Combinatorial DNA rearrangement facilitates the origin of new genes in ciliates

Abstract

Programmed genome rearrangements in the unicellular eukaryote Oxytricha trifallax produce a transcriptionally active somatic nucleus from a copy of its germline nucleus during development. This process eliminates noncoding sequences that interrupt coding regions in the germline genome, and joins over 225,000 remaining DNA segments, some of which require inversion or complex permutation to build functional genes. This dynamic genomic organization permits some single DNA segments in the germline to contribute to multiple, distinct somatic genes via alternative processing. Like alternative mRNA splicing, the combinatorial assembly of DNA segments contributes to genetic variation and facilitates the evolution of new genes. In this study, we use comparative genomic analysis to demonstrate that the emergence of alternative DNA splicing is associated with the origin of new genes. Short duplications give rise to alternative gene segments that are spliced to the shared gene segments. Alternative gene segments evolve faster than shared, constitutive segments. Genes with shared segments frequently have different expression profiles, permitting functional divergence. This study reports alternative DNA splicing as a mechanism of new gene origination, illustrating how the process of programmed genome rearrangement gives rise to evolutionary innovation.

Small RNA-mediated regulation of DNA dosage in the ciliate Oxytricha

“…We confirmed these results genome-wide by sequencing genomic DNA libraries prepared from wild-type, dcl-1 41 and rdrp 13 mutant cells and comparing DNA copy number for all fully assembled MAC chromosomes in the JRB310 and JRB510 reference genomes (Swart et al 2013;Chen et al 2015). Out of 12,203 contigs assayed, 12,132 and 9331 contigs show reduced DNA copy number in dcl-1 and rdrp, respectively (Fig.…”

“…In addition, reads of length 17-25 nt or 30-50 nt (for sRNA and presRNA, respectively) were filtered for mapping. Pie charts comparing small RNA mapping with genome annotation involved mapping on fully assembled two telomere MAC contigs from Oxytricha strains JRB310 and JRB510 (Swart et al 2013;Chen et al 2015). For metagene analysis, two-telomere MAC contigs were aligned at the transcription start sites (TSS).…”

Evolutionary origins and impacts of genome architecture in ciliates

“…), and scrambled, where some MDSs are in nonconsecutive order and/or encoded on opposing DNA strands (Fig. ) . While nonscrambled germ‐line organization is common across the ciliate phylogeny, emerging evidence from poorly sampled lineages suggests that scrambled germ‐line loci may be more common than previously expected …”

“…From these duplicated loci, combinatorial rearrangements can take place during development (guided by the large pool of redundant pointer sequences), generating identical somatic sequences (Fig. A) . Over time, decay/divergence of redundant pointers and/or identical coding regions could become fixed, with negligible impacts on fitness (Fig.…”

Embryonic development and a quantitative model of programmed DNA elimination in Mesocyclops edax (S. A. Forbes, 1891) (Copepoda: Cyclopoida)

“…Sun et al (2014) hypothesized that many of the eliminated TEs are active, potentially deleterious, and that the DNA elimination serves as a host-defense mechanism, consistent with other studies that have ascribed a role of host defense to the DNA elimination process in ciliates (e.g., Chalker and Yao, 2011; Noto et al, 2015). Additionally, DNA elimination in ciliates rearranges the genome and produces a new combinatorial assembly of DNA segments that might promote the evolution of new genes and speciation (Chen et al, 2015; Gao et al, 2015). The elimination of genes in nematodes has been ascribed to roles in gene silencing and sex determiniation (Wang et al, 2012; Streit et al, 2016), and in the lamprey, to gene silencing (Smith et al, 2013).…”