Restoration of cellular integrity following “ballistic” pronuclear exchange during Tetrahymena conjugation

• Published in: Developmental biology Vol. 444; no. 1; pp. 33 - 40
• Main Authors: Cole, Eric S., Dmytrenko, Oleksandr, Chmelik, Carl J., Li, Mark, Christensen, Trenton A., Macon, Elaine P., Nilsson, Hannah J., Blower, Ruth J., Reuter, Thomas G., Beckman, John P., Remmers, Bailey C., Smith, Claire L., O'Toole, Eileen, Ozzello, Courtney, Morgan, Garry, Giddings, Thomas
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2018
• Subjects: cell adhesion; cell walls; Ciliates; Conjugation; electron microscopy; Fertilization; furrows; Gametes; Membrane fusion; microtubules; mitosis; plasma membrane; Plasma membrane, Tetrahymena; pronucleus; sexual reproduction; Tetrahymena thermophila; tomography; Gametes; Membrane fusion; Ciliates; Conjugation; Fertilization; Plasma membrane, Tetrahymena
• ISSN: 0012-1606; 1095-564X; 1095-564X
• DOI: 10.1016/j.ydbio.2018.09.019

During sexual reproduction or conjugation, ciliates form a specialized cell adhesion zone for the purpose of exchanging gametic pronuclei. Hundreds of individual membrane fusion events transform the adhesion zone into a perforated membrane curtain, the mating junction. Pronuclei from each mating partner are propelled through this fenestrated membrane junction by a web of short, cris-crossing microtubules. Pronuclear passage results in the formation of two breaches in the membrane junction. Following pronuclear exchange and karyogamy (fertilization), cells seal these twin membrane breaches thereby re-establishing cellular independence. This would seem like a straightforward problem: simply grow membrane in from the edges of each breach in a fashion similar to how animal cells “grow” their cytokinetic furrows or how plant cells construct a cell wall during mitosis. Serial section electron microscopy and 3-D electron tomography reveal that the actual mechanism is less straightforward. Each of the two membrane breaches transforms into a bowed membrane assembly platform. The resulting membrane protrusions continue to grow into the cytoplasm of the mating partner, traverse the cytoplasm in anti-parallel directions and make contact with the plasma membrane that flanks the mating junction. This investigation reveals the details of a novel, developmentally-induced mechanism of membrane disruption and restoration associated with pronuclear exchange and fertilization in the ciliate, Tetrahymena thermophila. •Tetrahymena thermophila, a ciliate, undergoes complex membrane dynamics during sexual reproduction and pronuclear exchange.•Mating cells initially form a specialized mating junction, where the two plasma membranes adhere.•The adhesion zone undergoes membrane fusion events creating 100s of membrane pores that expand, creating a membrane curtain.•Gamete pronuclei are propelled through this membrane curtain by a meshwork of cris-crossing short microtubules.•Following bilateral nuclear exchange, the junction is restored by an elaborate process of membrane folding and growth.