Abstract
Plant mitochondrial genomes have been known to be highly unusual in their large sizes, frequent intra-genomic rearrangement, and generally conservative sequence evolution. Recent studies show that in early land plants the mitochondrial genomes exhibit a mixed mode of conservative yet dynamic evolution. Here, we report the completely sequenced mitochondrial genome from the liverwort Pleurozia purpurea. The circular genome has a size of 168,526 base pairs, containing 43 protein-coding genes, 3 rRNA genes, 25 tRNA genes, and 31 group I or II introns. It differs from the Marchantia polymorpha mitochondrial genome, the only other liverwort chondriome that has been sequenced, in lacking two genes (trnRucg and trnTggu) and one intron (rrn18i1065gII). The two genomes have identical gene orders and highly similar sequences in exons, introns, and intergenic spacers. Finally, a comparative analysis of duplicated trnRucu and other trnR genes from the two liverworts and several other organisms identified the recent lateral origin of trnRucg in Marchantia mtDNA through modification of a duplicated trnRucu. This study shows that the mitochondrial genomes evolve extremely slowly in liverworts, the earliest-diverging lineage of extant land plants, in stark contrast to what is known of highly dynamic evolution of mitochondrial genomes in seed plants.
Similar content being viewed by others
References
Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang CY, Du FY, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–1192
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Beckert S, Muhle H, Pruchner D, Knoop V (2001) The mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis of early land plants: a comparative analysis in mosses. Mol Phylogenet Evol 18:117–126
Bock H, Brennicke A, Schuster W (1994) Rps3 and rpl16 genes do not overlap in Oenothera mitochondria: GTG as a potential translation initiation codon in plant mitochondria? Plant Mol Biol 24:811–818
Chaw SM, Shih ACC, Wang D, Wu YW, Liu SM, Chou TY (2008) The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Mol Biol Evol 25:603–615
Clifton SW, Minx P, Fauron CMR, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503
Dombrovska O, Qiu Y-L (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32:246–263
Doyle JJ, Doyle JS (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Forrest LL, Davis EC, Long DG, Crandall-Stotler BJ, Clark A, Hollingsworth ML (2006) Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. Bryologist 109:303–334
Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481
Gray MW, Lang BF, Burger G (2004) Mitochondria of protists. Annu Rev Genet 38:477–524
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104
Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007a) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24:1068–1074
Groth-Malonek M, Rein T, Wilson R, Groth H, Heinrichs J, Knoop V (2007b) Different fates of two mitochondrial gene spacers in early land plant evolution. Int J Plant Sci 168:709–717
Joly S, Brouillet L, Bruneau A (2001) Phylogenetic implications of the multiple losses of the mitochondrial coxII.i3 intron in the angiosperms. Int J Plant Sci 162:359–373
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39
Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139
Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642
Lang BF, Burger G, Okelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–497
Lavrov DV, Lang BF (2005) Transfer RNA gene recruitment in mitochondrial DNA. Trends Genet 21:129–133
Lemieux C, Otis C, Turmel M (2007) A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5:2
Li L, Wang B, Liu Y, Qiu Y-L (2009) The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. J Mol Evol 68:665–678
Lin XY, Kaul SS, Rounsley S, Shea TP, Benito MI, Town CD, Fujii CY, Mason T, Bowman CL, Barnstead M, Feldblyum TV, Buell CR, Ketchum KA, Lee J, Ronning CM, Koo HL, Moffat KS, Cronin LA, Shen M, Pai G, Van Aken S, Umayam L, Tallon LJ, Gill JE, Adams MD, Carrera AJ, Creasy TH, Goodman HM, Somerville CR, Copenhaver GP, Preuss D, Nierman WC, White O, Eisen JA, Salzberg SL, Fraser CM, Venter JC (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402:761–768
Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW)—a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Malek O, Knoop V (1998) Trans-splicing group II introns in plant mitochondria: the complete set of cis-arranged homologs in ferns, fern allies, and a hornwort. RNA 4:1599–1609
Michel F, Dujon B (1983) Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J 2:33–38
Mishler BD, Churchill SP (1984) A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406–424
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA—a primitive form of plant mitochondrial genome. J Mol Biol 223:1–7
Palmer JD, Adams KL, Cho YR, Parkinson CL, Qiu YL, Song KM (2000) Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc Natl Acad Sci USA 97:6960–6966
Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306
Qiu Y-L, Cho YR, Cox JC, Palmer JD (1998) The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671–674
Qiu Y-L, Li LB, Wang B, Chen ZD, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516
Qiu Y-L, Li LB, Wang B, Chen ZD, Dombrovska O, Lee J, Kent L, Li RQ, Jobson RW, Hendry TA, Taylor DW, Testa CM, Ambros M (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708
Schuster RM (1966) The Hepaticae and Anthocerotae of North America, vol I. Columbia University Press, New York
Schuster W, Brennicke A (1994) The plant mitochondrial genome—physical structure, information content, RNA editing, and gene migration to the nucleus. Annu Rev Plant Physiol Plant Mol Biol 45:61–78
Stupar R, Lilly J, Town C, Cheng Z, Kaul S, Buell C, Jiang J (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci USA 98:5099–5103
Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24:699–709
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 15:1888–1903
Vangerow S, Teerkorn T, Knoop V (1999) Phylogenetic information in the mitochondrial nad5 gene of pteridophytes: RNA editing and intron sequences. Plant Biol 1:235–243
Wahrmund U, Groth-Malonek M, Knoop V (2008) Tracing plant mitochondrial DNA evolution: rearrangements of the ancient mitochondrial gene cluster trnA-trnT-nad7 in liverwort phylogeny. J Mol Evol 66:621–629
Acknowledgments
We would like to thank Jon Shaw and Blanka Shaw for help to obtain the plant material, and Volker Knoop for helpful discussion. YLQ acknowledges the support from NSF (grant DEB 0531689).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Bock.
B. Wang and J. Xue contributed equally to this work.
The mitochondrial genome sequence of Pleurozia purpurea reported here has been deposited in GenBank under the accession number FJ999996.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, B., Xue, J., Li, L. et al. The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55, 601–609 (2009). https://doi.org/10.1007/s00294-009-0273-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-009-0273-7