Abstract
Ciliates have two functionally distinct nuclei, a somatic macronucleus (MAC) and a germline micronucleus (MIC) that develop from daughter nuclei of the last postzygotic division (PZD) during the sexual process of conjugation. Understanding this nuclear dimorphism is a central issue in ciliate biology. We show, by live-cell imaging of Tetrahymena, that biased assembly of the nuclear pore complex (NPC) occurs immediately after the last PZD, which generates anterior-posterior polarized nuclei: MAC-specific NPCs assemble in anterior presumptive MACs but not in posterior presumptive MICs. MAC-specific NPC assembly in the anterior nuclei occurs much earlier than transport of Twi1p, which is required for MAC genome rearrangement. Correlative light-electron microscopy shows that addition of new nuclear envelope (NE) precursors occurs through the formation of domains of redundant NE, where the outer double membrane contains the newly assembled NPCs. Nocodazole inhibition of the second PZD results in assembly of MAC-specific NPCs in the division-failed zygotic nuclei, leading to failure of MIC differentiation. Our findings demonstrate that NPC type switching has a crucial role in the establishment of nuclear differentiation in ciliates.
Highlights
Ciliated protozoa are unique unicellular organisms in which two functionally and structurally distinct nuclei, a somatic macronucleus (MAC) and a germline micronucleus (MIC), exist in a single cytoplasm (Orias et al, 2011)
We demonstrate that de novo assembly of MAC-type nuclear pore complex (NPC) has a crucial role within MAC differentiation in T. thermophila: Nuclei that do not acquire MAC-type NPCs do not differentiate into MACs
In addition to de novo assembly of NPCs, we demonstrate that the bias in the assembly of de novo NPCs in the anterior and posterior nuclei is crucial in determining the fate of nuclei in T. thermophila: de novo assembly of NPCs occurs in the anterior nuclei and is prevented from occurring in the posterior nuclei
Summary
Ciliated protozoa are unique unicellular organisms in which two functionally and structurally distinct nuclei, a somatic macronucleus (MAC) and a germline micronucleus (MIC), exist in a single cytoplasm (Orias et al, 2011). The MIC is diploid and contains chromosomes that remain condensed and are not transcribed during vegetative growth, whereas the polyploid MAC exhibits active transcription during all cellular stages (Gorovsky and Woodard, 1969). Both MAC (Eisen et al, 2006) and MIC (http://www.broadinstitute.org/annotation/genome/ Tetrahymena/MultiHome.html) genomes have been completely sequenced. These two nuclei have distinct cell cycles, with distinct cycles of DNA replication and nuclear division at. Understanding the mechanisms that generate this nuclear dimorphism is one of the most fascinating unsolved biological problems (Goldfarb and Gorovsky, 2009; Karrer, 2012)
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