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Mutational Effects of Mobile Introns on the Mitochondrial Genomes of Metschnikowia Yeasts.

ABSTRACT: It has been argued that DNA repair by homologous recombination in the context of endonuclease-mediated cleavage can cause mutations. To better understand this phenomenon, we examined homologous recombination following endonuclease cleavage in a native genomic context: the movement of self-splicing introns in the mitochondrial genomes of Metschnikowia yeasts. Self-splicing mitochondrial introns are mobile elements, which can copy and paste themselves at specific insertion sites in mitochondrial DNA using a homing endonuclease in conjunction with homologous recombination. Here, we explore the mutational effects of self-splicing introns by comparing sequence variation within the intron-rich cox1 and cob genes from 71 strains (belonging to 40 species) from the yeast genus Metschnikowia. We observed a higher density of single nucleotide polymorphisms around self-splicing-intron insertion sites. Given what is currently known about the movement of organelle introns, it is likely that their mutational effects result from the high binding affinity of endonucleases and their interference with repair machinery during homologous recombination (or, alternatively, via gene conversion occurring during the intron insertion process). These findings suggest that there are fitness costs to harbouring self-splicing, mobile introns and will help us better understand the risks associated with modern biotechnologies that use endonuclease-mediated homologous recombination, such as CRISPR-Cas9 gene editing.

SUBMITTER: Thompson SRL

PROVIDER: S-EPMC8601654 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe genera Aspergillus and Penicillium include some of the most beneficial as well as the most harmful fungal species such as the penicillin-producer Penicillium chrysogenum and the human pathogen Aspergillus fumigatus, respectively. Their mitochondrial genomic sequences may hold vital clues into the mechanisms of their evolution, population genetics, and biology, yet only a handful of these genomes have been fully sequenced and annotated.ResultsHere we report the complete sequence and annotation of the mitochondrial genomes of six Aspergillus and three Penicillium species: A. fumigatus, A. clavatus, A. oryzae, A. flavus, Neosartorya fischeri (A. fischerianus), A. terreus, P. chrysogenum, P. marneffei, and Talaromyces stipitatus (P. stipitatum). The accompanying comparative analysis of these and related publicly available mitochondrial genomes reveals wide variation in size (25-36 Kb) among these closely related fungi. The sources of genome expansion include group I introns and accessory genes encoding putative homing endonucleases, DNA and RNA polymerases (presumed to be of plasmid origin) and hypothetical proteins. The two smallest sequenced genomes (A. terreus and P. chrysogenum) do not contain introns in protein-coding genes, whereas the largest genome (T. stipitatus), contains a total of eleven introns. All of the sequenced genomes have a group I intron in the large ribosomal subunit RNA gene, suggesting that this intron is fixed in these species. Subsequent analysis of several A. fumigatus strains showed low intraspecies variation. This study also includes a phylogenetic analysis based on 14 concatenated core mitochondrial proteins. The phylogenetic tree has a different topology from published multilocus trees, highlighting the challenges still facing the Aspergillus systematics.ConclusionsThe study expands the genomic resources available to fungal biologists by providing mitochondrial genomes with consistent annotations for future genetic, evolutionary and population studies. Despite the conservation of the core genes, the mitochondrial genomes of Aspergillus and Penicillium species examined here exhibit significant amount of interspecies variation. Most of this variation can be attributed to accessory genes and mobile introns, presumably acquired by horizontal gene transfer of mitochondrial plasmids and intron homing.

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Mutational Effects of Mobile Introns on the Mitochondrial Genomes of Metschnikowia Yeasts.

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