Programmed Genome Rearrangements in the Ciliate Oxytricha

Abstract

The ciliate Oxytricha is a microbial eukaryote with two genomes, one of which experiences extensive genome remodeling during development. Each round of conjugation initiates a cascade of events that construct a transcriptionally active somatic genome from a scrambled germline genome, with considerable help from both long and small noncoding RNAs. This process of genome remodeling entails massive DNA deletion and reshuffling of remaining DNA segments to form functional genes from their interrupted and scrambled germline precursors. The use of Oxytricha as a model system provides an opportunity to study an exaggerated form of programmed genome rearrangement. Furthermore, studying the mechanisms that maintain nuclear dimorphism and mediate genome rearrangement has demonstrated a surprising plasticity and diversity of non-coding RNA pathways, with new roles that go beyond conventional gene silencing. Another aspect of ciliate genetics is their unorthodox patterns of RNA-mediated, epigenetic inheritance, that rival Mendelian inheritance. This review takes the reader through the key experiments in a model eukaryote that led to fundamental discoveries in RNA biology and pushes the biological limits of DNA processing.

Comparative genome analysis of programmed DNA elimination in 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).…”

Polyteny: still a giant player in chromosome research

“…Under mating conditions, the ciliate micronucleus undergoes meiosis and fuses with the micronucleus of another cell from a compatible mating type. The fused micronuclei then divide, and one of the daughters becomes the future macronucleus (Yerlici and Landweber 2014). In some species (like Oxytricha ), development of the macronucleus passes through a polytene stage (Ammermann 1987, 1971).…”

“…Shortly after forming, they break up along their length and are encased in vesicle compartments within the nucleus (Kloetzel 1970). After being compartmentalized, the polytene chromosomes disperse, and the genome reduction characteristic of many ciliates takes place, resulting in hundreds or thousands of short chromosomes (Yerlici and Landweber 2014; Spear and Lauth 1976). After this genome reduction, polytene chromosomes are not observed during the vegetative cycle of the ciliate (Ammermann 1987).…”

Introduction to Genome Biology and Diversity

“…Furthermore, the production of a working macronucleus in the next generation cannot be accomplished without information contained within both small RNA molecules (piRNA) and long RNA templates (lncRNA), which are passed across generations via the cytoplasm of the maternal macronucleus [167,168]. The piRNA are crucial to the elimination of DNA during the development of an active macronucleus, and the lncRNA mediate (1) unscrambling of the inactive micronuclear DNA, (2) regulation of gene dosage in the macronucleus, and (3) epigenetic transfer of somatic (macronuclear) alterations that are not found within the germ-line (micronuclear) DNA [167]. Thus, without those RNA molecules, the DNA genome of the stichotrichous ciliates is an incomplete informational entity [4].…”