Mitochondria of diverse eukaryotes have evolved various departures from the standard genetic code, but the breadth of possible modifications and their phylogenetic distribution are known only incompletely. Furthermore, it is possible that some codon reassignments in previously sequenced mitogenomes have been missed, resulting in inaccurate protein sequences in databases. Here we show, considering the distribution of codons at conserved amino acid positions in mitogenome-encoded proteins, that mitochondria of the green algal order Sphaeropleales exhibit a diversity of codon reassignments, including previously missed ones and some that are unprecedented in any translation system examined so far, necessitating redefinition of existing translation tables and creating at least seven new ones. We resolve a previous controversy concerning the meaning the UAG codon in Hydrodictyaceae, which beyond any doubt encodes alanine. We further demonstrate that AGG, sometimes together with AGA, encodes alanine instead of arginine in diverse sphaeroplealeans. Further newly detected changes include Arg-to-Met reassignment of the AGG codon and Arg-to-Leu reassignment of the CGG codon in particular species. Analysis of tRNAs specified by sphaeroplealean mitogenomes provides direct support for and molecular underpinning of the proposed reassignments. Furthermore, we point to unique mutations in the mitochondrial release factor mtRF1a that correlate with changes in the use of termination codons in Sphaeropleales, including the two independent stop-to-sense UAG reassignments, the reintroduction of UGA in some Scenedesmaceae, and the sense-to-stop reassignment of UCA widespread in the group. Codon disappearance seems to be the main drive of the dynamic evolution of the mitochondrial genetic code in Sphaeropleales.

Department of Biology and Ecology Faculty of Science University of Ostrava Czech Republic

Institute of Environmental Technologies Faculty of Science University of Ostrava Czech Republic

Komentář v

Genome Biol Evol. 2019 Oct 1;11(10):2990-2991. doi: 10.1093/gbe/evz211. PubMed

Zobrazit více v PubMed

Abascal F, Posada D, Knight RD, Zardoya R.. 2006. Parallel evolution of the genetic code in arthropod mitochondrial genomes. PLoS Biol. 4(5):e127.. PubMed PMC

Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25(17):3389–3402. PubMed PMC

Barrell BG, Bankier AT, Drouin J.. 1979. A different genetic code in human mitochondria. Nature 282(5735):189–194. PubMed

Del Cortona A, et al. 2017. The plastid genome in Cladophorales green algae is encoded by hairpin chromosomes. Curr Biol. 27(24):3771–3782.e6. PubMed

Duarte I, Nabuurs SB, Magno R, Huynen M.. 2012. Evolution and diversification of the organellar release factor family. Mol Biol Evol. 29(11):3497–3512. PubMed PMC

Dutilh BE, et al. 2011. FACIL: fast and accurate genetic code inference and logo. Bioinformatics 27(14):1929–1933. PubMed PMC

Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797. PubMed PMC

Farwagi AA, Fučíková K, McManus HA.. 2015. Phylogenetic patterns of gene rearrangements in four mitochondrial genomes from the green algal family Hydrodictyaceae (Sphaeropleales, Chlorophyceae). BMC Genomics 16(1):826.. PubMed PMC

Fučíková K, Lewis PO, Gonzalez-Halphen D, Lewis LA.. 2014. Gene arrangement convergence, diverse intron content, and genetic code modifications in mitochondrial genomes of Sphaeropleales (Chlorophyta). Genome Biol. Evol. 6(8):2170–2180. PubMed PMC

Fučíková K, Lewis PO, Lewis LA.. 2014. Putting incertae sedis taxa in their place: a proposal for ten new families and three new genera in Sphaeropleales (Chlorophyceae, Chlorophyta). J Phycol. 50(1):14–25. PubMed

Fučíková K, Lewis PO, Lewis LA.. 2016. Chloroplast phylogenomic data from the green algal order Sphaeropleales (Chlorophyceae, Chlorophyta) reveal complex patterns of sequence evolution. Mol Phylogenet Evol. 98:176–183. PubMed

Fučíková K, Lewis PO, Neupane S, Karol KG, Lewis LA.. 2019. Order, please! Uncertainty in the ordinal-level classification of Chlorophyceae. PeerJ 7:e6899.. PubMed PMC

Greiner S, Lehwark P, Bock R.. 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 47(W1):W59–W64. PubMed PMC

Hayashi-Ishimaru Y, Ohama T, Kawatsu Y, Nakamura K, Osawa S.. 1996. UAG is a sense codon in several chlorophycean mitochondria. Curr Genet. 30(1):29–33. PubMed

Heaphy SM, Mariotti M, Gladyshev VN, Atkins JF, Baranov PV.. 2016. Novel ciliate genetic code variants including the reassignment of all three stop codons to sense codons in Condylostoma magnum. Mol Biol Evol. 33(11):2885–2889. PubMed PMC

Ivanova NN, et al. 2014. Stop codon reassignments in the wild. Science 344 (6186):909–913. PubMed

Jacob JE, Vanholme B, Van Leeuwen T, Gheysen G.. 2009. A unique genetic code change in the mitochondrial genome of the parasitic nematode Radopholus similis. BMC Res Notes. 2(1):192.. PubMed PMC

Jackman JE, Alfonzo JD.. 2013. Transfer RNA modifications: nature's combinatorial chemistry playground. Wiley Interdiscip Rev RNA. 4(1):35–48. PubMed PMC

Jia W, Higgs PG.. 2008. Codon usage in mitochondrial genomes: distinguishing context-dependent mutation from translational selection. Mol Biol Evol. 25(2):339–351. PubMed

Katoh K, Standley DM.. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 30(4):772–780. PubMed PMC

Knight RD, Freeland SJ, Landweber LF.. 2001. Rewiring the keyboard: evolvability of the genetic code. Nat Rev Genet. 2(1):49–58. PubMed

Kollmar M, Mühlhausen S.. 2017. Nuclear codon reassignments in the genomics era and mechanisms behind their evolution. Bioessays 39(5):1600221. PubMed

Kondow A, Suzuki T, Yokobori SI, Ueda T, Watanabe K.. 1999. An extra tRNA Gly (U* CU) found in ascidian mitochondria responsible for decoding non-universal codons AGA/AGG as glycine. Nucleic Acids Res. 27(12):2554–2559. PubMed PMC

Krassowski T, et al. 2018. Evolutionary instability of CUG-Leu in the genetic code of budding yeasts. Nat Commun. 9(1):1887.. PubMed PMC

Kück U, Jekosch K, Holzamer P.. 2000. DNA sequence analysis of the complete mitochondrial genome of the green alga Scenedesmus obliquus: evidence for UAG being a leucine and UCA being a non-sense codon. Gene 253(1):13–18. PubMed

Kumar S, Stecher G, Li M, Knyaz C, Tamura K.. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 35(6):1547–1549. PubMed PMC

Laforest MJ, Roewer I, Lang BF.. 1997. Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG ‘stop’ codons recognized as leucine. Nucleic Acids Res. 25(3):626–632. PubMed PMC

Lang BF, Lavrov D, Beck N, Steinberg SV.. 2012. Mitochondrial tRNA structure, identity, and evolution of the genetic code In: Bullerwell CE, editor. Organelle genetics. Berlin/Heidelberg: Springer; p. 431–474.

Larsson A. 2014. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30(22):3276–3278. PubMed PMC

Lavrov DV, et al. 2013. Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code. Mol Biol Evol. 30(4):865–680. PubMed

Ling J, et al. 2014. Natural reassignment of CUU and CUA sense codons to alanine in Ashbya mitochondria. Nucleic Acids Res. 42(1):499–508. PubMed PMC

Lowe TM, Eddy SR.. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25(5):955–964. PubMed PMC

McManus HA, Fučíková K, Lewis PO, Lewis LA, Karol KG.. 2018. Organellar phylogenomics inform systematics in the green algal family Hydrodictyaceae (Chlorophyceae) and provide clues to the complex evolutionary history of plastid genomes in the green algal tree of life. Am J Bot. 105(3):315–329. PubMed

Mühlhausen S, et al. 2018. Endogenous stochastic decoding of the CUG codon by competing Ser- and Leu-tRNAs in Ascoidea asiatica. Curr Biol. 28(13):2046–2057.e5. PubMed PMC

Nedelcu AM, Lee RW, Lemieux C, Gray MW, Burger G.. 2000. The complete mitochondrial DNA sequence of Scenedesmus obliquus reflects an intermediate stage in the evolution of the green algal mitochondrial genome. Genome Res. 10(6):819–831. PubMed PMC

Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ.. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 32(1):268–274. PubMed PMC

Noutahi E, Calderon V, Blanchette M, El-Mabrouk N, Lang BF.. 2019. Rapid genetic code evolution in green algal mitochondrial genomes. Mol Biol Evol. 36(4):766–783. PubMed PMC

Noutahi E, Calderon V, Blanchette M, Lang FB, El-Mabrouk N.. 2017. CoreTracker: accurate codon reassignment prediction, applied to mitochondrial genomes. Bioinformatics 33(21):3331–3339. PubMed

Pánek T, et al. 2017. Nuclear genetic codes with a different meaning of the UAG and the UAA codon. BMC Biol. 15(1):8.. PubMed PMC

Ponty Y, Leclerc F.. 2015. Drawing and editing the secondary structure(s) of RNA. Methods Mol Biol. 1269:63–100. PubMed

Sengupta S, Yang X, Higgs PG.. 2007. The mechanisms of codon reassignments in mitochondrial genetic codes. J Mol Evol. 64(6):662–688. PubMed PMC

Su HJ, et al. 2019. Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora. Proc Natl Acad Sci U S A. 116(3):934–943. PubMed PMC

Swart EC, Serra V, Petroni G, Nowacki M.. 2016. Genetic codes with no dedicated stop codon: context-dependent translation termination. Cell 166(3):691–702. PubMed PMC

Turmel M, Lemieux C.. 2017. Evolution of the plastid genome in green algae. Adv Bot Res. 85:157–193.

Turmel M, Lopes Dos Santos A, Otis C, Sergerie R, Lemieux C.. 2019. Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code. Genome Biol Evol. 11(4):1275–1292. PubMed PMC

Turmel M, Otis C, Lemieux C.. 2010. A deviant genetic code in the reduced mitochondrial genome of the picoplanktonic green alga Pycnococcus provasolii. J Mol Evol. 70(2):203–214. PubMed

Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ.. 2009. Jalview Version 2 – a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191. PubMed PMC

Will S, Joshi T, Hofacker IL, Stadler PF, Backofen R.. 2012. LocARNA-P: accurate boundary prediction and improved detection of structural RNAs. RNA 8(5):900–914. PubMed PMC

Záhonová K, Kostygov AY, Ševčíková T, Yurchenko V, Eliáš M.. 2016. An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr Biol. 26(17):2364–2369. PubMed

Zhou J, Korostelev A, Lancaster L, Noller HF.. 2012. Crystal structures of 70S ribosomes bound to release factors RF1, RF2 and RF3. Curr Opin Struct Biol. 22(6):733–742. PubMed PMC