Download PDF
Plant Biol (Stuttg) 2002; 4(1): 86-93
DOI: 10.1055/s-2002-20440
Original Paper
Georg Thieme Verlag Stuttgart ·New York

The Genus Clusia L.: Molecular Evidence for Independent Evolution of Photosynthetic Flexibility

A. Vaasen 1 , D. Begerow 1 , U. Lüttge 2 , R. Hampp 1
  • 1 Institute of Botany, University of Tübingen, Tübingen, Germany
  • 2 Institute of Botany, Darmstadt University of Technology, Darmstadt, Germany
Further Information

Publication History

October 10, 2001

November 13, 2001

Publication Date:
28 February 2002 (online)

   Permissions and Reprints

Abstract

Members of the Clusiaceae genus Clusia (tropical trees and shrubs) belong to the small group of dicotyledonous trees which are able to perform crassulacean acid metabolism (CAM). Most of the species are able to switch between C3 and CAM modes of photosynthesis and only a few are restricted to either C3 or CAM. In order to discover possible phylogenetic relationships with regard to the mode of photosynthesis, we investigated 17 species of the genus Clusia, and one species each of the Clusiaceae genera Oedematopus and Hypericum on the basis of internal transcribed spacer (ITS) sequences between the 18S and 26S coding regions of nuclear ribosomal DNA. Little length variation was detected in the ITS region of Clusia species. ITS1 sequences ranged from 255 to 260 bp and ITS2 sequences from 208 to 210 bp. Neighbour-joining and parsimony analyses of these sequences resulted in considerable differences in cluster formation when compared to a classification based on morphological characteristics. The molecular data also give no indication of a group-specific evolution of modes of photosynthesis, i.e., C3 and CAM. We thus conclude that CAM has evolved independently several times within the genus Clusia.

Abbreviations

CAM: crassulacean acid metabolism

EDTA: ethylenediamine tetraacetic acid

ITS: internal transcribed spacer

PAUP*: phylogenetic analysis using parsimony (*and other methods)

PCR: polymerase chain reaction

TAE: tris-glacial acetic acid-EDTA

Key words

Clusia - Clusiaceae - internal transcribed spacer (ITS) - ribosomal DNA - molecular phylogeny - crassulacean acid metabolism (CAM)

References

  • 01 Ainouche,  A.-K., and Bayer,  R. J.. (1999);  Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA.  American Journal of Botany. 86 590-607
    Google Scholar
  • 02 Alice,  L. A., and Campbell,  C. S.. (1999);  Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences.  American Journal of Botany. 86 81-97
    Google Scholar
  • 03 Baldwin,  B. G.. (1992);  Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae.  Molecular Phylogenetics and Evolution. 1 3-16
    Google Scholar
  • 04 Baldwin,  B. G.. (1993);  Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined.  American Journal of Botany. 80 222-238
    Google Scholar
  • 05 Baldwin,  B. G.,, Sanderson,  M. J.,, Porter,  J. M.,, Wojciechowski,  M. F.,, Campell,  C. S.,, and Donoghue,  M. J.. (1995);  The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny.  Annals of the Missouri Botanical Garden. 82 247-277
    Google Scholar
  • 06 Ball,  E.,, Hann,  J.,, Kluge,  M.,, Lee,  H. S. J.,, Lüttge,  U.,, Orthen,  B.,, Popp,  M.,, Schmitt,  A.,, and Ting,  I. P.. (1991);  Ecophysiological comportment of the tropical CAM-tree Clusia in the field.  New Phytologist. 117 473-481
    Google Scholar
  • 07 Bayer,  R. J.. (1996);  Phylogenetic relationships in Sarraceniaceae based on rbcL and ITS sequences.  Systematic Botany. 21 121-134
    Google Scholar
  • 08 Bittrich,  V., and Amaral,  M. C. E.. (1996);  Flower morphology and pollination biology of some Clusia species from the Gran Sabana (Venezuela).  Kew Bulletin. 51 681-694
    Google Scholar
  • 09 Borland,  A. M.,, Griffiths,  H.,, Maxwell,  C.,, Broadmeadow,  M. S. J.,, Griffiths,  N. M.,, and Barnes,  J. D.. (1992);  On the ecophysiology of the Clusiaceae in Trinidad: expression of CAM in Clusia minor L. during the transition from wet to dry season and characterization of three endemic species.  New Phytologist. 122 349-357
    Google Scholar
  • 10 D'Arcy,  W. G.. (1980) Family 123, Vol. 67. Guttiferae, Flora of Panama, Part VI. Woodson, R. E. Jr. and Schery, R. W., eds. Annals of the Missouri Botanical Garden pp. 969-1043
    Google Scholar
  • 11 Diaz,  M.,, Haag-Kerwer,  A.,, Wingfield,  R.,, Ball,  E.,, Olivares,  E.,, Grams,  T. E. E.,, Ziegler,  H.,, and Lüttge,  U.. (1996);  Relationships between carbon and hydrogen isotope ratios and nitrogen levels in leaves of Clusia species and two other Clusiaceae genera at various sites and different altitudes in Venezuela.  Trees. 10 351-358
    CrossrefPubMedGoogle Scholar
  • 12 Engler,  A.. (1858 - 1879) Guttiferae et Quiinaceae. Flora Brasiliensis, XII, pars. I. de Martius, C. F. P. and Eichler, A. G., eds. pp. 380 - 486
    Google Scholar
  • 13 Francisco-Ortega,  J.,, Fuertes-Aguilar,  J.,, Gomez-Campo,  C.,, Santos-Guerra,  A.,, and Jansen,  R. K.. (1999);  Internal transcribed spacer sequence phylogeny of Crambe L. (Brassicaceae): molecular data reveal two old world disjunctions.  Molecular Phylogenetics and Evolution. 11 361-380
    CrossrefPubMedGoogle Scholar
  • 14 Franco,  A. C.,, Ball,  E.,, and Lüttge,  U.. (1992);  Differential effects of drought and light levels on accumulation of citric and malic acids during CAM in Clusia. .  Plant, Cell and Environment. 15 390-829
    PubMedGoogle Scholar
  • 15 Franco,  A. C.,, Olivares,  E.,, Ball,  E.,, Lüttge,  U.,, and Haag-Kerwer,  A.. (1994);  In situ studies of crassulacean acid metabolism in several sympatric species of tropical trees of the genus Clusia. .  New Phytologist. 126 203-211
    PubMedGoogle Scholar
  • 16 Grams,  T. E. E.,, Haag-Kerwer,  A.,, Olivares,  E.,, Bass,  E.,, Arndt,  S.,, Popp,  M.,, Medina,  E.,, and Lüttge,  U.. (1997);  Comparative measurements of chlorophyll a fluorescence, acid accumulation and gas exchange in exposed and shaded plants of Clusia minor L. and Clusia multiflora H. B. K. in the field.  Trees. 11 240-247
    CrossrefPubMedGoogle Scholar
  • 17 Grams,  T. E. E.,, Herzog,  B.,, and Lüttge,  U.. (1998);  Are there species in the genus Clusia with obligate C3-photosynthesis?.  Journal of Plant Physiology. 152 1-9
    PubMedGoogle Scholar
  • 18 Gustafsson,  M. G. H.. (2000);  Floral morphology and relationships of Clusia gundlachii with a discussion of floral organ identity and diversity in the genus Clusia. .  International Journal of Plant Sciences. 161 43-53
    CrossrefPubMedGoogle Scholar
  • 19 Haag-Kerwer,  A.,, Grams,  T. E. E.,, Olivares,  E.,, Ball,  E.,, Arndt,  S.,, Popp,  M.,, Medina,  E.,, and Lüttge,  U.. (1996);  Comparative measurements of gas-exchange, acid accumulation and chlorophyll a fluorescence of different species of Clusia showing C3 photosynthesis, or crassulacean acid metabolism, at the same field site in Venezuela.  New Phytologist. 134 215-226
    PubMedGoogle Scholar
  • 20 Hammel,  B. E.. (1986);  New species of Clusiaceae from Central America with notes on Clusia and synonymy in the tribe Clusieae. .  Selbyana. 9 112-120
    PubMedGoogle Scholar
  • 21 Hershkovitz,  M. A., and Lewis,  L. A.. (1996);  Deep-level diagnostic value of the rDNA-ITS region.  Molecular Biology and Evolution. 13 1276-1295
    PubMedGoogle Scholar
  • 22 Hershkovitz,  M. A., and Zimmer,  E. A.. (1996);  Conservation pattern in angiosperm rDNA ITS2 sequences.  Nucleic Acids Research. 24 2857-2867
    CrossrefPubMedGoogle Scholar
  • 23 Herzog,  B.,, Hoffmann,  S.,, Hartung,  W.,, and Lüttge,  U.. (1999);  Comparison of photosynthetic responses of the sympatric tropical C3 species Clusia multiflora H. B. K. and the C3-CAM intermediate species Clusia minor L. to irradiance and drought stress in a phytotron.  Plant Biology. 1 460-470
    PubMedGoogle Scholar
  • 24 Herzog,  B.,, Hübner,  C.,, Ball,  E.,, Bastos,  R. d. N.,, Franco,  A. C.,, Scarano,  F. R.,, and Lüttge,  U.. (1999);  Comparative study of the C3/CAM intermediate species Clusia parviflora Saldanha et Engl. and the obligate CAM species Clusia hilariana Schlecht. growing sympatrically exposed and shaded in the coastal restinga of Brazil.  Plant Biology. 1 453-459
    PubMedGoogle Scholar
  • 25 Jobes,  D. V., and Thien,  L. B.. (1997);  A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences.  Plant Molecular Biology Reporter. 15 326-334
    CrossrefPubMedGoogle Scholar
  • 26 Käss,  E., and Wink,  M.. (1997);  Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbsL gene and ITS 1 + 2 regions of rDNA.  Plant Systematics and Evolution. 208 139-167
    CrossrefPubMedGoogle Scholar
  • 27 Kim,  K.-J., and Jansen,  R. K.. (1994);  Comparisons of phylogenetic hypotheses among different data sets in dwarf dandelions (Krigia, Asteraceae): Additional information from internal transcribed spacer sequences of nuclear ribosomal DNA.  Plant Systematics and Evolution. 190 157-185
    CrossrefPubMedGoogle Scholar
  • 28 Liu,  J.-S., and Schardl,  C. L.. (1994);  A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes.  Plant Molecular Biology. 26 775-778
    CrossrefPubMedGoogle Scholar
  • 29 Lüttge,  U.. (1991);  Clusia - Morphogenetische, physiologische und biochemische Strategien von Baumwürgern im tropischen Wald.  Naturwissenschaften. 78 49-58
    CrossrefPubMedGoogle Scholar
  • 30 Lüttge,  U.. (1999);  One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour - Review.  Plant Biology. 1 138-148
    PubMedGoogle Scholar
  • 31 Lüttge,  U.. (2000);  Photosynthese-Physiotypen unter gleichen Morphotypen, Species und bei Klonen: Kann ökophysiologische Plastizität zur Entstehung von Diversität beitragen?.  Berichte der Reindhold Tüxen-Gesellschaft. 12 319-334
    PubMedGoogle Scholar
  • 32 Maguire,  B.. (1958) Guttiferae. The botany of the Guayana Highland III. Maguire, B. and Wurdack, J. J., eds. Memoirs of the New York Botanical Garden 10 Nr. 1 pp. 49-61
    Google Scholar
  • 33 Maguire,  B.. (1961) Guttiferae. The botany of the Guayana Highland IV. (2). Maguire, B. and Wurdack, J. J., eds. Memoirs of the New York Botanical Garden 10 Nr. 4 pp. 21-32
    Google Scholar
  • 34 Maguire,  B.. (1966);  The genus Clusia (Guttiferae) in Suriname.  Acta Botanica Neerlandica. 15 63-75
    PubMedGoogle Scholar
  • 35 Maguire,  B.. (1976);  Apomixis in the genus Clusia (Clusiaceae) - a preliminary report.  Taxon. 25 241-244
    PubMedGoogle Scholar
  • 36 Maguire,  B.. (1978);  Notes on the Clusiaceae - chiefly of Panama. II.  Phytologia. 38 203-214
    PubMedGoogle Scholar
  • 37 Maguire,  B.. (1979);  On the genus Clusia (Clusiaceae) in Mexico.  Taxon. 28 13-18
    PubMedGoogle Scholar
  • 38 Möller,  M., and Cronk,  Q. C. B.. (1997);  Origin and relationships of Saintpaulia (Gesneriaceae) based on ribosomal DNA internal transcribed spacer (ITS) sequences.  American Journal of Botany. 84 956-965
    PubMedGoogle Scholar
  • 39 Nogueira,  P. C. d. L.,, Bittrich,  V.,, Shepherd,  G. J.,, Lopes,  A. V.,, and Marsaioli,  A. J.. (2001);  The ecological and taxonomic importance of flower volatiles of Clusia species (Guttiferae).  Phytochemistry. 56 443-452
    CrossrefPubMedGoogle Scholar
  • 40 Pipoly,  J. J. I., and Graff,  A.. (1995);  A synopsis of the genus Clusia sections Criuvopsis and Brachystemon (Clusiaceae) in northern South America.  Sida. 16 505-528
    PubMedGoogle Scholar
  • 41 Pipoly,  J. J.,, Kearns,  D. M.,, and Berry,  P. E.. (1998) Clusia. . Flora of the Venezuelan Guayana, Vol. 4. Caesalpiniaceae-Ericaceae. Berry, P. E., Holst, B. K., and Yatskievych, K., eds. St. Louis, Missouri; Missouri Botanical Garden Press pp. 260-294
    Google Scholar
  • 42 Planchon,  M. J.-E., and Triana,  J.. (1860);  Mémoire sur la famille des Guttifères.  Annales des Sciences Naturelles, Série 4, Botanique. 13 306-376
    PubMedGoogle Scholar
  • 43 Posada,  D., and Drandall,  K. A.. (1998);  Modeltest: testing the model of DNA substitution.  Bioinformatics. 9 817-818
    PubMedGoogle Scholar
  • 44 Raven,  J. A., and Spicer,  R. A.. (1996) The evolution of crassulacean acid metabolism. Crassulacean acid metabolism. Biochemisty, ecophysiology and evolution, Ecological Studies 114. Winter, K. and Smith, J. A. C., eds. Berlin, Heidelberg; Springer-Verlag pp. 360-385
    Google Scholar
  • 45 Sage,  R. F.. (2001);  Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome.  Plant Biology. 3 202-213
    Article in Thieme ConnectPubMedGoogle Scholar
  • 46 Sambrook,  J., and Russell,  D. W.. (2001) Molecular Cloning: a laboratory manual. 1. New York; Cold Spring Harbor
    Google Scholar
  • 47 Sang,  T.,, Crawford,  D. J.,, Kim,  S.-C.,, and Stuessy,  T. F.. (1994);  Radiation of the endemic genus Dendroseris (Asteraceae) on the Juan Fernandez Islands: evidence from sequences of the ITS regions of nuclear ribosomal DNA.  American Journal of Botany. 81 1494-1501
    PubMedGoogle Scholar
  • 48 Sang,  T.,, Crawford,  D. J.,, and Stuessy,  T. F.. (1995);  Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution.  Proceedings of the National Academy of Science of the United States of America. 92 6813-6817
    PubMedGoogle Scholar
  • 49 Standley,  P. C.. (1937);  Flora of Costa Rica.  (Publications of) Field Museum of Natural History - Botanical Series. 18 1-780
    PubMedGoogle Scholar
  • 50 Suh,  Y.,, Thien,  L. B.,, Reeve,  H. E.,, and Zimmer,  E. A.. (1993);  Molecular evolution and phylogenetic implications of internal transcribed spacer sequences of ribosomal DNA in Winteraceae.  American Journal of Botany. 80 1042-1055
    PubMedGoogle Scholar
  • 51 Susanna,  A.,, Garcia Jacas,  N.,, Soltis,  D. E.,, and Soltis,  P. S.. (1995);  Phylogenetic relationships in tribe Cardueae (Asteraceae) based on ITS sequences.  American Journal of Botany. 82 1056-1068
    PubMedGoogle Scholar
  • 52 Swofford,  D. L.. (1999) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sunderland, Massachusetts; Sinauer Associates
    Google Scholar
  • 53 Vesque,  J.. (1893) Guttiferae. Monographieae Phanerogamarum, Vol. 8. de Candolle, A. and de Candolle, C., eds. Paris; G. Masson
    Google Scholar
  • 54 White,  T. J.,, Bruns,  T.,, Lee,  S.,, and Taylor,  J.. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: A guide to methods and applications. Innis, M. A., Gelfand, D. H., Sninsky, J. J., and White, T. J., eds. San Diego; Academic Press pp. 315-322
    Google Scholar
  • 55 Willis,  J. C.. (1973) A dictionary of the flowering plants and ferns. Cambridge; University Press
    Google Scholar
  • 56 Winter,  K., and Smith,  J. A. C.. (1996) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution. Ecological studies 114. Berlin, Heidelberg; Springer-Verlag pp. 449
    Google Scholar
  • 57 Wojciechowski,  M. F.,, Sanderson,  M. J.,, Baldwin,  B. G.,, and Donoghue,  M. J.. (1993);  Monophyly of aneuploid Astragalus (Fabaceae): evidence from nuclear ribosomal DNA internal transcribed spacer sequences.  American Journal of Botany. 80 711-722
    PubMedGoogle Scholar
  • 58 Yang,  Y.-W.,, Lai,  K.-N.,, Tai,  P.-Y.,, Ma,  D.-P.,, and Li,  W.-H.. (1999);  Molecular phylogenetic studies of Brassica, Rorippa, Arabidopsis and allied genera based on the internal transcribed spacer region of 18S-25S rDNA.  Molecular Phylogenetics and Evolution. 13 455-462
    CrossrefPubMedGoogle Scholar
  • 59 Yuan,  Y.-M., and Küpfer,  P.. (1995);  Molecular phylogenetics of the subtribe Gentianinae (Gentianaceae) inferred from the sequences of internal transcribed spacers (ITS) of nuclear ribosomal DNA.  Plant Systematics and Evolution. 196 207-226
    CrossrefPubMedGoogle Scholar
  • 60 Zotz,  G., and Winter,  K.. (1993);  Short-term regulation of crassulacean acid metabolism activity in a tropical hemiepiphyte, Clusia uvitana. .  Plant Physiology. 102 835-841
    PubMedGoogle Scholar

A. Vaasen

Institute of Botany
University of Tübingen

72076 Tübingen
Germany

Email: anja.vaasen@uni-tuebingen.de

Section Editor: H. Rennenberg

      >