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Breakdown of distyly in a tetraploid variety of Ophiorrhiza japonica (Rubiaceae) and its phylogenetic analysis

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Abstract

We examined the floral morph of tetraploid Ophiorrhiza japonica Blume var. amamiana Hatus. and diploid O. japonica var. japonica to elucidate the association of distyly and ploidy levels. Chloroplast DNA phylogeny was reconstructed to determine the number of tetraploidization events and floral morph shifts in O. japonica. All individuals of O. japonica var. amamiana proved to be long-homostylous, whereas O. japonica var. japonica was distylous with typical long- and short-styled flowers. Distyly is related to the ploidy level. The bagging treatment of flowers indicated that O. japonica var. amamiana is self-compatible and potentially automatically self-pollinating. In cpDNA sequencing analysis, no haplotype was shared between the two varieties. The cpDNA haplotype network displayed the monophyly of O. japonica var. amamiana, suggesting a single origin of this variety. Hence, both tetraploidization and the breakdown of distyly to homostyly in O. japonica var. amamiana likely occurred just once. Because O. japonica var. amamiana having the morphological and cytological entity is recognized as a single lineage and clearly separated from O. japonica var. japonica, this variety can be considered to be a distinct species. We therefore propose to raise O. japonica var. amamiana to the rank of species.

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References

  • Arnold ES, Richards AJ (1998) On the occurrence of unilateral imcompatibility in Primula section Aleuritia Duby and the origin of Primula scotica Hook. Bot J Linn Soc 128:359–368

    Article  Google Scholar 

  • Arroyo J, Barrett SCH, Hidalgo R, Cole WW (2002) Evolutionary maintenance of stigma-height dimorphism in Narcissus paryraceus (Amaryllidaceae). Am J Bot 89:1242–1249

    Google Scholar 

  • Bahadur B (1968) Heterostyly in Rubiaceae. J Osmania Univ (Golden Jubilee Vol): 207–238

  • Barrett SCH (1992) Heterostylous genetic polymorphisms: model systems for evolutionary analysis. In: Barrett SCH (ed) Evolution and function of heterostyly (Monogr Theor Applied Genet 15). Springer, Berlin, pp 1–29

  • Barrett SCH, Shore JS (1987) Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41:340–354

    Article  Google Scholar 

  • Barrier M, Robichaux RH, Purugganan MD (2001) Accelerated regulatory gene evolution in an adaptive radiation. Proc Natl Acad Sci USA 98:10208–10213

    Article  PubMed  CAS  Google Scholar 

  • Chao JM (1978) Ophiorrhiza L. In: Editorial Committee of the Flora of Taiwan (ed) Flora of Taiwan, vol 4. Epoch, Taipei, pp 317–323

  • Charlesworth B, Charlesworth D (1979) The maintenance and breakdown of distyly. Am Nat 114:499–513

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Google Scholar 

  • Darwin SP (1976) The pacific species of Ophiorrhiza L. (Rubiaceae). Lyonia 1:47–102

    Google Scholar 

  • Dowrick VPJ (1956) Heterostyly and homostyly in Primula obconica. Heredity 10:219–236

    Google Scholar 

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

    Google Scholar 

  • Faivre AE, McDade LA (2001) Population-level variation in the expression of heterostyly in three species of Rubiaceae: does reciprocal placement of anthers and stigmata characterize heterostyly? Am J Bot 85:841–853

    Article  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Ganders FR (1979) The biology of heterostyly. NZ J Bot 17:607–635

  • Glazko GV, Nei M (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20:424–434

    Article  PubMed  CAS  Google Scholar 

  • Graham SW, Barrett SCH (2004) Phylogenetic reconstruction of the evolution of stylar polymorphisms in Narcissus (Amaryllidaceae). Am J Bot 91:1007–1021

    Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Longman, London

    Google Scholar 

  • Guggisberg A, Mansion G, Kelso S, Conti E (2006) Evolution of biogeographic patterns, ploidy levels, and breeding systems in a diploid–polyploid species complex of Primula. New Phytol 171:617–632

    Google Scholar 

  • Hatusima S (1961) On the genus Ophiorrhiza from the Ryukyus and Formosa. In: Kagoshima University, Ryukyu University (eds) Kagoshima University and Ryukyu University reports on cooperative investigation of science and industry in the Ryukyu Islands 1. Kagoshima University, Kagoshima, pp 61–66

  • Hatusima S (1975) Flora of the Ryukyus, added and corrected. Okinawa Association of Biology Education, Naha

    Google Scholar 

  • Hatusima S, Amano T (1994) Flora of the Ryukyus, south of Amami Island, 2nd edn. The Biological Society of Okinawa, Nishihara

  • Hedrén M (2003) Plastid DNA variation in the Dactylorhiza incarnata/maculata polyploid complex and the origin of allotetraploid D. sphagnicola (Orchidaceae). Mol Ecol 12:2669–2680

    Article  PubMed  CAS  Google Scholar 

  • Hooker JD (1880) The flora of British India III. Reeve, Ashford

    Google Scholar 

  • Johnson LA, Soltis DE (1994) atpB-rbcL sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156

  • Kéry M, Matthies D, Schmid B (2003) Demographic stochasticity in population fragments of the declining distylous perennial Primula veris (Primulaceae). Basic Appl Ecol 4:197–206

    Article  Google Scholar 

  • Kohn JR, Graham SW, Morton B, Doyle JJ, Barrett SCH (1996) Reconstruction of the evolution of reproductive characters in Pontederiaceae using phylogenetic evidence from chloroplast DNA restriction-site variation. Evolution 50:1454–1469

    Article  Google Scholar 

  • Kudoh H, Sugawara T, Wu SG, Murata J (2001) Morph-specific correlations between floral traits in a distylous Ophiorrhiza napoensis (Rubiaceae) population in southern China. J Trop Ecol 17:719–728

    Article  Google Scholar 

  • Levin DA (1975) Minority cytotype exclusion in local plant populations. Taxon 24:35–43

    Article  Google Scholar 

  • Lewis WH (1980) Polyploidy in angiosperms: dicotyledons. In: Lewis WH (ed) Polyploidy—biological relevance. Plenum, New York, pp 241–268

  • Liu HY, Yang TYA (1998) Ophiorrhiza L. In: Editorial Committee of the Flora of Taiwan (ed) Flora of Taiwan 2nd edn, vol 4. Editorial Committee of the Flora of Taiwan, Taipei, pp 306–311

  • Lo HS (1990) Taxonomic revision of the Chinese species of Ophiorrhiza (Rubiaceae). Bull Bot Res 10:1–82

    Google Scholar 

  • Lo HS (1999) Ophiorrhiza Linn. In: Delectis florae Reipublicae Popularis Sinicae Agendae Academiae Sinicae (ed) Flora Reipublicae Popularis Sinicae, vol 71. Science Press, Beijing, pp 110–174

  • Mabberley DJ (1997) The plant book. A portable dictionary of the vascular plants, 2nd edn. Cambridge University Press, Cambridge

  • Mable BK (2004) Polyploidy and self-compatibility: is there an association? New Phytol 162:803–811

    Article  Google Scholar 

  • Murakami N, Watanabe M, Yokoyama J, Yatabe Y, Iwasaki H, Serizawa S (1999) Molecular taxonomic study and revision of the three Japanese species of Asplenium sect. Thamnopteris. J Plant Res 112:15–25

    Article  CAS  Google Scholar 

  • Naiki A, Nagamasu H (2003) Distyly and pollen dimorphism in Damnacanthus (Rubiaceae). J Plant Res 116:105–113

    PubMed  Google Scholar 

  • Naiki A, Nagamasu H (2004) Correlation between distyly and ploidy level in Damnacanthus (Rubiaceae). Am J Bot 91:664–671

    Google Scholar 

  • Nakamura K, Denda T, Yokota M (2006b) Homostyly and autogamy in Ophiorrhiza pumila (Rubiaceae) from the Ryukyu Archipelago. J Jpn Bot 81:113–120

    Google Scholar 

  • Nakamura K, Chung SW, Kokubugata G, Denda T, Yokota M (2006a) Phylogenetic systematics of the monotypic genus Hayataella (Rubiaceae) endemic to Taiwan. J Plant Res 119:657–661

    Article  PubMed  CAS  Google Scholar 

  • Nakamura K, Denda T, Kameshima K, Uehara M, Yokota M (2003) Chromosome numbers of Ophiorrhiza and Psychotria (Rubiaceae) in the Ryukyus. Biol Mag Okinawa 41:15–24

    Google Scholar 

  • Ohi T, Kajita T, Murata J (2003) Distinct geographic structure as evidenced by chloroplast DNA haplotypes and ploidy level in Japanese Aucuba (Aucubaceae). Am J Bot 90:1645–1652

    Google Scholar 

  • Ohwi J (1938) The genus Ophiorrhiza of Japan. Acta Phytotax Geobot 7:195–196

    Google Scholar 

  • Ooi K, Endo Y, Yokoyama J, Murakami N (1995) Useful primer designs to amplify DNA fragment of the plastid gene matK from angiosperm plants. J Jpn Bot 70:328–331

    Google Scholar 

  • Pailler T, Thompson JD (1997) Distyly and variation in heteromorphic incompatibility in Gaertena vaginata (Rubiaceae) endemic to La Reunion Island. Am J Bot 84:315–327

    Article  Google Scholar 

  • Piper JG, Charlesworth B, Charlesworth D (1984) A high rate of self-fertilization and increased seed fertility of homostyle primroses. Nature 310:50–51

    Article  Google Scholar 

  • Pitard CJ (1922) Ophiorrhiza Linn. In: Lecomte MH (ed) Flora Général de l’Indo-Chine 3. Masson, Paris, pp 155–167

    Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  PubMed  Google Scholar 

  • Ray PM, Chisaki HF (1957) Studies of Amsinckia. II. Relationships among the primitive species. Am J Bot 44:537–544

    Article  Google Scholar 

  • Renno JF, Mariac C, Poteaux C, Bezançon, Lumaret R (2001) Haplotype variation of cpDNA in the agamic grass complex Pennisetum section Brevivalvula (Poaceae). Heredity 86:537–544

    Article  PubMed  CAS  Google Scholar 

  • Ridley HN (1923) The flora of the Malay Peninsula II. Reeve, Ashford

    Google Scholar 

  • Santos IAD (2002) Flower-visiting bees and the breakdown of the tristylous breeding system of Eichhornia azurea (Swartz) Kunth (Pontederiaceae). Biol J Linn Soc 77:499–507

    Article  Google Scholar 

  • Schoen DJ, Johnston MO, L’Heureux AM, Marsolais JV (1997) Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51:1090–1099

    Article  Google Scholar 

  • Segraves KA, Thompson JN, Soltis PS, Soltis DE (1999) Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia. Mol Ecol 8:253–262

    Article  Google Scholar 

  • Setoguchi H, Ohba H (1995) Phylogenetic relationships in Crossostylis (Rhizophoraceae) inferred from restriction site variation of chloroplast DNA. J Plant Res 108:87–92

    Article  CAS  Google Scholar 

  • Shaw KL (1999) A nested analysis of song groups and species boundaries in the Hawaiian cricket genus Laupala. Mol Phylogenet Evol 11:332–341

    Article  PubMed  CAS  Google Scholar 

  • Shinohara W, Takamiya M, Murakami N (2003) Taxonomic study of Japanese Deparia petersenii (Woodsiaceae) based on cytological and molecular information. Acta Phytotax Geobot 54:137–148

    Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Sobrevila C, Ramirez N, De Enrech NX (1983) Reproductive biology of Palicourea fendleri and P. petiolaris (Rubiaceae), heterostylous shrubs of a tropical cloud forest in Venezuela. Biotropica 15:161–169

    Article  Google Scholar 

  • Soltis DE, Soltis PS (1989) Allopolyploid speciation in Tragopogon: insights from chloroplast DNA. Am J Bot 76:1119–1124

    Article  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Tate JA (2003) Advance in the study of polyploidy since Plant speciation. New Phytol 161:173–191

    Article  CAS  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold, London

    Google Scholar 

  • Stebbins GL (1974) Flowering plants: evolution above the species level. Harvard University Press, Cambridge

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, MA

  • Takezaki N, Rzhetsky A, Nei M (1995) Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823–833

    PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    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 

  • Truyens S, Arbo MM, Shore JS (2005) Phylogenetic relationships, chromosome and breeding system evolution in Turnera (Turneraceae): inferences from ITS sequence data. Am J Bot 92:1749–1758

    CAS  Google Scholar 

  • Wang Y, Wang QF, Guo YH, Barrett SCH (2004) Reproductive consequences of interactions between clonal growth and sexual reproduction in Nymphoides peltata: a distylous aquatic plant. New Phytol 165:329–336

    Article  Google Scholar 

  • Washitani I, Osawa R, Namai H, Niwa M (1994) Patterns of female fertility in heterostylous Primula sieboldii under severe pollinator limitation. J Ecol 82:571–579

    Article  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42: 225–249

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki T (1993) Rubiaceae. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan IIIa. Kodansha, Tokyo, pp 206–240

    Google Scholar 

  • Yeung K, Miller JS, Savage AE, Husband BC, Igic B, Kohn JR (2005) Association of ploidy and sexual system in Lycium californicum (Solanaceae). Evolution 59:2048–2055

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Drs. G. Ishida, H. Kamiaka, S. Kobayashi, G. Kokubugata, N. Kurosaki, T. Kosaka, K. Matsubara, S. Matsumura, K. Oginuma, H. Sudo, M. Tabata, M. Takamiya, Y. Tateishi, N. Wakita, and H. Yamashita for providing plant materials and facilities in their herbaria. This study was supported in part by a Research Fellowship for Young Scientists from the Japan Society for the Promotion of Science (JSPS) to K.N., a Grant-in-Aid for Scientific Research (C) (no. 17570083) to M.Y., and a grant for the 21st Century COE program of the University of the Ryukyus.

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Correspondence to Koh Nakamura.

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Nakamura, K., Denda, T., Kameshima, O. et al. Breakdown of distyly in a tetraploid variety of Ophiorrhiza japonica (Rubiaceae) and its phylogenetic analysis. J Plant Res 120, 501–509 (2007). https://doi.org/10.1007/s10265-007-0089-9

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