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Phylogeny of the family hydrocharitaceae inferred fromrbcL andmatK gene sequence data

Abstract

The family Hydrocharitaceae, with 15 genera and ca. 80 species, shows a remarkable morphological diversity which presumably developed as an adaptation to their aquatic habitat. This is particularly true in the case of the many different kinds of pollination mechanisms. To gather more basic information regarding the adaptive evolution of Hydrocharitaceae, we have carried out a phylogenetic analysis based on the sequences of therbcL andmatK. Our resulting neighbor-joining distance tree provides the following insights: (1) none of the previous classification systems were supported by molecular phylogenetic tree; (2) Najas (Najadaceae), which has never been included in Hydrocharitaceae except in Shaffer-Fehre's (1991) system based on seed coat structures, is an ingroup of Hydrocharitaceae; (3) Limnocharitaceae and Alismataceae are sister groups of Hydrocharitaceae; (4) the three marine genera,Halophila, Enhalus andThalassia, are monophyletic; and (5) a peculiar pollination mechanism specific to Hydrocharitaceae (Hydrocharitaceae-epihydrophily), underwent a parallel evolution.

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References

  • Adachi, J. andHasegawa, M. 1996. MOLPHY: Programs for Molecular Phylogenetics, ver. 2.3. Institute of Statistical Mathematics, Tokyo.

    Google Scholar 

  • Ancibor, E. 1979. Systematic anatomy of vegetative organs of Hydrocharitaceae. Bot. J. Linn. Soc.78: 237–266.

    Google Scholar 

  • Ascherson, P. andGurke, M. 1889. Hydrocharitaceae.In A. Engler and K. Prantl, eds., Die Naturlichen Pflanzenfamilien, vol. 1. Engelmann, Leipzig, pp. 238–258.

    Google Scholar 

  • Cao, Y., Adachi, J., Janke, A., Paabo, S. andHasegawa, M. 1994a. Phylogenetic relationships among Eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of s tree based on a single gene. J. Mol. Evol.39: 519–527.

    PubMed  CAS  Article  Google Scholar 

  • Cao, Y., Adachi, J., Yano, T. andHasegawa, M. 1994b. Phylogenetic place of guinea pigs: no support of the Rodent-polyphyly hypothesis from Maximum-Likelihood analyses of multiple protein sequences. Mol. Biol. Evol.11: 593–604.

    PubMed  CAS  Google Scholar 

  • Chase, M.W., Soltis, D.E., Olmstead, R.G., Morgan, D., Les, D.H., Mishler, B.D., Duvall, M.R., Price, R.A., Hills, H.G., Qiu, Y.-L., Kron, K.A., Rettigg, J.H., Michaels, H.J., Kress, W.J., Karol, K.G., Clark, W.D., Hedren, M., Gaut, B.S., Jansen, R.K., Kim, K.-J., Wimpee, C.F., Smith, J.F., Furnier, G.R., Strauss, S.H., Xiang, Q.-Y., Plunkett, G.M., Soltis, P.S., Swensen, S.M., Williams, S.E., Gadek, P.A., Quinn, C.J., Eguiarte, L.E., Golenberg, E., Learn, G.H., Graham, S.W., Barrett, S.C.H., Dayanandan, S. andAlbert, V.A. 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid generbcL. Ann. Missouri Bot. Gard.80: 528–580.

    Article  Google Scholar 

  • Cook, C.D.K. 1982. Pollination mechanisms in the Hydrocharitaceae.In J.J. Symoens, S.S. Hooper and P. Compere, eds. Studies on Aquatic Vascular Plants, Royal Botanical Society of Belgium, Brussels, pp. 1–15.

    Google Scholar 

  • Cook, C.D.K. andLuond, R. 1982. A revision of the genusNechamandra (Hydrocharitaceae). Aquat. Bot.13: 505–513.

    Article  Google Scholar 

  • Cox, P.A. 1983. Search theory, random motion, and the convergent evolution of pollen and spore morphology in aquatic plans. Am. Nat.121: 9–31.

    Article  Google Scholar 

  • Cox, P.A. 1988. Hydrophilous pollination. Ann. Rev. Ecol. Syst.19: 261–280.

    Article  Google Scholar 

  • Cox, P.A. 1991. Abiotic pollination: an evolutionary escape for animal-pollinated angiosperms. Phill. Trans. R. Soc. Lond. B333:217–224.

    Google Scholar 

  • Cox, P.A. andTomlinson, P.B. 1988. Pollination ecology of a seagrass,Thalassia testudinum (Hydrocharitaceae). in St. Croix. Amer. J. Bot.75: 958–965.

    Article  Google Scholar 

  • Dahlgren, R.M.T. 1985. The Families of the Monocytyledons. Springer-Verlag, Berlin.

    Google Scholar 

  • Eckhardt, T. 1964. Monocotyledonae 1. Reihe Helobiae.In H. Melchior, ed., A. Engler's Syllabus der Pflanzenfamilien, 12th edn, Borntraeger, Berlin, pp. 499–512.

    Google Scholar 

  • Engler, A. 1904. Syllabus der Pflanzenfamilien. Edn. IV. Wihelm Engelmann, Leipzig.

    Google Scholar 

  • Ernst-schwarzenbach, M. 1945. Zur Blutenbiologie einiger Hydrocharitaceen. Ber. Schweiz. Bot. Ges.55: 33–69.

    Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution39: 783–791.

    Article  Google Scholar 

  • Felsenstein, J. 1993. Phylogeny inference Package (PHYLIP) version 3.5c. University of Washington, Seattle.

    Google Scholar 

  • Felsentein, J. andKishino, H. 1993. Is there something wrong with the bootstrap on phylogenies? A reply to Hills and Bull. Syst. Biol.42: 193–200.

    Article  Google Scholar 

  • Hasebe, M., Omori, T., Nakazawa, M., Sano, T., Kato, M. andIwatsuki, K. 1994.rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proc. Natl. Acad. Sci. USA91: 5730–5734.

    PubMed  CAS  Article  Google Scholar 

  • Hasegawa, M., Kishino, H. andYano, T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol.22: 160–174.

    PubMed  CAS  Article  Google Scholar 

  • Hutchinson, J. 1959. The Families of Flowering Plants. 2: Monocotyledons. 2nd edn. Oxford, Clarendon Press.

    Google Scholar 

  • Johnson, L.A., Schultz, J.L., Soltis, D.E. andSoltis, P.A. 1996. Monophyly and generic relationships of Polemoniaceae based onmatK sequences. Amer. J. Bot.83: 1207–1224.

    CAS  Article  Google Scholar 

  • Johnson, L.A. andSoltis, D.E. 1994.matK sequences and phylogenetic reconstruction in Saxifragacae s. s.. Syst. Bot.19: 143–156.

    Article  Google Scholar 

  • Johnson, L.A. andSoltis, D.E. 1995. Phylogenetic inference in Saxifragaceae sensu stricto andGilia (Polemoniaceae) usingmatK sequences. Ann. Missouri Bot. Gard.82: 149–175.

    Article  Google Scholar 

  • Kadono, Y. 1994. Aquatic Plants of Japan. Buń-ichi Sogo Shuppan, Co., Ltd, Tokyo.

    Google Scholar 

  • Kaul, R.B. 1968. Floral morphology and phylogeny in the Hydrocharitaceae. Phytomorphology18: 13–35.

    Google Scholar 

  • Kaul, R.B. 1969. Morphology and development of the flowers ofBootia cordata, Ottelia alismoides, and their synthetic hybrid (Hydrocharitaceae). Amer. J. Bot.56: 951–959.

    Article  Google Scholar 

  • Kaul, R.B. 1970. Evolution and adaptation of inflorescences in the Hydrocharitaceae. Amer. J. Bot.57: 708–715.

    Article  Google Scholar 

  • Kimura, M. 1980. A simple for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol.16: 111–120.

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Les, D.H., Garvin, D.K. andWimpee, C.F. 1993. Phylogenetic studies in the monocot subclass Alismatidae: evidence for a reappraisal of the aquatic order Najadales. Mol. Phylogenet. Evol.2: 304–314.

    PubMed  CAS  Article  Google Scholar 

  • Les, D.H. andHaynes, R.R. 1995. Systematics of subclass Alismatidae: a systhesis of approaches.In P.J. Rudall, P.J. Cribb, D.F. Culter and C.J. Humphries, eds., Monocotyledons: Systematics and Evolution, Royal Botanic Gardens, Kew, pp. 353–377.

    Google Scholar 

  • Maddison, W.P. andMaddison, D.R. 1992. MacClade: Analysis of Phylogeny and Character Evolution. Version 3.0. Sinauer, Sunderland, MA.

    Google Scholar 

  • Maier, R.M., Neckermann, K., Igloi, G.L. andKossel, H. 1995. Complete sequence of the maize chroloplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J. Mol. Biol.251: 614–628.

    PubMed  CAS  Article  Google Scholar 

  • McConchie, C.A. 1983. Floral development ofMaidenia rubra Rendle (Hydrocharitaceae). Aust. J. Bot.31: 585–603.

    Article  Google Scholar 

  • Miki, S. 1937. The origin ofNajas andPotamogeton. Bot. Mag. Tokyo51: 472–480.

    Google Scholar 

  • Palmer, J.D. 1986. Isolation and structural analysis of chroloplast DNA. Methods in Enzymology118: 167–186.

    CAS  Article  Google Scholar 

  • Pettitt, J.M. 1980. Reproduction in seagrasses: Nature of the pollen and receptive surface of the stigma in the Hydrocharitaceae. Ann. Bot.45: 257–272.

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sculthorpe, C.D. 1967. The Biology of Aquatic Vascular Plants. Edward Arnold, London.

    Google Scholar 

  • Shaffer-Fehre, M. 1991a The endotegmen tuberculae: an account of little-known structures from the seed coat of the Hydrocharitoideae (Hydrocharitaceae) andNajas (Najadaceae). Bot. J. Linn. Soc.107: 169–188.

    Google Scholar 

  • Shaffer-Fehre, M. 1991b The position ofNajas within the subclass Alismatidae (Monocotyledones) in the light of new evidence from seed coat structures in the Hydrocharitoideae (Hydrocharitaceae). Bot. J. Linn. Soc.107: 189–209.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Singh, V. 1965. Morphological and anatomical studies in Helobiae. III. Vascular anatomy of the node and flower of Najadaceae. Proc. Indian Acad. Sci. B.61: 98–108.

    Google Scholar 

  • Soltis, D.E., Kuzoff, R.E., Conti, E., Gornall, R. andFerguson, K. 1996.matK andrbcL gene sequence data indicate thatSaxifraga (saxifragaceae) is polyphyletic. Amer. J. Bot.83: 371–382.

    CAS  Article  Google Scholar 

  • Soltis, D.E., Soltis, P.S., Clegg, M.T. andDurbin, M. 1990.rbcL sequence and chroloplast divergence and phylogenetic relationships in Saxifragaceae sensu lato. Proc. Natl. Acad. Sci. USA.87: 4640–4644.

    PubMed  CAS  Article  Google Scholar 

  • Takhtajan, A. 1966. Systema et Phylogenia Magnoliophytorum. Nauka, Moscow.

    Google Scholar 

  • Tomlinson, P. B. 1982. Anatomy of the Monocotyledons VII. Helobiae (Alismatidae). Clarendon Press, Oxford.

    Google Scholar 

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Tanaka, N., Setoguchi, H. & Murata, J. Phylogeny of the family hydrocharitaceae inferred fromrbcL andmatK gene sequence data. J. Plant Res. 110, 329–337 (1997). https://doi.org/10.1007/BF02524931

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  • DOI: https://doi.org/10.1007/BF02524931

Key words

  • Hydrocharitaceae
  • Hydrophily
  • matK gene sequences
  • Molecular phylogeny
  • Pollination mechanisms
  • rbcL gene sequences