Massive programmed translational jumping in mitochondria.
Programmed translational bypassing is a process whereby ribosomes "ignore" a substantial interval of mRNA sequence. Although discovered 25 y ago, the only experimentally confirmed example of this puzzling phenomenon is expression of the bacteriophage T4 gene 60. Bypassing requires translational blockage at a "takeoff codon" immediately upstream of a stop codon followed by a hairpin, which causes peptidyl-tRNA dissociation and reassociation with a matching "landing triplet" 50 nt downstream, where translation resumes. Here, we report 81 translational bypassing elements (byps) in mitochondria of the yeast Magnusiomyces capitatus and demonstrate in three cases, by transcript analysis and proteomics, that byps are retained in mitochondrial mRNAs but not translated. Although mitochondrial byps resemble the bypass sequence in the T4 gene 60, they utilize unused codons instead of stops for translational blockage and have relaxed matching rules for takeoff/landing sites. We detected byp-like sequences also in mtDNAs of several Saccharomycetales, indicating that byps are mobile genetic elements. These byp-like sequences lack bypassing activity and are tolerated when inserted in-frame in variable protein regions. We hypothesize that byp-like elements have the potential to contribute to evolutionary diversification of proteins by adding new domains that allow exploration of new structures and functions.
Robert Cedergren Centre for Bioinformatics and Genomics, Département de Biochimie, Université de Montréal, Montréal, QC, Canada H3T 1J4.
B Franz
BF
Lang
Michaela
M
Jakubkova
Eva
E
Hegedusova
Rachid
R
Daoud
Lise
L
Forget
Brona
B
Brejova
Tomas
T
Vinar
Peter
P
Kosa
Dominika
D
Fricova
Martina
M
Nebohacova
Peter
P
Griac
Lubomir
L
Tomaska
Gertraud
G
Burger
Jozef
J
Nosek
D002244:Carbon / Q000494:pharmacology; D004272:DNA, Mitochondrial / Q000378:metabolism; D005285:Fermentation / Q000187:drug effects / Q000235:genetics; D005800:Genes, Fungal / Q000235:genetics; D050259:Genes, Mitochondrial / Q000235:genetics; D008928:Mitochondria / Q000235:genetics*; D008969:Molecular Sequence Data; D016254:Mutagenesis, Insertional / Q000235:genetics; D016366:Open Reading Frames / Q000235:genetics; D010802:Phylogeny; D014176:Protein Biosynthesis / Q000235:genetics*; D012323:RNA Processing, Post-Transcriptional / Q000187:drug effects / Q000235:genetics; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015003:Yeasts / Q000187:drug effects / Q000235:genetics* / Q000254:growth & development
D004272:DNA, Mitochondrial; D012333:RNA, Messenger; D002244:Carbon
heterologous expression; mitochondrial genome; proteome analysis; ribosome hopping