Functional chimeric genes in ciliates: An instructive case from Euplotes raikovi

• Published in: Gene Vol. 767; p. 145186
• Main Authors: Ricci, Francesca, Luporini, Pierangelo, Alimenti, Claudio, Vallesi, Adriana
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 30.01.2021
• Subjects: Amino Acid Sequence - genetics; Base Sequence - genetics; Chimera - genetics; Chimeric genes; Ciliophora; Ciliophora - genetics; DNA - genetics; epigenetics; Euplotes - genetics; Euplotes macronuclear genes; Gene Rearrangement - genetics; genes; genetic variation; germ cells; Introns - genetics; Nano-chromosomes; nucleotide sequences; Pheromone genes; pheromones; Pheromones - genetics; RNA - genetics; RNA Splicing - genetics; Somatic recombination; synthesis; transcription (genetics); Nano-chromosomes; Euplotes macronuclear genes; Chimeric genes; Pheromone genes; Somatic recombination
• ISSN: 0378-1119; 1879-0038; 1879-0038
• DOI: 10.1016/j.gene.2020.145186

•Chimeric genes are generated by ciliates during the macronuclear development.•In Euplotes raikovi, a pheromone-coding gene, mac-er-1, coexists with a chimeric copy, mac-er-1*.•mac-er-1* originates from the mac-er-1 assembly with an extraneous sequence.•mac-er-1* is functional and practically duplicates the mac-er-1 activity. In ciliates, with every sexual event the transcriptionally active genes of the sub-chromosomic somatic genome that resides in the cell macronucleus are lost. They are de novo assembled starting from ‘Macronuclear Destined Sequences’ that arise from the fragmentation of transcriptionally silent DNA sequences of the germline chromosomic genome enclosed in the cell micronucleus. The RNA-mediated epigenetic mechanism that drives the assembly of these sequences is subject to errors which result in the formation of chimeric genes. Studying a gene family that in Euplotes raikovi controls the synthesis of protein signal pheromones responsible for a self/not-self recognition mechanism, we identified the chimeric structure of an 851-bp macronuclear gene previously known to specify soluble and membrane-bound pheromone molecules through an intron-splicing mechanism. This chimeric gene, designated mac-er-1*, conserved the native pheromone-gene structure throughout its coding and 3′ regions. Instead, its 5′ region is completely unrelated to the pheromone gene structure at the level of a 360-bp sequence, which derives from the assembly with a MDS destined to compound a 2417-bp gene encoding a 696-amino acid protein with unknown function. This mac-er-1* gene characterization provides further evidence that ciliates rely on functional chimeric genes that originate in non-programmed phenomena of somatic MDS recombination to increase the species genetic variability independently of gene reshuffling phenomena of the germline genome.