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The nuclear receptor gene E75 plays a key role in regulating the molting process of the spider mite, Tetranychus urticae

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Abstract

The nuclear receptor gene Ecdysone-induced protein 75 (E75), as the component of ecdysone response genes in the ecdysone signaling pathway, has important regulatory function for insect molting. However, the regulatory function of E75 during the molting process of spider mites is not yet clear. In this study, the expression pattern of E75 in the molting process of the spider mite Tetranychus urticae was analyzed. The results showed that there was a peak at 8 h post-molting, followed by a decline 8 h after entering each respective quiescent stage across various developmental stages. During the deutonymph stage, the expression dynamics of E75, observed at 4-h intervals, indicated that the transcript levels of TuE75 peaked at 24 h, coinciding with the onset of molting in the mites. To investigate the function of TuE75 during the molting process, silencing TuE75 through dsRNA injection into deutonymph mites at the age of 8 h yielded a notable outcome: 78% of the deutonymph mites were unable to progress to the adult stage. Among these phenotypic mites, 37% were incapable of transitioning into the quiescent state and eventually succumbed after a certain period. An additional 41% of the mites successfully entered the quiescent state but encountered difficulties in shedding the old epidermis, leading to eventual mortality. In summary, these results suggested that TuE75 plays a key role in the molting process of T. urticae.

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References

  • Bialecki M, Shilton A, Fichtenberg C, Segraves WA, Thummel CS (2002) Loss of the ecdysteroid-inducible E75A orphan nuclear receptor uncouples molting from metamorphosis in Drosophila. Dev Cell 3:209–220

    Article  CAS  PubMed  Google Scholar 

  • Cheong SP, Huang J, Bendena WG, Tobe SS, Hui JH (2015) Evolution of ecdysis and metamorphosis in arthropods: the rise of regulation of juvenile hormone. Integr Comp Biol 55:878–890

    Article  PubMed  Google Scholar 

  • Christiaens O, Iga M, Velarde RA, Rouge P, Smagghe G (2010) Halloween genes and nuclear receptors in ecdysteroid biosynthesis and signalling in the pea aphid. Insect Mol Biol 19(Suppl 2):187–200

    Article  CAS  PubMed  Google Scholar 

  • Dermau W, Jonckheere W, Riga M, Livadaras I, Vontas J, Van Leeuwen T (2020) Targeted mutagenesis using crispr-cas9 in the chelicerate herbivore tetranychus urticae. Insect Biochem Mol Biol 120:103347

    Article  Google Scholar 

  • Fahrbach SE, Smagghe G, Velarde RA (2012) Insect nuclear receptors. Ann Rev Entomol 57:83–106

    Article  CAS  Google Scholar 

  • Giguere V (1999) Orphan nuclear receptors: from gene to function. Endocr Rev 20:689–725

    CAS  PubMed  Google Scholar 

  • Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Thi Ngoc PC, Ortego F, Hernández-Crespo P, Diaz I, Martinez M, Navajas M, Sucena É, Magalhães S, Nagy L, Pace RM, Djuranović S, Smagghe G, Iga M, Christiaens O, Veenstra JA, Ewer J, Villalobos RM, Hutter JL, Hudson SD, Velez M, Yi SV, Zeng J, Pires-daSilva A, Roch F, Cazaux M, Navarro M, Zhurov V, Acevedo G, Bjelica A, Fawcett JA, Bonnet E, Martens C, Baele G, Wissler L, Sanchez-Rodriguez A, Tirry L, Blais C, Demeestere K, Henz SR, Gregory TR, Mathieu J, Verdon L, Farinelli L, Schmutz J, Lindquist E, Feyereisen R, Van de Peer Y (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nat 479: 487–492

  • Gronemeyer H, Gustafsson JA, Laudet V (2004) Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov 3:950–964

    Article  CAS  PubMed  Google Scholar 

  • Guo WC, Liu XP, Fu KY, Shi JF, Lu FG, Li GQ (2016) Nuclear receptor ecdysone-induced protein 75 is required for larval-pupal metamorphosis in the Colorado potato beetle Leptinotarsa decemlineata (say). Insect Mol Biol 25:44–57

    Article  CAS  PubMed  Google Scholar 

  • He HJ, Wang Q, Zheng WW, Wang JX, Song QS, Zhao XF (2010) Function of nuclear transport factor 2 and ran in the 20E signal transduction pathway in the cotton bollworm, Helicoverpa armigera. BMC Cell Biol 11:1–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiruma K, Riddiford LM (2004) Differential control of MHR3 promoter activity by isoforms of the ecdysone receptor and inhibitory effects of E75A and MHR3. Dev Biol 272:510–521

    Article  CAS  PubMed  Google Scholar 

  • Ji M, Vandenhole M, De Beer B, De Rouck S, Villacis-Perez E, Feyereisen R, Clark RM, Van Leeuwen T (2023) A nuclear receptor HR96-related gene underlies large trans-driven differences in detoxification gene expression in a generalist herbivore. Nat Commun 14:4990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia S, Wan PJ, Li GQ (2015) Molecular cloning and characterization of the putative Halloween gene phantom from the small brown planthopper Laodelphax striatellus. Insect Sci 22:707–718

    Article  CAS  PubMed  Google Scholar 

  • Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204

    Article  CAS  PubMed  Google Scholar 

  • King-Jones K, Thummel CS (2005) Nuclear receptors–a perspective from Drosophila. Nat Rev Genet 6:311–323

    Article  CAS  PubMed  Google Scholar 

  • Lenaerts C, Van Wielendaele P, Peeters P, Vanden Broeck J, Marchal E (2016) Ecdysteroid signalling components in metamorphosis and development of the desert Locust, Schistocerca Gregaria. Insect Biochem Mol Biol 75:10–23

    Article  CAS  PubMed  Google Scholar 

  • Li K, Tian L, Guo Z, Guo S, Zhang J, Gu SH, Palli SR, Cao Y, Li S (2016) 20-hydroxyecdysone (20E) primary response gene E75 isoforms mediate steroidogenesis autoregulation and regulate developmental timing in Bombyx. J Biol Chem 291:18163–18175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li G, Niu JZ, Zotti M, Sun QZ, Zhu L, Zhang J, Liao CY, Dou W, Wei DD, Wang JJ, Smagghe G (2017) Characterization and expression patterns of key ecdysteroid biosynthesis and signaling genes in a spider mite (Panonychus Citri). Insect Biochem Mol Biol 87:136–146

    Article  CAS  PubMed  Google Scholar 

  • Li G, Sun QZ, Liu XY, Zhang J, Dou W, Niu JZ, Wang JJ (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

    Article  CAS  PubMed  Google Scholar 

  • Liu XP, Fu KY, Lu FG, Meng QW, Guo WC, Li GQ (2014) Involvement of FTZ-F1 in the regulation of pupation in Leptinotarsa decemlineata (say). Insect Biochem Mol Biol 55:51–60

    Article  CAS  PubMed  Google Scholar 

  • Mane-Padros D, Cruz J, Vilaplana L, Pascual N, Belles X, Martin D (2008) The nuclear hormone receptor BgE75 links molting and developmental progression in the direct-developing insect Blattella germanica. Dev Biol 315:147–160

    Article  CAS  PubMed  Google Scholar 

  • Okamoto N, Viswanatha R, Bittar R, Li Z, Haga-Yamanaka S, Perrimon N, Yamanaka N (2018) A membrane transporter is required for steroid hormone uptake in Drosophila. Dev Cell 47:294–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palanker L, Necakov AS, Sampson HM, Ni R, Hu C, Thummel CS, Krause HM (2006) Dynamic regulation of Drosophila nuclear receptor activity in vivo. Development 133:3549–3562

    Article  CAS  PubMed  Google Scholar 

  • Parvy JP, Wang P, Garrido D, Maria A, Blais C, Poidevin M, Montagne J (2014) Forward and feedback regulation of cyclic steroid production in Drosophila melanogaster. Development 141:3955–3965

    Article  CAS  PubMed  Google Scholar 

  • Reinking J, Lam MM, Pardee K, Sampson HM, Liu S, Yang P, Williams S, White W, Lajoie G, Edwards A, Krause HM (2005) The Drosophila nuclear receptor E75 contains heme and is gas responsive. Cell 122:195–207

    Article  CAS  PubMed  Google Scholar 

  • Segraves WA, Hogness DS (1990) The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev 4:204–219

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite tetranychus urticae and other important acari: a review. Insect Biochem Mol Biol 40:563–572

    Article  PubMed  Google Scholar 

  • Wei P, Wang C, Li C, Chen M, Sun J, Van Leeuwen T, He L (2021) Comparing the efficiency of RNAi after feeding and injection of dsRNA in spider mites. Pestic Biochem Physiol 179:104966

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka N, Rewitz KF, O’Connor MB (2013) Ecdysone control of developmental transitions: lessons from Drosophila research. Annu Rev Entomol 58:497–516

    Article  CAS  PubMed  Google Scholar 

  • Yang ZM, Yu N, Wang SJ, Korai SK, Liu ZW (2021) Characterization of ecdysteroid biosynthesis in the pond wolf spider, Pardosa pseudoannulata. Insect Mol Biol 30:71–80

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Yan Y, Wei G, Merchant A, Gu Y, Zhou X, Zhu X, Zhang Y, Li X (2023) Functional characterization of the nuclear receptor gene SaE75 in the grain aphid, Sitobion avenae. Insects 14:383

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was supported by the Guizhou Provincial Science and Technology Foundation (QianKeHeJiChu ZK [2022]-YiBan065), the Special Natural Science Foundation of Guizhou University (Gui Da Te Gang He Zi [2022]13) and National Natrual Science Foundation of China (3175002).

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Z. L., G. L., and D.C. J. conceived the study and participated in its design. L.W. performed the population of spider mites. Z.L. performed all of experiments. Z.L., T.C. Y., and G. L. analyzed the data. Z.L., D.C. J., and G. L. prepared the paper. All authors have read and agreed to the published version of manuscript.

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Correspondence to Gang Li or Dao-Chao Jin.

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Li, Z., Wang, L., Yi, T. et al. The nuclear receptor gene E75 plays a key role in regulating the molting process of the spider mite, Tetranychus urticae. Exp Appl Acarol 92, 1–11 (2024). https://doi.org/10.1007/s10493-023-00868-2

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