Conservative and Dynamic Evolution of Mitochondrial Genomes in Early Land Plants

  • Chapter
  • First Online:
Genomics of Chloroplasts and Mitochondria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 35))

Summary

Early land plant mitochondrial genomes (chondromes) might have captured important changes of mitochondrial genome evolution when photosynthetic eukaryotes colonized land in a unprecedented scale, and thus deserve special attention in investigation of plant mitochondrial genomes. The chondromes of land plants that are well adapted to the terrestrial environment, namely seed plants, show many derived characteristics, including large genome size variation, frequent occurrence of intra-genomic rearrangements, abundant introns and high levels of RNA editing. In contrast, the chondromes of charophytes, the closest algal relatives of land plants, are still largely ancestral in these aspects, resembling chondromes of early eukaryotes. Several recently sequenced chondromes from basal land plants including liverworts, mosses, hornworts and lycophytes have provided fresh insights into mitochondrial genome evolution of early land plants. Comparative analyses of these genomes have identified lycophytes, which represent the most ancient extant vascular plants, as the major point of change in plant mitochondrial genome evolution, with long conserved mitochondrial gene synteny largely disrupted. The chondromes of bryophytes are conservative in gene order, but rather dynamic in intron content. The gene contents and RNA editing levels also show wide variation from lineage to lineage. Overall, the mitochondrial genomes experienced dynamic evolutionary changes during the origin and early evolution of land plants when the major lineages of bryophytes and vascular plants appeared, but have remained relatively conservative afterwards except in vascular plants.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

bp –:

Base pairs;

kbp –:

Kilobase pairs

References

  • 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 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 27:1436–1448

    Article  PubMed  CAS  Google Scholar 

  • Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011a) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–2513

    Article  PubMed  CAS  Google Scholar 

  • Andre C, Levy A, Walbot V (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet 8:128–132

    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

    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 et al (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503

    Article  PubMed  CAS  Google Scholar 

  • Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno M, Buss LW, Schierwater B (2006) Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proc Natl Acad Sci USA 103:8751–8756

    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 

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

    Article  Google Scholar 

  • Gillham NW (1994) Organelle genes and genomes. Oxford University Press, New York

    Google Scholar 

  • Goffinet B, Cox CJ, Shaw AJ, Hedderson TAJ (2001) The bryophyta (mosses): systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Ann Bot 87:191–208

    Article  CAS  Google Scholar 

  • Goremykin VV, Salamini F, Velasco R, Viola R (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26:99–110

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 15:5093–5104

    Article  Google Scholar 

  • Grewe F, Herres S, Viehoever P, Polsakiewicz M, Weisshaar B, Knoop V (2010) A unique transcriptome: 1728 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Res 39:2890–2902

    Google Scholar 

  • Grewe F, Herres S, Viehoever P, Polsakiewicz M, Weisshaar B et al (2011) A unique transcriptome: 1728 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Res 39:2890–2902

    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 

  • Hecht J, Grewe F, Knoop V (2011) Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biol Evol 3:344–358

    Google Scholar 

  • Hernick LV, Landing E, Bartowski KE (2008) Earth’s oldest liverworts – Metzgeriothallus sharonae sp. nov. from the Middle Devonian (Giventian) of ­eastern New York, USA. Rev Palaeobot Palynol 148:154–162

    Article  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 

  • Jobson RW, Qiu Y-L (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct 3:43

    Article  PubMed  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  PubMed  CAS  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 

  • Kubo N, Arimura S-I (2010) Discovery of a functional rpl10 gene in diverse plant mitochondrial genomes and its functional replacement by a nuclear gene for chloroplast RPL10 in two lineages of angiosperms. DNA Res 17:1–9

    Article  PubMed  CAS  Google Scholar 

  • Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A et al (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 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Xue J-Y, Wang B, Li L, Qiu Y-L (2011) The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii: dynamic and conservative evolution. PLoS One 6(10):e25836

    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 

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

    Article  PubMed  Google Scholar 

  • Mishler BD, Churchill SP (1984) A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406–424

    Article  Google Scholar 

  • Mower JP, Bonen L (2009) Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae. BMC Evol Biol 9:265

    Article  PubMed  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G et al (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445

    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, 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

    Article  PubMed  CAS  Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574

    Article  CAS  Google Scholar 

  • Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97

    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 

  • Qiu Y-L, Palmer JD (2004) Many independent origins of trans splicing of a plant mitochondrial group 2 intron. J Mol Evol 59:80–89

    PubMed  CAS  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, 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

    Article  PubMed  CAS  Google Scholar 

  • Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699

    Article  PubMed  CAS  Google Scholar 

  • Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V (2009) RNA editing: 11 sites only in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics 281:473–481

    Article  PubMed  Google Scholar 

  • Schuster W, Brennicke A (1994) The plant mitochondrial genome – physical structure, information content, RNA editing, and gene migration to the nucleus. Ann Rev Plant Physiol Plant Mol Biol 45:61–78

    Article  CAS  Google Scholar 

  • Sloan DB, Alverson AJ, Storchova H, Palmer JD, Taylor DR (2010) Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol 10:274

    Article  PubMed  Google Scholar 

  • Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312

    Article  PubMed  CAS  Google Scholar 

  • Stewart WN (1983) Paleobotany and the evolution of plants. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S et al (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 

  • 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

    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

    Article  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

    Article  PubMed  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 

  • Wang B, Xue J-Y, Li L, Liu L, Qiu Y-L (2009) The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55:601–609

    Article  PubMed  CAS  Google Scholar 

  • Ward B, Anderson R, Bendich A (1981) The size of the mitochondrial genome is large and variable in a family of plants. Cell 25:793–803

    Article  PubMed  CAS  Google Scholar 

  • Xue J-Y, Liu Y, Li L, Wang B, Qiu Y-L (2010) The complete mitochondrial genome sequence of the hornwort Phaeoceros laevis: retention of many ancient pseudogenes and conservative evolution of mitochondrial genomes in hornworts. Curr Genet 56:53–61

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We thank Ken D. McFarland, Blanka Shaw, Jon Shaw, and David K. Smith for help with obtaining plant material, and Volker Knoop for informative discussion. This work was supported by NSF grants DEB 0531689 and 0332298 to YLQ.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yin-Long Qiu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Liu, Y., Wang, B., Li, L., Qiu, YL., Xue, J. (2012). Conservative and Dynamic Evolution of Mitochondrial Genomes in Early Land Plants. In: Bock, R., Knoop, V. (eds) Genomics of Chloroplasts and Mitochondria. Advances in Photosynthesis and Respiration, vol 35. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2920-9_7

Download citation

Publish with us

Policies and ethics

Navigation