Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-14T22:26:54.780Z Has data issue: false hasContentIssue false

Primary structure and expression of vitellogenin A and vitellogenin B in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae)

Published online by Cambridge University Press:  17 October 2022

Ahmed Sayed Ahmed
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada
Norbert H. Haunerland*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada
*
*Corresponding author. Email: haunerla@sfu.ca

Abstract

Vitellogenins are the major yolk protein precursors found throughout the animal kingdom. In insects, the primary structures of vitellogenins have been determined in species from most major orders, except for Orthoptera, where only partial sequences have been reported. We amplified and sequenced the complete complementary DNA for two vitellogenins from the desert locust, Schistocerca gregaria (Orthoptera: Acrididae), which code for vitellogenin A and vitellogenin B, two proteins of approximately 200 kDa each. Both proteins are highly expressed at similar rates in adult females only, and their expression can be completely abolished by RNA interference–mediated silencing of the juvenile hormone receptor, methoprene-tolerant (Met). Homologous sequences were inferred from the genome of Locusta migratoria (Orthoptera: Acrididae), yielding complete coding sequences considerably larger than previously published. Vitellogenin A and vitellogenin B from S. gregaria are highly similar to their respective homologues from L. migratoria but show relatively low similarity between each other, suggesting that these genes originated from a common ancestor long before these species diverged.

Type
Research Paper
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Jeremy deWaard

References

Anderson, T.A., Levitt, D.G., and Banaszak, L.J. 1998. The structural basis of lipid interactions in lipovitellin, a soluble lipoprotein. Structure, 6: 895909.CrossRefGoogle ScholarPubMed
Babin, P.J., Bogerd, J., Kooiman, F.P., Van Marrewijk, W.J., and Van der Horst, D.J. 1999. Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor. Journal of Molecular Evolution, 49: 150160.CrossRefGoogle ScholarPubMed
Badisco, L., Huybrechts, J., Simonet, G., Verlinden, H., Marchal, E., Huybrechts, R., et al. 2011a. Transcriptome analysis of the desert locust central nervous system: production and annotation of a Schistocerca gregaria EST database. PLOS One, 6: e17274. https://doi.org/10.1371/journal.pone.0017274.CrossRefGoogle ScholarPubMed
Badisco, L., Marchal, E., Van Wielendaele, P., Verlinden, H., Vleugels, R., and Vanden Broeck, J. 2011b. RNA interference of insulin-related peptide and neuroparsins affects vitellogenesis in the desert locust Schistocerca gregaria . Peptides, 32: 573580.CrossRefGoogle ScholarPubMed
Barr, P.J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell, 66: 13.CrossRefGoogle ScholarPubMed
Borst, D.W., Eskew, M.R., Wagner, S.J., Shores, K., Hunter, J., Luker, L., et al. 2000. Quantification of juvenile hormone III, vitellogenin, and vitellogenin-mRNA during the oviposition cycle of the lubber grasshopper. Insect Biochemistry and Molecular Biology, 30: 813819.CrossRefGoogle ScholarPubMed
Camacho, J.P.M., Ruiz-Ruano, F.J., Martín-Blázquez, R., López-León, M.D., Cabrero, J., Lorite, P., et al. 2015. A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs. Chromosoma, 124: 263275.CrossRefGoogle Scholar
Chen, J.S. and Raikhel, A.S. 1996. Subunit cleavage of mosquito pro-vitellogenin by a subtilisin-like convertase. Proceedings of the National Academy of Sciences, 93: 61866190.CrossRefGoogle ScholarPubMed
Chen, T.T., Couble, P., Abu-Hakima, R., and Wyatt, G.R. 1979. Juvenile hormone-controlled vitellogenin synthesis in Locusta migratoria fat body. Hormonal induction in vivo. Developmental Biology, 69: 5972.CrossRefGoogle ScholarPubMed
Chino, H., Hirayama, Y., Kiyomoto, Y., Downer, R.G.H., and Takahashi, K. 1987. Spontaneous aggregation of locust lipophorin during hemolymph collection. Insect Biochemistry, 17: 8997.CrossRefGoogle Scholar
Chinzei, Y., White, B.N., and Wyatt, G.R. 1982. Vitellogenin mRNA in locust fat body: identification, isolation, and quantitative changes induced by juvenile hormone. Canadian Journal of Biochemistry, 60: 243251.CrossRefGoogle ScholarPubMed
Chinzei, Y. and Wyatt, G.R. 1985. Vitellogenin titre in haemolymph of Locusta migratoria in normal adults, after ovariectomy, and in response to methoprene. Journal of Insect Physiology, 31: 441445.CrossRefGoogle Scholar
Comas, D., Piulachs, M.D., and Bellés, X. 2000. Vitellogenin of Blattella germanica (L.) (Dictyoptera, Blattellidae): nucleotide sequence of the cDNA and analysis of the protein primary structure. Archives of Insect Biochemistry and Physiology, 45: 111.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Dhadialla, T.S. and Raikhel, A.S. 1990. Biosynthesis of mosquito vitellogenin. Journal of Biological Chemistry, 265: 99249933.CrossRefGoogle ScholarPubMed
Dhadialla, T.S. and Wyatt, G.R. 1983. Juvenile hormone–dependent vitellogenin synthesis in Locusta migratoria fat body: inducibility related to sex and stage. Developmental Biology, 96: 436444.CrossRefGoogle ScholarPubMed
Glinka, A.V. and Wyatt, G.R. 1996. Juvenile hormone activation of gene transcription in locust fat body. Insect Biochemistry and Molecular Biology, 26: 1318.CrossRefGoogle Scholar
Guo, W., Wu, Z., Song, J., Jiang, F., Wang, Z., Deng, S., et al. 2014. Juvenile hormone-receptor complex acts on Mcm4 and Mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLOS Genetics, 10: 1004702. https://doi.org/10.1371/journal.pgen.1004702.CrossRefGoogle ScholarPubMed
Hagedorn, H.H. and Kunkel, J.G. 1979. Vitellogenin and vitellin in insects. Annual Review of Entomology, 24: 475505.CrossRefGoogle Scholar
Hughes, A.L. 2010. Evolutionary conservation of amino acid composition in paralogous insect vitellogenins. Gene, 467: 3540.CrossRefGoogle ScholarPubMed
Jindra, M., Palli, S.R., and Riddiford, L.M. 2013. The juvenile hormone signaling pathway in insect development. Annual Review of Entomology, 58: 181204.CrossRefGoogle ScholarPubMed
Livak, K.J. and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25: 402408.CrossRefGoogle Scholar
Locke, J., White, B., and Wyatt, G.R. 1987. Cloning and 5′ end nucleotide sequences of two juvenile hormone-inducible vitellogenin genes of the African migratory locust. DNA, 6: 331342.CrossRefGoogle ScholarPubMed
Mei, Y., Jing, D., Tang, S., Chen, S., Chen, H., Duanmu, H., et al. 2022. InsectBase 2.0: a comprehensive gene resource for insects. Nucleic Acids Research, 50: D1040D1045. https://doi.org/10.1093/nar/gkab1090.CrossRefGoogle ScholarPubMed
Nair, K.K., Chen, T.T., and Wyatt, G.R. 1981. Juvenile hormone-stimulated polyploidy in adult locust fat body. Developmental Biology, 81: 356360.CrossRefGoogle ScholarPubMed
Oishi, M., Locke, J., and Wyatt, G.R. 1985. The ribosomal RNA genes of Locusta migratoria: copy number and evidence for underreplication in a polyploid tissue. Canadian Journal of Cell Biology, 63: 10641070.CrossRefGoogle Scholar
Pener, M.P. and Simpson, S.J. 2009. Locust phase polyphenism: an update. Advances in Insect Physiology, 36: 1272.CrossRefGoogle Scholar
Rajapakse, S., Qu, D., Syed Ahmed, A., Rickers-Haunerland, J., and Haunerland, N.H. 2019. Knock down of muscle fatty acid binding protein (FABP) impedes endurance flight of the desert locust, Schistocerca gregaria. Journal of Experimental Biology, 222: jeb203455. https://doi.org/10.1242/jeb.203455.CrossRefGoogle Scholar
Sappington, T.W. and Raikhel, A.S. 1998. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology, 28: 277300.CrossRefGoogle ScholarPubMed
Song, J., Guo, W., Jiang, F., Kang, L., and Zhou, S. 2013. Argonaute 1 is indispensable for juvenile hormone mediated oogenesis in the migratory locust, Locusta migratoria . Insect Biochemistry and Molecular Biology, 43: 879887.CrossRefGoogle ScholarPubMed
Telfer, W.H. 1954. Immunological studies of insect metamorphosis. II. The role of a sex-limited blood protein in egg formation by the Cecropia silkworm. Journal of General Physiology, 37: 539558.CrossRefGoogle ScholarPubMed
Texas A&M University. 2020. Transcriptome sequencing of four related species of grasshopper in the genus Schistocerca. National Center for Biotechnology Information BioProject PRJNA633949. Available from http://www.ncbi.nlm.nih.gov/bioproject/PRJNA633949 [accessed 26 January 2022].Google Scholar
Tufail, M., Hatakeyama, M., and Takeda, M. 2001. Molecular evidence for two vitellogenin genes and processing of vitellogenins in the American cockroach, Periplaneta americana . Archives of Insect Biochemistry and Physiology, 48: 7280.CrossRefGoogle ScholarPubMed
Tufail, M., Nagaba, Y., Elgendy, A.M., and Takeda, M. 2014. Regulation of vitellogenin genes in insects. Entomological Science, 17: 269282.CrossRefGoogle Scholar
Tufail, M. and Takeda, M. 2008. Molecular characteristics of insect vitellogenins. Journal of Insect Physiology, 54: 14471458.CrossRefGoogle ScholarPubMed
Van der Horst, D.J. and Rodenburg, K.W. 2010. Locust flight activity as a model for hormonal regulation of lipid mobilization and transport. Journal of Insect Physiology, 56: 844853.CrossRefGoogle ScholarPubMed
Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., et al. 2014. The locust genome provides insight into swarm formation and long-distance flight. Nature Communications, 5: 2957. https://doi.org/10.1038/ncomms3957.CrossRefGoogle ScholarPubMed
Wu, Z., Yang, L., He, Q., and Zhou, S. 2021. Regulatory mechanisms of vitellogenesis in insects. Frontiers of Cell and Developmental Biology, 8: 593613. https://doi.org/10.3389/fcell.2020.593613.CrossRefGoogle ScholarPubMed
Wyatt, G.R. 1988. Vitellogenin synthesis and the analysis of juvenile hormone action in locust fat body. Canadian Journal of Zoology, 66: 26002610.CrossRefGoogle Scholar
Wyatt, G.R. and Davey, K.G. 1996. Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Advances in Insect Physiology, 26: 1155.CrossRefGoogle Scholar