PDF herunterladen
Plant Biol (Stuttg) 2006; 8(6): 758-764
DOI: 10.1055/s-2006-924459
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

A New Model for the Evolution of Carnivory in the Bladderwort Plant (Utricularia): Adaptive Changes in Cytochrome c Oxidase (COX) Provide Respiratory Power

L. Laakkonen1 , R. W. Jobson2 , V. A. Albert3
  • 1Helsinki Bioenergetics Group, Programme for Structural Biology and Biophysics, Institute of Biotechnology, Biocenter 3 (Viikinkaari 1), PB 65, University of Helsinki, 00014 Helsinki, Finland
  • 2Department of Ecology and Evolutionary Biology, 2052 Kraus Natural Science Bldg., 830 N. University, Ann Arbor, MI 48109-1048, USA
  • 3Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway
Weitere Informationen

Publikationsverlauf

Received: December 28, 2005

Accepted: June 30, 2006

Publikationsdatum:
03. Januar 2007 (online)

   Lizenzen und Reprints

Abstract

The evolution of carnivorous plants has been modeled as a selective tradeoff between photosynthetic costs and benefits in nutrient-poor habitats. Although possibly applicable for pitfall and flypaper trappers, more variables may be required for active trapping systems. Bladderwort (Utricularia) suction traps react to prey stimuli with an extremely rapid release of elastic instability. Trap setting requires considerable energy to engage an active ion transport process whereby water is pumped out through the thin bladder walls to create negative internal pressure. Accordingly, empirical estimates have shown that respiratory rates in bladders are far greater than in leafy structures. Cytochrome c oxidase (COX) is a multi-subunit enzyme that catalyzes the respiratory reduction of oxygen to water and couples this reaction to translocation of protons, generating a transmembrane electrochemical gradient that is used for the synthesis of adenosine triphosphate (ATP). We have previously demonstrated that two contiguous cysteine residues in helix 3 of COX subunit I (COX I) have evolved under positive Darwinian selection. This motif, absent in ≈ 99.9 % of databased COX I proteins from eukaryotes, Archaea, and Bacteria, lies directly at the docking point of COX I helix 3 and cytochrome c. Modeling of bovine COX I suggests the possibility that a vicinal disulfide bridge at this position could cause premature helix termination. The helix 3-4 loop makes crucial contacts with the active site of COX, and we postulate that the C‐C motif might cause a conformational change that decouples (or partly decouples) electron transport from proton pumping. Such decoupling would permit bladderworts to optimize power output (which equals energy times rate) during times of need, albeit with a 20 % reduction in overall energy efficiency of the respiratory chain. A new model for the evolution of bladderwort carnivory is proposed that includes respiration as an additional tradeoff parameter.

Key words

Bladderworts - carnivorous plants - cytochrome c oxidase - conformational change - COX - electron transport - energetics - protein structure - proton pumping - respiration - Utricularia.

References

  • 1 Abramson J., Riistama S., Larsson G., Jasaitis A., Svensson-Ek M., Laakkonen L., Puustinen A., Iwata S., Wikstrom M.. The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site.  Nature Structural Biology. (2000);  7 910-917
    CrossrefPubMedSuche in Google Scholar
  • 2 Adamec L.. Photosynthetic characteristics of the aquatic carnivorous plant Aldrovanda vesiculosa.  Aquatic Botany. (1997);  59 297-306
    CrossrefPubMedSuche in Google Scholar
  • 45 Adamec L.. Respiration and photosynthesis of bladders and leaves of aquatic Utricularia species.  Plant Biology. (2006);  8 765-769
    Thieme ConnectPubMedSuche in Google Scholar
  • 46 Albert V. A., Williams S. E., Chase M. W.. Carnivorous plants: phylogeny and structural evolution.  Science. (1992);  257 1491-1495
    PubMedSuche in Google Scholar
  • 3 Brooks B. R., Bruccoleri R. E., Olafson B. D., States B. J., Swaminathan S., Kaplus M.. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations.  Journal of Computational Chemistry. (1983);  4 187-217
    CrossrefPubMedSuche in Google Scholar
  • 4 Burke P. V., Poyton R. O.. Structure/function of oxygen-regulated isoforms in cytochrome c oxidase.  Journal of Experimental Biology. (1998);  201 1163-1175
    PubMedSuche in Google Scholar
  • 5 Ellison A. M., Gotelli N. J.. Evolutionary ecology of carnivorous plants.  Trends in Ecology and Evolution. (2001);  16 623-629
    CrossrefPubMedSuche in Google Scholar
  • 6 Ferguson-Miller S., Brautigan D. L., Margoliash E.. Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding to mitochondrial cytochrome c oxidase.  Journal of Biological Chemistry. (1976);  251 1104-1115
    PubMedSuche in Google Scholar
  • 7 Fineran B. A., Lee M. S. L.. Organization of mature glands on the trap and other organs of the bladderwort Utricularia monanthos.  Protoplasma. (1980);  103 17-34
    CrossrefPubMedSuche in Google Scholar
  • 8 Flöck D., Helms V.. Protein-protein docking of electron transfer complexes: cytochrome c oxidase and cytochrome c.  Proteins. (2002);  47 75-85
    CrossrefPubMedSuche in Google Scholar
  • 9 Forterre Y., Skotheim J. M., Dumais J., Mahadevan L.. How the Venus flytrap snaps.  Nature. (2005);  433 421-425
    PubMedSuche in Google Scholar
  • 10 Friday L. E.. Measuring investment in carnivory: seasonal and individual variation in trap number and biomass in Utricularia vulgaris L.  New Phytologist. (1992);  121 439-445
    CrossrefPubMedSuche in Google Scholar
  • 11 Givnish T. J.. Ecology and evolution of carnivorous plants. Abrahamson, W. G., ed. Plant-Animal Interactions. New York; McGraw-Hill (1989): 242-290
    Suche in Google Scholar
  • 12 Givnish T. J., Burkhardt E. L., Happel R. E., Weintraub J. D.. Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist nutrient-poor habitats.  American Naturalist. (1984);  124 479-497
    CrossrefPubMedSuche in Google Scholar
  • 13 Grossman L. I., Schmidt T. R., Wildman D. E., Goodman M.. Molecular evolution of aerobic energy metabolism in primates.  Molecular Phylogenetics and Evolution. (2001);  18 26-36
    CrossrefPubMedSuche in Google Scholar
  • 14 Guisande C., Andrade C., Granado-Lorencio C., Duque S. R., Nunez-Avellaneda M.. Effects of zooplankton and conductivity on tropical Utricularia foliosa investment in carnivory.  Aquatic Ecology. (2000);  34 137-142
    CrossrefPubMedSuche in Google Scholar
  • 15 Guisande C., Aranguren N., Andrade-Sossa C., Prat N., Granado-Lorencio C., Barrios M. L., Bolivar A., Nunez-Avellaneda M., Duque S. R.. Relative balance of the cost and benefit associated with carnivory in the tropical Utricularia foliosa.  Aquatic Botany. (2004);  80 271-282
    CrossrefPubMedSuche in Google Scholar
  • 16 Hodick D., Sievers A.. On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis).  Planta. (1989);  179 32-42
    CrossrefPubMedSuche in Google Scholar
  • 17 Humphrey W., Dalke A., Schulten K.. VMD: visual molecular dynamics.  Journal of Molecular Graphics. (1996);  14 33-38
    CrossrefPubMedSuche in Google Scholar
  • 18 Jobson R. W., Albert V. A.. Molecular rates parallel diversification contrasts between carnivorous plant sister lineages.  Cladistics. (2002);  18 127-136
    PubMedSuche in Google Scholar
  • 19 Jobson R. W., Nielsen R., Laakkonen L., Wikström M., Albert V. A.. Adaptive evolution of cytochrome c oxidase: infrastructure for a carnivorous plant radiation.  Proceedings of the National Academy of Sciences of the USA. (2004);  101 18064-18068
    CrossrefPubMedSuche in Google Scholar
  • 20 Jobson R. W., Playford J., Cameron K. M., Albert V. A.. Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL‐F DNA sequences: implications for character evolution and biogeography.  Systematic Botany. (2003);  28 157-171
    PubMedSuche in Google Scholar
  • 21 Juniper B. E., Robins R. J., Joel D. M.. The Carnivorous Plants. London, UK; Academic Press, Ltd (1989)
    Suche in Google Scholar
  • 22 Kadenbach B.. Intrinsic and extrinsic uncoupling of oxidative phosphorylation.  Biochimica et Biophysica Acta. (2003);  1604 77-94
    PubMedSuche in Google Scholar
  • 23 Knight S. E.. Costs of carnivory in the common bladderwort, Utricularia macrorhiza.  Oecologia. (1992);  89 348-355
    PubMedSuche in Google Scholar
  • 24 Méndez M., Karlsson P. S.. Costs and benefits of carnivory in plants: insights from the photosynthetic performance of four carnivorous plants in a subarctic environment.  Oikos. (1999);  86 105-112
    PubMedSuche in Google Scholar
  • 25 Mitchell P.. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism.  Nature. (1961);  191 144-148
    PubMedSuche in Google Scholar
  • 26 Mitchell P.. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation.  Biological Reviews of the Cambridge Philosophical Society. (1966);  41 445-502
    PubMedSuche in Google Scholar
  • 27 Müller K., Borsch T., Legendre L., Porembski S., Theisen I., Barthlott W.. Evolution of carnivory in Lentibulariaceae and the Lamiales.  Plant Biology. (2004);  6 447-490
    Thieme ConnectPubMedSuche in Google Scholar
  • 28 Ostermeier C., Harrenga A., Ermler U., Michel H.. Structure at 2.7 Å resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 10547-10553
    CrossrefPubMedSuche in Google Scholar
  • 29 Ribacka C., Verkhovsky M. I., Belevich I., Bloch D.A., Puustinen A., Wikström M.. An elementary reaction step of the proton pump is revealed by mutation of tryptophan-164 to phenylalanine in cytochrome c oxidase from Paracoccus denitrificans.  Biochemistry. (2005);  44 16502-16512
    CrossrefPubMedSuche in Google Scholar
  • 30 Roberts V.A., Pique M. E.. Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete, systematic search.  Journal of Biological Chemistry. (1999);  274 38051-38060
    CrossrefPubMedSuche in Google Scholar
  • 31 Richards J. H.. Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important?.  American Journal of Botany. (2001);  88 170-176
    PubMedSuche in Google Scholar
  • 32 Saraste M.. Oxidative phophorylation at the fin de siecle.  Science. (1999);  283 1488-1492
    CrossrefPubMedSuche in Google Scholar
  • 33 Schmidt T. R., Wildman D. E., Uddin M., Opazo J. C., Goodman M., Grossman L. I.. Rapid electrostatic evolution at the binding site for cytochrome c on cytochrome c oxidase in anthropoid primates.  Proceedings of the National Academy of Sciences of the USA. (2005);  102 6379-6384
    CrossrefPubMedSuche in Google Scholar
  • 34 Sharma V., Puustinen A., Wikström M., Laakkonen L.. Sequence analysis of the cbb3 oxidases and an atomic model for the Rhodobacter sphaeroides enzyme.  Biochemistry. (2006);  45 5754-5765
    CrossrefPubMedSuche in Google Scholar
  • 35 Skotheim J. M., Mahadevan L.. Physical limits and design principles for plant and fungal movements.  Science. (2005);  308 1308-1310
    CrossrefPubMedSuche in Google Scholar
  • 36 Soulimane T., Buse G., Bourenkov G. P., Bartunik H. D., Huber R., Than M. E.. Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus.  EMBO Journal. (2000);  17 1766-1776
    PubMedSuche in Google Scholar
  • 37 Stucki J.. The optimal efficiency and the economic degtrees of coupling of oxidative phosphorylation.  European Journal of Biochemistry. (1980);  109 269-283
    CrossrefPubMedSuche in Google Scholar
  • 38 Svensson-Ek M., Abramson J., Larsson G., Tornroth S., Brzezinski P., Iwata S.. The X‐ray crystal structures of wild-type and EQ(I‐286) mutant cytochrome c oxidases from Rhodobacter sphaeroides.  Journal of Molecular Biology. (2002);  321 329-339
    CrossrefPubMedSuche in Google Scholar
  • 39 Sydenham P. H., Findlay G. P.. Solute and water transport in the bladders of Utricularia. Anderson, W. P., ed. Ion Transport in Plants. New York; Academic Press (1973 a): 583-587
    Suche in Google Scholar
  • 40 Sydenham P. H., Findlay G. P.. The rapid movement of the bladders of Utricularia sp.  Australian Journal of Biological Sciences. (1973 b);  26 1115-1126
    PubMedSuche in Google Scholar
  • 41 Sydenham P. H., Findlay G. P.. Transport of solutes and water by resetting bladders of Utricularia.  Australian Journal of Plant Physiology. (1975);  2 335-351
    PubMedSuche in Google Scholar
  • 42 Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., Yoshikawa S.. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process.  Proceedings of the National Academy of Sciences of the USA. (2003);  100 15304-15309
    CrossrefPubMedSuche in Google Scholar
  • 43 Wakefield A. E., Gotelli N. J., Wittman S. E., Ellison A. M.. Prey addition alters nutrient stoichiometry of the carnivorous plant Sarracenia purpurea.  Ecology. (2005);  86 1737-1743
    PubMedSuche in Google Scholar
  • 44 Wikström M. K. F.. Proton pump coupled to cytochrome c oxidase in mitochondria.  Nature. (1977);  266 271-273
    PubMedSuche in Google Scholar

V. A. Albert

Natural History Museum
University of Oslo

P.O. Box 1172 Blindern

0318 Oslo

Norway

eMail: victor.albert@nhm.uio.no

Guest Editor: S. Porembski