Skip to main content
SpringerLink
Log in

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

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

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguirre SA, Frede S, Rubiolo ER, Canavoso LE (2008) Vitellogenesis in the hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae), a vector of Chagas' disease. J Insect Physiol 54:393–402

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Assis MQ, Dohanik VT, Oliveira LL, Zanuncio JC, Serrao JE (2019) Evidence for a transcellular route for vitellogenin transport in the telotrophic ovary of Podisus nigrispinus (Hemiptera: Pentatomidae). Sci Rep 9:16441

    Article  PubMed  PubMed Central  Google Scholar 

  • Atella GC, Gondim KC, Machado EA, Medeiros MN, Silva-Neto MA, Masuda H (2005) Oogenesis and egg development in triatomines: a biochemical approach. An Acad Bras Cienc 77:405–430

    Article  CAS  PubMed  Google Scholar 

  • Aviv T, Lin Z, Ben-Ari G, Smibert CA, Sicheri F (2006) Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol 13:168–176

    Article  CAS  PubMed  Google Scholar 

  • Beament JW (1946) The formation and structure of the chorion of the egg in an hemipteran, Rhodnius prolixus. Q J Microsc Sci 87:393–439

    CAS  PubMed  Google Scholar 

  • Berni M, Fontenele MR, Tobias-Santos V, Caceres-Rodrigues A, Mury FB, Vionette-do-Amaral R, Masuda H, Sorgine M, da Fonseca RN, Araujo H (2014) Toll signals regulate dorsal-ventral patterning and anterior-posterior placement of the embryo in the hemipteran Rhodnius prolixus. Evodevo 5:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Blariza MJ, Leyria J, Canavoso LE, Soria NW, Garcia BA (2016) Dynamics of expression of two vitellogenin genes in the Chagas' disease vector Triatoma infestans: Analysis throughout pre-vitellogenesis and vitellogenesis. Acta Trop 156:100–107

    Article  PubMed  Google Scholar 

  • Bonhag PF (1958) Ovarian structure and vitellogenesis in insects. Annu Rev Entomol 3:137–160

    Article  Google Scholar 

  • Bouts DM, Melo AC, Andrade AL, Silva-Neto MA, Paiva-Silva Gde O, Sorgine MH, da Cunha Gomes LS, Coelho HS, Furtado AP, Aguiar EC, de Medeiros LN, Kurtenbach E, Rozental S, Cunha ESNL, de Souza W, Masuda H (2007) Biochemical properties of the major proteins from Rhodnius prolixus eggshell. Insect Biochem Mol Biol 37:1207–1221

    Article  CAS  PubMed  Google Scholar 

  • Braz GR, Abreu L, Masuda H, Oliveira PL (2001) Heme biosynthesis and oogenesis in the blood-sucking bug, Rhodnius prolixus. Insect Biochem Mol Biol 31:359–364

    Article  CAS  PubMed  Google Scholar 

  • Brito T, Julio A, Berni M, de Castro Poncio L, Bernardes ES, Araujo H, Sammeth M, Pane A (2018) Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus. PLoS Negl Trop Dis 12:e0006760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Büning JR (1994) The insect ovary: ultrastructure, previtellogenic growth, and evolution, 1st edn. Chapman & Hall, London ; New York

    Book  Google Scholar 

  • Buxton PA (1930) The Biology of A Blood-Sucking Bug, Rhodnius Prolixus. Trans Royal Entomol Soc London 78:227–256

    Article  Google Scholar 

  • Coelho HS, Atella GC, Moreira MF, Gondim KC, Masuda H (1997) Lipophorin density variation during oogenesis on Rhodnius prolixus. Arch Insect Biochem Physiol 35:301–313

    Article  CAS  PubMed  Google Scholar 

  • Costa-Filho A, Werneck CC, Nasciutti LE, Masuda H, Atella GC, Silva LF (2001) Sulfated glycosaminoglycans from ovary of Rhodnius prolixus. Insect Biochem Mol Biol 31:31–40

    Article  CAS  PubMed  Google Scholar 

  • Coura JR, Borges-Pereira J (2012) Chagas disease. What is known and what should be improved: a systemic review. Rev Soc Bras Med Trop 45:286–296

    Article  PubMed  Google Scholar 

  • Chagas CRJ (1909) Nova tripanosomíase humana. Estudos sobre a morphologia e o ciclo evolutivo do Schizotrypanum cruzi n. gen. n. esp., agente da nova entidade mórbida do homem. Mem Inst Oswaldo Cruz 1:159–218

    Article  Google Scholar 

  • Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P (2007) Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell 13:691–704

    Article  CAS  PubMed  Google Scholar 

  • Chmiel NH, Rio DC, Doudna JA (2006) Distinct contributions of KH domains to substrate binding affinity of Drosophila P-element somatic inhibitor protein. RNA 12:283–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey KG (1965) Reproduction in the insects. W.H. Freeman, San Francisco

    Google Scholar 

  • Davey KG (1981) Hormonal control of vitellogenin uptake in Rhodnius prolixus Stal. Am Zool 21:701–705

    Article  CAS  Google Scholar 

  • de Cuevas M (2005) Drosophila Oogenesis. eLS:1–7

  • Dohanik VT, Goncalves WG, Oliveira LL, Zanuncio JC, Serrao JE (2018) Vitellogenin transcytosis in follicular cells of the honeybee Apis mellifera and the wasp Polistes simillimus. Protoplasma 255:1703–1712

    Article  CAS  PubMed  Google Scholar 

  • Driever W, Nusslein-Volhard C (1988a) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54:95–104

    Article  CAS  PubMed  Google Scholar 

  • Driever W, Nusslein-Volhard C (1988b) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Fausto AM, Gambellini G, Mazzini M, Cecchettini A, Giorgi F (2005) Yolk uptake through the follicle epithelium in the ovary of the stick insect Carausius morosus. Arthropod Struct Develop 34:89–95

    Article  CAS  Google Scholar 

  • Fortes P, Salvador G, Consoli FL (2011) Ovary development and maturation in Nezara viridula (L.) (Hemiptera: Pentatomidae). Neotrop Entomol 40:89–96

    Article  CAS  PubMed  Google Scholar 

  • Gaffield MA, Tabares L, Betz WJ (2009) Preferred sites of exocytosis and endocytosis colocalize during high- but not lower-frequency stimulation in mouse motor nerve terminals. J Neurosci 29:15308–15316. https://doi.org/10.1523/JNEUROSCI.4646-09.2009

  • Gamberi C, Hipfner DR, Trudel M, Lubell WD (2017) Bicaudal C mutation causes myc and TOR pathway up-regulation and polycystic kidney disease-like phenotypes in Drosophila. PLoS Genet 13:e1006694

    Article  PubMed  PubMed Central  Google Scholar 

  • Ginzburg N, Cohen M, Chipman AD (2017) Factors involved in early polarization of the anterior-posterior axis in the milkweed bug Oncopeltus fasciatus. Genesis:55

  • Giorgi F, Falleni A, Cecchettini A, Gremigni V (1998) A fat body derived protein is selectively sulfated in the stick insect ovary by transcytosis through the follicular epithelium. Biol Cell 90:183–197

    Article  CAS  PubMed  Google Scholar 

  • Gondim KC, de Oliveira PL, Masuda H (1987) The roles of haemolymphatic lipoproteins in the oogenesis of Rhodnius prolixus. Mem Inst Oswaldo Cruz 82(Suppl 3):89–92

    Article  PubMed  Google Scholar 

  • Harrison RE, Huebner E (1997) Unipolar microtubule array is directly involved in nurse cell-oocyte transport. Cell Motil Cytoskeleton 36:355–362

    Article  CAS  PubMed  Google Scholar 

  • Huebner E (1981a) Nurse cell-oocyte interaction in the telotrophic ovarioles of an insect, Rhodnius prolixus. Tissue Cell 13:105–125

    Article  CAS  PubMed  Google Scholar 

  • Huebner E (1981b) Oocyte-follicle cell interaction during normal oogenesis and atresia in an insect. J Ultrastruct Res 74:95–104

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Anderson E (1970) The effects of vinblastine sulfate on the microtubular organization of the ovary of Rhodnius prolixus. J Cell Biol 46:191–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huebner E, Anderson E (1972a) A cytological study of the ovary of Rhodnius prolixus. Cytoarchitecture and development of the trophic chamber. J Morphol 138:1–40

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Anderson E (1972b) A cytological study of the ovary of Rhodnius prolixus. I. The ontogeny of the follicular epithelium. J Morphol 136:459–493

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Anderson E (1972c) A cytological study of the ovary of Rhodnius prolixusII. Oocyte differentiation. J Morphol 137:385–415

    Article  CAS  PubMed  Google Scholar 

  • Huebner E, Injeyan H (1980) Patency of the follicular epithelium in Rhodnius prolixus: A re-examination of the hormone response and technique refinement. Can J Zool 58:1617–1625

    Article  Google Scholar 

  • Huebner E, Injeyan H (1981) Follicular modulation during oocyte development in an insect: formation and modification of septate and gap junctions. Dev Biol 83:101–113

    Article  CAS  PubMed  Google Scholar 

  • Johnson PE, Donaldson LW (2006) RNA recognition by the Vts1p SAM domain. Nat Struct Mol Biol 13:177–178

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lavore A, Esponda-Behrens N, Pagola L, Rivera-Pomar R (2014) The gap gene Kruppel of Rhodnius prolixus is required for segmentation and for repression of the homeotic gene sex comb-reduced. Dev Biol 387:121–129

    Article  CAS  PubMed  Google Scholar 

  • Lavore A, Pagola L, Esponda-Behrens N, Rivera-Pomar R (2012) The gap gene giant of Rhodnius prolixus is maternally expressed and required for proper head and abdomen formation. Dev Biol 361:147–155

    Article  CAS  PubMed  Google Scholar 

  • Lavore A, Pascual A, Salinas FM, Esponda-Behrens N, Martinez-Barnetche J, Rodriguez M, Rivera-Pomar R (2015) Comparative analysis of zygotic developmental genes in Rhodnius prolixus genome shows conserved features on the tracheal developmental pathway. Insect Biochem Mol Biol 64:32–43

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyria J, Orchard I, Lange AB (2020) Transcriptomic analysis of regulatory pathways involved in female reproductive physiology of Rhodnius prolixus under different nutritional states. Sci Rep 10:11431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lutz DA, Huebner E (1980) Development and cellular differentiation of an insect telotrophic ovary (Rhodnius prolixus). Tissue Cell 12:773–794

    Article  CAS  PubMed  Google Scholar 

  • Lutz DA, Huebner E (1981) Development of nurse cell-oocyte interactions in the insect telotrophic ovary (Rhodnius prolixus). Tissue Cell 13:321–335

    Article  CAS  PubMed  Google Scholar 

  • Lynch JA, Roth S (2011) The evolution of dorsal-ventral patterning mechanisms in insects. Genes Dev 25:107–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado EA, Atella GC, Gondim KC, de Souza W, Masuda H (1996) Characterization and immunocytochemical localization of lipophorin binding sites in the oocytes of Rhodnius prolixus. Arch Insect Biochem Physiol 31:185–196

    Article  CAS  PubMed  Google Scholar 

  • Machado EA, Oliveira PL, Moreira MF, de Souza W, Masuda H (1998) Uptake of Rhodnius heme-binding protein (RHBP) by the ovary of Rhodnius prolixus. Arch Insect Biochem Physiol 39:133–143

    Article  CAS  PubMed  Google Scholar 

  • Mahone M, Saffman EE, Lasko PF (1995) Localized Bicaudal-C RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J 14:2043–2055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medeiros MN, Logullo R, Ramos IB, Sorgine MH, Paiva-Silva GO, Mesquita RD, Machado EA, Coutinho MA, Masuda H, Capurro ML, Ribeiro JM, Cardoso Braz GR, Oliveira PL (2011a) Transcriptome and gene expression profile of ovarian follicle tissue of the triatomine bug Rhodnius prolixus. Insect Biochem Mol Biol 41:823–831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medeiros MN, Ramos IB, Oliveira DM, da Silva RC, Gomes FM, Medeiros LN, Kurtenbach E, Chiarini LB, Masuda H, de Souza W, Machado EA (2011b) Microscopic and molecular characterization of ovarian follicle atresia in Rhodnius prolixus Stahl under immune challenge. J Insect Physiol 57:945–953

    Article  CAS  PubMed  Google Scholar 

  • Melo AC, Valle D, Machado EA, Salerno AP, Paiva-Silva GO, Cunha ESNL, de Souza W, Masuda H (2000) Synthesis of vitellogenin by the follicle cells of Rhodnius prolixus. Insect Biochem Mol Biol 30:549–557

    Article  CAS  PubMed  Google Scholar 

  • Mesquita RD, Vionette-Amaral RJ, Lowenberger C, Rivera-Pomar R, Monteiro FA, Minx P, Spieth J, Carvalho AB, Panzera F, Lawson D, Torres AQ, Ribeiro JM, Sorgine MH, Waterhouse RM, Montague MJ, Abad-Franch F, Alves-Bezerra M, Amaral LR, Araujo HM, Araujo RN, Aravind L, Atella GC, Azambuja P, Berni M, Bittencourt-Cunha PR, Braz GR, Calderon-Fernandez G, Carareto CM, Christensen MB, Costa IR, Costa SG, Dansa M, Daumas-Filho CR, De-Paula IF, Dias FA, Dimopoulos G, Emrich SJ, Esponda-Behrens N, Fampa P, Fernandez-Medina RD, da Fonseca RN, Fontenele M, Fronick C, Fulton LA, Gandara AC, Garcia ES, Genta FA, Giraldo-Calderon GI, Gomes B, Gondim KC, Granzotto A, Guarneri AA, Guigo R, Harry M, Hughes DS, Jablonka W, Jacquin-Joly E, Juarez MP, Koerich LB, Lange AB, Latorre-Estivalis JM, Lavore A, Lawrence GG, Lazoski C, Lazzari CR, Lopes RR, Lorenzo MG, Lugon MD, Majerowicz D, Marcet PL, Mariotti M, Masuda H, Megy K, Melo AC, Missirlis F, Mota T, Noriega FG, Nouzova M, Nunes RD, Oliveira RL, Oliveira-Silveira G, Ons S, Orchard I, Pagola L, Paiva-Silva GO, Pascual A, Pavan MG et al (2015) Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proc Natl Acad Sci U S A 112:14936–14941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Comput Environ Workshop (GCE):1–8

  • Mohler J, Wieschaus EF (1986) Dominant maternal-effect mutations of Drosophila melanogaster causing the production of double-abdomen embryos. Genetics 112:803–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nusslein-Volhard C (1977) Genetic analysis of pattern-formation in the embryo ofDrosophila melanogaster : Characterization of the maternal-effect mutantBicaudal. Wilehm Roux Arch Dev Biol 183:249–268

    Article  PubMed  Google Scholar 

  • Nusslein-Volhard C, Roth S (1989) Axis determination in insect embryos. CIBA Found Symp 144:37–55 discussion 55-64, 92-38

    CAS  PubMed  Google Scholar 

  • Oliveira PL, Gondim KC, Guedes DM, Masuda H (1986) Uptake of yolk proteins in Rhodnius prolixus. J Insect Physiol 32:859–866

    Article  CAS  Google Scholar 

  • Park S, Blaser S, Marchal MA, Houston DW, Sheets MD (2016) A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators. Development 143:864–871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pascual, A. (2019). Genómica del desarrollo embrionario de Rhodnius prolixus. Facultad de Ciencias Exactas, Área Ciencias Biológicas UNLP,180

  • Pereira J, Diogo C, Fonseca A, Bomfim L, Cardoso P, Santos A, Dittz U, Miranda K, de Souza W, Gioda A, Calderon ERD, Araripe L, Bruno R, Ramos I (2020) Silencing of RpATG8 impairs the biogenesis of maternal autophagosomes in vitellogenic oocytes, but does not interrupt follicular atresia in the insect vector Rhodnius prolixus. PLoS Negl Trop Dis 14:e0008012

    Article  PubMed  PubMed Central  Google Scholar 

  • Raikhel AS (2005) Vitellogenesis of disease vectors, from physiology to genes. In: Marquardt W (ed) Biology of Disease Vectors. Elsevier Academic Press, London

    Google Scholar 

  • Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–251

    Article  CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro JM, Genta FA, Sorgine MH, Logullo R, Mesquita RD, Paiva-Silva GO, Majerowicz D, Medeiros M, Koerich L, Terra WR, Ferreira C, Pimentel AC, Bisch PM, Leite DC, Diniz MM, da, S.G.V.J.J.L., Da Silva ML, Araujo RN, Gandara AC, Brosson S, Salmon D, Bousbata S, Gonzalez-Caballero N, Silber AM, Alves-Bezerra M, Gondim KC, Silva-Neto MA, Atella GC, Araujo H, Dias FA, Polycarpo C, Vionette-Amaral RJ, Fampa P, Melo AC, Tanaka AS, Balczun C, Oliveira JH, Goncalves RL, Lazoski C, Rivera-Pomar R, Diambra L, Schaub GA, Garcia ES, Azambuja P, Braz GR, Oliveira PL (2014) An insight into the transcriptome of the digestive tract of the bloodsucking bug, Rhodnius prolixus. PLoS Negl Trop Dis 8:e2594

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronnau M, Azevedo DO, Fialho M, Gonclaves WG, Zanuncio JC, Serrao JE (2016) Changes in follicular cells architecture during vitellogenin transport in the ovary of social Hymenoptera. Protoplasma 253:815–820

    Article  CAS  PubMed  Google Scholar 

  • Roth S, Schupbach T (1994) The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120:2245–2257

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Schupbach T, Roth S (1994) Dorsoventral patterning in Drosophila oogenesis. Curr Opin Genet Dev 4:502–507

    Article  CAS  PubMed  Google Scholar 

  • Schupbach T, Wieschaus E (1986) Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux Arch Dev Biol 195:302–317

    Article  PubMed  Google Scholar 

  • Schupbach T, Wieschaus E (1991) Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129:1119–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CB, Betz WJ (1996) Simultaneous independent measurement of endocytosis and exocytosis. Nature 380:531–534

    Article  CAS  PubMed  Google Scholar 

  • Snodgrass RE (1935) Principles of insect morphology, 1st edn. McGraw-Hill Book Company, inc., New York, London

    Google Scholar 

  • Sorrivas de Lozano, V., Morales, A., Yañez, M.J. (2014). Principios y práctica de la Microscopía Electrónica. in: UAT, E. (Ed.), CONICET Bahía Blanca.

  • Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28(1102):1104

    Google Scholar 

  • Urbani E (1970) A survey on some aspects of oogenesis in Dytiscus, Cybister and Hygrobia (Coleoptera). Acta Embryol Exp (Palermo) 3:281–297

    CAS  Google Scholar 

  • Valdimarsson G, Huebner E (1989) The development of microtubular arrays in the germ tissue of an insect telotrophic ovary. Tissue Cell 21:123–138

    Article  CAS  PubMed  Google Scholar 

  • Vieira PH, Bomfim L, Atella GC, Masuda H, Ramos I (2018) Silencing of RpATG6 impaired the yolk accumulation and the biogenesis of the yolk organelles in the insect vector R. prolixus. PLoS Negl Trop Dis 12:e0006507

    Article  PubMed  PubMed Central  Google Scholar 

  • Wanderley-Teixeira V, Teixeira AA, Cunha FM, Costa MK, Veiga AF, Oliveira JV (2006) Histological description of the midgut and the pyloric valve of Tropidacris collaris (Stoll, 1813) (Orthopetera: Romaleidae). Braz J Biol 66:1045–1049

    Article  CAS  PubMed  Google Scholar 

  • Wigglesworth VB (1934) The physiology of ecdysis in Rhodnius prolixus (Hemiptera). II. Factors controlling moulting and metamorphosis. Q J Microscopy Sci 77:191–222

    Google Scholar 

  • Wigglesworth VB (1939) The Principles of Insect Physiology. Methuen, London

    Google Scholar 

  • Wigglesworth VB (1953) The origin of sensory neurons in an insect. Q J Microscopy Sci 93:93–112

    Google Scholar 

  • Wigglesworth VB (1964) The hormonal regularion of growth and reproduction in insects. Adv Insect Physiol 2

  • Zhang BX, Huang HJ, Yu B, Lou YH, Fan HW, Zhang CX (2015) Bicaudal-C plays a vital role in oogenesis in Nilaparvata lugens (Hemiptera: Delphacidae). J Insect Physiol 79:19–26

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

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

Authors
  1. Agustina Pascual
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emiliano S. Vilardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catalina Taibo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julia Sabio y García
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rolando Rivera Pomar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Agustina Pascual or Rolando Rivera Pomar.

Additional information

Communicated by Siegfried Roth

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

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)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

Keywords

Search

Navigation