult female mosquitoes. Insect Biochem. Mol. Biol. 40:23-29. https://doi.org/10.1016/j.ibmb.2009.12.004
  47. Zitnan D, YJ Kim, I Zitnanova, L Roller and ME Adams. 2007. Complex steroid-peptide-receptor cascade controls insect ecdysis. Gen. Comp. Endocrinol. 153:88-96. https://doi.org/10.1016/j.ygcen.2007.04.002