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High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants

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Abstract

Relative rate tests, using Gnetum as a reference taxon, were conducted on nuclear 18S rRNA sequences from 10 angiosperms including autotrophic nonparasites (Arabidopsis, Asarum, Glycine, Malpighia, and Zea), a chlorophyllous hemiparasite (Arceuthobium—Viscaceae), and achlorophyllous holoparasites (Balanophora—Balanophoraceae, Prosopanche—Hydnoraceae, and Rafflesia and Rhizanthes—Rafflesiaceae). Compared with Glycine, the mean number of substitutions per site (K) for five autotrophic angiosperms is 0.036 whereas for the holoparasites K = 0.126, i.e., 3.5 times higher. Comparisons of autotrophic species with short and long generation times showed no differences in K; hence, divergent rRNA sequences in the holoparasites are likely attributable to other mechanisms. These might include genetic bottlenecks, effective population size, and/or molecular drive. High substitution rates appear to be associated only with those parasitic angiosperms that have developed a highly modified haustorial system and extreme nutritional dependence upon the host. At present, high substitution rates in these parasites confound attempts to determine their phylogenetic position relative to other angiosperms.

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References

  • Albert VA, Williams SE, Chase MW (1992) Carnivorous plants: phylogeny and structural evolution. Science 257:1491–1495

    Google Scholar 

  • Arnheim ND Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E (1980) Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci USA 77:7323–7327

    Google Scholar 

  • Bosquet J, Strauss SH, Doerksen AH, Price RA (1992) Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc Natl Acad Sci USA 89:7844–7848

    Google Scholar 

  • Brown DD, Wensink PC, Jordan E (1972) A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: The evolution of tandem genes. J Mol Biol 63:57–73

    Google Scholar 

  • Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comp Appl Biosci 5:233–234

    Google Scholar 

  • Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu Y-L, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedrén M, Gaut BS, Jansen RK, Kim K-J, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang QY, Plunkett GM, Soltis PS, Swensen SM, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn GH Jr, Graham SW, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Mo Bot Gard 80:528–580

    Google Scholar 

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

    Google Scholar 

  • Cronquist A (1988) The evolution and classification of flowering plants, 2nd ed. The New York Botanical Garden, Bronx, NY

    Google Scholar 

  • Cullings KW, Bruns TD (1992) Phylogenetic origin of the Monotropoideae inferred from partial 28S ribosomal RNA gene sequences. Can J Bot 70:1703–1708

    Google Scholar 

  • Cullis CA (1984) Quantitative variation of the ribosomal RNA genes. In: Jordan EG, Cullis CA (eds) The nucleolus. Cambridge University Press, Cambridge, pp 103–112

    Google Scholar 

  • dePamphilis CW, Palmer JD (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348:337–339

    Google Scholar 

  • Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117

    CAS  PubMed  Google Scholar 

  • Dover GA (1987) DNA turnover and the molecular clock. J Mol Evol 26:47–58

    Google Scholar 

  • Dover G, Coen E (1981) Springcleaning ribosomal DNA: a model for multgene evolution? Nature 290:731–732

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Eckenrode VK, Arnold J, Meagher RB (1985) Comparison of the nucleotide sequence of soybean 18S rRNA with the sequences of other small-subunit rRNAs. J Mol Evol 21:259–269

    Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility will be positively misleading. Syst Zool 27:410–410

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    CAS  PubMed  Google Scholar 

  • Gaut BS, Muse SV, Clark WD, Clegg MT (1992) Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants. J Mol Evol 35:292–303

    Google Scholar 

  • Gedalovich-Shedletzky E, Kuijt J (1990) An ultrastructural study of the tuber stands of Balanophora (Balanophoraceae). Can J Bot 68: 1271–1279

    Google Scholar 

  • Gutell RR (1993) Collection of small subunit (168- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 21:3051–3054

    CAS  PubMed  Google Scholar 

  • Hamby KR, Zimmer EA (1992) Ribosomal RNA as a phylogenetic tool in plant systematics. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 50–91

    Google Scholar 

  • Ismail G (1988) Conservation of the giant Rafflesia in Sabah, Malaysia. TREE 3:316–317

    Google Scholar 

  • Kimura M (1987) Molecular evolutionary clock and the neutral theory. J Mol Evol 26:24–33

    Google Scholar 

  • Klekowski EJ (1988) Mechanisms that maintain the genetic integrity of plants. In: Greuter W, Zimmer B (eds) Proceedings of the XIV International Botanical Congress. Koeltz, Königstein/Taunus, pp 137–152

    Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley, p 246

    Google Scholar 

  • Kunkel TA, Loeb LA (1982) Fidelity of mammalian DNA polymerases. Science 213:765–767

    Google Scholar 

  • Lake JA (1987) Determining evolutionary distances from highly diverged nucleic acid sequences: operator metrics. J Mol Evol 26: 59–73

    Google Scholar 

  • Meijer W (1958) A contribution to the taxonomy and biology of Rafflesia arnoldi in West Sumatra. Ann Bogorienses 3:33–44

    Google Scholar 

  • Messing J, Carlson J, Hagen G, Rubenstein I, Oleson A (1984) Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. DNA 3:31–40

    Google Scholar 

  • Mullis KB, Faloona FA (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol 155: 335–350

    Google Scholar 

  • Neefs J-M, Van de Peer Y, De Rijk P, Chapelle S, De Wachter R (1993) Compilation of small subunit RNA structures. Nucleic Acids Res 21:3025–3049

    CAS  PubMed  Google Scholar 

  • Nickrent DL, Sargent ML (1991) An overview of the secondary structure of the V4 region of eukaryotic small-subunit ribosomal RNA. Nucleic Acids Res 19:227–235

    Google Scholar 

  • Nickrent DL, Franchina CR (1990) Phylogenetic relationships of the] Santalales and relatives. J Mol Evol 31:294–301

    Google Scholar 

  • Nickrent DL (1994) From field to film: rapid sequencing methods for field-collected plant species. Biotechniques 16:470–475

    Google Scholar 

  • Price PW (1980) Evolutionary biology of parasites. Monographs in Population Biology No. 15. Princeton University Press, Princeton, p 237

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sarich VM, Wilson AC (1967) Rates of albumin evolution in primates. Proc Natl Acad Sci USA 58:142–148

    Google Scholar 

  • Sogin ML, Elwood HH, Gunderson HH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383–1387

    Google Scholar 

  • Takhtajan AL (1980) Outline of the classification of flowering plants (Magnoliophyta). Bot Rev 46:225–359

    Google Scholar 

  • Takhtajan AL (1987) Systema Magnoliophytorum. Nauka, Leningrad (in Russian)

    Google Scholar 

  • Thorne RF (1992) An updated classification of the flowering plants. Aliso 13:365–389

    Google Scholar 

  • Topal MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263:285–289

    Google Scholar 

  • Unfried I, Stocker U, Gruendler P (1989) Nucleotide sequence of the 18S rRNA gene from Arabidopsis thaliana Co10. Nucleic Acids Res 17:7513

    Google Scholar 

  • Van de Peer Y, Neefs J-M, De Rijk P, De Wachter R (1993) Reconstructing evolution from eukaryotic small-ribosomal-subunit RNA sequences: calibration of the molecular clock. J Mol Evol 37:221–232

    Google Scholar 

  • Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196

    Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    CAS  PubMed  Google Scholar 

  • Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058

    Google Scholar 

  • Wolfe KH, Katz-Downie DS, Morden CW, Palmer JD (1992) Evolution of the plastid ribosomal RNA operon in a nongreen parasitic plant: accelerated evolution, altered promoter structure, and tRNA pseudogenes. Plant Mol Biol 18:1037–1048

    Google Scholar 

  • Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989a) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    Google Scholar 

  • Wolfe KH, Sharp PM, Li W-H (1989b) Rates of synonymous substitution in plant nuclear genes. J Mol Evol 29:208–211

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

Download references

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Correspondence to: D.L. Nickrent

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Nickrent, D.L., Starr, E.M. High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants. J Mol Evol 39, 62–70 (1994). https://doi.org/10.1007/BF00178250

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  • DOI: https://doi.org/10.1007/BF00178250

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