The tunicate mitochondrial genome
Genetic code
https://www.ncbi.nlm.nih.gov/Taxonomy/taxonomyhome.html/index.cgi?chapter=cgencodes#SG13
https://en.wikipedia.org/wiki/Ascidian_mitochondrial_code
- Yokobori and coll, 1993 sequenced cox1 in Halocynthia roretzi and proposed that AGR codes for Gly. The same year, Durrheim and coll. made the same observation on the cox3 sequence of Pyura stolonifera.
- Yokobori and coll, 1993 also noted that ATA and TGA are likely to code for M and W like in vertebtates. Durrheim and coll. also translated that way, but did not report it explicitely.
- Delarbre and coll, 1997 proposed an AGR → Gly reassignment in amphioxus, based on a AGG/GGG polymorphism, and Spruyt and coll, 1998 found a putative TCT (Gly) tRNA in the mitochondrial genome of the amphioxus (in which they also show that the AGG codon is not used), but Boore, Daehler and Brown, 1999 rebutted the suggestion of a AGA reassignment to Gly.
- Kondow and coll, 1999 sequenced a Gly(U*CU) tRNA in Halocynthia roretzi..
- Yokobori and coll, 1999 sequenced the mitochondrial genome of Halocynthia roretzi and found the predicted Gly tRNA.
- Sequence of a thaliacean (Doliolum nationalis) mitochondrial genome suggests they also decode AGR as glycine (Yokobori, Oshima and Wada, 2005).
- Deneoud and coll, 2010 reported that mitochondrial genes of O. dioica translate well with the ascidian code.
- Another case, unrelated, of reassignment to glycin is know: UGA → Gly in SR1 bacteria (Campbell and coll, 2013).
- In the hemichordate Balanoglossus carnosus (Castresana and coll., 1998): ATA → Ile, AGA → Ser, AGG → ø and AAA → ø.
- In echinoderms (Himeno and coll., 1987): AGA, AGG → Ser, ATA → Ile, AAA → Asn.
- Ciona savignyi uses the same mitochodrial genetic code as of other ascidians studied before (Yokobori, Watanabe and Oshima, 2003).
- Pichon, Luscombe and Plessy, 2019 confirms that O. dioica's mitochondrial sequences can be translated with the ascidian genetic code, and suggests that O. lon, B. sty and perhaps M. ery use different code(s).
- Another hemichordate code, in cephalodiscidae: TAA → Y, TGA → W, AGA → Ser AGG → Lys (Li and coll., 2019).
- The codon capture hypothesis: Osawa and coll., 1989.
AGA AGG ATA AAA TGA
Standard (non-mito) R R I K *
Yeast R R M K W (plus other yeast-specific changes)
Invertebrates S S M K W
Vertebrates * * M K W
Tunicates G G M K W (O. di, salps, ascidians)
O. longicauda G G I K ø?
M. erythrocephalus G G ø? K ?
B. stygius G G I K R
Cephalochordates S S,ø? M K W (standard invertebrate)
Hemichordates S ø I ø W
Hemichordates (alt) S K I K W And also TAA → Y
Echinoderms S S I N W
Genes
- All protein-coding genes are transcribed from the same strand. See for instance (Gissi, Iannelli and Pesole, 2004).
- cox2 and cytb are usually adjascent in tunicates, but they were found to be separated in the ascidians Herdmania momus (Singh and coll, 2009) or Lissoclinum patella (Kwan and coll, 2014).
- Contrary to statements in some early publication, the atp8 gene can be found in ascidians (Gissi, Iannelli and Pesole, 2004).
Transcription
- EST data shows the presence of polycistronic precursor and mature RNAs (Gissi & Pessole, 2003).
Homopolymers in appendicularians
- Poly-T regions in O. dioica's mitogenome were found by Denoeud and coll., 2010 to be reduced to T hexamers in the transcriptome.
- Diercksens and coll., 2024 and Klirs and coll., 2024 found that occasional presences of Cs in the poly-T regions does not block editing.
Other
Mitochondria can be lost in eukaryotes, be them monocellular (Karnkowska and coll., 2019), or multicellular (Yahalomi and coll., 2020).
Mitochondrial DNA has a few rNTP misincorporated, but they do not seem to be detrimental (Wanrooij and coll., 2020).
The presence of mtDNA concatemers in nuclear genomes was postulated by Balciuniene and Balciunas (2019).
The Vertebrate Genome Project has a tool to remove NUMTs (?Rhie and coll., 2021).
Tracing Homopolymers in Oikopleura dioica's mitogenome.
Dierckxsens N, Watanabe K, Tan Y, Masunaga A, Mansfield MJ, Miao J, Luscombe NM, Plessy C.
Genome Biol Evol. 2024 Aug 20:evae182. doi: 10.1093/gbe/evae182
Klirs Y, Novosolov M, Gissi C, Garic R, Pupko T, Stach T, Huchon D.
Genome Biol Evol. 2024 Aug 20:evae181. doi:10.1093/gbe/evae181
Evolutionary Insights from the Mitochondrial Genome of Oikopleura dioica: Sequencing Challenges, RNA Editing, Gene Transfers to the Nucleus, and tRNA Loss.
Rhle and many collaborators.
Nature. 2021 Apr;592(7856):737-746. doi:10.1038/s41586-021-03451-0
Towards complete and error-free genome assemblies of all vertebrate species
Balciuniene J, Balciunas D.
Front Genet. 2019 Jun 6;10:518. doi:10.3389/fgene.2019.00518
A Nuclear mtDNA Concatemer (Mega-NUMT) Could Mimic Paternal Inheritance of Mitochondrial Genome.
Postulates the existence of concatemerised mtDNA copies in nuclear genomes.
Elimination of rNMPs from mitochondrial DNA has no effect on its stability.
Proc Natl Acad Sci U S A. 2020 Jun 23;117(25):14306-14313
Wanrooij PH, Tran P, Thompson LJ, Carvalho G, Sharma S, Kreisel K, Navarrete C, Feldberg AL, Watt DL, Nilsson AK, Engqvist MKM, Clausen AR, Chabes A.
Karnkowska A, Treitli SC, Brzoň O, Novák L, Vacek V, Soukal P, Barlow LD, Herman EK, Pipaliya SV, Pánek T, Žihala D, Petrželková R, Butenko A, Eme L, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Hampl V.
Mol Biol Evol. 2019 Oct 1;36(10):2292-2312. doi:10.1093/molbev/msz147
The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion.
Proc Natl Acad Sci U S A. 2020 Mar 10;117(10):5358-5363. doi:10.1073/pnas.1909907117
Yahalomi D, Atkinson SD, Neuhof M, Chang ES, Philippe H, Cartwright P, Bartholomew JL, Huchon D.
A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome.
J Mol Evol. 1989 Nov;29(5):373-80 doi:10.1007/bf02602907
Osawa S, Ohama T, Jukes TH, Watanabe K, Yokoyama S.
Evolution of the mitochondrial genetic code. II. Reassignment of codon AUA from isoleucine to methionine.
Li Y, Kocot KM, Tassia MG, Cannon JT, Bernt M, Halanych KM.
Genome Biol Evol. 2019 Jan 1;11(1):29-40. doi:10.1093/gbe/evy254
Mitogenomics Reveals a Novel Genetic Code in Hemichordata.
Himeno H, Masaki H, Kawai T, Ohta T, Kumagai I, Miura K, Watanabe K.
Gene. 1987;56(2-3):219-30 doi:10.1016/0378-1119(87)90139-9
Unusual genetic codes and a novel gene structure for tRNA(AGYSer) in starfish mitochondrial DNA.
Pichon J, Luscombe NM, Plessy C.
F1000Res. 2019 Dec 10;8:2072. doi:10.12688/f1000research.21551.1
Widespread use of the "ascidian" mitochondrial genetic code in tunicates.
Bioinformatics. 2011 Jul 15;27(14):1929-33. doi:10.1093/bioinformatics/btr316
Dutilh BE, Jurgelenaite R, Szklarczyk R, van Hijum SA, Harhangi HR, Schmid M, de Wild B, Françoijs KJ, Stunnenberg HG, Strous M, Jetten MS, Op den Camp HJ, Huynen MA.
FACIL: Fast and Accurate Genetic Code Inference and Logo.
Bioinformatics. 2017 Nov 1;33(21):3331-3339. doi: 10.1093/bioinformatics/btx421.
Noutahi E, Calderon V, Blanchette M, Lang FB, El-Mabrouk N.
CoreTracker: accurate codon reassignment prediction, applied to mitochondrial genomes.
Genetics. 1998 Nov;150(3):1115-23.
Castresana J, Feldmaier-Fuchs G, Yokobori S, Satoh N, Pääbo S.
The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria.
J Mol Evol. 2004 Apr;58(4):376-89 doi:10.1007/s00239-003-2559-6
Gissi C, Iannelli F, Pesole G.
Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians.
Gene order varies even within the Ciona genus. A short atp8 gene is found in Ciona and Halocynthia.
Genome Res. 2003 Sep;13(9):2203-12. doi:10.1101/gr.1227803
Gissi C, Pesole G.
Transcript mapping and genome annotation of ascidian mtDNA using EST data.
Observation of polycistronic precursor and mature RNAs in ascidians.
Durrheim GA, Corfield VA, Harley EH, Ricketts MH.
Nucleic Acids Res. 1993 Jul 25;21(15):3587-8.
Nucleotide sequence of cytochrome oxidase (subunit III) from the mitochondrion of the tunicate Pyura stolonifera: evidence that AGR encodes glycine.
Kwan JC, Tianero MD, Donia MS, Wyche TP, Bugni TS, Schmidt EW.
PLoS One. 2014 May 2;9(5):e95850. doi:10.1371/journal.pone.0095850
Host Control of Symbiont Natural Product Chemistry in Cryptic Populations of the Tunicate Lissoclinum patella
Another ascidian where cox2 and cytb are not adjascent. This ascidian has an endosymbiont.
Tiratha Raj Singh, Georgia Tsagkogeorga, Frédéric Delsuc, Samuel Blanquart, Noa Shenkar, Yossi Loya, Emmanuel JP Douzery and Dorothée Huchon
BMC Genomics. 2009 Nov 17;10:534. doi: 10.1186/1471-2164-10-534
Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny
Yokobori S, Oshima T, Wada H.
Mol Phylogenet Evol. 2005 Feb;34(2):273-83. Epub 2004 Nov 19 doi:10.1016/j.ympev.2004.10.002
Complete nucleotide sequence of the mitochondrial genome of Doliolum nationalis with implications for evolution of urochordates.
William P. Goodall-Copestake
Biological Journal of the Linnean Society, Volume 120, Issue 3, 1 March 2017, Pages 637–648, https://doi.org/10.1111/bij.12915
One tunic but more than one barcode: evolutionary insights from dynamic mitochondrial DNA in Salpa thompsoni (Tunicata: Salpida)
Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5540-5. doi:10.1073/pnas.1303090110
Campbell JH, O'Donoghue P, Campbell AG, Schwientek P, Sczyrba A, Woyke T, Söll D, Podar M.
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota.
Mol Biol Evol. 1997 Aug;14(8):807-13 doi:10.1093/oxfordjournals.molbev.a025821
Delarbre C, Barriel V, Tillier S, Janvier P, Gachelin G.
The main features of the craniate mitochondrial DNA between the ND1 and the COI genes were established in the common ancestor with the lancelet.
Proposes AGR -> Gly based on AGG / GGG polymorphisms in the population.
Mol Biol Evol. 1999 Mar;16(3):410-8 doi:10.1093/oxfordjournals.molbev.a026122
Boore JL, Daehler LL, Brown WM.
Complete sequence, gene arrangement, and genetic code of mitochondrial DNA of the cephalochordate Branchiostoma floridae (Amphioxus)
Spruyt N, Delarbre C, Gachelin G, Laudet V.
Nucleic Acids Res. 1998 Jul 1;26(13):3279-85 doi:10.1093/nar/26.13.3279
Complete sequence of the amphioxus (Branchiostoma lanceolatum) mitochondrial genome: relations to vertebrates.
Genetics. 1999 Dec;153(4):1851-62
Yokobori Si, Ueda T, Feldmaier-Fuchs G, Pääbo S, Ueshima R, Kondow A, Nishikawa K, Watanabe K.
Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata).
The nucleotide sequence of Halocynthia mtDNA has been deposited in the DDBJ/GenBank/EMBL DNA databases under the accession no. AB024528
Nucleic Acids Res. 1999 Jun 15;27(12):2554-9 doi:10.1093/nar/27.12.2554
Kondow A, Suzuki T, Yokobori S, Ueda T, Watanabe K.
An extra tRNAGly(U*CU) found in ascidian mitochondria responsible for decoding non-universal codons AGA/AGG as glycine.
Jose Castresana, Gertraud Feldmaier-Fuchs, and Svante Pääbo
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3703-7 doi:10.1073/pnas.95.7.3703
J Mol Evol. 1993 Jan;36(1):1-8. doi:10.1007/BF02407301
Yokobori S, Ueda T, Watanabe K.
Codons AGA and AGG are read as glycine in ascidian mitochondria.
J Mol Evol. 2003 Nov;57(5):574-87 doi: 10.1007/s00239-003-2511-9
Yokobori S, Watanabe Y, Oshima T.
Mitochondrial genome of Ciona savignyi (Urochordata, Ascidiacea, Enterogona): comparison of gene arrangement and tRNA genes with Halocynthia roretzi mitochondrial genome.
The DDBJ accession number of complete nucleotide sequence of the Ciona mtDNA is AB079784.
Iannelli F, Griggio F, Pesole G, Gissi C.
BMC Evol Biol. 2007 Aug 31;7:155 doi:10.1186/1471-2148-7-155
The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level.
The complete mtDNA sequences of P. mammillata and P. fumigata were deposited at EMBL database under accession numbers AM292320 and AM292602, respectively.
Tarassov IA and Martin RP.
Biochimie. 1996;78(6):502-10 doi:10.1016/0300-9084(96)84756-0
Mechanisms of tRNA import into yeast mitochondria: an overview.
Gan HM, Grandjean F, Jenkins TL, Austin CM.
BMC Genomics. 2019 May 3;20(1):335. doi: 10.1186/s12864-019-5704-3.
Absence of evidence is not evidence of absence: Nanopore sequencing and complete assembly of the European lobster (Homarus gammarus) mitogenome uncovers the missing nad2 and a new major gene cluster duplication.
Canu assembly after collecting reads matching an illumina-assembled draft genome.
Wang S, Song Q, Li S, Hu Z, Dong G, Song C, Huang H, Liu Y.
Genes (Basel). 2018 Nov 12;9(11). pii: E547. doi:10.3390/genes9110547
Assembly of a Complete Mitogenome of Chrysanthemum nankingense Using Oxford Nanopore Long Reads and the Diversity and Evolution of Asteraceae Mitogenomes.
Gan HM, Linton SM, Austin CM.
Mar Genomics. 2019 Mar 27. pii: S1874-7787(18)30218-6. doi:10.1016/j.margen.2019.02.002
Two reads to rule them all: Nanopore long read-guided assembly of the iconic Christmas Island red crab, Gecarcoidea natalis (Pocock, 1888), mitochondrial genome and the challenges of AT-rich mitogenomes.
Istace B, Friedrich A, d'Agata L, Faye S, Payen E, Beluche O, Caradec C, Davidas S, Cruaud C, Liti G, Lemainque A, Engelen S, Wincker P, Schacherer J, Aury JM.
Gigascience. 2017 Feb 1;6(2):1-13. doi:10.1093/gigascience/giw018
de novo assembly and population genomic survey of natural yeast isolates with the Oxford Nanopore MinION sequencer.
Mitogenomics reveals two cryptic species in Ciona intestinalis.
Trends Genet. 2007 Sep;23(9):419-22 doi:10.1016/j.tig.2007.07.001
Iannelli F, Pesole G, Sordino P, Gissi C.
Mitochondrial gene order differs between C. robusta and C. intestinalis.
Heredity (Edinb). 2008 Oct;101(4):301-20. doi:10.1038/hdy.2008.62
Gissi C, Iannelli F, Pesole G.
Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species.
Sci Rep. 2018 Jun 22;8(1):9500. doi:10.1038/s41598-018-27805-3
Lajbner Z, Pnini R, Camus MF, Miller J, Dowling DK.
Experimental evidence that thermal selection shapes mitochondrial genome evolution.
Miettinen TP, Pessa HK, Caldez MJ, Fuhrer T, Diril MK, Sauer U, Kaldis P, Björklund M.
Curr Biol. 2014 Mar 4. pii: S0960-9822(14)00136-5. doi:10.1016/j.cub.2014.01.071
Identification of Transcriptional and Metabolic Programs Related to Mammalian Cell Size.
Nucleic Acids Res. 2012 Jul 3.
Tsuji J, Frith MC, Tomii K, Horton P.
Mammalian NUMT insertion is non-random.