Skip to main content
SpringerLink
Log in

Hormonal Regulation of Development and Reproduction

  • Chapter
  • First Online:
Management of Insect Pests to Agriculture

Abstract

The two major insect hormones ecdysterioids (the most active form is the 20-hydroxyecdysone, 20E), sequiterpenoids (juvenile hormones, JH) regulate almost every aspect of insect life including embryogenesis, molting, metamorphosis and reproduction. The physiological and biological processes regulated by these hormones have been studied over the last century and well documented in several reviews. After the advent of genomic technologies, the molecular processes that are regulated by these hormones and the genes targeted by receptors and transcription factors that transduce signals of these hormones are being actively investigated. With the sequencing of genomes and transcriptomes of many pest insects, we began to identify key players involved in action of these hormones in pest insects. Insulin-like peptides have been identified in Drosophila melanogaster and shown to play key roles in regulation of growth, development of nervous system, reproduction and lifespan. Recently, insulin-like peptides have been identified in several insect pests and disease vectors and shown to play key roles in regulation of growth, development and reproduction.

In this review, I will focus on the hormonal regulation of embryogenesis, metamorphosis and reproduction. I shall focus on systems and physiological processes that are amenable for development of methods including double-stranded RNA or small molecules to interfere with these processes with a goal to develop novel pest and disease vector control strategies.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrisqueta, M., Suren-Castillo, S., & Maestro, J. L. (2014). Insulin receptor-mediated nutritional signalling regulates juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochemistry and Molecular Biology, 49, 14–23.

    Article  CAS  PubMed  Google Scholar 

  • Amdam, G. V., Simoes, Z. L. P., Hagen, A., Norberg, K., Schroder, K., Mikkelsen, O., Kirkwood, T. B. L., & Omholt, S. W. (2004). Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology, 39, 767–773.

    Article  CAS  PubMed  Google Scholar 

  • Attardo, G. M., Hansen, I. A., Shiao, S. H., & Raikhel, A. S. (2006). Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. Journal of Experimental Biology, 209, 3071–3078.

    Article  CAS  PubMed  Google Scholar 

  • Baehrecke, E. H., & Thummel, C. S. (1995). The Drosophila E93 gene from the 93 F early puff displays stage- and tissue-specific regulation by 20-hydroxyecdysone. Developmental Biology, 171, 85–97.

    Article  CAS  PubMed  Google Scholar 

  • Belles, X., & Santos, C. G. (2014). The MEKRE93 (Methoprene tolerant-Kruppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect Biochemistry and Molecular Biology, 52C, 60–68.

    Article  CAS  Google Scholar 

  • Belyaeva, E. S., Aizenzon, M. G., Semeshin, V. F., Kiss, I. I., Koczka, K., Baritcheva, E. M., Gorelova, T. D., & Zhimulev, I. F. (1980). Cytogenetic analysis of the 2b3-4-2b11 region of the x-chromosome of Drosophila melanogaster. 1. Cytology of the region and mutant complementation groups. Chromosoma, 81, 281–306.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bergot, B., Baker, F., Cerf, D., Jamieson, G., & Schooley, D. A. (1981). Qualitative and quantitative aspects of juvenile hormone titers in developing embryos of several insect species: discovery of a new JH-like substance extracted from eggs of Manduca sexta. In G. E. Pratt & G. T. Brooks (Eds.), Juvenile hormone biochemistry (pp. 33–45). Amsterdam: Elsevier.

    Google Scholar 

  • Bitra, K., & Palli, S. R. (2010). The members of bHLH transcription factor superfamily are required for female reproduction in the red flour beetle, Tribolium castaneum. Journal of Insect Physiology, 56, 1481–1489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borovsky, D., Carlson, D. A., Hancock, R. G., Rembold, H., & Vanhandel, E. (1994). De-novo biosynthesis of juvenile hormone III and hormone-i by the accessory glands of the male mosquito. Insect Biochemistry and Molecular Biology, 24, 437–444.

    Article  CAS  PubMed  Google Scholar 

  • Bownes, M., & Blair, M. (1986). The effects of a sugar diet and hormones on the expression of the Drosophila yolk protein genes. Journal of Insect Physiology, 32, 493–501.

    Article  CAS  Google Scholar 

  • Bownes, M., & Reid, G. (1990). The role of the ovary and nutritional signals in the regulation of fat-body yolk protein geneexpression in Drosophila melanogaster. Journal of Insect Physiology, 36, 471–479.

    Article  CAS  Google Scholar 

  • Brent, C., Peeters, C., Dietmann, V., Crewe, R., & Vargo, E. (2006). Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi. Journal of Comparative Physiology A, 192, 315–320.

    Article  Google Scholar 

  • Broadus, J., McCabe, J. R., Endrizzi, B., Thummel, C. S., & Woodard, C. T. (1999). The Drosophila beta FTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Molecular Cell, 3, 143–149.

    Article  CAS  PubMed  Google Scholar 

  • Brown, M. R., Clark, K. D., Gulia, M., Zhao, Z., Garczynski, S. F., Crim, J. W., Sulderman, R. J., & Strand, M. R. (2008). An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 105, 5716–5721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buszczak, M., Freeman, M. R., Carlson, J. R., Bender, M., Cooley, L., & Segraves, W. A. (1999). Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development, 126, 4581–4589.

    CAS  PubMed  Google Scholar 

  • Carney, G. E., & Bender, M. (2000). The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis. Genetics, 154, 1203–1211.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carney, G. E., Wade, A. A., Sapra, R., Goldstein, E., & Bender, M. (1997). DHR3, an ecdysone-inducible early-late gene encoding a Drosophila nuclear receptor, is required for embryogenesis. Proceedings of the National Academy of Sciences of the United States of America, 94, 12024–12029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charles, J. P., Iwema, T., Epa, V. C., Takaki, K., Rynes, J., & Jindra, M. (2011). Ligand-binding properties of a juvenile hormone receptor, Methoprene tolerant. Proceedings of the National Academy of Sciences of the United States of America, 108, 21128–21133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chavez, V. M., Marques, G., Delbecque, J. P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J. E., & O’Connor, M. B. (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 

  • Chavoshi, T. M., Moussian, B., & Uv, A. (2010). Tissue-autonomous EcR functions are required for concurrent organ morphogenesis in the Drosophila embryo. Mechanisms of Development, 127, 308–319.

    Article  CAS  PubMed  Google Scholar 

  • Couche, G. A., Gillott, C., Tobe, S. S., & Feyereisen, R. (1985). Juvenile-hormone biosynthesis during sexual-maturation and after mating in the adult male migratory grasshopper, Melanoplus sanguinipes. Canadian Journal of Zoology, 63, 2789–2792.

    Article  CAS  Google Scholar 

  • Cui, Y., Sui, Y., Xu, J., Zhu, F., & Palli, S. R. (2014). Juvenile hormone regulates aedes aegypti kruppel homolog 1 through a conserved E box motif. Insect Biochemistry and Molecular Biology, 52C, 23–32.

    Article  CAS  Google Scholar 

  • Cusson, M., Delisle, J., & Miller, D. (1999). Juvenile hormone titers in virgin and mated Choristoneura fumiferana and C. rosaceana females: Assessment of the capacity of males to produce and transfer JH to the female during copulation. Journal of Insect Physiology, 45, 637–646.

    Article  CAS  PubMed  Google Scholar 

  • Dong, S. Z., Ye, G. Y., Guo, J. Y., & Hu, C. (2009). Roles of ecdysteroid and juvenile hormone in vitellogenesis in an endoparasitic wasp, Pteromalus puparum (Hymenoptera: Pteromalidae). General and Comparative Endocrinology, 160, 102–108.

    Article  CAS  PubMed  Google Scholar 

  • Dumser, J. B. (1980). Regulation of spermatogenesis in insects. Annual Review of Entomology, 25, 341–369.

    Article  CAS  Google Scholar 

  • Erezyilmaz, D. F., Riddiford, L. M., & Truman, J. W. (2004). Juvenile hormone acts at embryonic molts and induces the nymphal cuticle in the direct developing cricket. Development Genes and Evolution, 214, 313–323.

    Article  CAS  PubMed  Google Scholar 

  • Erezyilmaz, D. F., Rynerson, M. R., Truman, J. W., & Riddiford, L. M. (2009). The role of the pupal determinant broad during embryonic development of a directdeveloping insect. Development Genes and Evolution, 219, 535–544.

    Article  PubMed  Google Scholar 

  • Fugo, H., Yamauchi, M., & Dedos, S. G. (1996). Testicular ecdysteroids in the silkmoth, Bombyx mori. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences, 72, 34–37.

    Article  Google Scholar 

  • Gallois, D. (1989). Control of cell-differentiation in the male accessory reproductive glands of Locusta migratoria acquisition and reversal of competence to imaginal secretion. Journal of Insect Physiology, 35, 189–195.

    Article  Google Scholar 

  • Garofalo, R. S. (2002). Genetic analysis of insulin signaling in Drosophila. Trends in Endocrinology and Metabolism, 13, 156–162.

    Article  CAS  PubMed  Google Scholar 

  • Glinka, A. V., & Wyatt, G. R. (1996). Juvenile hormone activation of gene transcription in locust fat body. Insect Biochemistry and Molecular Biology, 26, 13–18.

    Article  CAS  Google Scholar 

  • Gold, S. M. W., & Davey, K. G. (1989). The effect of juvenile hormone on protein synthesis in the transparent accessory gland of male Rhodnius prolixus. Insect Biochemistry and Molecular Biology, 19, 139–143.

    CAS  Google Scholar 

  • Hagedorn, H. H., & Kunkel, J. G. (1979). Vitellogenin and vitellin in insects. Annual Review of Entomology, 24, 475–505.

    Article  CAS  Google Scholar 

  • Hansen, I. A., Attardo, G. M., Park, J. H., Peng, Q., & Raikhel, A. S. (2004). Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proceedings of the National Academy of Sciences of the United States of America, 101, 10626–10631.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen, I. A., Attardo, G. M., Roy, S. G., & Raikhel, A. S. (2005). Target of rapamycin-dependent activation of S6 kinase is a central step in the transduction of nutritional signals during egg development in a mosquito. The Journal of Biological Chemistry, 280, 20565–20572.

    Article  CAS  PubMed  Google Scholar 

  • Hansen, I. A., Sieglaff, D. H., Shiao, S. H., Munro, J. B., Knox, J., & Raikhel, A. S. (2006). The forkhead box gene family of transcription factors of the yellow fever mosquito Aedes aegypti and its role in mosquito reproduction. The American Journal of Tropical Medicine and Hygiene, 75, 262.

    Google Scholar 

  • Hansen, I. A., Sieglaff, D. H., Munro, J. B., Shiao, S. H., Cruz, J., Lee, I. W., Heraty, J. M., & Raikhel, A. S. (2007). Forkhead transcription factors regulate mosquito reproduction. Insect Biochemistry and Molecular Biology, 37, 985–997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen, I. A., Boudko, D. Y., Shiao, S. H., Voronov, D. A., Meleshkevitch, E. A., Drake, L. L., Aguirre, S. E., Fox, J. M., Attardo, G. M., & Raikhel, A. S. (2011). AACAT1 of the yellow fever mosquito, Aedes aegypti a novel histidine-specific amino acid transporter from the SLC7 family. The Journal of Biological Chemistry, 286, 10803–10813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holbrook, G. L., Chiang, A. S., & Schal, C. (1996). Allatostatin inhibition and farnesol stimulation of corpus allatum activity in embryos of the viviparous cockroach, Diploptera punctata. Archives of Insect Biochemistry and Physiology, 32, 341–352.

    Article  CAS  Google Scholar 

  • Holbrook, G. L., Chiang, A. S., Lee, Y. J., Lin, C. Y., & Schal, C. (1998). Juvenile hormone synthesis in relation to corpus allatum development in embryos of the viviparous cockroach Diploptera punctata. Invertebrate Reproduction & Development, 33, 69–79.

    Article  CAS  Google Scholar 

  • Iga, M., Blais, C., & Smagghe, G. (2013). Study on ecdysteroid levels and gene expression of enzymes related to ecdysteroid biosynthesis in the larval testis of Spodoptera littoralis. Archives of Insect Biochemistry and Physiology, 82, 14–28.

    Article  CAS  PubMed  Google Scholar 

  • Kageyama, Y., Masuda, S., Hirose, S., & Ueda, H. (1997). Temporal regulation of the mid-prepupal gene FTZ-F1: DHR3 early late gene product is one of the plural positive regulators. Genes to Cells, 2, 559–569.

    Article  CAS  PubMed  Google Scholar 

  • Kamimura, M., Tomita, S., & Fujiwara, H. (1996). Molecular cloning of an ecdysone receptor (B1 isoform) homologue from the silkworm, Bombyx mori, and its mRNA expression during wing disc development. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 113, 341–347.

    Article  CAS  Google Scholar 

  • Kayukawa, T., Minakuchi, C., Namiki, T., Togawa, T., Yoshiyama, M., Kamimura, M., Mita, K., Imanishi, S., Kiuchi, M., Ishikawa, Y., & Shinoda, T. (2012). Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proceedings of the National Academy of Sciences of the United States of America, 109, 11729–11734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayukawa, T., Tateishi, K., & Shinoda, T. (2013). Establishment of a versatile cell line for juvenile hormone signaling analysis in Tribolium castaneum. Science Reports, 3, 1570.

    Article  CAS  Google Scholar 

  • Keeley, L. L., & Mckercher, S. R. (1985). Endocrine regulations of ovarian maturation in the cockroach Blaberus discoidalis. Comparative Biochemistry and Physiology. Part A, 80, 115–121.

    Article  CAS  Google Scholar 

  • Kiss, I., Beaton, A. H., Tardiff, J., Fristrom, D., & Fristrom, J. W. (1988). Interactions and developmental effects of mutations in the broad-complex of Drosophila melanogaster. Genetics, 118, 247–259.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koelle, M. R., Segraves, W. A., & Hogness, D. S. (1992). Dhr3 – a Drosophila steroid-receptor homolog. Proceedings of the National Academy of Sciences of the United States of America, 89, 6167–6171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konopova, B., & Jindra, M. (2007). Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proceedings of the National Academy of Sciences of the United States of America, 104, 10488–10493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozlova, T., & Thummel, C. S. (2003). Essential roles for ecdysone signaling during Drosophila mid-embryonic development. Science, 301, 1911–1914.

    Article  CAS  PubMed  Google Scholar 

  • Lam, G. T., Jiang, C. A., & Thummel, C. S. (1997). Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development, 124, 1757–1769.

    CAS  PubMed  Google Scholar 

  • Lanzrein, B., Imboden, H., Burgin, C., Bruning, E., & Gfeller, H. (1984). On titers, origin, and functions of juvenile hormone III, methylfarnesoate and ecdysteroids in embryonic development of the ovoviviparous cockroach Nauphoeta cinerea. In J. Hoffmann & M. Porchet (Eds.), Biosynthesis, metabolism and mode of action of invertebrate hormones. Heidelberg: Springer.

    Google Scholar 

  • Lanzrein, B., Gentinetta, V., Abegglen, H., Baker, F. C., Miller, C. A., & Schooley, D. A. (1985). Titers of ecdysone, 20-hydroxyecdysone and juvenile hormone-III throughout the life-cycle of a hemimetabolous insect, the ovoviviparous cockroach Nauphoeta cinerea. Experientia, 41, 913–917.

    Article  CAS  Google Scholar 

  • Lee, C. Y., Wendel, D. P., Reid, P., Lam, G., Thummel, C. S., & Baehrecke, E. H. (2000). E93 directs steroid-triggered programmed cell death in Drosophila. Molecular Cell, 6, 433–443.

    Article  CAS  PubMed  Google Scholar 

  • Li, M., Mead, E. A., & Zhu, J. (2011). Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proceedings of the National Academy of Sciences of the United States of America, 108, 638–643.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Wang, J., & Li, S. (2014). E93 predominantly transduces 20-hydroxyecdysone signaling to induce autophagy and caspase activity in Drosophila fat body. Insect Biochemistry and Molecular Biology, 45, 30–39.

    Article  CAS  PubMed  Google Scholar 

  • Loeb, M. J., Brandt, E. P., & Birnbaum, M. J. (1984). Ecdysteroid production by testes of the tobacco budworm, Heliothis virescens, from last larval instar to adult. Journal of Insect Physiology, 30, 375–381.

    Article  CAS  Google Scholar 

  • Maeda, S., Nakashima, A., Yamada, R., Hara, N., Fujimoto, Y., Ito, Y., & Sonobe, H. (2008). Molecular cloning of ecdysone 20-hydroxylase and expression pattern of the enzyme during embryonic development of silkworm Bombyx mori. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 149, 507–516.

    Article  CAS  Google Scholar 

  • Maestro, J. L., Pascual, N., Treiblmayr, K., Lozano, J., & Belles, X. (2010). Juvenile hormone and allatostatins in the German cockroach embryo. Insect Biochemistry and Molecular Biology, 40, 660–665.

    Article  CAS  PubMed  Google Scholar 

  • Margam, V. M., Gelman, D. B., & Palli, S. R. (2006). Ecdysteroid titers and developmental expression of ecdysteroid-regulated genes during metamorphosis of the yellow fever mosquito, Aedes aegypti (Diptera : Culicidae). Journal of Insect Physiology, 52, 558–568.

    Article  CAS  PubMed  Google Scholar 

  • Maroy, P., Kaufmann, G., & Dubendorfer, A. (1988). Embryonic ecdysteroids of Drosophila melanogaster. Journal of Insect Physiology, 34, 633–637.

    Article  CAS  Google Scholar 

  • Minakuchi, C., Namiki, T., & Shinoda, T. (2009). Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Developmental Biology, 325, 341–350.

    Article  CAS  PubMed  Google Scholar 

  • Mou, X., Duncan, D. M., Baehrecke, E. H., & Duncan, I. (2012). Control of target gene specificity during metamorphosis by the steroid response gene E93. Proceedings of the National Academy of Sciences of the United States of America, 109, 2949–2954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novak, V. J. A. (1969). Morphogenetic analysis of effects of juvenile hormone analogues and other morphogenetically active substances on embryos of schistocerca GREGARIA (forskal). Journal of Embryology and Experimental Morphology, 21, 1–21.

    CAS  PubMed  Google Scholar 

  • Ono, H., Rewitz, K. F., Shinoda, T., Itoyama, K., Petryk, A., Rybczynski, R., Jarcho, M., Warren, J. T., Marques, G., Shimell, M. J., Gilbert, L. I., & O’Connor, M. B. (2006). Spook and Spookier code for stage-specific components of the ecdysone biosynthetic pathway in Diptera. Developmental Biology, 298, 555–570.

    Article  CAS  PubMed  Google Scholar 

  • Parthasarathy, R., & Palli, S. R. (2011). Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 41, 294–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy, R., Tan, A., Bai, H., & Palli, S. R. (2008a). Transcription factor broad suppresses precocious development of adult structures during larval-pupal metamorphosis in the red flour beetle, Tribolium castaneum. Mechanisms of Development, 125, 299–313.

    Article  CAS  PubMed  Google Scholar 

  • Parthasarathy, R., Tan, A. J., & Palli, S. R. (2008b). bHLH-PAS family transcription factor methoprene-tolerant plays a key role in JH action in preventing the premature development of adult structures during larval-pupal metamorphosis. Mechanisms of Development, 125, 601–616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy, R., Tan, A., Sun, Z., Chen, Z., Rankin, M., & Palli, S. R. (2009). Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mechanisms of Development, 126, 563–579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy, R., Sheng, Z., Sun, Z., & Palli, S. R. (2010a). Ecdysteroid regulation of ovarian growth and oocyte maturation in the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 40, 429–439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy, R., Sun, Z., Bai, H., & Palli, S. R. (2010b). Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 40, 405–414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy, R., Farkas, R., & Palli, S. R. (2012). Recent progress in Juvenile Hormone Analogs (JHA) Research. In T. S. Dhadialla (Ed.), Advances in insect physiology (Insect growth disruptors, Vol. 43, pp. 353–436). London: Academic Press Ltd/Elsevier Science Ltd.

    Google Scholar 

  • Paul, R. K., Takeuchi, H., Matsuo, Y., & Kubo, T. (2005). Gene expression of ecdysteroid-regulated gene E74 of the honeybee in ovary and brain. Insect Molecular Biology, 14, 9–15.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Hedo, M., Rivera-Perez, C., & Noriega, F. G. (2013). The insulin/TOR signal transduction pathway is involved in the nutritional regulation of juvenile hormone synthesis in Aedes aegypti. Insect Biochemistry and Molecular Biology, 43, 495–500.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pierceall, W. E., Li, C., Biran, A., Miura, K., Raikhel, A. S., & Segraves, W. A. (1999). E75 expression in mosquito ovary and fat body suggests reiterative use of ecdysone-regulated hierarchies in development and reproduction. Molecular and Cellular Endocrinology, 150, 73–89.

    Article  CAS  PubMed  Google Scholar 

  • Pinto, L. Z., Bitondi, M. M. G., & Simoes, Z. L. P. (2000). Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. Journal of Insect Physiology, 46, 153–160.

    Article  CAS  PubMed  Google Scholar 

  • Piulachs, M. D., Pagone, V., & Belles, X. (2010). Key roles of the broad-complex gene in insect embryogenesis. Insect Biochemistry and Molecular Biology, 40, 468–475.

    Article  CAS  PubMed  Google Scholar 

  • Polanska, M. A., Maksimiuk-Ramirez, E., Ciuk, M. A., Kotwica, J., & Bebas, P. (2009). Clock-controlled rhythm of ecdysteroid levels in the haemolymph and testes, and its relation to sperm release in the Egyptian cotton leafworm, Spodoptera littoralis. Journal of Insect Physiology, 55, 426–434.

    Article  CAS  PubMed  Google Scholar 

  • Raikhel, A. S., & Dhadialla, T. S. (1992). Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology, 37, 217–251.

    Article  CAS  PubMed  Google Scholar 

  • Raikhel, A. S., Kokoza, V. A., Zhu, J. S., Martin, D., Wang, S. F., Li, C., Sun, G. Q., Ahmed, A., Dittmer, N., & Attardo, G. (2002). Molecular biology of mosquito vitellogenesis: From basic studies to genetic engineering of antipathogen immunity. Insect Biochemistry and Molecular Biology, 32, 1275–1286.

    Article  CAS  PubMed  Google Scholar 

  • Ramaswamy, S. B., Shu, S. Q., Park, Y. I., & Zeng, F. R. (1997). Dynamics of juvenile hormone-mediated gonadotropism in the lepidoptera. Archives of Insect Biochemistry and Physiology, 35, 539–558.

    Article  CAS  Google Scholar 

  • Regis, L., Gomes, Y. D., & Furtado, A. F. (1985). Factors influencing male accessory-gland activity and 1st mating in Triatoma infestans and Panstrongylus megistus (Hemiptera, Reduviidae). Insect Science and Its Application, 6, 579–583.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Restifo, L. L., & Wilson, T. G. (1998). A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible broad complex transcription factors. Developmental Genetics, 22, 141–159.

    Article  CAS  PubMed  Google Scholar 

  • Reynolds, J. A., & Hand, S. C. (2009). Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket allonemobius socius. Journal of Experimental Biology, 212, 2074–2083.

    Google Scholar 

  • Richard, D. S., Jones, J. M., Barbarito, M. R., Cerula, S., Detweiler, J. P., Fisher, S. J., Brannigan, D. M., & Scheswohl, D. M. (2001). Vitellogenesis in diapausing and mutant Drosophila melanogaster: Further evidence for the relative roles of ecdysteroids and juvenile hormones. Journal of Insect Physiology, 47, 905–913.

    Article  CAS  Google Scholar 

  • Riddiford, L. M., Hiruma, K., Lan, Q., & Zhou, B. H. (1999). Regulation and role of nuclear receptors during larval molting and metamorphosis of lepidoptera. American Zoologist, 39, 736–746.

    Article  CAS  Google Scholar 

  • Riddiford, L. M., Cherbas, P., & Truman, J. W. (2001). Ecdysone receptors and their biological actions. Vitamins and Hormones – Advances in Research and Applications, 60, 1–73.

    CAS  Google Scholar 

  • Riehle, M. A., & Brown, M. R. (2002). Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti. Cell and Tissue Research, 308, 409–420.

    Article  CAS  PubMed  Google Scholar 

  • Ruaud, A. F., Lam, G., & Thummel, C. S. (2010). The Drosophila nuclear receptors DHR3 and beta FTZ-F1 control overlapping developmental responses in late embryos. Development, 137, 123–131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz, M. B., Kelly, T. J., Imberski, R. B., & Rubenstein, E. C. (1985). The effects of nutrition and methoprene treatment on ovarian ecdysteroid synthesis in Drosophila melanogaster. Journal of Insect Physiology, 31, 947.

    Article  CAS  Google Scholar 

  • Shemshedini, L., Lanoue, M., & Wilson, T. G. (1990). Evidence for a juvenile hormone receptor involved in protein synthesis in Drosophila melanogaster. The Journal of Biological Chemistry, 265, 1913–1918.

    CAS  PubMed  Google Scholar 

  • Sheng, Z. T., Xu, J. J., Bai, H., Zhu, F., & Palli, S. R. (2011). Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. The Journal of Biological Chemistry, 286, 41924–41936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinbo, H., & Happ, G. M. (1989). Effects of ecdysteroids on the growth of the post-testicular reproductive organs in the silkworm, Bombyx mori. Journal of Insect Physiology, 35, 855–864.

    Article  CAS  Google Scholar 

  • Shirk, P. D., Dahm, K. H., & Roller, H. (1976). Accessory sex glands as repository for juvenile hormone in male cecropia moths. Zeitschrift Fur Naturforschung C-A Journal of Biosciences, 31, 199–200.

    CAS  Google Scholar 

  • Shukla, J. N., & Palli, S. R. (2012). Doublesex target genes in the red flour beetle, Tribolium castaneum. Science Reports, 2, 948.

    Google Scholar 

  • Smykal, V., Bajgar, A., Provaznik, J., Fexova, S., Buricova, M., Takaki, K., Hodkova, M., Jindra, M., & Dolezel, D. (2014). Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. Insect Biochemistry and Molecular Biology, 45, 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Sondergaard, L., Mauchline, D., Egetoft, P., White, N., Wulff, P., & Bownes, M. (1995). Nutritional response in a Drosophila yolk protein gene promoter. Molecular Genetics and Genomics, 248, 25–32.

    Article  CAS  Google Scholar 

  • Sridevi, R., Bajaj, P., & Duttagupta, A. (1989). Hormonal regulation of macromolecular-synthesis in testes and accessory reproductive glands of Spodoptera litura during post-embryonic and adult development. Indian Journal of Experimental Biology, 27, 699–703.

    CAS  PubMed  Google Scholar 

  • Stay, B., Zhang, J. R., & Tobe, S. S. (2002). Methyl farnesoate and juvenile hormone production in embryos of Diploptera punctata in relation to innervation of corpora allata and their sensitivity to allatostatin. Peptides, 23, 1981–1990.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan, A. A., & Thummel, C. S. (2003). Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. Molecular Endocrinology, 17, 2125–2137.

    Article  CAS  PubMed  Google Scholar 

  • Suren-Castillo, S., Abrisqueta, M., & Maestro, J. L. (2012). FoxO inhibits juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochemistry and Molecular Biology, 42, 491–498.

    Article  CAS  PubMed  Google Scholar 

  • Swevers, L., & Iatrou, K. (1999). The ecdysone agonist tebufenozide (RH-5992) blocks the progression into the ecdysteroid-induced regulatory cascade and arrests silkmoth oogenesis at mid-vitellogenesis. Insect Biochemistry and Molecular Biology, 29, 955–963.

    Article  CAS  Google Scholar 

  • Swevers, L., & Iatrou, K. (2003). The ecdysone regulatory cascade and ovarian development in lepidopteran insects: Insights from the silkmoth paradigm. Insect Biochemistry and Molecular Biology, 33, 1285–1297.

    Article  CAS  PubMed  Google Scholar 

  • Swevers, L., Drevet, J. R., Lunke, M. D., & Iatrou, K. (1995). The silkmoth homolog of the Drosophila ecdysone receptor (BI Isoform): Cloning and analysis of expression during follicular cell differentiation. Insect Biochemistry and Molecular Biology, 25, 857–866.

    Article  CAS  PubMed  Google Scholar 

  • Swevers, L., Eystathioy, T., & Iatrou, K. (2002). The orphan nuclear receptors BmE75A and BmE75C of the silkmoth Bombyx mori: Hornmonal control and ovarian expression. Insect Biochemistry and Molecular Biology, 32, 1643–1652.

    Article  CAS  PubMed  Google Scholar 

  • Tan, A., & Palli, S. R. (2008a). Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Molecular and Cellular Endocrinology, 291, 42–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan, A., & Palli, S. R. (2008b). Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology, 38, 430–439.

    Article  CAS  PubMed  Google Scholar 

  • Tawfik, A. I., Tanaka, Y., & Tanaka, S. (2002). Possible involvement of ecdysteroids in embryonic diapause of Locusta migratoria. Journal of Insect Physiology, 48, 743–749.

    Article  CAS  PubMed  Google Scholar 

  • Temin, G., Zander, M., & Roussel, J. P. (1986). Physicochemical (Gc-Ms) Measurements of juvenile hormone III titers during embryogenesis of Locusta migratoria. International Journal of Invertebrate Reproduction and Development, 9, 105–112.

    Article  CAS  Google Scholar 

  • Terashima, J., & Bownes, M. (2004). Translating available food into the number of eggs laid by Drosphila melanogaster. Genetics, 167, 1711–1719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchida, K., Nagata, M., & Suzuki, A. (1987). Hormonal control of ovarian development in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology, 5, 167–177.

    Article  CAS  Google Scholar 

  • Uhlirova, M., Foy, B. D., Beaty, B. J., Olson, K. E., Riddiford, L. M., & Jindra, M. (2003). Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proceedings of the National Academy of Sciences of the United States of America, 100, 15607–15612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urena, E., Manjon, C., Franch-Marro, X., & Martin, D. (2014). Transcription factor E93 specifies adult metamorphosis in hemimetabolous and holometabolous insects. Proceedings of the National Academy of Sciences of the United States of America, 111, 7024–7029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White, K. P., Hurban, P., Watanabe, T., & Hogness, D. S. (1997). Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science, 276, 114–117.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, T. G., & Turner, C. (1992). Molecular analysis of methoprene-tolerant, a gene in Drosophila involved in resistance to juvenile hormone analog insect growth-aegulators. ACS Symposium Series, 505, 99–112.

    CAS  Google Scholar 

  • Wilson, T. G., DeMoor, S., & Lei, J. (2003). Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant(27) mutant phenotype. Insect Biochemistry and Molecular Biology, 33, 1167–1175.

    Article  CAS  PubMed  Google Scholar 

  • Woodard, C. T., Baehrecke, E. H., & Thummel, C. S. (1994). A molecular mechanism for the stage specificity of the Drosophila prepupal genetic response to ecdysone. Cell, 79, 607–615.

    Article  CAS  PubMed  Google Scholar 

  • Wyatt, G. R. (1988). Vitellogenin synthesis and the analysis of juvenile hormone action in locust fat body. Canadian Journal of Zoology, 66, 2600–2610.

    Article  CAS  Google Scholar 

  • Wyatt, G. R., & Davey, K. G. (1996). Cellular and molecular actions of juvenile hormone. 2. Roles of juvenile hormone in adult insects. Advances in Insect Physiology, 26, 1–155.

    Article  CAS  Google Scholar 

  • Xu, J. J., Tan, A. J., & Palli, S. R. (2010). The function of nuclear receptors in regulation of female reproduction and embryogenesis in the red flour beetle, Tribolium castaneum. Journal of Insect Physiology, 56, 1471–1480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada, M., Murata, T., Hirose, S., Lavorgna, G., Suzuki, E., & Ueda, H. (2000). Temporally restricted expression of transcription factor beta FTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster. Development, 127, 5083–5092.

    CAS  PubMed  Google Scholar 

  • Yamamoto, K., Chadarevian, A., & Pellegrini, M. (1988). Juvenile-hormone action mediated in male accessory-glands of Drosophila by calcium and kinase-c. Science, 239, 916–919.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J. Z., Mccracken, A., & Wyatt, G. R. (1993). Properties and sequence of a female-specific, juvenile hormone-induced protein from Locust Hemolymph. The Journal of Biological Chemistry, 268, 3282–3288.

    CAS  PubMed  Google Scholar 

  • Zhang, Z. L., Xu, J. J., Sheng, Z. T., Sui, Y. P., & Palli, S. R. (2011). Steroid Receptor Co-activator Is Required for Juvenile Hormone Signal Transduction through a bHLH-PAS Transcription Factor, Methoprene Tolerant. The Journal of Biological Chemistry, 286, 8437–8447.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, B. H., & Riddiford, L. M. (2001). Hormonal regulation and patterning of the broad-complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta. Developmental Biology, 231, 125–137.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, X. F., & Riddiford, L. M. (2002). Broad specifies pupal development and mediates the ‘status quo’ action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development, 129, 2259–2269.

    CAS  PubMed  Google Scholar 

  • Zhou, B. H., Hiruma, K., Shinoda, T., & Riddiford, L. M. (1998). Juvenile hormone prevents ecdysteroid-induced expression of broad complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Developmental Biology, 203, 233–244.

    Article  CAS  PubMed  Google Scholar 

  • Zollman, S., Godt, D., Prive, G. G., Couderc, J. L., & Laski, F. A. (1994). The BTB domain, found primarily in zinc-finger proteins, defines an evolutionarily conserved family that includes several developmentally-regulated genes in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 91, 10717–10721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Research in Palli laboratory is supported by USDA-NRI-CSREES (2011–04636) and National Institutes of Health (GM070559-11). This is contribution number 14-08-05 from the Kentucky Agricultural Experimental Station.

Author information

Authors and Affiliations

  1. Department of Entomology, College of Agriculture, University of Kentucky, Lexington, KY, 40546, USA

    Subba Reddy Palli

Authors
  1. Subba Reddy Palli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Subba Reddy Palli .

Editor information

Editors and Affiliations

  1. Institute of Plant Sciences and Genetics in Agriculture Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

    Henryk Czosnek

  2. Department of Entomology, Volcani Center, Bet Dagan, Israel

    Murad Ghanim

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Palli, S.R. (2016). Hormonal Regulation of Development and Reproduction. In: Czosnek, H., Ghanim, M. (eds) Management of Insect Pests to Agriculture. Springer, Cham. https://doi.org/10.1007/978-3-319-24049-7_4

Download citation

Publish with us

Policies and ethics

Search

Navigation