Plastomes of Bryophytes, Lycophytes and Ferns

  • Paul G. Wolf
  • Kenneth G. Karol
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 35)


We review current progress in our understanding of chloroplast genomes (plastomes) of liverworts, mosses, hornworts, lycophytes and monilophytes. We briefly cover some of the methods used to obtain complete nucleotide sequences of plastomes and we summarize the published sequences from the plant groups above. We explore some of the evolutionary changes that have occurred in terms of gene content, introns and position of the inverted repeat boundaries. We also discuss RNA editing, which is especially high in plastome genes of some non-seed land plants. We finish with a phylogenetic analysis of available plastome genes and we suggest some possible directions for future research.


Inverted Repeat Land Plant Large Single Copy Small Single Copy Leptosporangiate Fern 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Inverted repeat




Large single copy


Million years ago


Polymerase chain reaction


Pentatricopeptide repeat


Small single copy



This work was supported by NSF DEB1020660 and DEB1036466 to KGK and NSF DEB-0228432 to PGW.


  1. Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292CrossRefGoogle Scholar
  2. Bedbrook JR, Kolodner R (1979) Structure of chloroplast DNA. Annu Rev Plant Physiol Plant Mol Biol 30:593–620Google Scholar
  3. Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666PubMedCrossRefGoogle Scholar
  4. Bock R (2007) Structure, function, and inheritance of plastid genomes. Cell Mol Biol Plastids 19:29–63CrossRefGoogle Scholar
  5. Bock R, Timmis JN (2008) Reconstructing evolution: gene transfer from plastids to the nucleus. Bioessays 30:556–566PubMedCrossRefGoogle Scholar
  6. Boffey SA, Leech RM (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol 69:1387–1391PubMedCrossRefGoogle Scholar
  7. Bransteitter R, Prochnow C, Chen XJS (2009) The current structural and functional understanding of APOBEC deaminases. Cell Mol Life Sci 66:3137–3147PubMedCrossRefGoogle Scholar
  8. Brouard JS, Otis C, Lemieux C, Turmel M (2010) The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biol Evol 2:240–256PubMedCrossRefGoogle Scholar
  9. Cox CJ, Goffinet B, Shaw AJ, Boles SB (2004) Phylogenetic relationships among the mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomic compartments. Syst Bot 29:234–250CrossRefGoogle Scholar
  10. Cronn R, Liston A, Parks M, Gernandt DS, Shen R, Mockler T (2008) Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Res 36:e122PubMedCrossRefGoogle Scholar
  11. Der JP (2010) Genomic perspectives on evolution in bracken fern. Utah State University, LoganGoogle Scholar
  12. Donoghue MJ, Cracraft J (2004) Charting the tree of life. In: Donoghue MJ, Cracraft J (eds) Assembling the tree of life. Oxford University Press, New York, pp 1–4Google Scholar
  13. Duff RJ (2006) Divergent RNA editing frequencies in hornwort mitochondrial nad5 sequences. Gene 366:285–291PubMedCrossRefGoogle Scholar
  14. Duff RJ, Moore FBG (2005) Pervasive RNA editing among hornwort rbcL transcripts except Leiosporceros. J Mol Evol 61:571–578PubMedCrossRefGoogle Scholar
  15. Duff RJ, Schilling EE (2000) The chloroplast genome structure of the vascular plant Isoetes is similar to that of the liverwort Marchantia. Am Fern J 90:51–59CrossRefGoogle Scholar
  16. Duff RJ, Cargill DC, Villarreal JC, Renzaglia KS (2004) Phylogenetic relationships of the hornworts based on rbcL sequence data: novel relationships and new insights. Monogr Syst Bot Ann Missouri Bot Gard 98:41–58Google Scholar
  17. Duff RJ, Villarreal JC, Caagill DC, Renzaglia KS (2007) Progress and challenges toward developing a phylogeny and classification of the hornworts. Bryologist 110:214–243CrossRefGoogle Scholar
  18. 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 109:303–334CrossRefGoogle Scholar
  19. Gao L, Yi X, Yang YX, Su YJ, Wang T (2009) Complete chloroplast genome sequence of a tree fern Alsophila spinulosa: insights into evolutionary changes in fern chloroplast genomes. BMC Evol Biol 9:130PubMedCrossRefGoogle Scholar
  20. Goffinet B, Buck WR (2004) Systematics of the Bryophyta (Mosses): from molecules to a revised classification. Monog Syst Bot Missouri Bot Gard 98:203–223Google Scholar
  21. Goffinet B, Wickett NJ, Werner O, Ros RM, Shaw AJ, Cox CJ (2007) Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae (Bryophyta). Ann Bot 99:747–753PubMedCrossRefGoogle Scholar
  22. Goulding SE, Olmstead RG, Morden CW, Wolfe KH (1996) Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet 252:195–206PubMedCrossRefGoogle Scholar
  23. 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 22:117–125PubMedCrossRefGoogle Scholar
  24. Hammani K, Okuda K, Tanz SK, Chateigner-Boutin AL, Shikanai T, Small I (2009) A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell 21:3686–3699PubMedCrossRefGoogle Scholar
  25. Hirose A, Kusumegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262:462–467PubMedCrossRefGoogle Scholar
  26. Holton TA, Pisani D (2010) Deep genomic-scale analyses of the Metazoa reject Coelomata: evidence from single- and multigene families analyzed under a supertree and supermatrix paradigm. Genome Biol Evol 2:310–324PubMedCrossRefGoogle Scholar
  27. Jansen RK, Raubeson LA, Boore JL, dePamphilis CW, Chumley TW, Haberle RC, Wyman SK, Alverson AJ, Peery R, Herman SJ (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Methods Enzymol 395:348–384PubMedCrossRefGoogle Scholar
  28. Jansen RK, Cai Z, Raubeson LA, Daniell H, dePamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S-B, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374PubMedCrossRefGoogle Scholar
  29. Jobson RW, Qiu YL (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct 3:43PubMedCrossRefGoogle Scholar
  30. Karol KG, Arumuganathan K, Boore JL, Duffy AM, Everett KDE, Hall JD, Hansen SK, Kuehl JV, Mandoli DF, Mishler BD, Olmstead RG, Renzaglia KS, Wolf PG (2010) Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages. BMC Evol Biol 10:321PubMedCrossRefGoogle Scholar
  31. Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Press, Washington, DCGoogle Scholar
  32. Kobayashi Y, Matsuo M, Sakamoto K, Wakasugi T, Yamada K, Obokata J (2008) Two RNA editing sites with cis-acting elements of moderate sequence identity are recognized by an identical site-recognition protein in tobacco chloroplasts. Nucleic Acids Res 36:311–318PubMedCrossRefGoogle Scholar
  33. Kolodner R, Tewari KK (1975a) Chloroplast DNA from higher plants replicates by both the Cairns and the rolling circle mechanism. Nature 256:708–711PubMedCrossRefGoogle Scholar
  34. Kolodner R, Tewari KK (1975b) Presence of displacement loops in covalently closed circular chloroplast deoxyribonucleic-acid from higher-plants. J Biol Chem 250:8840–8847PubMedGoogle Scholar
  35. Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330PubMedCrossRefGoogle Scholar
  36. Kranz HD, Huss VAR (1996) Molecular evolution of pteridophytes and their relationship to seed plants: evidence from complete 18S rRNA gene sequences. Plant Syst Evol 202:1–11CrossRefGoogle Scholar
  37. Krishnan NM, Rao BJ (2009) A comparative approach to elucidate chloroplast genome replication. BMC Genomics 10:237PubMedCrossRefGoogle Scholar
  38. Krishnan NM, Seligmann H, Raina SZ, Pollock DD (2004) Detecting gradients of asymmetry in site-specific substitutions in mitochondrial genomes. DNA Cell Biol 23:707–714PubMedCrossRefGoogle Scholar
  39. Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003a) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423PubMedCrossRefGoogle Scholar
  40. Kugita M, Kaneko A, Yamamoto Y, Takeya Y, Matsumoto T, Yoshinaga K (2003b) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res 31:716–721PubMedCrossRefGoogle Scholar
  41. Kunnimalaiyaan M, Nielsen BL (1997) Chloroplast DNA replication: mechanism, enzymes and replication origins. J Plant Biochem Biotech 6:1–7Google Scholar
  42. Miller MA, Holder MT, Vos R, Midford PE, Liebowitz T, Chan L, Hoover P, Warnow T (2009) The CIPRES Portals.
  43. Mishler BD, Churchill SP (1984) A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406–424CrossRefGoogle Scholar
  44. Newton AE, Cox CJ, Duckett JG, Wheeler JA, Goffinet B, Hedderson TAJ, Mishler BD (2000) Evolution of the major moss lineages: phylogenetic analyses based on multiple gene sequences and morphology. Bryologist 103:187–211CrossRefGoogle Scholar
  45. Nickrent DL, Parkinson CL, Palmer JD, Duff RJ (2000) Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol Biol Evol 17:1885–1895PubMedCrossRefGoogle Scholar
  46. 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 223:1–7PubMedCrossRefGoogle Scholar
  47. 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 322:572–574CrossRefGoogle Scholar
  48. Okuda K, Shikanai T (2008) PPR proteins function as a trans-factor in chloroplast RNA editing. In: Allen JF, Gantt E, Golbeck J (eds) Photosynthesis energy from the sun. Springer, New York, pp 1211–1214Google Scholar
  49. Oldenburg DJ, Bendich AJ (2004a) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335:953–970PubMedCrossRefGoogle Scholar
  50. Oldenburg DJ, Bendich AJ (2004b) Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. J Mol Biol 344:1311–1330PubMedCrossRefGoogle Scholar
  51. Oliver MJ, Murdock AG, Mishler BD, Kuehl JV, Boore JL, Mandoli DF, Everett KDE, Wolf PG, Duffy AM, Karol KG (2010) Chloroplast genome sequence of the moss Tortula ruralis: gene content, polymorphism, and structural arrangement relative to other green plant chloroplast genomes. BMC Genomics 11:143PubMedCrossRefGoogle Scholar
  52. Palmer JD (1983) Chloroplast DNA exists in 2 orientations. Nature 301:92–93CrossRefGoogle Scholar
  53. Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354PubMedCrossRefGoogle Scholar
  54. Palmer JD, Stein DB (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10:823–833CrossRefGoogle Scholar
  55. Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622PubMedCrossRefGoogle Scholar
  56. 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. Amer J Bot 91:1582–1598CrossRefGoogle Scholar
  57. Qiu YL (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306Google Scholar
  58. Qiu YL, Cho YR, Cox JC, Palmer JD (1998) The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671–674PubMedCrossRefGoogle Scholar
  59. Qiu YL, 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 103:15511–15516PubMedCrossRefGoogle Scholar
  60. Qiu YL, 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 168:691–708CrossRefGoogle Scholar
  61. Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699PubMedCrossRefGoogle Scholar
  62. Renzaglia KS, Garbary DJ (2001) Motile gametes of land plants: diversity, development, and evolution. Crit Rev Plant Sci 20:107–213Google Scholar
  63. Renzaglia KS, Schuette S, Duff RJ, Ligrone R, Shaw AJ, Mishler BD, Duckett JG (2007) Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110:179–213CrossRefGoogle Scholar
  64. Roper JM, Hansen SK, Wolf PG, Karol KG, Mandoli DF, Everett KDE, Kuehl J, Boore JL (2007) The complete plastid genome sequence of Angiopteris evecta (G. Forst.) Hoffm. (Marattiaceae). Am Fern J 97:95–106CrossRefGoogle Scholar
  65. Rothwell GW, Nixon KC (2006) How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? Int J Plant Sci 167:737–749CrossRefGoogle Scholar
  66. Rowan BA, Oldenburg DJ, Bendich AJ (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J Exp Bot 61:2575–2588PubMedCrossRefGoogle Scholar
  67. Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P (2010) Early middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol 188:365–369PubMedCrossRefGoogle Scholar
  68. Sato N, Terasawa K, Miyajima K, Kabeya Y (2003) Organization, developmental dynamics, and evolution of plastid nucleoids. Int Rev Cytol Surv Cell Biol 232:217–262Google Scholar
  69. Schneider H, Smith AR, Pryer KM (2009) Is morphology really at odds with molecules in estimating fern phylogeny? Syst Bot 34:455–475CrossRefGoogle Scholar
  70. Shalchian-Tabrizi K, Minge MA, Espelund M, Orr R, Ruden T, Jakobsen KS, Cavalier-Smith T (2008) Multigene phylogeny of Choanozoa and the origin of animals. PLoS One 3:e2098PubMedCrossRefGoogle Scholar
  71. Shaw J, Renzaglia K (2004) Phylogeny and diversification of bryophytes. Amer J Bot 91:1557–1581CrossRefGoogle Scholar
  72. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049PubMedGoogle Scholar
  73. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  74. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  75. Stein DB, Palmer JD, Thompson WF (1986) Structural evolution and flip-flop recombination of chloroplast DNA in the fern genus Osmunda. Curr Genet 10:835–841CrossRefGoogle Scholar
  76. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155PubMedCrossRefGoogle Scholar
  77. Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331PubMedCrossRefGoogle Scholar
  78. Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921PubMedCrossRefGoogle Scholar
  79. 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, transpositions and many gene losses. J Plant Res 120:281–290PubMedCrossRefGoogle Scholar
  80. Turmel M, Pombert J-F, Charlebois P, Otis C, Lemieux C (2007) The green algal ancestry of land plants as revealed by the chloroplast genome. Int J Plt Sci 168:679–689CrossRefGoogle Scholar
  81. Wahrmund U, Rein T, Müller KF, Groth-Malonek M, Knoop V (2009) Fifty mosses on five trees: comparing phylogenetic information in three types of non-coding mitochondrial DNA and two chloroplast loci. Plant Syst Evol 282:241–255CrossRefGoogle Scholar
  82. Wahrmund U, Quandt D, Knoop V (2010) The phylogeny of mosses – addressing open issues with a new mitochondrial locus: group I intron cobi420. Mol Phylogen Evol 54:417–426CrossRefGoogle Scholar
  83. Wickett NJ, Fan Y, Lewis PO, Goffinet B (2008a) Distribution and evolution of pseudogenes, gene losses, and a gene rearrangement in the plastid genome of the nonphotosynthetic liverwort, Aneura mirabilis (metzgeriales, jungermanniopsida). J Mol Evol 67:111–122PubMedCrossRefGoogle Scholar
  84. Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, dePamphilis CW, Boore JL, Goffinet B (2008b) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25:393–401PubMedCrossRefGoogle Scholar
  85. Wolf PG, Rowe CA, Sinclair RB, Hasebe M (2003) Complete nucleotide sequence of the chloroplast genome from a leptosporangiate fern, Adiantum capillus-veneris L. DNA Res 10:59–65PubMedCrossRefGoogle Scholar
  86. Wolf 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 339:89–97PubMedCrossRefGoogle Scholar
  87. 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 350:117–128PubMedCrossRefGoogle Scholar
  88. Wolf PG, Roper JM, Duffy AM (2010) The evolution of chloroplast genome structure in ferns. Genome 53:731–738PubMedCrossRefGoogle Scholar
  89. Wolf PG, Der JP, Duffy AM, Jacobson JB, Grusz AL, Pryer KM (2011) The evolution of chloroplast genes and genomes in ferns. Plant Mol Biol 76:251–261Google Scholar
  90. Wolfe KH, Morden CW, Palmer JD (1992) Functions and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department of BiologyUtah State UniversityLoganUSA
  2. 2.The Lewis B. and Dorothy Cullman Program for Molecular Systematics StudiesThe New York Botanical GardenBronxUSA

Personalised recommendations