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Independent origins of tetraploid cryptic species in the fern Ceratopteris thalictroides

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Abstract

Ceratopteris thalictroides (L.) Brongn is a tetraploid fern species that contains at least three cryptic species, the south, the north and the third type. In this study we combined data from both chloroplast DNA (cpDNA) and nuclear DNA sequences of three diploid species and three cryptic species of C. thalictroides to unravel the origin of the cryptic species, particularly of the reticulate relationships among the diploid and tetraploid taxa in the genus Ceratopteris. Of the three diploid species examined, C. cornuta had cpDNA identical to that of the tetraploid third type plants, and this diploid species is a possible maternal ancestor of the tetraploid third type. Analysis of the homologue of the Arabidopsis thaliana LEAFY gene (CLFY1) identified ten alleles in the genus Ceratopteris, with six alleles found in C. thalictroides. The unrooted tree of the CLFY1 gene revealed four clusters. Each cryptic species showed fixed heterozygosity at the CLFY1 locus and had two alleles from different clusters of the CLFY1 tree. Consideration of the cpDNA sequences, CLFY1 genotypes of the cryptic species and CLFY1 gene tree in concert suggested that the cryptic species of C. thalictroides had originated through independent allopolyploidization events involving C. cornuta and two unknown hypothetical diploid species.

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References

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

    Google Scholar 

  • Ebihara A, Ishikawa H, Matsumoto S, Lin S, Iwatsuki K, Takamiya M, Watano Y, Ito M (2005) Nuclear DNA, chloroplast DNA, and ploidy analysis clarified biological complexity of the Vandenboschia radicans complex (Hymenophyllaceae) in Japan and adjacent areas. Am J Bot 92:1535–1547

    CAS  Google Scholar 

  • Gastony GJ, Yatskievichi G (1992) Maternal inheritance of the chloroplast and mitochondrial genomes in Cheilantoids ferns. Am J Bot 79:716–722

    Article  CAS  Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Grob GBJ, Gravendeel B, Eurlings MCM (2004) Potential phylogenetic utility of the nuclear FLORICAULA/LEAFY second intron: comparison with three chloroplast DNA regions in Amorphophallus (Araceae). Mol Phylogenet Evol 30:387–393

    Article  Google Scholar 

  • Hasebe M, Omori T, Nakazawa M, Sano T, Kato M, Iwatsuki K (1994) rbcL gene sequences provide evidence for the evolutionary lineages of Leptosporangiate ferns. Proc Natl Acad Sci U S A 91:5730–5734

    Article  PubMed  CAS  Google Scholar 

  • Hasebe M, Wolf PG, Pryer KM, Ueda K, Ito M, Sano R, Gastoney G, Yokoyama J, Manhart JR, Murakami N, Crane EH, Haufler CH, Hauk WD (1995) Fern phylogeny based on rbcL nucleotide sequences. Am Fern J 85:134–181

    Article  Google Scholar 

  • Haufler CH, Windham MD (1991) New species of North American Cystopteris and Polypodium, with comments on their reticulate relationships. Am Fern J 81:7–23

    Article  Google Scholar 

  • Hauk WD, Haufler CH (1999) Isozyme variability among cryptic species of Botrychium subgenus Botrychium (Ophioglossaceae). Am J Bot 86:614–633

    Article  PubMed  CAS  Google Scholar 

  • Hickok LG (1977) Cytological relationships between three diploid species of the ferns genus Ceratopteris. Can J Bot 55:1660–1667

    Google Scholar 

  • Hickok LG (1979) Cytological study of intraspecific variation in Ceratopteris thalictroides. Can J Bot 57:1694–1700

    Google Scholar 

  • Himi S, Sano R, Nishiyama T, Tanahashi T, Kato M, Ueda K, Hasebe M (2001) Evolution of MADS-Box gene induction by FLO/LFY gene. J Mol Evol 53:387–393

    Article  PubMed  CAS  Google Scholar 

  • Hoot SB, Taylor WC (2001) The utility of nuclear ITS, a LEAFY homolog intron, and chloroplast atpB-rbcL spacer region data in phylogenetic analyses and species delimitation in Isoëtes. Am Fern J 91:166–177

    Article  Google Scholar 

  • Ishikawa H, Ito M, Watano Y, Kurita S (2003) Electrophoretic evidence for homoeologous chromosome pairing in the apogamous fern species Dryopteris nipponensis (Dryopteridaceae). J Plant Res 116:165–167

    PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimation of evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:110–120

    Article  Google Scholar 

  • Klekowski EJ Jr (1972) Genetical features of ferns as contrasted to seed plants. Ann Miss Bot Gard 59:138–151

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kurihara T, Watano Y, Takamiya M, Shimizu T (1996) Electrophoretic and cytological evidence for genetic heterogeneity and hybrid origin of Athyrium oblitescens. J Plant Res 109:29–36

    Article  Google Scholar 

  • Lloyd RM (1974) Systematic of the genus Ceratopteris Brongn. (Parkeriaceae) II. Taxonomy. Brittonia 26:139–160

    Article  Google Scholar 

  • Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinform Appl Note 16:562–563

    Article  CAS  Google Scholar 

  • Masuyama S (1992) Clinal variation of frond morphology and its adaptive implication in the fern Ceratopteris thalictroides in Japan. Plant Species Biol 7:87–96

    Article  Google Scholar 

  • Masuyama S, Watano Y (1994) Hybrid sterility between two isozymic types of the fern Ceratopteris thalictroides in Japan. J Plant Res 107:269–274

    Article  Google Scholar 

  • Masuyama S, Watano Y (2005) Cryptic species in the fern Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae). II. Cytological characteristics of three cryptic species. Acta Phytotax Geobot 56:231–240

    Google Scholar 

  • Masuyama S, Yatabe Y, Murakami N, Watano Y (2002) Cryptic species in the fern Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae). I. Molecular analyses and crossing tests. J Plant Res 115:87–97

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa T, Watano Y (2000) Primer pairs suitable for PCR–SSCP analysis of chloroplast DNA in Angiosperms. J Phytogeogr Taxon 48:63–66

    Google Scholar 

  • Nishimoto Y, Ohnishi O, Hasegawa M (2003) Topological incongruence between nuclear and chloroplast DNA trees suggesting hybridization in the urophyllum group of the genus Fagopyrum (Polygonaceae). Genes Genet Syst 78:139–153

    Article  PubMed  CAS  Google Scholar 

  • Oh S, Potter D (2003) Phylogenetic utility of the second intron of LEAFY in Neillia and Stephanandra (Rosaceae) and implications for the origin of Stephanandra. Mol Phylogenet Evol 29:203–215

    Article  PubMed  CAS  Google Scholar 

  • Oh S, Potter D (2005) Molecular phylogenetic systematics and biogeography of tribe Neillieae (Rosaceae) using DNA sequences of cpDNA, rDNA, and LEAFY. Am J Bot 92:179–192

    CAS  Google Scholar 

  • Pal N, Pal S (1963) Studies on morphology and affinity of the Parkeriaceae. II. Sporogenesis, development of the gametophyte and cytology of Ceratopteris thalictroides. Bot Gaz Chic 124:405–412

    Article  Google Scholar 

  • Paris CA, Widham MD (1988) A biosystematic investigation of the Adiantum pedatum complex in Eastern North America. Syst Bot 13:240–255

    Article  Google Scholar 

  • Paris CA, Wagner FS, Wagner WH Jr (1989) Cryptic species, species delimitation and taxonomic practice in homosporous ferns. Am Fern J 79:46–55

    Article  Google Scholar 

  • Pryer KM, Haufler CH (1993) Isozymic and chromosomal evidence for the allotetraploid origin of Gymnocarpium dryopteris (Dryopteridaceae). Syst Bot 18:150–172

    Article  Google Scholar 

  • Raymond O, Piola F, Sanlaville-Boisson C (2002) Inference of reticulation in outcrossing allopolyploid taxa: caveats, likelihood and perspectives. Trends Ecol Evol 17:3–6

    Article  Google Scholar 

  • Shaw AJ, Cox CJ, Boles SB (2003) Polarity of peatmoss (Sphagnum) evolution: who says Bryophytes have no roots? Am J Bot 90:1777–1787

    Google Scholar 

  • Small RL, Wendel JF (2002) Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol Biol Evol 19:597–607

    PubMed  CAS  Google Scholar 

  • Stein DB, Barrington DS (1990) Recurring hybrid formation in a population of Polystichum x potteri: evidence from chloroplast and comparisons. Ann Miss Bot Gard 77:334–339

    Article  Google Scholar 

  • Swofford DL (1993) PAUP* version 4.0b10. Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland

    Google Scholar 

  • Taberlet P, Gully L, Pautau G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1110

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tryon RM, Tryon AF (1982) Fern and allied plants. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Vogel JC, Russel SJ, Rumsey FJ, Barrett JA, Gibby M (1998) Evidence of maternal transmission of chloroplast DNA in the genus Asplenium (Aspleniaceae, Pteridophyta). Bot Acta 111:247–249

    CAS  Google Scholar 

  • Watano Y, Masuyama S (1994) Genetic differentiation in population of the polymorphic fern Ceratopteris thalictroides in Japan. J Plant Res 107:139–146

    Article  Google Scholar 

  • Watano Y, Kanai A, Tani N (2004) Genetic structure of hybrid zones between Pinus pumila and P. parviflora var. pentaphylla (Pinaceae) revealed by molecular hybrid index analysis. Am J Bot 9:65–72

    Google Scholar 

  • Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci U S A 100:10824–10829

    Article  PubMed  CAS  Google Scholar 

  • Xiang L, Werth CH, Emery SN, McCauley DE (2000) Population-specific gender-biased hybridization between Dryopteris intermedia and D. carthusiana: evidence from chloroplast DNA. Am J Bot 87:1175–1180

    Article  PubMed  CAS  Google Scholar 

  • Yatabe Y, Masuyama S, Darnaedi D, Murakami N (2001) Molecular systematics of the Asplenium nidus complex from Mt. Halimun National Park, Indonesia: evidence for reproductive isolation among three sympatric rbcL sequence types. Am J Bot 88:1517–1522

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the following persons who helped collect materials: Wenni S. Lestari, Pak Cecep, Pak Kiswoyo and Ms. Anti. The authors also thank Dr. Tim Utteridge (The Royal Botanic Gardens, Kew, UK) for checking and correcting the English manuscript. We also thank the two anonymous reviewers for their helpful comments. This study was supported by a Monbukagakusho (Ministry of Education, Culture, Sports, Science and Technology, Government of Japan: MEXT) scholarship to B. A., who is on the research staff of the Eka Karya Botanical Gardens, Bali, Indonesian Institute of Sciences.

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Authors and Affiliations

  1. Graduate School of Science and Technology, Chiba University, Yayoi 1-33, Inage, Chiba, 263-8522, Japan

    Bayu Adjie

  2. Department of Mathematics and Natural Sciences, College of Arts and Sciences, Tokyo Woman’s Christian University, Tokyo, Japan

    Shigeo Masuyama

  3. Department of General System Studies, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan

    Hiroshi Ishikawa

  4. Department of Biology, Faculty of Science, Chiba University, Chiba, Japan

    Yasuyuki Watano

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  1. Bayu Adjie
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  2. Shigeo Masuyama
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  3. Hiroshi Ishikawa
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  4. Yasuyuki Watano
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Correspondence to Bayu Adjie.

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Adjie, B., Masuyama, S., Ishikawa, H. et al. Independent origins of tetraploid cryptic species in the fern Ceratopteris thalictroides . J Plant Res 120, 129–138 (2007). https://doi.org/10.1007/s10265-006-0032-5

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