Skip to main content
Log in

The effect of manipulating ecdysteroid signaling on embryonic eye development in the locust Schistocerca americana

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Adult body plan differentiation in holometabolous insects depends on global induction and control by ecdysteroid hormones during the final phase of postembryogenesis. Studies in Drosophila melanogaster and Manduca sexta have shown that this pertains also to the development of the compound eye retina. It is unclear whether the hormonal control of postembryonic eye development in holometabolous insects represents evolutionary novelty or heritage from hemimetabolous insects, which develop compound eyes during embryogenesis. We therefore investigated the effect of manipulating ecdysteroid signaling in cultured embryonic eye primordia of the American desert locust Schistocerca americana, in which ecdysteroid level changes are known to induce three rounds of embryonic molt. Although at a considerably reduced rate compared to in vivo development, early differentiation and terminal maturation of the embryonic retina was observed in culture even if challenged with the ecdysteroid antagonist cucurbitacin B. Supplementing cultures with 20-hydroxyecdysone (20E) accelerated differentiation and maturation, and enhanced cell proliferation. Considering these results, and the relation between retina differentiation and ecdysteroid level changes during locust embryogenesis, we conclude that ecdysteroids are not an essential but possibly a modulatory component of embryonic retina development in S. americana. We furthermore found evidence that 20E initiated precocious epithelial morphogenesis of the posterior retinal margin indicating a more general role of ecdysteroids in insect embryogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–J
Fig. 2A–J
Fig. 3
Fig. 4A–D
Fig. 5A–F
Fig. 6A–I
Fig. 7

Similar content being viewed by others

References

  • Bender M, Imam FB, Talbot W, Ganetzky B, Hogness D (1997) Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 91:777–788

    CAS  PubMed  Google Scholar 

  • Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47–74

    CAS  PubMed  Google Scholar 

  • Brennan CA, Ashburner M, Moses K (1998) Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development 125:2653–2664

    CAS  PubMed  Google Scholar 

  • Brennan CA, Li TR, Bender M, Hsiung F, Moses K (2001) Broad-complex, but not ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development 128:1–11

    CAS  PubMed  Google Scholar 

  • Champlin DT, Truman JW (1998) Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta. Development 125:2009–2018

    CAS  PubMed  Google Scholar 

  • Chavez M, Marques G, Delpecque J, Kobayashi K, Holingsworth M, et al (2000) The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 127:4115–4126

    CAS  PubMed  Google Scholar 

  • Cherbas L, Lee K, Cherbas P (1991) Identification of ecdysone response elements by analysis of the Drosophila Elp28/29 gene. Genes Dev 5:120–131

    CAS  PubMed  Google Scholar 

  • Cherbas L, Hu X, Zhimulev I, Belyaeva E, Cherbas P (2003) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130:271–284

    Article  CAS  PubMed  Google Scholar 

  • Denlinger DL (1985) Hormonal control of diapause. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 353–412

  • Dinan L, Whiting P, Girault JP, Lafont R, Dhadialla TS, et al (1997) Cucurbitacins are insect steroid hormone antagonists acting at the ecdysteroid receptor. Biochem J 327:643–650

    CAS  PubMed  Google Scholar 

  • Dinan LN, Rees HH (1981) The identification and titres of conjugated and free ecdysteroids in developing ovaries and newly-laid eggs of Schistocerca gregaria. J Insect Physiol 27:51–58

    Article  CAS  Google Scholar 

  • Gande AR, Morgan ED (1979) Ecdysteroids in the developing eggs of the desert locust, Schistocerca gregaria. J Insect Physiol 25:289–293

    Article  CAS  Google Scholar 

  • Ghbeish N, McKeown M (2002) Analyzing the repressive function of ultraspiracle, the Drosophila RXR, in Drosophila eye development. Mech Dev 111:89–98

    Article  CAS  PubMed  Google Scholar 

  • Giesen K, Lammel U, Langehans D, Krukkert K, Bunse I, et al (2003) Regulation of glial cell number and differentiation by ecdysone and Fos signaling. Mech Dev 120:401–413

    Article  CAS  PubMed  Google Scholar 

  • Hayward D, Bastiani MJ, Trueman J, Truman J, Riddiford LM, et al (1999) The sequence of Locusta RXR, homologous to Drosophila Ultraspiracle, and its evolutionary implications. Dev Genes Evol 209:564–571

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann JA, Lagueux M (1985) Endocrine aspects of embryonic development in insects. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 435–460

  • Kuitert LC, Connin RV (1952) Biology of the American grasshopper in the southeastern United States. Fla Entomol 35:22–33

    Google Scholar 

  • Lagueux M, Hetru C, Coltzene F, Kappler C, Hoffmann JA (1979) Ecdysone titre and metabolism in relation to cuticulogenesis in embryos of Locusta migratoria. J Insect Physiol 25:709–723

    Article  CAS  Google Scholar 

  • Li C, Meinertzhagen IA (1995) Conditions for the primary culture of eye imaginal discs from Drosophila melanogaster. J Neurobiol 28:363–380

    CAS  PubMed  Google Scholar 

  • Li C, Meinertzhagen IA (1997) The effects of 20-hydroxyecdysone on the differentiation in vitro of cells from the eye imaginal disc from Drosophila melanogaster. Invert Neurosci 3:57–69

    CAS  PubMed  Google Scholar 

  • Longley RL Jr, Ready DF (1995) Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171:415–433

    CAS  PubMed  Google Scholar 

  • Makka T, Seino A, Tomita S, Fujiwara H, Sonobe H (2002) A possible role of 20-hydroxyecdysone in embryonic development of the silkworm Bombyx mori. Arch Insect Biochem 51:111–120

    Article  CAS  Google Scholar 

  • Morgan ED, Poole CF (1976) The pattern of ecdysone levels during development in the desert locust, Schistocerca gregaria. J Insect Physiol 22:885–889

    Article  CAS  Google Scholar 

  • Mueller NS (1963) An experimental analysis of molting in embryos of Melanoplus differentialis. Dev Biol 8:222–240

    Google Scholar 

  • Myers PZ, Bastiani MJ (1993) Growth cone dynamics during the migration of an identified commissural growth cone. J Neurosci 13:127–143

    CAS  PubMed  Google Scholar 

  • Nijhout HF (1994) Insect hormones. Princeton University Press, Princeton, N.J.

  • Oro AE, McKeown M, Evans RM (1992) The Drosophila retinoid X receptor homolog ultraspiracle functions in both female and eye morphogenesis. Development 119:462

    Google Scholar 

  • Orsulic S, Peifer M (1994) A method to stain nuclei of Drosophila for confocal microscopy. Biotechniques 16:441–447

    CAS  PubMed  Google Scholar 

  • Riddiford LM (1993) Hormones and Drosophila development. In: Lawrence P, Martinez AM (eds) The development of Drosophila melanogaster. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, N.Y., pp 899–939

  • Riddiford LM, Cherbas P, Truman JW (2001) Ecdysone receptors and their biological actions. Vitam Horm NY 60:1–67

    CAS  Google Scholar 

  • Saleh DS, Zhang J, Wyatt G, Walker V (1998) Cloning and characterization of an ecdysone receptor cDNA from Locusta migratoria. Mol Cell Endocrinol 143:91–99

    Google Scholar 

  • Sall C, Tsourpas G, Kappler C, Lagueux M, Zachary D, et al (1983) Fate of maternal conjugated ecdysteroids during embryonic development in Locusta migratoria. J Insect Physiol 29:491–507

    Article  CAS  Google Scholar 

  • Sbrenna G, Chicca M, Bonora M, Sbrenna Micciarelli A (1989) The response of embryonic epidermal tissue of Schistocerca gregaria (Orhoptera, Acrididae) to 20-OH-ecdysone in vitro. Acta Embryol Exp Morphol 10:221–226

    Google Scholar 

  • Scalia S, Morgan ED (1982) A re-investigation of the ecdysteroids during embryogenesis in the desert locust, Schistocerca gregaria. J Insect Physiol 28:647–654

    Article  CAS  Google Scholar 

  • Scalia S, Sbrenna-Micciarelli A, Sbrenna G, Morgan ED (1987) Ecdysteroid titres and location in developing eggs of Schistocerca gregaria. Insect Biochem 17:227–236

    Article  CAS  Google Scholar 

  • Schubiger M, Truman JW (2000) The RXR-ortholog USP suppresses early metamorphic processes in the absence of ecdysteroids. Development 127:1151–1159

    CAS  PubMed  Google Scholar 

  • Slama K (2000) Correlation between metabolic depression and ecdysteroid peak during embryogenesis of the desert locust, Schistocerca gregaria. Eur J Entomol 97:141–148

    CAS  Google Scholar 

  • Tawfik AI, Tanaka Y, Tanaka S (2002) Possible involvement of ecdysteroids in embryonic diapause of Locusta migratoria. J Insect Physiol 48:743–749

    Article  CAS  PubMed  Google Scholar 

  • Thummel CS (1996) Flies on steroids—Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12:306–310

    Article  CAS  PubMed  Google Scholar 

  • Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447–452

    Article  CAS  PubMed  Google Scholar 

  • Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500

    Article  CAS  PubMed  Google Scholar 

  • Tsai C, Kao H, Yao T, McKeown M, Evans R (1999) SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol Cell 4:175–186

    CAS  PubMed  Google Scholar 

  • Whiting P, Sparks S, Dinan LN (1993) Ecdysteroids during embryogenesis of the house cricket, Acheta domesticus: occurrence of novel ecdysteroid conjugates in developing eggs. Insect Biochem Mol Biol 23:319–329

    Article  CAS  Google Scholar 

  • Wolff T, Ready D (1993) Pattern formation in the Drosophila retina. In: Lawrence P, Martinez AM (eds) The development of Drosophila melanogaster. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, N.Y., pp 1277–1326

  • Zelhof AC, Ghbeish N, Tsai C, Evans RM, McKeown M (1997) A role for Ultraspiracle, the Drosophila RXR, in morphogenetic furrow movement and photoreceptor cluster formation. Development 124:2499–2506

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Kaushiki Menon, Kai Zinn, Nipam Patel and Barry Condron for helping out with grasshopper embryos at times of drought. This work was supported by NSF grants DBI-0070099 and DBI-0091926.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Markus Friedrich.

Additional information

Edited by C. Desplan

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dong, Y., Dinan, L. & Friedrich, M. The effect of manipulating ecdysteroid signaling on embryonic eye development in the locust Schistocerca americana . Dev Genes Evol 213, 587–600 (2003). https://doi.org/10.1007/s00427-003-0367-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-003-0367-z

Keywords

Navigation