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Blastocrithidia nonstop mitochondrial genome and its expression are remarkably insulated from nuclear codon reassignment

DA. Afonin, ES. Gerasimov, I. Škodová-Sveráková, K. Záhonová, O. Gahura, ATS. Albanaz, E. Myšková, A. Bykova, Z. Paris, J. Lukeš, FR. Opperdoes, A. Horváth, SL. Zimmer, V. Yurchenko

. 2024 ; 52 (7) : 3870-3885. [pub] 20240424

Language English Country England, Great Britain

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
22-01026S Czech Republic
19-74-10008 Russian Science Foundation
University of Ostrava
INTER-EXCELLENCE-LUASK22033 Ministry of Education
313021X329 ERDF
Slovak Ministry of Education
VEGA 1/0553/21 Academy of Sciences
SK-CZ-RD-21-0038 Slovak Research and Development Agency
90254 Ministry of Education, Youth and Sports of the Czech Republic
CZ.10 .03.01/00/22_003/0000003 Just Transition

The canonical stop codons of the nuclear genome of the trypanosomatid Blastocrithidia nonstop are recoded. Here, we investigated the effect of this recoding on the mitochondrial genome and gene expression. Trypanosomatids possess a single mitochondrion and protein-coding transcripts of this genome require RNA editing in order to generate open reading frames of many transcripts encoded as 'cryptogenes'. Small RNAs that can number in the hundreds direct editing and produce a mitochondrial transcriptome of unusual complexity. We find B. nonstop to have a typical trypanosomatid mitochondrial genetic code, which presumably requires the mitochondrion to disable utilization of the two nucleus-encoded suppressor tRNAs, which appear to be imported into the organelle. Alterations of the protein factors responsible for mRNA editing were also documented, but they have likely originated from sources other than B. nonstop nuclear genome recoding. The population of guide RNAs directing editing is minimal, yet virtually all genes for the plethora of known editing factors are still present. Most intriguingly, despite lacking complex I cryptogene guide RNAs, these cryptogene transcripts are stochastically edited to high levels.

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$a The canonical stop codons of the nuclear genome of the trypanosomatid Blastocrithidia nonstop are recoded. Here, we investigated the effect of this recoding on the mitochondrial genome and gene expression. Trypanosomatids possess a single mitochondrion and protein-coding transcripts of this genome require RNA editing in order to generate open reading frames of many transcripts encoded as 'cryptogenes'. Small RNAs that can number in the hundreds direct editing and produce a mitochondrial transcriptome of unusual complexity. We find B. nonstop to have a typical trypanosomatid mitochondrial genetic code, which presumably requires the mitochondrion to disable utilization of the two nucleus-encoded suppressor tRNAs, which appear to be imported into the organelle. Alterations of the protein factors responsible for mRNA editing were also documented, but they have likely originated from sources other than B. nonstop nuclear genome recoding. The population of guide RNAs directing editing is minimal, yet virtually all genes for the plethora of known editing factors are still present. Most intriguingly, despite lacking complex I cryptogene guide RNAs, these cryptogene transcripts are stochastically edited to high levels.
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