Programmed Rearrangement in Ciliates: Paramecium

Abstract

Programmed genome rearrangements in the ciliate Paramecium provide a nice illustration of the impact of transposons on genome evolution and plasticity. During the sexual cycle, development of the somatic macronucleus involves elimination of ∼30% of the germline genome, including repeated DNA (e.g., transposons) and ∼45,000 single-copy internal eliminated sequences (IES). IES excision is a precise cut-and-close process, in which double-stranded DNA cleavage at IES ends depends on PiggyMac, a domesticated piggyBac transposase. Genome-wide analysis has revealed that at least a fraction of IESs originate from Tc/mariner transposons unrelated to piggyBac. Moreover, genomic sequences with no transposon origin, such as gene promoters, can be excised reproducibly as IESs, indicating that genome rearrangements contribute to the control of gene expression. How the system has evolved to allow elimination of DNA sequences with no recognizable conserved motif has been the subject of extensive research during the past two decades. Increasing evidence has accumulated for the participation of noncoding RNAs in epigenetic control of elimination for a subset of IESs, and in trans-generational inheritance of alternative rearrangement patterns. This chapter summarizes our current knowledge of the structure of the germline and somatic genomes for the model species Paramecium tetraurelia, and describes the DNA cleavage and repair factors that constitute the IES excision machinery. We present an overview of the role of specialized RNA interference machineries and their associated noncoding RNAs in the control of DNA elimination. Finally, we discuss how RNA-dependent modification and/or remodeling of chromatin may guide PiggyMac to its cognate cleavage sites.

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.…”

“…A 15-bp conserved motif is used in Tetrahymena (Yao et al 1990), whereas a different 10-bp sequence in Euplotes defines where chromosomal breaks will occur (Baird and Klobutcher 1989). However, in other ciliates (Paramecium and isotrichs) no sequences or structures that guide chromosome breakage are apparent (Betermier and Duharcourt 2014;Yerlici and Landweber 2014). Finally, a palindrome was observed at one break site in the sea lamprey (Smith et al 2012).…”

Host–transposon interactions: conflict, cooperation, and cooption

“…4B). In Paramecium, PiggyMac (Pgm) is a piggyBac-derived transposase required for DNA elimination that catalyzes and interacts with five additional related Pgm-like proteins to ensure complete IES targeting (Bétermier and Duharcourt 2014;Bischerour et al 2018). Tetrahymena also uses a suite of related transposase-derived genes (TBP, TBP2, TBP6, and LIA5) to ensure proper genome rearrangement and IES deletion Cheng et al 2016;Feng et al 2017).…”

“…Tetrahymena also uses a suite of related transposase-derived genes (TBP, TBP2, TBP6, and LIA5) to ensure proper genome rearrangement and IES deletion Cheng et al 2016;Feng et al 2017). Although these proteins are all clearly related to piggyBac transposases, they are extremely diverged from each other and share no close similarity to any extant TEs in these species, indicating that they have been fully and possibly independently coopted (Cheng et al 2010;Bétermier and Duharcourt 2014). Whether these transposases were once derived from elements with an activity similar to TBEs in Oxytricha is unknown, but there are clear sequence similarities between ciliate IESs and the TIRs of transposons (Fass et al 2011;Cheng et al 2016;Hamilton et al 2016).…”

Next-Generation Analysis of Trypanosomatid Genome Stability and Instability

“…These dramatic changes are not frequently found as examples of evolution but instead are normally genetically programmed reactions that reflect specific aspects of organism biology and development. Prominent examples of such adaptive change are immunoglobulin gene rearrangements during B-and T-cell development [1,2], mating type switching during yeast life cycles [3], and genome reconstruction in a range of ciliates [4][5][6]. In all cases, understanding of the timing, rate and mechanism of such dramatic change relative to the slower accrual of evolution-directing mutations is greatly aided by mapping the nature and location of the changes.…”