Programmed Genome Rearrangements in Tetrahymena

Abstract

Ciliates are champions in programmed genome rearrangements. They carry out extensive restructuring during differentiation to drastically alter the complexity, relative copy number, and arrangement of sequences in the somatic genome. This chapter focuses on the model ciliate Tetrahymena, perhaps the simplest and best-understood ciliate studied. It summarizes past studies on various genome rearrangement processes and describes in detail the remarkable progress made in the past decade on the understanding of DNA deletion and other processes. The process occurs at thousands of specific sites to remove defined DNA segments that comprise roughly one-third of the genome including all transposons. Interestingly, this DNA rearranging process is a special form of RNA interference. It involves the production of double-stranded RNA and small RNA that guides the formation of heterochromatin. A domesticated piggyBac transposase is believed to cut off the marked chromatin, and the retained sequences are joined together through nonhomologous end-joining processes. Many of the proteins and DNA players involved have been analyzed and are described. This link provides possible explanations for the evolution, mechanism, and functional roles of the process. The article also discusses the interactions between parental and progeny somatic nuclei that affect the selection of sequences for deletion, and how the specific deletion boundaries are determined after heterochromatin marking.

Comparative genome analysis of programmed DNA elimination in nematodes

“…Thus, sites of telomere healing may not be coincident with double-strand break locations. In addition, in contrast with what has been observed in ciliate programmed DNA rearrangements (Betermier and Duharcourt 2014;Yao et al 2014; Yerlici and Landweber 2014), we did not observe any chromosomal fusions or rearrangements associated with DNA elimination in any of the nematodes. We conclude that complex removal of internally eliminated sequences or the sequence rearrangements that have been observed in ciliates does not appear to occur in these nematodes.…”

Selfing mutants link Ku proteins to mating type determination in Tetrahymena

“…Presumably, recombination between these homologous regions completes the C-terminal exon and joins the mating-type-specific N-terminal region, results in a complete, mating-type-specific gene pair in the macronucleus [ 10 ]. During conjugation, DNA endoduplication occurs in the developing macronucleus, and the macronuclear genome is amplified to about 67 copies [ 17 ]. It has been proposed that an “intranuclear coordination” process reduces the multiple types of mating-type genes to few genes, which are further reduced by random segregation (phenotypic assortment) during amitotic macronuclear division in vegetative growth [ 18 ].…”

“…In addition to the mat genes rearrangements, several types of programmed DNA rearrangements occur in the developing macronucleus during conjugation, including the deletion of thousands of internal eliminated sequences (IESs) that contain approximately 34% of the micronuclear genome, DNA fragmentation at specific chromosome breakage sequences, and endoduplication that generates approximately 67 copies of most genomic sequences and approximately 13,000 copies of the ribosomal RNA gene (rDNA) in each macronuclear genome [ 17 ]. Some of the generated minichromosomes are also eliminated between 6 and 20 fissions after conjugation [ 22 ].…”

Exploring the Histone Acetylation Cycle in the Protozoan Model Tetrahymena thermophila

“…MAC development includes a variety of programmed DNA rearrangements that includes chromosome fragmentation, and programmed deletion of DNA sequence called internal eliminated sequences (IESs) which is epigenetically regulated in a process that is initiated by genomewide transcription of non-coding RNAs (Chalker and Yao, 2001) (ncRNAs) from the normally silent MIC. The ncRNAs then direct RNAi-dependent assembly of distinct chromatin domains in the new MAC (Taverna et al, 2002;Liu et al, 2007), a prelude to DNA deletion (Yao et al, 2015) thought to be similar to the chromatin diminution seen in the parasitic nematode Ascaris (Wang et al, 2017).…”