Advertisement

Plant Systematics and Evolution

, Volume 282, Issue 3–4, pp 241–255 | Cite as

Fifty mosses on five trees: comparing phylogenetic information in three types of non-coding mitochondrial DNA and two chloroplast loci

  • Ute Wahrmund
  • Theresia Rein
  • Kai F. Müller
  • Milena Groth-Malonek
  • Volker Knoop
Original Article

Abstract

Given the frequent genomic recombinations in plant mitochondrial DNA, intergenic regions of this organelle genome had so far not been considered as loci of potential phylogenetic information. Based on the recent evidence that an evolutionary ancient mitochondrial nad5-nad4 gene continuum is conserved in bryophytes we have compiled a dataset for a phylogenetically wide sampling of 50 mosses covering this intergenic region. The length of the intergenic region was generally in the range of 585 (Diphyscium) to 646 bp (Tomentypnum) with rare exceptions, for example all Polytrichales taxa showing a 200 bp deletion as an apparent synapomorphy of this order. Phylogenetic information in the novel marker sequence was compared with that of a nad5 gene region containing a group I intron and a nad2 gene region containing a group II intron as well as with two widely sampled chloroplast data sets, rbcL and rps4. Indel evolution in the three types of non-coding mitochondrial sequences is obviously more taxon-dependent than locus-dependent, indicating lineage-specific insertion/deletion rates. For example, larger sequence deletions are a general feature in Schistostega and Tetraphis. Although confidence for particular nodes in the phylogeny was found to vary among data sets, gene trees were essentially without conflict with respect to well-supported ones and add up in information towards a reasonably well-resolved moss phylogeny. However, while a consensus on the latter is clearly emerging, sufficient confidence is still lacking for the first dichotomies among the arthrodontous mosses leading into subclasses Bryidae, Dicranidae and Funariidae and the relative placement of nematodontous mosses (Polytrichales and Tetraphidales) on the backbone of early moss phylogeny.

Keywords

Bryophytes Group I intron Group II intron Indels Intergenic region Mitochondrial DNA Mosses Phylogeny RNA editing 

Abbreviations

bp

Base pairs

mtDNA

Mitochondrial DNA

Notes

Acknowledgments

The authors are very grateful to Drs. Jan-Peter Frahm, Bonn; Bernard Goffinet, Storrs CT; Hermann Muhle, Ulm; Yin-Long Qiu, Ann Arbor MI and Dietmar Quandt, Dresden, who made biological material or DNA samples, respectively, available. Financial support through the Deutsche Forschungsgemeinschaft (DFG) is gratefully acknowledged. The last author is grateful to the Deutsche Bahn for continuous, reliable and comfortable ICE transportation commuting between Bonn and Ulm on a weekly basis also in preparation of the present manuscript.

References

  1. Beckert S, Steinhauser S, Muhle H, Knoop V (1999) A molecular phylogeny of bryophytes based on nucleotide sequences of the mitochondrial nad5 gene. Pl Syst Evol 218:179–192CrossRefGoogle Scholar
  2. Beckert S, Muhle H, Pruchner D, Knoop V (2001) The mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis of early land plants: a comparative analysis in mosses. Molec Phylogenet Evol 18:117–126CrossRefPubMedGoogle Scholar
  3. Bell NE, Quandt D, O’Brien TJ, Newton AE (2007) Taxonomy and phylogeny in the earliest diverging pleurocarps: square holes and bifurcating pegs. Bryologist 110:533–560CrossRefGoogle Scholar
  4. Budke JM, Goffinet B (2006) Phylogenetic analyses of Timmiaceae (Bryophyta: Musci) based on nuclear and chloroplast sequence data. Syst Bot 31:633–641CrossRefGoogle Scholar
  5. Budke JM, Jones CS, Goffinet B (2007) Development of the enigmatic peristome of Timmia megapolitana (Timmiaceae; Bryophyta). Amer J Bot 94:460–467CrossRefGoogle Scholar
  6. Cox CJ, Goffinet B, Newton AE, Shaw AJ, Hedderson TAJ (2000) Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclear and chloroplast DNA sequences. Bryologist 103:224–241CrossRefGoogle Scholar
  7. 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
  8. Crandall-Stotler B, Forrest LL, Stotler RE (2005) Evolutionary trends in the simple thalloid liverworts (Marchantiophyta, Jungermanniopsida subclass Metzgeriidae). Taxon 54:299–316Google Scholar
  9. Davis EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae: Marchantiophyta). In: Goffinet B, Hollowell V, Magill R (eds) Molecular systematics of bryophytes. Missouri Botanical Garden Press, St Louis, pp 61–86Google Scholar
  10. Forrest LL, Crandall-Stotler BJ (2005) Progress towards a robust phylogeny for the liverworts, with particular focus on the simple thalloids. J Hattori Bot Lab 97:127–159Google Scholar
  11. Goffinet B, Buck WR (2004) Systematics of the bryophyta (mosses): from molecules to a revised classification. In: Goffinet B, Hollowell V, Magill R (eds) Molecular systematics of bryophytes. Missouri Botanical Garden Press, St Louis, pp 205–239Google Scholar
  12. Goffinet B, Cox CJ (2000) Phylogenetic relationships among basal-most arthrodontous mosses with special emphasis on the evolutionary significance of the Funariineae. Bryologist 103:212–223CrossRefGoogle Scholar
  13. Goffinet B, Cox CJ, Shaw AJ, Hedderson TAJ (2001) The bryophyta (mosses): systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Ann Bot 87:191–208CrossRefGoogle Scholar
  14. Goffinet B, Wickett NJ, Shaw AJ, Cox CJ (2005) Phylogenetic significance of the rpoA loss in the chloroplast genome of mosses. Taxon 54:353–360Google Scholar
  15. 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 (Lond) 99:747–753CrossRefGoogle Scholar
  16. Groth-Malonek M, Rein T, Wilson R, Groth H, Heinrichs J, Knoop V (2007) Different fates of two mitochondrial gene spacers in early land plant evolution. Int J Pl Sci 168:709–717CrossRefGoogle Scholar
  17. Hedderson TA, Murray DJ, Cox CJ, Nowell TL (2004) Phylogenetic relationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences. Syst Bot 29:29–41CrossRefGoogle Scholar
  18. Hyvönen J, Koskinen S, Smith Merrill GL, Hedderson TA, Stenroos S (2004) Phylogeny of the Polytrichales (Bryophyta) based on simultaneous analysis of molecular and morphological data. Molec Phylogenet Evol 31:915–928CrossRefPubMedGoogle Scholar
  19. Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353CrossRefPubMedGoogle Scholar
  20. Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139CrossRefPubMedGoogle Scholar
  21. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf 5:150–163CrossRefGoogle Scholar
  22. La Farge C, Mishler BD, Wheeler JA, Wall DP, Johannes K, Schaffer S, Shaw AJ (2000) Phylogenetic relationships within the haplolepideous mosses. Bryologist 103:257–276CrossRefGoogle Scholar
  23. La Farge C, Shaw AJ, Vitt DH (2002) The circumscription of the Dicranaceae (Bryopsida) based on the chloroplast regions trnL-trnF and rps4. Syst Bot 27:435–452Google Scholar
  24. Löhne C, Borsch T (2005) Molecular evolution and phylogenetic utility of the petD group II intron: a case study in basal angiosperms. Molec Biol Evol 22:317–332CrossRefPubMedGoogle Scholar
  25. Maddison WP, Maddison DR (2003) Mesquite: a modular system for evolutionary analysis. [1.0]Google Scholar
  26. Magombo ZLK (2003) The phylogeny of basal peristomate mosses: evidence from cpDNA, and implications for peristome evolution. Syst Bot 28:24–38Google Scholar
  27. Müller K (2004) PRAP-computation of Bremer support for large data sets. Molec Phylogenet Evol 31:780–782CrossRefPubMedGoogle Scholar
  28. Müller K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Appl Bioinformatics 4:65–69CrossRefPubMedGoogle Scholar
  29. Müller K (2006) Incorporating information from length-mutational events into phylogenetic analysis. Molec Phylogenet Evol 38:667–676CrossRefPubMedGoogle Scholar
  30. Quandt D, Bell N, Stech M (2007) Unravelling the knot: the Pulchrinodaceae fam. nov (Bryales). Nova Hedwigia 21–39Google Scholar
  31. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinf 19:1572–1574CrossRefGoogle Scholar
  32. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  33. Simmons MP, Müller K, Norton AP (2007) The relative performance of indel-coding methods in simulations. Molec Phylogenet Evol 44:724–740CrossRefPubMedGoogle Scholar
  34. Sugita M, Sugiura C, Arikawa T, Higuchi M (2004) Molecular evidence of an rpoA gene in the basal moss chloroplast genomes: rpoA is a useful molecular marker for phylogenetic analysis of mosses. Hikobia 14:171–175Google Scholar
  35. 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 the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331CrossRefPubMedGoogle Scholar
  36. Swofford DL (2003) PAUP* Phylogenetic analysis using parsimony (* and Other Methods). Version 4. Sinauer Assoc., Sunderland, MA. [4]. Sunderland, MA, Sinauer AssociatesGoogle Scholar
  37. Worberg A, Quandt D, Barniske A-M, Löhne C, Hilu KW, Borsch T (2007) Phylogeny of basal eudicots: insights from non-coding and rapidly evolving DNA. Organisms Diversity & Evolution 7:55–77CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Ute Wahrmund
    • 1
  • Theresia Rein
    • 1
  • Kai F. Müller
    • 2
  • Milena Groth-Malonek
    • 1
  • Volker Knoop
    • 1
  1. 1.IZMB, Institut für Zelluläre und Molekulare Botanik, Abt. Molekulare EvolutionUniversität BonnBonnGermany
  2. 2.Nees-Institut für Biodiversität der PflanzenUniversität BonnBonnGermany

Personalised recommendations