Cyanophora paradoxa mitochondrial tRNAs play a double game.
evolution
green lineage
mitochondrial RNA processing
organelles
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
revised:
26
02
2021
received:
08
01
2021
accepted:
01
03
2021
pubmed:
6
3
2021
medline:
15
12
2021
entrez:
5
3
2021
Statut:
ppublish
Résumé
Present-day mitochondria derive from a single endosymbiosis of an α-proteobacterium into a proto-eukaryotic cell. Since this monophyletic event, mitochondria have evolved considerably, and unique traits have been independently acquired in the different eukaryotic kingdoms. Mitochondrial genome expression and RNA metabolism have diverged greatly. Here, Cyanophora paradoxa, a freshwater alga considered as a living fossil among photosynthetic organisms, represents an exciting model for studying the evolution of mitochondrial gene expression. As expected, fully mature tRNAs are released from primary transcripts to function in mitochondrial translation. We also show that these tRNAs take part in an mRNA processing punctuation mechanism in a non-conventional manner, leading to mRNA-tRNA hybrids with a CCA triplet at their 3'-extremities. In this case, tRNAs are probably used as stabilizing structures impeding the degradation of mRNA by exonucleases. From our data we propose that the present-day tRNA-like elements (t-elements) found at the 3'-terminals of mitochondrial mRNAs in land plants originate from true tRNAs like those observed in the mitochondria of this basal photosynthetic glaucophyte.
Substances chimiques
RNA, Messenger
0
RNA, Mitochondrial
0
mitochondrial messenger RNA
0
RNA, Transfer
9014-25-9
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1105-1115Informations de copyright
© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
Bellaoui, M., Pelletier, G. & Budar, F. (1997) The steady-state level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3' region. EMBO J. 16, 5057-5068.
Canino, G., Bocian, E., Barbezier, N., Echeverria, M., Forner, J., Binder, S. et al. (2009) Arabidopsis encodes four tRNase Z enzymes. Plant Physiol. 150, 1494-1502.
Cognat, V., Pawlak, G., Duchêne, A.M., Daujat, M., Gigant, A., Salinas, T. et al. (2013) PlantRNA, a database for tRNAs of photosynthetic eukaryotes. Nucleic Acids Res. 41, D273-D279.
Dombrowski, S., Brennicke, A. & Binder, S. (1997) 3'-inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminator. EMBO J. 16, 5069-5076.
Dreher, T.W. (2009) Role of tRNA-like structures in controlling plant virus replication. Virus Res. 139, 217-229.
Forner, J., Weber, B., Thuss, S., Wildum, S. & Binder, S. (2007) Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: T-elements contribute to 5' and 3' end formation. Nucleic Acids Res. 35, 3676-3692.
Gobert, A., Gutmann, B., Taschner, A., Gossringer, M., Holzmann, J., Hartmann, R.K. et al. (2010) A single Arabidopsis organellar protein has RNase P activity. Nat. Struct. Mol. Biol. 17, 740-744.
Gobert, A., Pinker, F., Fuchsbauer, O., Gutmann, B., Boutin, R., Roblin, P. et al. (2013) Structural insights into protein-only RNase P complexed with tRNA. Nat. Commun. 4, 1353.
Grant, D. & Chiang, K.S. (1980) Physical mapping and characterization of Chlamydomonas mitochondrial DNA molecules: their unique ends, sequence homogeneity, and conservation. Plasmid, 4, 82-96.
Hammani, K. & Giegé, P. (2014) RNA metabolism in plant mitochondria. Trends Plant Sci. 19, 380-389.
Hanic-Joyce, P.J., Spencer, D.F. & Gray, M.W. (1990) In vitro processing of transcripts containing novel tRNA-like sequences ('t-elements') encoded by wheat mitochondrial DNA. Plant Mol. Biol. 15, 551-559.
Hellen, C.U. & Sarnow, P. (2001) Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15, 1593-1612.
Hinnebusch, A.G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75, 434-467.
Hopper, A. (2013) Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae. Genetics, 194, 43-67.
Huot, J.L., Enkler, L., Megel, C., Karim, L., Laporte, D., Becker, H.D. et al. (2014) Idiosyncrasies in decoding mitochondrial genomes. Biochimie, 100, 95-106.
Jackson, C., Clayden, S. & Reyes-Prieto, A. (2015) The Glaucophyta: the blue-green plants in a nutshell. Acta Soc. Bot. Polon. 84, 144-165.
Lavrov, D.V. & Pett, W. (2016) Animal mitochondrial DNA as we do not know it: mt-genome organization and evolution in nonbilaterian lineages. Genome Biol. Evol. 8, 2896-2913.
Leblanc, C., Boyen, C., Richard, O., Bonnard, G., Grienenberger, J.M. & Kloareg, B. (1995) Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J. Mol. Biol. 250, 484-495.
Lechner, M., Rossmanith, W., Hartmann, R.K., Tholken, C., Gutmann, B., Giegé, P. et al. (2015) Distribution of ribonucleoprotein and protein-only RNase P in Eukarya. Mol. Biol. Evol. 32, 3186-3193.
Mörl, M. & Marchfelder, A. (2001) The final cut. The importance of tRNA 3'-processing. EMBO Rep. 2, 17-20.
Ohyama, K. (1996) Chloroplast and mitochondrial genomes from a liverwort, Marchantia polymorpha - gene organization and molecular evolution. Biosci. Biotechnol. Biochem. 60, 16-24.
Ojala, D., Merkel, C., Gelfand, R. & Attardi, G. (1980) The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell, 22, 393-403.
Ojala, D., Montoya, J. & Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature, 290, 470-474.
Pearce, S.F., Rebelo-Guiomar, P., D'Souza, A.R., Powell, C.A., Van Haute, L. & Minczuk, M. (2017) Regulation of mammalian mitochondrial gene expression: recent advances. Trends Biochem. Sci. 42, 625-639.
Price, D.C., Chan, C.X., Yoon, H.S., Yang, E.C., Qiu, H., Weber, A.P. et al. (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science, 335, 843-847.
Roger, A.J., Munoz-Gomez, S.A. & Kamikawa, R. (2017) The origin and diversification of mitochondria. Curr. Biol. 27, R1177-R1192.
Ryabova, L.A., Pooggin, M.M. & Hohn, T. (2006) Translation reinitiation and leaky scanning in plant viruses. Virus Res. 119, 52-62.
Salinas-Giegé, T., Cavaiuolo, M., Cognat, V., Ubrig, E., Remacle, C., Duchêne, A.M. et al. (2017) Polycytidylation of mitochondrial mRNAs in Chlamydomonas reinhardtii. Nucleic Acids Res. 45, 12963-12973.
Sieber, F., Placido, A., El Farouk-Ameqrane, S., Duchene, A.M. & Marechal-Drouard, L. (2011) A protein shuttle system to target RNA into mitochondria. Nucleic Acids Res. 39, e96.
Sloan, D.B., Alverson, A.J., Chuckalovcak, J.P., Wu, M., McCauley, D.E., Palmer, J.D. et al. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10, e1001241.
Smith, D.R. & Keeling, P.J. (2015) Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc. Natl Acad. Sci. USA, 112, 10177-10184.
Torres, A.G., Piñeyro, D., Rodriguez-Escribà, M., Camacho, N., Reina, O., Saint-Léger, A. et al. (2015) Inosine modifications in human tRNAs are incorporated at the precursor tRNA level. Nucleic Acids Res. 43, 5145-5157.
Unseld, M., Marienfeld, J.R., Brandt, P. & Brennicke, A. (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15, 57-61.
Varre, J.S., D'Agostino, N., Touzet, P., Gallina, S., Tamburino, R., Cantarella, C. et al. (2019) Complete sequence, multichromosomal architecture and transcriptome analysis of the Solanum tuberosum mitochondrial genome. Int. J. Mol. Sci. 20(19), 4788.
Wu, Z., Cuthbert, J.M., Taylor, D.R. & Sloan, D.B. (2015) The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes. Proc. Natl Acad. Sci. USA, 112, 10185-10191.
Yot, P., Pinck, M., Haenni, A.L., Duranton, H.M. & Chapeville, F. (1970) Valine-specific tRNA-like structure in turnip yellow mosaic virus RNA. Proc. Natl Acad. Sci. USA, 67, 1345-1352.