Programmed genome rearrangements in ciliates

Abstract

Ciliates are a highly divergent group of unicellular eukaryotes with separate somatic and germline genomes found in distinct dimorphic nuclei. This characteristic feature is tightly linked to extremely laborious developmentally regulated genome rearrangements in the development of a new somatic genome/nuclei following sex. The transformation from germline to soma genome involves massive DNA elimination mediated by non-coding RNAs, chromosome fragmentation, as well as DNA amplification. In this review, we discuss the similarities and differences in the genome reorganization processes of the model ciliates Paramecium and Tetrahymena (class Oligohymenophorea), and the distantly related Euplotes, Stylonychia, and Oxytricha (class Spirotrichea).

Keywords: Ciliates; DNA elimination; Genome rearrangement; Nuclear dimorphism; Small non-coding RNAs.

Fig. 1

Representative differences between germline and somatic nuclei ciliates

Fig. 2

The Paramecium sexual cycle (autogamy and conjugation). (1) A vegetative cell with diploid micronuclei and polyploid macronucleus. (2) Meiosis of the micronuclei and beginning of old macronucleus fragmentation. (3a) Mitotic division of one remaining micronucleus (seven out of eight micronuclei degenerates) leading to the production of two identical gametic nuclei. (3b) Alternatively, during conjugation, exchange of haploid nuclei occurs. (4) Zygotic nuclei formation through the fusion of two haploid products. (5) Two subsequent mitotic divisions of the zygotic nuclei. (6) Differentiation of the two mitotic products into new macronuclei. (7) Caryonidal division/separation leading to the formation of two cells each containing two micronuclei and new macronucleus as well as fragments of old macronucleus

Fig. 3

Macronuclear differentiation process is shown on Paramecium example. a Imprecise elimination of repeated sequences like minisatellites and transposons followed by re-joining of the flanking sequences or de novo telomere addition. b Precise excision of internal eliminated sequences (IESs) possessing two TA repeats at each boundary one copy of which remains after excision

Fig. 4

The scanning model in Paramecium. a Bi-directional transcription of the parental micronuclear genome during meiosis and scnRNA production by Dcl2/Dcl3. b Scanning process between scnRNA and transcript of somatic DNA. c scnRNA targeting IES for excision by PiggyMac. d Concatenation and circularization of excised IESs. Transcription of excised and circularized IESs to produce dsRNA. dsRNA cleavage by Dcl5 to produce iesRNA ensuring elimination of all copies of IESs. Old macronucleus degradation and development of the new macronucleus

Fig. 5

Unscrambling process in Oxytricha