Different molecular bases underlie the mitochondrial respiratory activity in the homoeothermic spadices of Symplocarpus renifolius and the transiently thermogenic appendices of Arum maculatum

Biochemical Journal

Volumn 445, Issue 2, 2012, Pages 237-246

  Kakizaki, Yusuke ^a   Moore, Anthony L ^b   Ito, Kikukatsu ^a  

^a IWATE UNIVERSITY   (Japan)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Alternative oxidase (AOX); Blue native PAGE; Mitochondrial respiratory chain; Thermogenic plants; Type II NAD(P)H dehydrogenase

Indexed keywords

ALTERNATIVE OXIDASE; OLIGOMER; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ARTICLE; ARUM; ARUM MACULATUM; CABBAGE; ENZYME STRUCTURE; GENE EXPRESSION PROFILING; MITOCHONDRIAL RESPIRATION; MONOCOT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY CHAIN; SPECIES DIFFERENCE; SYMPLOCARPUS RENIFOLIUS; THERMOGENESIS; THERMOREGULATION;

AMINO ACID SEQUENCE; ARACEAE; ARUM; BLOTTING, WESTERN; ELECTRON TRANSPORT; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLOWERS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NADPH DEHYDROGENASE; OXIDOREDUCTASES; PHYLOGENY; PLANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TANDEM MASS SPECTROMETRY; THERMOGENESIS;

ARUM MACULATUM; SYMPLOCARPUS FOETIDUS;

EID: 84863184200     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111978     Document Type: Article

References (37)

1. Skubatz, H., Nelson, T. A., Dong, A. M., Meeuse, B. J. D. and Bendich, A. J. (1990) Infrared thermography of Arum lily inflorescences. Planta 182, 432-436
2. Seymour, R. S. and Schultze-Motel, P. (1996) Thermoregulating lotus flowers. Nature 383, 305
3. Skubatz, H., Tang, W. and Meeuse, B. J. D. (1993) Oscillatory heat-production in the male cones of cycads. J. Exp. Bot. 44, 489-492
4. Meeuse, B. J. D. (1975) Thermogenic respiration in aroids. Ann. Rev. Plant Physiol. 26, 117-126
5. Wagner, A. M., Wagner, M. J. and Moore, A. L. (1998) In vivo ubiquinone reduction levels during thermogenesis in Araceae. Plant Physiol. 117, 1501-1506 (Pubitemid 128652922)
6. Bermadinger-Stabentheiner, E. and Stabentheiner, A. (1995) Dynamics of thermogenesis and structure of epidermal tissues in inflorescences of Arum maculatum. New Phytol. 131, 41-50
7. Ito, K., Ogata, T., Kakizaki, Y., Elliott, C., Albury, M. S. and Moore, A. L. (2011) Identification of a gene for pyruvate-insensitive mitochondrial alternative oxidase expressed in the thermogenic appendices in Arum maculatum. Plant Physiol. 157, 1721-1732
8. Uemura, S., Ohkawara, K., Kudo, G., Wada, N. and Higashi, S. (1993) Heat-production and cross-pollination of the Asian skunk cabbage Symplocarpus renifolius (Araceae). Am. J. Bot. 80, 635-640 (Pubitemid 24412668)
9. Ito, K., Onda, Y., Sato, T., Abe, Y. and Uemura, M. (2003) Structural requirements for the perception of ambient temperature signals in homeothermic heat production of skunk cabbage (Sympocarpus foetidus). Plant Cell Environ. 26, 783-788 (Pubitemid 36737986)
10. Kamata, T., Matsukawa, K., Kakizaki, Y. and Ito, K. (2009) In vivo redox state of the ubiquinone pool in the spadices of the thermogenic skunk cabbage, Symplocarpus renifolius. J. Plant Res. 122, 645-649
11. Affourtit, C., Albury, M. S., Crichton, P. G. and Moore, A. L. (2002) Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Lett. 510, 121-126 (Pubitemid 34093809)
12. Leach, G. R., Krab, K., Whitehouse, D. G. and Moore, A. L. (1996) Kinetic analysis of the mitochondrial quinol-oxidizing enzymes during development of thermogenesis in Arum maculatum L. Biochem. J. 317, 313-319 (Pubitemid 26238362)
13. Grant, N. M., Miller, R. E., Watling, J. R. and Robinson, S. A. (2008) Synchronicity of thermogenic activity, alternative pathway respiratory flux, AOX protein content, and carbohydrates in receptacle tissues of sacred lotus during floral development. J. Exp. Bot. 59, 705-714 (Pubitemid 351640736)
14. Rhoads, D. M. and McIntosh, L. (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4, 1131-1139
15. Eubel, H., Braun, H. P. and Millar, A. H. (2005) Blue-native PAGE in plants: a tool in analysis of protein-protein interactions. Plant Methods 1, 11-23
16. Eubel, H., Jänsch, L. and Braun, H. P. (2003) New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol. 133, 274-286 (Pubitemid 37144100)
17. Eubel, H., Heinemeyer, J. and Braun, H. P. (2004) Identification and characterization of respirasomes in potato mitochondria. Plant Physiol. 134, 1450-1459 (Pubitemid 38527355)
18. Millar, A. H., Eubel, H., Jänsch, L., Kruft, V., Heazlewood, J. L. and Braun, H. P. (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 56, 77-90 (Pubitemid 40134262)
19. Sunderhaus, S., Klodmann, J., Lenz, C. and Braun, H. P. (2010) Supramolecular structure of the OXPHOS system in highly thermogenic tissue of Arum maculatum. Plant Physiol. Biochem. 48, 265-272
20. James, W. O. and Beevers, H. (1950) The respiration of Arum spadix. A rapid respiration, resistant to cyanide. New Phytol. 49, 353-374
21. Onda, Y., Kato, Y., Abe, Y., Ito, T., Ito-Inaba, Y., Morohashi, M., Ito, Y., Ichikawa, M., Matsukawa, K., Otsuka, M. et al. (2007) Pyruvate-sensitive AOX exists as a non-covalently associated dimer in the homeothermic spadix of the skunk cabbage, Symplocarpus renifolius. FEBS Lett. 581, 5852-5858 (Pubitemid 50008508)
22. Moore, A. L., Fricaud, A. C., Walters, A. J. and Whitehouse, D. G. (1993) Isolation and purification of functionally intact mitochondria from plant cells. Methods Mol. Biol. 19, 133-139
23. Moore, A. L., Walters, A. J., Thorpe, J., Fricaud, A. C. and Watts, F. Z. (1992) Schizosaccharomyces pombe mitochondria: morphological, respiratory and protein import characteristics. Yeast 8, 923-933
24. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (Pubitemid 47236692)
25. Gray, R. E., Grasso, D. G., Maxwell, R. J., Finnegan, P. M., Nagley, P. and Devenish, R. J. (1990) Identification of a 66 KDa protein associated with yeast mitochondrial ATP synthase as heat shock protein hsp60. FEBS Lett. 268, 265-268 (Pubitemid 20233882)
26. Ito, K. (1999) Isolation of two distinct cold-inducible cDNAs encoding plant uncoupling proteins from the spadix of skunk cabbage (Symplocarpus foetidus). Plant Sci. 149, 167-173
27. Joshi, C. P., Zhou, H., Huang, X. and Chiang, V. L. (1997) Context sequences of translation initiation codon in plants. Plant Mol. Biol. 35, 993-1001 (Pubitemid 28016959)
28. Rasmusson, A. G., Svensson, A. S., Knoop, V., Grohmann, L. and Brennicke, A. (1999) Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J. 20, 79-87 (Pubitemid 29519959)
29. Kerscher, S. J. (2000) Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim. Biophys. Acta 1459, 274-283
30. Melo, A. M. P., Duarte, M. and Videira, A. (1999) Primary structure and characterization of a 64 kDa NADH dehydrogenase from the inner membrane of Neurospora crassa mitochondria. Biochim. Biophys. Acta 1412, 282-287 (Pubitemid 29356108)
31. Rasmusson, A. G., Soole, K. L. and Elthon, T. E. (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Ann. Rev. Plant Biol. 55, 23-39 (Pubitemid 38940924)
32. ap Rees, T., Wright, B. W. and Fuller, W. A. (1977) Measurements of starch breakdown as estimates of glycolysis during thermogenesis by the spadix of Arum maculatum L. Planta 134, 53-56
33. Cook, N. D. and Cammack, R. (1985) Effects of temperature on electron transport in Arum maculatum mitochondria. Plant Physiol. 79, 332-335
34. Seymour, R. S., Lindshau, G. and Ito, K. (2010) Thermal clamping of temperature-regulating flowers reveals the precision and limits of the biochemical regulatory mechanism. Planta 231, 1291-1300
35. Sun, F., Huo, X., Zhai, Y., Wang, A., Xu, J., Su, D., Bartlam, M. and Rao, Z. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057 (Pubitemid 40884395)
36. Yankovskaya, V., Horsefield, R., Tornroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C., Byrne, B., Cecchini, G. and Iwate, S. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704 (Pubitemid 36159483)
37. Schägger, H. and Pfeiffer, K. (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777-1783 (Pubitemid 30204389)