Journal of Molecular Evolution

, Volume 35, Issue 4, pp 292–303

Relative rates of nucleotide substitution at the rbcl locus of monocotyledonous plants

  • Brandon S. Gaut
  • Spencer V. Muse
  • W. Dennis Clark
  • Michael T. Clegg
Article

Summary

We subjected 35 rbcL nucleotide sequences from monocotyledonous taxa to maximum likelihood relative rate tests and estimated relative differences in rates of nucleotide substitution between groups of sequences without relying on knowledge of divergence times between taxa. Rate tests revealed that there is a hierarchy of substitution rate at the rbcL locus within the monocots. Among the taxa analyzed the grasses have the most rapid substitution rate; they are followed in rate by the Orchidales, the Liliales, the Bromeliales, and the Arecales. The overall substitution rate for the rbcL locus of grasses is over 5 times the substitution rate in the rbcL of the palms. The substitution rate at the third codon positions in the rbcL of the grasses is over 8 times the third position rate in the palms. The pattern of rate variation is consistent with the generation-time-effect hypothesis. Heterogenous rates of substitution have important implications for phylogenetic reconstruction.

Key words

rbcRelative rates of nucleotide substitution Generation time Phylogeny construction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ash J (1988) Demography and production of Balaka microcarpa Burret (Arecaceae), a tropical understory palm in Fiji. Aust J Bot 6:67–68Google Scholar
  2. Augsburger CK (1985) Demography and life history variation of Puya dasylirioides, a long-lived rosette in tropical subalpine bogs. Oikos 45(3):341–352Google Scholar
  3. Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398Google Scholar
  4. Bulmer R, Wolfe KH, Sharp PM (1991) Synonomous nucleotide substitution rates in mammalian genes: implication for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci USA 88:5974–5978Google Scholar
  5. Clark WD, Gaut BS, Duvall MR, Clegg, MT (1993) Phylogenetic relationships of the Bromeliaceae based on rbcL sequence comparisons. Ann Miss Bot Gard, submittedGoogle Scholar
  6. Cowley EJ (1988) Burmmaniaceae. In: Polhill RM (ed) Flora of tropical East Africa. AA Balkema, Rotterdam, pp 1–9Google Scholar
  7. Cronquist A (1988) The evolution and classification of flowering plants, 2nd edition. The New York Botanical Garden, Bronx, NYGoogle Scholar
  8. Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the Monocotyledons: structure, evolution and taxonomy. Springer-Verlag, BerlinGoogle Scholar
  9. Doebley J, Renfroe W, Blanton A (1987) Restriction site variation in the Zea chloroplast genome. Genetics 117:139–147Google Scholar
  10. Doebley J, Durbin M, Golenberg EM, Clegg MT, Ma D-P (1990) Evolutionary analysis of the large subunit of carboxylase rbcL nucleotide sequence among the Grasses (Gramineae). Evolution 44:1097–1108Google Scholar
  11. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  12. Duvall MR, Clegg MT, Chase MW, Clark WD, Kress WJ, Zimmer EA, Hills HG, Eguiarte LE, Smith JF, Gaut BS, Learn GH (1993) Rapid radiation of ancestral monocotyledons into seven primary lineages indicated by analysis of DNA sequence of a plastid locus obtained from 104 species. Ann Miss Bot Gard, in pressGoogle Scholar
  13. Farris JS (1983) The logical basis of phylogenetic analysis. In: Platnick NI, Funk VA (eds) Advances in cladistics vol. 2. Columbia University Press, New York, pp 7–36Google Scholar
  14. Felsenstein JF (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zoo 27:401–410Google Scholar
  15. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376Google Scholar
  16. Felsenstein JF (1983) Parsimony in systematics: biological and statistical issues. Ann Rev Ecol Syst 14:313–333Google Scholar
  17. Fitch WM (1976) Molecular evolutionary clocks. In: Ayala FJ (ed) Molecular evolution. Sinauer Associates, Sunderland, MA, pp 160–178Google Scholar
  18. Garcia P, Clegg MT (1991) The gene rbcL for Avena sativa L. 26th Portugese-Spanish meetings of Genetics. CoimbraGoogle Scholar
  19. Gaut BS, Clegg MT (1991) Molecular evolution of alcohol dehydrogenase 1 in members of the grass family. Proc Natl Acad Sci USA 88:2060–2064Google Scholar
  20. Giannasi DE, Zurawski G, Learn GH, Clegg MT (1992) Evolutionary relationships of the Caryophillidae based on comparative rbcL sequences. Syst Bot 17:1–5Google Scholar
  21. Gillespie JH (1984) The molecular clock may be an episodic clock. Proc Natl Acad Sci USA 81:8009–8013Google Scholar
  22. Gillespie JH (1986) Natural selection and the molecular clock. Mol Biol Evol 3:138–155Google Scholar
  23. Gob C-J, Strauss MS, Arditti J (1982) Flower induction and physiology in orchids. In: Arditti J (ed) Orchid biology, reviews and perspectives, vol 2. Cornell University Press, Ithaca, pp 213–241Google Scholar
  24. Golenberg EM, Giannasi DE, Clegg MT, Smiley CJ, Durbin M, Henderson D, Zurawski G (1990) Chloroplast DNA sequence from a Miocene Magnolia species. Nature 344(6267):656–658Google Scholar
  25. Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenetics. J Mol Evol 32: 443–445Google Scholar
  26. Hitchcock AS (1935) Manual of the grasses of the United States. US Government Printing Office, WashingtonGoogle Scholar
  27. Hudson GS, Mahon JD, Anderson PA, Gibbs MJ, Badger MR, Andrew TJ, Whitfield PR (1990) Comparisons of the rbcL genes for the large subunit of ribulose bisphosphate carboxyase from closely related C3 and C4 plant species. J Biol Chem 265:808–814Google Scholar
  28. Ivashchenko AA (1979) Characteristics of the greater life cycle of the Yellow Autumn Crocus at the northern boundary of its range. Sov J Ecol 10:431–432Google Scholar
  29. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, p 70Google Scholar
  30. Kimura M (1989) The neutral theory of evolution and the world view of the neutralists. Genome 31:24–31Google Scholar
  31. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 16:111–120Google Scholar
  32. Kreppers ET, Larrinua IM, McIntosh L, Bogorad L (1982) The maize chloroplast genes for the β and ε subunits for the photosynthetic coupling factor CF1 are fused. Nucleics Acid Res 10:4985–5002Google Scholar
  33. Li W-H, Luo C-C, Wu C-I (1985) Evolution of DNA sequences. In: Macintyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 1–94Google Scholar
  34. Li W-H, Tanimura M, Sharp PM (1987a) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342Google Scholar
  35. Li W-H, Wolfe KH, Sourdis J, Sharp PM (1987b) Reconstruction of phylogenetic trees and estimation of divergence times under nonconstant rates of evolution. Cold Spring Harbor Symp Quant Biol 52:854–856Google Scholar
  36. McIntosh L, Poulsen C, Bogorad L (1980) Chloroplast gene sequences for the large subunit of ribulose bisphosphate carboxylase of maize. Nature 288:556–560Google Scholar
  37. Moon E, Kao TH, Wu R (1987) Rice chloroplast DNA molecules are heterogenous as revealed by DNA sequences of a cluster of genes. Nucl Acids Res 15:611–630Google Scholar
  38. Muse SV, and Weir BS (1992) Testing for equality of evolutionary rates. Genetics, in pressGoogle Scholar
  39. Ohta T (1987) Very slightly deleterious mutations and the molecular clock. J Mol Evol 26:1–6Google Scholar
  40. Penny D, Hendy MD, Henderson IM (1987) Reliability of evolutionary trees. Cold Spring Harbor Symp Quant Biol 52:857–862Google Scholar
  41. Poulsen C (1981) Comments on the structure and function of the large subunit of the enzyme ribulose bisphosphate carboxylase-oxygenase. Carsberg Res Commun 46:259–278Google Scholar
  42. Rauh W (1979) Bromeliads for home, garden and greenhouse. Blandford Press, Poole, p 19Google Scholar
  43. Saitou N, Nei M (1987) The neighbor joining method for molecular phylogeny. J Mol Evol 27:261–273Google Scholar
  44. Saitou N, Imanishi T (1989) Relative efficiencies of the Fitch-Margoliash, Maximum-Parsimony, Maximum-Likelihood, Minimum-Evolution, and Neighbor joining Methods of phylogenetic tree construction in obtaining the correct tree. Mol Biol Evol 6:514–525Google Scholar
  45. Sanger FS, Nicklen S, Colson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467Google Scholar
  46. Smith JF, Doyle JJ (1986) Chloroplast DNA variation and evolution in the Juglandaceae. Am J Bot 78:730Google Scholar
  47. Sober E (1983) Parsimony in systematics: philosophical issues. Ann Rev Ecol Syst 14:335–357Google Scholar
  48. Soltis DE, Soltis PS, Clegg MT, Durbin M (1990) rbcL sequence divergence and phylogenetic relationships in Saxifragaceae sensu lato. Proc Natl Acad Sci USA 87:4640–4644Google Scholar
  49. Terachi T, Ofihara Y, Tsunewaki K (1987) The molecular basis of genetic diversity among cytoplasms of Triticum and Aegilops. VI. Complete nucleotide sequences of the rbcL genes encoding H and L type rubisco large subunits in common wheat and Aegilops crassa. 4X. Jpn J Genet 62:375–387Google Scholar
  50. Uhl NW, Dransfield J (1987) Genera Plamarum, LH Bailey Horatorium and the International Palm Society. Allen Press, Lawrence, KansasGoogle Scholar
  51. Wilson AC, Carlson SS, White T (1977) Biochemical evolution. Ann Rev Biochem 46:573–639Google Scholar
  52. Wilson MA, Gaut B, Clegg MT (1990) Chloroplast DNA evolves slowly in the Palm family (Arecaceae). Mol Biol Evol 7:303–314Google Scholar
  53. Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745Google Scholar
  54. Zuckerkandl E, Pauling L (1965) In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166Google Scholar
  55. Zurawski G, Clegg MT, Brown AHD (1984) The nature of nucleotide sewuence divergence between barley and maize chloroplast DNA. Genetics 106:735–749Google Scholar

Copyright information

© Springer-Verlag New York Inc 1992

Authors and Affiliations

  • Brandon S. Gaut
    • 1
  • Spencer V. Muse
    • 2
  • W. Dennis Clark
    • 3
  • Michael T. Clegg
    • 1
  1. 1.Department of Botany and Plant SciencesUniversity of CaliforniaRiverside, RiversideUSA
  2. 2.Program in Statistical GeneticsNorth Carolina State UniversityRaleighUSA
  3. 3.Department of BotanyArizona State UniversityTempeUSA

Personalised recommendations