Abstract
Creophilus maxillosus (Staphylinidae, Coleoptera, Polyphaga) has a meroistic-telotrophic ovary composed of tropharium, which contains trophocytes (nurse cells) and vitellarium, which contains growing oocytes. The trophocytes are connected to the oocytes by cytoplasmic nutritive cords, which deliver nutrients to the oocytes. The formation/differentiation of the oocytes and trophocytes takes place in the pupal ovary within linear chains of sibling cells. Each chain is composed of a single oocyte connected to a linear chain of sister trophocytes. The nuclei of the oocytes contain an extrachromosomal DNA body (extra DNA body) consisting of amplified ribosomal DNA (rDNA). During oogenesis, the prospective oocyte, located at the base (posterior) of each chain, is the only cell within the chain that amplifies rDNA and retains permanent contact with the somatic pre-follicular cells. The oogonial divisions leading to the formation of the oocyte/trophocytes chain are asymmetric, and during consecutive divisions, the rDNA body always segregates basally (posteriorly) to the prospective oocyte abutted on the somatic cells. However, the segregation of rDNA is imperfect, and within each oocyte/trophocytes chain, there is a gradient of rDNA: the prospective oocyte has the highest amount of rDNA and the trophocyte that is most distant (most anterior) from the oocyte has no or the lowest amount of rDNA. In addition, the divisions within each chain are parasynchronous, with the pro-oocyte being the most mitotically advanced cell in the chain. These observations indicate the presence of a signaling gradient emanating from the somatic cells and/or oocyte; this gradient diminishes in strength with the increasing distance from its source, i.e., the oocyte/somatic cells. Because of this phenomenon, C. maxillosus is the perfect model in which to study the germ-somatic cell interactions and signaling. This chapter describes the methods for the collection and laboratory culture of C. maxillosus and the analysis of divisions and signaling in the C. maxillosus ovary.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bang C, Cheng J (2015) Dynamic interplay of spectrosome and centrosome organelles in asymmetric stem cell divisions. PLoS One 10(4):e0123294. https://doi.org/10.1371/journal.pone.0123294
Brubacher JL, Huebner E (2011) Evolution and development of polarized germ cell cysts: new insights from a polychaete worm, Ophryotrocha labronica. Dev Biol 357:96–107
Buning J (1979a) The trophic tissue of telotrophic ovarioles in polyphage Coleoptera. Zoomorphology 93:33–50
Buning J (1979b) The telotrophic nature of ovarioles of polyphage Coleoptera. Zoomorphology 93:51–57
Buning J (1993) Germ cell cluster formation in insect oocytes. Int J Insect Morphol Embryol 22:237–253
Buning J (1994) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman & Hall, London
Cave MD (1972) Localization of ribosomal DNA within oocytes of the house cricket, Acheta domesticus (Orthoptera: Gryllidae). J Cell Biol 55:310–321
Dajoz R, Caussanel C (1968) Morphologic et biologie d’un Coleoptere predateur: Creophilus maxillosus (L.) (Staphylinidae). Cah Nat (N ser) 24:65–102
Deng W, Lin H (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol 189:79–94
Deng W, Lin H (2001) Asymmetric germ cell division and oocyte determination during Drosophila oogenesis. Int Rev Cytol 203:93–138
Fichelson P, Huynh JR (2007) Asymmetric divisions of germline cells. Prog Mol Subcell Biol 45:97–120
Frątczak K, Matuszewski S (2014) Instar determination in forensically useful beetles Necrodes littoralis (Silphidae) and Creophilus maxillosus (Staphylinidae). Forensic Sci Int 241:20–26
Godt D, Tepass U (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–391
Gonzalez-Reyes A, St. Johnston D (1998) The Drosophila AP axis is polarized by the cadherin-mediated positioning of the oocyte. Development 125:3635–3644
Gonzalez-Reyes A, Elliott H, St. Johnston D (1997) Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. Development 124:4927–4937
Huynh J-R (2018) Fusome as a cell-cell communication channel of Drosophila ovarian cyst. Madame Curie Bioscience Database [Internet]
Jaglarz M (1992) Peculiarities of the organization of egg chambers in carabid ground beetles and their phylogenetic implications. Tissue Cell 24:397–409
Jaglarz M (1998) The number that counts. Phylogenetic implications of the number of nurse cells in ovarian follicles of Coleoptera-Adephaga. Folia Histochem Cytobiol 36:167–178
Kloc M (1980) Extrachromosomal DNA and its activity in RNA synthesis in oogonia and oocytes in the pupal ovary of Creophilus maxillosus (Staphylinidae, Coleoptera-Polyphaga). Eur J Cell Biol 21:328–334
Kloc M, Matuszewski B (1977) Extrachromosomal DNA and the origin of oocytes in the telotrophic-meroistic ovary of Creophilus maxillosus (L) (Staphylinidae Coleoptera-Polyphaga). Wilhelm Roux’s Arch 183:351–368
Kloc M, Matuszewski B, Nurkowska J (1995) Ribosomal gene amplification in the oocytes of Creophilus maxillosus (Staphylinidae, Coleoptera-polyphaga) – an insect with telotrophic ovaries. Folia Histochem Cytobiol 33:267–276
Kloc M, Larabell C, Chan AP, Etkin LD (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75:81–93
Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266:43–61
León A, McKearin D (1999) Identification of TER94, an AAA ATPase protein, as a bam-dependent component of the Drosophila fusome. Mol Biol Cell 10:3825–3834
Lin H, Spradling AC (1995) Fusome asymmetry and oocyte determination in drosophila. Dev Genet 16:6–12
Matuszewski B, Kloc M (1976) Gene amplification in oocytes of the rove beetle Creophilus maxillosus (Staphylinidae, Coleoptera-Polyphaga). Experientia 32:34–36
Matuszewski B, Ciechomski K, Nurkowska J, Kloc M (1985) The linear clusters of oogonial cells in the development of telotrophic ovarioles in polyphage Coleoptera. Wilhelm Roux’s Arch Dev Biol 194:462–469
Matuszewski B, Ciechomski K, Kloc M (1999) Extrachromosomal rDNA and polarity of pro-oocytes during ovary development in Creophilus maxillosus (Coleoptera, Staphylinidae). Folia Histochem Cytobiol 37:179–190
Mazurkiewicz M, Kubrakiewicz J (2002) Nucleolar activity of germ cells in polytrophic ovaries of crane flies (Diptera: Tipulidae). Ultrastructural and cytochemical studies. Folia Histochem Cytobiol 40:47–50
Megraw TL, Kaufman TC (2000) The centrosome in Drosophila oocyte development. Curr Top Dev Biol 49:385–407
Miyauchi C, Kitazawa D, Ando I, Hayashi D, Inoue YH (2013) Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males. PLoS One 8(3):e58220. https://doi.org/10.1371/journal.pone.0058220
Snapp EL, Iida T, Frescas D, Lippincott-Schwartz J, Lilly MA (2004) The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 15:4512–4521
Szklarzewicz T, Wnek A, Bilinski SM (2000) Structure of ovarioles in Adelges laricis, a representative of primitive family Adelgidae. Acta Zool (Stockholm) 81:307–313
Trendelenburg MF, Franke WW, Scheer U (1977) Frequencies of circular units of nucleolar DNA in oocytes of two insects, Acheta domesticus and Dytiscus marginalis, and changes of nucleolar morphology during oogenesis. Differentiation 7:133–158
van Eeden F, St. Johnston D (1999) The polarization of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr Opin Genet Dev 9:396–404
Varadarajan R, Ayeni J, Jin Z, Homola E, Campbell SD (2016) Myt1 inhibition of cyclin a/Cdk1 is essential for fusome integrity and premeiotic centriole engagement in Drosophila spermatocytes. Mol Biol Cell 27:2051–2063
Zhang Y, Kalderon D (2000) Regulation of cell proliferation and patterning in Drosophila oogenesis by hedgehog signaling. Development 127:2165–2176
Acknowledgments
I am very grateful to Tom Murray, Dr. Salvador Vitanza-Hedman, Dr. Szymon Matuszewski and Anna Mądra-Bielewicz, MSc for allowing me to use their photographs of Creophilus.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Kloc, M. (2019). The Rove Beetle Creophilus maxillosus as a Model System to Study Asymmetric Division, Oocyte Specification, and the Germ-Somatic Cell Signaling. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_9
Download citation
DOI: https://doi.org/10.1007/978-3-030-23459-1_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23458-4
Online ISBN: 978-3-030-23459-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)