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Bicaudal C is required for the function of the follicular epithelium during oogenesis in Rhodnius prolixus

Development Genes and Evolution volume 231, pages 33–45 (2021)Cite this article

Abstract

The morphology and physiology of the oogenesis have been well studied in the vector of Chagas disease Rhodnius prolixus. However, the molecular interactions that regulate the process of egg formation, key for the reproductive cycle of the vector, is still largely unknown. In order to understand the molecular and cellular basis of the oogenesis, we examined the function of the gene Bicaudal C (BicC) during oogenesis and early development of R. prolixus. We show that R. prolixus BicC (Rp-BicC) gene is expressed in the germarium, with cytoplasmic distribution, as well as in the follicular epithelium of the developing oocytes. RNAi silencing of Rp-BicC resulted in sterile females that lay few, small, non-viable eggs. The ovaries are reduced in size and show a disarray of the follicular epithelium. This indicates that Rp-BicC has a central role in the regulation of oogenesis. Although the follicular cells are able to form the chorion, the uptake of vitelline by the oocytes is compromised. We show evidence that the polarity of the follicular epithelium and the endocytic pathway, which are crucial for the proper yolk deposition, are affected. This study provides insights into the molecular mechanisms underlying oocyte development and show that Rp-BicC is important for de developmental of the egg and, therefore, a key player in the reproduction of this insect.

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Acknowledgements

The authors thank all members of Rivera-Pomar and Andrés Lavore labs for fruitful discussions, L. Canavoso (CIBICI –CCT CONICET, Córdoba, Argentina) for kindly sharing the anti-vitellin antibody, A. Nazar for her contribution to develop the in situ protocol for R. prolixus, and Reprosemyx S.A. for kindly allowing the use of their confocal facility. R.R.-P is investigator and A.P postdoctoral fellow of CONICET.

Funding

This work was funded by ANPCyT and UNNOBA.

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Authors and Affiliations

  1. Centro de Bioinvestigaciones (UNNOBA-CICBA), CITNOBA (UNNOBA-CONICET), 2700, Pergamino, Buenos Aires, Argentina

    Agustina Pascual & Rolando Rivera Pomar

  2. Centro Regional de Estudios Genómicos (Facultad de Ciencias Exactas, CREG-UNLP), 1900, La Plata, Buenos Aires, Argentina

    Emiliano S. Vilardo & Rolando Rivera Pomar

  3. Laboratorio de Microscopia Integral (LIM), (CICVyA, INTA), 1686, Hurlingham, Buenos Aires, Argentina

    Catalina Taibo & Julia Sabio y García

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  1. Agustina Pascual
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  2. Emiliano S. Vilardo
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  3. Catalina Taibo
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  4. Julia Sabio y García
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Correspondence to Agustina Pascual or Rolando Rivera Pomar.

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ESM 1

Sequence alignment of BicC orthologues and phylogenetic analysis. (A) Alignment of the protein sequence of Rp-BicC with orthologues species, extracted from NCBI sequence database Harpegnathos saltator (gi|749730745 - gi|749730739-X1), Bombus terrestris (gi|808147069), Apis florea (gi|820865347), Megachile rotundata (gi|805824678), Acromyrmex echinatior (gi|332022439), Tribolium castaneum (gi|91089717), Pediculus humanus (gi|242009357), Drosophila melanogaster (gi|24584541 and NP_723949.1), Mus musculus (AAK27347.1), Nilaparvata lugens (Zhang et al. 2015), Danio rerio (NP_981965.1), Xenopus laevis (NP_001081996.1), Brugia malayi (XP_001898754.1). The amino acid conservation is visualized with black blocks, the amino acid group level conservation with gray blocks. The dashes show the absence of sequence aligned along the alignment. Oblique lines refer to continuity of alignment. (B) The pylogenetic tree was generated by Bayesian inference; the node values indicate the posterior probabilities. Tissues expression of Rp-BicC. Detection of BicC transcript by RT-PCR in Malpighian tubules (MT), Fat body (FB) and Ovaries (OV) from control and silenced (RNAiBicC) females. Upper panel: expression in females without feeding. Lower panel: expression in females 144 hours (h) post feeding. (PDF 1.23 mb)

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Pascual, A., Vilardo, E.S., Taibo, C. et al. Bicaudal C is required for the function of the follicular epithelium during oogenesis in Rhodnius prolixus. Dev Genes Evol 231, 33–45 (2021). https://doi.org/10.1007/s00427-021-00673-0

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  • DOI: https://doi.org/10.1007/s00427-021-00673-0

Keywords

  • Bicaudal C
  • Vitellogenesis
  • Follicular cells
  • Oogenesis
  • Embryonic development