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.
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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
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
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
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
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
Andre C, Levy A, Walbot V (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet 8:128–132
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
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 et al (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503
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
Denovan-Wright EM, Nedelcu AM, Lee RW (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36:285–295
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
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
Gillham NW (1994) Organelle genes and genomes. Oxford University Press, New York
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
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
Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481
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
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
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
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
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
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
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
Hernick LV, Landing E, Bartowski KE (2008) Earth’s oldest liverworts – Metzgeriothallus sharonae sp. nov. from the Middle Devonian (Giventian) of Âeastern New York, USA. Rev Palaeobot Palynol 148:154–162
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
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
Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353
Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, Washington, DC
Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139
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
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
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
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
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
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
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
Mishler BD, Churchill SP (1984) A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406–424
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
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
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
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
Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354
Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97
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, Palmer JD (2004) Many independent origins of trans splicing of a plant mitochondrial group 2 intron. J Mol Evol 59:80–89
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
Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699
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
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
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
Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312
Stewart WN (1983) Paleobotany and the evolution of plants. Cambridge University Press, Cambridge, UK
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
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
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
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
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
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
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
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
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
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
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
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.
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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
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