A new model for the evolution of carnivory in the bladderwort plant (Utricularia): Adaptive changes in cytochrome c oxidase (COX) provide respiratory power

Plant Biology

Volumn 8, Issue 6, 2006, Pages 758-764

  Laakkonen, L ^a   Jobson, R W ^b   Albert, V A ^c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Department of Ecology and Evolutionary Biology   (United States)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Bladderworts; Carnivorous plants; Conformational change; COX; Cytochrome c oxidase; Electron transport; Energetics; Protein structure; Proton pumping; Respiration; Utricularia

Indexed keywords

CYTOCHROME C OXIDASE; PROTON PUMP;

AQUATIC PLANT; BIOENERGETICS; CARNIVOROUS PLANT; CYTOCHROME; DICOTYLEDON; ECOPHYSIOLOGY; ELECTRON; INSECTIVORY; PROTEIN; RESPIRATION;

ADAPTATION; ANGIOSPERM; ANIMAL; BIOLOGICAL MODEL; CONFERENCE PAPER; ELECTRON TRANSPORT; GENETICS; INSECT; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANGIOSPERMS; ANIMALS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; INSECTS; MODELS, BIOLOGICAL; PHYLOGENY; PROTON PUMPS;

ARCHAEA; BACTERIA (MICROORGANISMS); BOS TAURUS; EUKARYOTA; UTRICULARIA;

EID: 33846265017     PISSN: 14358603     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2006-924459     Document Type: Conference Paper

References (46)

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