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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

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Abstract

Land plants possess some of the most unusual mitochondrial genomes among eukaryotes. However, in early land plants these genomes resemble those of green and red algae or early eukaryotes. The question of when during land plant evolution the dramatic change in mtDNAs occurred remains unanswered. Here we report the first completely sequenced mitochondrial genome of the hornwort, Megaceros aenigmaticus, a member of the sister group of vascular plants. It is a circular molecule of 184,908 base pairs, with 32 protein genes, 3 rRNA genes, 17 tRNA genes, and 30 group II introns. The genome contains many genes arranged in the same order as in those of a liverwort, a moss, several green and red algae, and Reclinomonas americana, an early-branching eukaryote with the most ancestral form of mtDNA. In particular, the gene order between mtDNAs of the hornwort and Physcomitrella patens (moss) differs by only 8 inversions and translocations. However, the hornwort mtDNA possesses 4 derived features relative to green alga mtDNAs—increased genome size, RNA editing, intron gains, and gene losses—which were all likely acquired during the origin and early evolution of land plants. Overall, this genome and those of other 2 bryophytes show that mitochondrial genomes in early land plants, unlike their seed plant counterparts, exhibit a mixed mode of conservative yet dynamic evolution.

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References

  • Adams KL, Qiu YL, Stoutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci USA 99:9905–9912

    Article  PubMed  CAS  Google Scholar 

  • Adams KL, Rosenblueth M, Qiu Y-L, Palmer JD (2001) Multiple losses and transfers to the nucleus of two mitochondrial respiratory genes during angiosperm evolution. Genetics 158:1289–1300

    PubMed  CAS  Google Scholar 

  • Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang CY et al (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–1192

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706

    Article  PubMed  CAS  Google Scholar 

  • Beckert S, Steinhauser S, Muhle H, Knoop V (1999) A molecular phylogeny of bryophytes based on nucleotide sequences of the mitochondrial nad5 gene. Plant Syst Evol 218:179–192

    Article  CAS  Google Scholar 

  • Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34

    Article  PubMed  CAS  Google Scholar 

  • Burger G, Saint-Louis D, Gray MW, Lang BF (1999) Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11:1675–1694

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Clifton SW, Minx P, Fauron CMR, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C et al (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503

    Article  PubMed  CAS  Google Scholar 

  • Denovan-Wright EM, Nedelcu AM, Lee RW (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36:285–295

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JS (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Duff RJ, Villarreal JC, Cargill DC, Renzaglia KS (2007) Progress and challenges toward developing a phylogeny and classification of the hornworts. Bryologist 110:214–243

    Article  Google Scholar 

  • Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Lang BF, Burger G (2004) Mitochondria of protists. Annu Rev Genet 38:477–524

    Article  PubMed  CAS  Google Scholar 

  • Groth-Malonek M, Pruchner D, Grewe F, Knoop V (2005) Ancestors of trans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol Biol Evol 22:117–125

    Article  PubMed  CAS  Google Scholar 

  • Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) 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

    Article  PubMed  CAS  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907–5916

    Article  PubMed  CAS  Google Scholar 

  • Hiesel R, Combettes B, Brennicke A (1994) Evidence for RNA editing in mitochondria of all major groups of land plants except the Bryophyta. Proc Natl Acad Sci USA 91:629–633

    Article  PubMed  CAS  Google Scholar 

  • Kelch DG, Driskell A, Mishler BD (2004) Inferring phylogeny using genomic characters: a case study using land plant plastomes. In: Goffinet B, Hollowell V, Magill R (eds) Molecular systematics of bryophytes. Missouri Botanical Garden Press, St. Louis, MO, pp 3–11

    Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139

    Article  PubMed  CAS  Google Scholar 

  • Knoop V, Altwasser M, Brennicke A (1997) A tripartite group II intron in mitochondria of an angiosperm plant. Mol Gen Genet 255:269–276

    Article  PubMed  CAS  Google Scholar 

  • Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14

    Article  PubMed  CAS  Google Scholar 

  • Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucleic Acids Res 28:2571–2576

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mabberley DJ (1987) The plant book. Cambridge University Press, Cambridge, MA

    Google Scholar 

  • Malek O, Brennicke A, Knoop V (1997) Evolution of trans-splicing plant mitochondrial introns in pre-Permian times. Proc Natl Acad Sci USA 94:553–558

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Manhart JR, Palmer JD (1990) The gain of two chloroplast transfer-RNA introns marks the green algal ancestors of land plants. Nature 345:268–270

    Article  PubMed  CAS  Google Scholar 

  • Marechal-Drouard L, Guillemaut P, Cosset A, Arbogast M, Weber F, Weil J-H, Dietrich A (1990) Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res 18:3689–3696

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Mohr G, Perlman PS, Lambowitz AM (1993) Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucleic Acids Res 21:4991–4997

    Article  PubMed  CAS  Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T et al (1992a) 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

    Article  PubMed  CAS  Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Ohyama K (1992b) Transfer RNA genes in the mitochondrial genome from a liverwort, Marchantia polymorpha—the absence of chloroplast-like transfer-RNAs. Nucleic Acids Res 20:3773–3777

    Article  PubMed  CAS  Google Scholar 

  • Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nasuda S, Nakamura C, Mori N et al (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res 33:6235–6250

    Article  PubMed  CAS  Google Scholar 

  • Ohta N, Sato N, Kuroiwa T (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26:5190–5198

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Soltis D, Soltis P (1992) Large size and complex structure of mitochondrial DNA in two nonflowering land plants. Curr Genet 21:125–129

    Article  PubMed  CAS  Google Scholar 

  • Pombert JF, Otis C, Lemieux C, Turmel M (2004) The complete mitochondrial DNA sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the Chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Mol Biol Evol 21:922–935

    Article  PubMed  CAS  Google Scholar 

  • Pruchner D, Beckert S, Muhle H, Knoop V (2002) Divergent intron conservation in the mitochondrial nad2 gene: signatures for the three bryophyte classes (Mosses, liverworts, and hornworts) and the lycophytes. J Mol Evol 55:265–271

    Article  PubMed  CAS  Google Scholar 

  • Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Qiu Y-L, Li LB, Wang B, Chen ZD, Dombrovska O, Lee J, Kent L, Li RQ, Jobson RW, Hendry TA et al (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708

    Article  CAS  Google Scholar 

  • Qiu Y-L, Li LB, Wang B, Chen ZD, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J et al (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516

    Article  PubMed  CAS  Google Scholar 

  • Qiu Y-L, Palmer JD (2004) Many independent origins of trans splicing of a plant mitochondrial group II intron. J Mol Evol 59:80–89

    PubMed  CAS  Google Scholar 

  • Richard O, Bonnard G, Grienenberger JM, Kloareg B, Boyen C (1998) Transcription initiation and RNA processing in the mitochondria of the red alga Chondrus crispus: convergence in the evolution of transcription mechanisms in mitochondria. J Mol Biol 283:549–557

    Article  PubMed  CAS  Google Scholar 

  • Robbens S, Derelle E, Ferraz C, Wuyts J, Moreau H, Van de Peer Y (2007) The complete chloroplast and mitochondrial DNA sequence of Ostreococcus tauri: organelle genomes of the smallest eukaryote are examples of compaction. Mol Biol Evol 24:956–968

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Ezpeleta N, Brinkmann H, Burger G, Roger AJ, Gray MW, Philippe H, Lang BF (2007) Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. Curr Biol 17:1420–1425

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272:603–615

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tian XJ, Zheng J, Hu SN, Yu J (2006) The rice mitochondrial genomes and their variations. Plant Physiol 140:401–410

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW (1999) The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor: two radically different evolutionary patterns within green algae. Plant Cell 11:1717–1729

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002a) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275–11280

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002b) The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol Biol Evol 19:24–38

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2007) An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus. BMC Genomics 8:137

    Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366, 924 nucleotides. Nat Genet 15:57–61

    Article  PubMed  CAS  Google Scholar 

  • van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, Cambridge, MA

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285

    Article  PubMed  CAS  Google Scholar 

  • Wolff G, Plante I, Lang BF, Kuck U, Burger G (1994) Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii: gene content and genome organization. J Mol Biol 237:75–86

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank David K. Smith and Ken D. McFarland for helping obtaining the plant material; Jeffrey D. Palmer for making useful suggestions; and Jiayu Xue for assisting with data analyses. This work was supported by a National Science Foundation Early Career Award DEB 0332298 to Y.-L.Q. The M. aenigmaticus mitochondrial genome sequence reported in this study has been deposited in GenBank under accession number EU660574.

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Correspondence to Yin-Long Qiu.

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Libo Li and Bin Wang contributed equally to this work.

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Li, L., Wang, B., Liu, Y. et al. 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 (2009). https://doi.org/10.1007/s00239-009-9240-7

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