Plant Molecular Biology

, 71:627

Unparalleled GC content in the plastid DNA of Selaginella



One of the more conspicuous features of plastid DNA (ptDNA) is its low guanine and cytosine (GC) content. As of February 2009, all completely-sequenced plastid genomes have a GC content below 43% except for the ptDNA of the lycophyte Selaginella uncinata, which is 55% GC. The forces driving the S. uncinata ptDNA towards G and C are undetermined, and it is unknown if other Selaginella species have GC-biased plastid genomes. This study presents the complete ptDNA sequence of Selaginella moellendorffii and compares it with the previously reported S. uncinata plastid genome. Partial ptDNA sequences from 103 different Selaginella species are also described as well as a significant proportion of the S. moellendorffii mitochondrial genome. Moreover, S. moellendorffii express sequence tags are data-mined to estimate levels of plastid and mitochondrial RNA editing. Overall, these data are used to show that: (1) there is a genus-wide GC bias in Selaginella ptDNA, which is most pronounced in South American articulate species; (2) within the Lycopsida class (and among plants in general), GC-biased ptDNA is restricted to the Selaginella genus; (3) the cause of this GC bias is arguably a combination of reduced AT-mutation pressure relative to other plastid genomes and a large number of C-to-U RNA editing sites; and (4) the mitochondrial DNA (mtDNA) of S. moellendorffii is also GC biased (even more so than the ptDNA) and is arguably the most GC-rich organelle genome observed to date—the high GC content of the mtDNA also appears to be influenced by RNA editing. Ultimately, these findings provide convincing support for the earlier proposed theory that the GC content of land-plant organelle DNA is positively correlated and directly connected to levels of organelle RNA editing.


Chloroplast Lycophyte Nucleotide composition GC content RNA editing 

Supplementary material


  1. Banks JA (2009) Selaginella and 400 million years of separation. Annu Rev Plant Biol 60:223–238CrossRefPubMedGoogle Scholar
  2. Covello PS, Gray MW (1993) On the evolution of RNA editing. Trends Genet 9:265–268CrossRefPubMedGoogle Scholar
  3. Dybvig K, Voelker LL (1996) Molecular biology of mycoplasmas. Ann Rev Microbiol 50:25–57CrossRefGoogle Scholar
  4. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953–971CrossRefPubMedGoogle Scholar
  5. Eyre-Walker A (1998) Problems with parsimony in sequences of biased base composition. J Mol Evol 47:686–690CrossRefPubMedGoogle Scholar
  6. Freyer R, Kiefer-Meyer MC, Kössel H (1997) Occurrence of plastid RNA editing in all major lineages of land plants. Proc Natl Acad Sci 94:6285–6290CrossRefPubMedGoogle Scholar
  7. Glover KE, Spencer DF, Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276:639–648CrossRefPubMedGoogle Scholar
  8. Howe CJ, Barbrook AC, Koumandou VL, Nisbet RER, Symington HA, Wightman TF (2003) Evolution of the chloroplast genome. Philos Trans R Soc Lond B Biol Sci 358:99–107CrossRefPubMedGoogle Scholar
  9. Jobson RW, Qiu YL (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct 3:43CrossRefPubMedGoogle Scholar
  10. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  11. Khakhlova O, Bock R (2006) Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J 46:85–94CrossRefPubMedGoogle Scholar
  12. Korall P, Kenrick P (2002) Phylogenetic relationships in Selaginellaceae based on rbcL sequences. Am J Bot 89:506–517CrossRefGoogle Scholar
  13. Korall P, Kenrick P (2004) The phylogenetic history of Selaginellaceae based on DNA sequences from the plastid and nucleus: extreme substitution rates and rate heterogeneity. Mol Phylogenet Evol 31:852–864CrossRefPubMedGoogle Scholar
  14. Korall P, Kenrick P, Therrien JP (1999) Phylogeny of Selaginellaceae: evaluation of generic/subgeneric relationships based on rbcL gene sequences. Int J Plant Sci 160:585–594CrossRefGoogle Scholar
  15. Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423CrossRefPubMedGoogle Scholar
  16. Kusumi J, Tachida H (2005) Compositional properties of green-plant plastid genomes. J Mol Evol 60:417–425CrossRefPubMedGoogle Scholar
  17. Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons B, Bowman S, Archibald JM (2007) Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci USA 104:19908–19913CrossRefPubMedGoogle Scholar
  18. Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730CrossRefPubMedGoogle Scholar
  19. Mabberley DJ (1997) The plant-book: a portable dictionary of the vascular plants. Cambridge University Press, CambridgeGoogle Scholar
  20. Malek O, Lättig K, Hiesel R, Brennicke A, Knoop V (1996) RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J 15:1403–1411PubMedGoogle Scholar
  21. Mallet M, Lee RW (2006) Identification of three distinct Polytmella lineages based on mitochondrial DNA features. J Eukaryot Microbiol 53:79–84CrossRefPubMedGoogle Scholar
  22. Miyata Y, Sugita M (2004) Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J Plant Physiol 161:113–115CrossRefPubMedGoogle Scholar
  23. Modern CW, Wofe K, dePamphilis CW, Palmer JD (1991) Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288Google Scholar
  24. Morton BR (1993) Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability. J Mol Evol 37:273–280CrossRefPubMedGoogle Scholar
  25. Morton BR (1998) Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. J Mol Evol 46:449–459CrossRefPubMedGoogle Scholar
  26. Ogata H, Audic S, Renesto-Audiffren P et al (2001) Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293:2093–2098CrossRefPubMedGoogle Scholar
  27. Palmer JD, Stein DB (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10:823–833CrossRefGoogle Scholar
  28. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598CrossRefGoogle Scholar
  29. Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699CrossRefPubMedGoogle Scholar
  30. Richly E, Leister D (2004) NUPTs in sequenced eukaryotes and their genomic organization in relation to NUMTs. Mol Biol Evol 21:1972–1980CrossRefPubMedGoogle Scholar
  31. Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V (2009) RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics 281:473–481CrossRefPubMedGoogle Scholar
  32. Smith DR, Lee RW (2008a) Mitochondrial genome of the colorless green alga Polytomella capuana: a linear molecule with an unprecedented GC content. Mol Biol Evol 25:487–496CrossRefPubMedGoogle Scholar
  33. Smith DR, Lee RW (2008b) Nucleotide diversity in the mitochondrial and nuclear compartments of Chlamydomonas reinhardtii: investigating the origins of genome architecture. BMC Evol Biol 8:156CrossRefPubMedGoogle Scholar
  34. Smith DR, Lee RW (2009) The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10:132CrossRefPubMedGoogle Scholar
  35. Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V (1999) Plant mitochondrial RNA editing. J Mol Evol 48:303–312CrossRefPubMedGoogle Scholar
  36. Supek F, Vlahovicek K (2004) INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics 20:2329–2330CrossRefPubMedGoogle Scholar
  37. Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921CrossRefPubMedGoogle Scholar
  38. Tsuji S, Ueda K, Nishiyama T, Hasebe M, Yoshikawa S, Konagaya A, Nishiuchi T, Yamaguchi K (2007) The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transposition and many gene losses. J Plant Res 120:281–290CrossRefPubMedGoogle Scholar
  39. Wolf PG, Karol KG, Mandoli DF, Kuehl J, Arumuganathan K, Ellis MW, Mishler BD, Kelch DG, Olmstead RG, Boore JL (2005) The first complete chloroplast genome sequence of a lycophyte Huperzia lucidula (Lycopodiaceae). Gene 350:117–128CrossRefPubMedGoogle Scholar
  40. Wolfe PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:87–89Google Scholar
  41. Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

Personalised recommendations