Skip to main content
Log in

Phylogenetic relationships of ferns deduced from rbcL gene sequence

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Part of the large subunit of the ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) gene (rbcL) was sequenced from three fern species: Adiantum capillus-veneris, Botrypus strictus, and Osmunda cinnamomea var. fokiensis. This region included 1,333 base pairs, about 90% of the gene. Maximum likelihood analysis of the deduced amino acid sequences indicated that (1) Botrypus (Ophioglossaceae) clustered monophyletically with other ferns (Adiantum, Angiopteris, Osmunda); the closest relative to Botrypus among the three species was Osmunda, which did not support the hypothesis that the Ophioglossaceae are linked to the progymnosperm-seed plant lineage. (2) Eusporangiate ferns containing Botrypus (Ophioglossaceae) and Angiopteris (Marattiaceae) were a paraphyletic group. (3) Seed plants and the four fern species examined formed a monophyletic group, but ferns and bryophytes (liverwort) did not. Variations in rates of substitution for synonymous and nonsynonymous codons were found in fern lineages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adachi J, Hasegawa M (1992) Computer science monographs, vol 27. MOLPHY: Programs for molecular phylogenetics, I. PROTML: Maximum likelihood inference of protein phylogeny. The Institute of Statistical Mathematics, Tokyo

    Google Scholar 

  • Bierhorst DW (1971) Morphology of vascular plants. Macmillan, New York

    Google Scholar 

  • Bremer K (1985) Summary of green plant phylogeny and classification. Cladistics 1:369–385

    Google Scholar 

  • Chan RI (1986) Xylem structure in Botrychium dissectum Sprengel and its relevance to the taxonomic position of the Ophioglossaceae. Am J Bot 73:1201–1208

    Google Scholar 

  • Christensen C (1938) Filicinae. In: Verdoorn F (ed) Manual of pteridology. Martinus Nijhoff, The Hague, pp 522–550

    Google Scholar 

  • Copeland EB (1947) Genera filicum. Chronica Botanica, Boston, MA

    Google Scholar 

  • Crane PR (1985) Phylogenetic analysis of seed plants and the origin of angiosperms. Ann Missouri Bot Gard 72:716–793

    Google Scholar 

  • Doebley J, Durbin M, Golenberg EM, Clegg MT, Ma DP (1990) Evolutionary analysis of the large subunit of carboxylase (rbcL) nucleotide sequence among the grasses (Gramineae). Evolution 44:1097–1108

    Google Scholar 

  • Doyle JA, Donoghue MJ (1986) Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot Rev 52:321–431

    Google Scholar 

  • Dron M, Rahire M, Rochaix JD (1982) Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793

    Google Scholar 

  • Gifford EM, Foster AS (1988) Morphology and evolution of vascular plants, 3rd. WH Freeman, New York

    Google Scholar 

  • Golenberg EM, Giannasi DE, Clegg MT, Smiley CJ, Durbin M, Henderson D, Zurawski G (1990) Chloroplast DNA sequence from a miocene Magnolia species. Nature 344:656–658

    Google Scholar 

  • Hasebe M, Iwatsuki K (1990a) Adiantum capillus-veneris chloroplast DNA clone bank: as useful heterologous probes in the systematics of the leptosporangiate ferns. Amer Fern J 80:20–25

    Google Scholar 

  • Hasebe M, Iwatsuki K (1990b) Chloroplast DNA from Adiantum capillus-veneris L., a fern species (Adiantaceae); clone bank, physical map and unusual gene localization in comparison with angiosperm chloroplast DNA. Curr Genet 17:359–364

    Google Scholar 

  • Hasebe M, Iwatsuki K (1992) Gene localization on the chloroplast DNA of the maiden hair fern; Adiantum capillusveneris. Bot Mag Tokyo 105:413–419

    Google Scholar 

  • Hasebe M, Ito M, Kofuji R, Iwatsuki K, Ueda K (1992a) Phylogenetic relationships in Gnetophyta deduced from rbcL gene sequences. Bot Mag Tokyo 105:385–391

    Google Scholar 

  • Hasebe M, Kofuji R, Ito M, Kato M, Iwatsuki K, Ueda K (1992b) Phylogeny of gymnosperms inferred from rbcL gene sequences. Bot Mag Tokyo 105:673–679

    Google Scholar 

  • Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993) Early branching in the evolution of eukaryotes: ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388

    Google Scholar 

  • Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenetics. J Mol Evol 32:443–445

    Google Scholar 

  • Hill CR, Camus JM (1986) Evolutionary cladistics of marattialean ferns. Bull Br Mus Nat Hist (Bot) 14:219–300

    Google Scholar 

  • Hill CR, Crane PR (1982) Evolutionary cladistics and the origin of angiosperms. In: Joysey KA, Friday AE (ed) Problems of phylogenetic reconstruction. Academic Press, London, pp 269–361

    Google Scholar 

  • Hipkins VD, Tsai C-H, Strauss SH (1990) Sequence of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from a gymnosperm, Douglas fir. Plant Mol Biol 15:505–507

    Google Scholar 

  • Hiratsuka J, Shimada H, Whittier RF, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sative) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194

    Google Scholar 

  • Hori H, Lim B-L, Osawa S (1985) Evolution of green plants as deduced from 5S rRNA sequences. Proc Natl Acad Sci USA 82:820–823

    Google Scholar 

  • Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472

    Google Scholar 

  • Hudson GS, Mahon JD, Anderson PA, Gibbs MJ, Badger MR, Andrews TJ, Whitfeld PR (1990) Comparisons of rbcL genes for the large subunit of ribulose-bisphosphate carboxylase from closely related C3 and C4 plant species. J Biol Chem 265:808–814

    Google Scholar 

  • Kato M (1983) The classification of major groups of pteridophytes. J Fac Sci Univ Tokyo ser. 313:267–283

    Google Scholar 

  • Kato M (1987) A phylogenetic classification of Ophioglossaceae. Gard Bull Singapore 40:1–14

    Google Scholar 

  • Kato M (1988) The phylogenetic relationship of Ophioglossaceae. Taxon 37:381–386

    Google Scholar 

  • Kato M, Takahashi A, Imaichi R (1988) Anatomy of the axillary bud of Helmintostachys zeylanica (Ophioglossaceae) and its systematic implications. Bot Gaz 149:57–63

    Google Scholar 

  • 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 29:170–179

    Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160

    Google Scholar 

  • Les DH, Garvin DK, Wimpee CF (1991) Molecular evolutionary history of ancient aquatic angiosperms. Proc Natl Acad Sci USA 88:10119–10123

    Google Scholar 

  • Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174

    Google Scholar 

  • Loconte H, Stevenson DW (1990) Cladistics of the spermatophyta. Brittonia 42:197–211

    Google Scholar 

  • 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

    Google Scholar 

  • Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart J (1988) Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75:1180–1206

    Google Scholar 

  • Pichi Sermolli REG (1973) Historical review of the higher classification of the Filicopsida. In: Jermy AC, Crabbe JA, Thomas BA (eds) The phylogeny and classification of the ferns. Academic Press, London, pp 11–40

    Google Scholar 

  • Reimers H (1954) Pteridophyta. In: Melchior H, Werdermann E (eds) A Engler's Syllabus der Pflanzenfamilien. Borntraeger, Berlin, pp 269–311

    Google Scholar 

  • Ritland K, Clegg MT (1987) Evolutionary analysis of plant DNA sequences. Am Natur 130(Suppl):S74-S100

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY

    Google Scholar 

  • Sarich VM, Wilson AC (1973) Generation time and genomic evolution in primates. Science 179:1144–1147

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohta C, Torazawa K, Meng BY, Sugita M, Deno H, Kamagashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    Google Scholar 

  • Soltis DE, Soltis PS, Clegg MT, Durbin M (1990) rbcL sequence devergence and phylogenetic relationships in Saxifragaceae sense lato. Proc Nail Acad Sci USA 87:4640–4644

    Google Scholar 

  • Steele KP, Holsinger KE, Jansen RK, Taylor DW (1991) Assessing the reliability of 5S rRNA sequence data for phylogenetic analysis in green plants. Mol Biol Evol 8:240–248

    Google Scholar 

  • Stein DB, Conant DS, Ahearn ME, Jordan ET, Kirch SA, Hasebe M, Iwatsuki K, Tan MK, Thomson JA (1992) Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns. Proc Natl Acad Sci USA 89:1856–1860

    Google Scholar 

  • Takahashi A, Kato M (1988) Developmental anatomy of vascular cambium and periderm of Botrypus virginianus and its bearing on the systematic position of Ophioglossaceae. Bot Mag Tokyo 101:373–385

    Google Scholar 

  • Troitsky AV, Melekhovets YF, Rakhimova GM, Bobrova VK, Valiejo-Roman KM, Antonov AS (1991) Angiosperm origin and early stages of seed plant evolution deduced from rRNA sequence comparisons. J Mol Evol 32:253–261

    Google Scholar 

  • Tryon RM, Tryon AF (1982) Ferns and allied plants with special reference to tropical america. Springer-Verlag, New York

    Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates and nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    Google Scholar 

  • Yang RCA, Dove M, Seligy VL, Lemieux C, Turmel M, Narang SA (1986) Complete nucleotide sequence and m-RNA-mapping of the large subunit gene of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) from Chlamydomonas moewusii. Gene 50:259–270

    Google Scholar 

  • Yoshinaga K, Ohta T, Suzuki Y, Sugiura M (1988) Chlorella chloroplast DNA sequence containing a gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase and a part of a possible gene for the β′ subunit of RNA polymerase. Plant Mol Biol 10:245–250

    Google Scholar 

  • Yoshinaga K, Kubota Y, Ishii T, Wada K (1992) Nucleotide sequence of atpB, rbcL trnR, dedB and psaI chloroplast genes from a fern Angiopteris lygodiifolia: a possible emergence of Spermatophyta lineage before the separation of Bryophyta and Pteridophyta. Plant Mol Biol 18:79–82

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: M. Hasebe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hasebe, M., Ito, M., Kofuji, R. et al. Phylogenetic relationships of ferns deduced from rbcL gene sequence. J Mol Evol 37, 476–482 (1993). https://doi.org/10.1007/BF00160428

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160428

Key words

Navigation