Russian doll genes and complex chromosome rearrangements inOxytricha trifallax

Abstract

Ciliates have two different types of nuclei per cell, with one acting as a somatic, transcriptionally active nucleus (macronucleus; abbr. MAC) and another serving as a germline nucleus (micronucleus; abbr. MIC). Furthermore, Oxytricha trifallax undergoes extensive genome rearrangements during sexual conjugation and post-zygotic development of daughter cells. These rearrangements are necessary because the precursor MIC loci are often both fragmented and scrambled, with respect to the corresponding MAC loci. Such genome architectures are remarkably tolerant of encrypted MIC loci, because RNA-guided processes during MAC development reorganize the gene fragments in the correct order to resemble the parental MAC sequence.Here, we describe the germline organization of several nested and highly scrambled genes in Oxytricha trifallax. These include cases with multiple layers of nesting, plus highly interleaved or tangled precursor loci that appear to deviate from previously described patterns. We present mathematical methods to measure the degree of nesting between precursor MIC loci, and revisit a method for a mathematical description of scrambling. After applying these methods to the chromosome rearrangement maps of O. trifallax we describe cases of nested arrangements with up to five layers of embedded genes, as well as the most scrambled loci in O. trifallax.

Constructive Neutral Evolution 20 Years Later

“…For example, ciliates are protists that develop their somatic genome through massive rearrangements from their germline genome. These genomic rearrangements require the massive removal of non-coding DNA, and sometimes even the unscrambling of gene pieces (Braun et al 2018 ; Rzeszutek et al 2020 ). Another example involves kinetoplastids (which include parasitic protists), that exhibit a dense mass of DNA inside their mitochondria called the kinetoplast.…”

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

“…Genome rearrangements in the Oxytricha lineage can include overlapping and nested loci, with MDSs for different MAC loci embedded in each other (1, 59). When multiple gene loci are nested in each other, these have been called Russian doll loci (59). Oxytricha contains two loci with five or more layers of nested genes (59).…”

“…When multiple gene loci are nested in each other, these have been called Russian doll loci (59). Oxytricha contains two loci with five or more layers of nested genes (59). Oxytricha and Tetmemena display a high degree of synteny and conservation in both Russian doll loci.…”

“…We used the genome rearrangement annotation tool SDRAP (52) to annotate the MIC genomes of Oxytricha, Tetmemena and E. woodruffi (Methods). Consistent with their close genetic distance, the genomes of O. trifallax and Tetmemena have similarly high levels of discontinuity (Figure 3A): We annotated over 215,299 MDSs in Oxytricha and over 215,624 in Tetmemena MDSs with similar MDS length distributions (Figure 3A).…”

“…SDRAP (52) was used to annotate MDSs, pointers and MIC-specific regions (minimum percent identity for preliminary match annotation=95, minimum percent identity for additional match annotation=90, minimum length of pointer annotation=2). SDRAP requires MAC and MIC genomes as input.…”