Abstract
Thermogenesis during the blooming of inflorescence is found in several but not all aroids. To understand what is critical for thermogenesis, we investigated the difference between thermogenic and non-thermogenic skunk cabbages (Symplocarpus renifolius and Lysichiton camtschatcensis), which are closely related in morphology and phylogeny. Critical parameters of mitochondrial biogenesis, including density, respiratory activity, and protein expression were compared between these two species. Mitochondrial density, respiratory activity, and the amount of alternative oxidase (AOX) in L. camtschatcensis spadix mitochondria were lower than in S. renifolius spadix mitochondria, while the level of uncoupling protein (UCP) was higher. AOX and UCP mRNAs in L. camtschatcensis were constitutively expressed in various tissues, such as the spadix, the spathe, the stalk, and the leaves. cDNA encoding two putative thermogenic proteins, AOX and UCP were isolated from L. camtschatcensis, and their primary structure was analyzed by multiple alignment and phylogenetic tree reconstruction. AOX and UCP protein of two the skunk cabbage species are closely related in structure, compared with other isoforms in thermogenic plants. Our results suggest that mitochondrial density, respiratory activity, and protein expression, rather than the primary structure of AOX or UCP proteins, may play critical roles in thermogenesis in plants.
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Abbreviations
- AOX:
-
Alternative oxidase
- UCP:
-
Uncoupling protein
- RT-PCR:
-
Reverse transcription-PCR
References
Andersson ME, Nordlund P (1999) A revised model of the active site of alternative oxidase. FEBS Lett 449:17–22
Berthold DA, Andersson ME, Nordlund P (2000) New insight into the structure and function of the alternative oxidase. Biochim Biophys Acta 1460:241–254
Brandalise M, Maia IG, Borecky J, Vercesi AE, Arruda P (2003) Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress. J Bioenerg Biomembr 35:203–209
Considine MJ, Goodman M, Echtay KS, Laloi M, Whelan J, Brand MD, Sweetlove LJ (2003) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. J Biol Chem 278:22298–22302
Gibernau M, Barabe D, Moisson M, Trombe A (2005) Physical constraints on temperature difference in some thermogenic aroid inflorescences. Ann Bot (Lond) 96:117–125
Grant N, Onda Y, Kakizaki Y, Ito K, Watling J, Robinson S (2009) Two cys or not two cys? That is the question; alternative oxidase in the thermogenic plant sacred lotus. Plant Physiol 150:987–995
Ito K, Seymour RS (2005) Expression of uncoupling protein and alternative oxidase depends on lipid or carbohydrate substrates in thermogenic plants. Biol Lett 1:427–430
Ito K, Abe Y, Johnston SD, Seymour RS (2003) Ubiquitous expression of a gene encoding for uncoupling protein isolated from the thermogenic inflorescence of the dead horse arum Helicodiceros muscivorus. J Exp Bot 54:1113–1114
Ito K, Ito T, Onda Y, Uemura M (2004) Temperature-triggered periodical thermogenic oscillations in skunk cabbage (Symplocarpus foetidus). Plant Cell Physiol 45:257–264
Ito-Inaba Y, Hida Y, Ichikawa M, Kato Y, Yamashita T (2008a) Characterization of the plant uncoupling protein, SrUCPA, expressed in spadix mitochondria of the thermogenic skunk cabbage. J Exp Bot 59:995–1005
Ito-Inaba Y, Hida Y, Mori H, Inaba T (2008b) Molecular identity of uncoupling proteins in thermogenic skunk cabbage. Plant Cell Physiol 49:1911–1916
Ito-Inaba Y, Sato M, Masuko H, Hida Y, Toyooka K, Watanabe M, Inaba T (2009) Developmental changes and organelle biogenesis in the reproductive organs of thermogenic skunk cabbage (Symplocarpus renifolius). J Exp Bot 60:3909–3922
Knutson RM (1974) Heat production and temperature regulation in eastern skunk cabbage. Science 186:746–747
Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6:248–261
Mayo SJ, Bogner J, Boyce PC (1997) The genera of Araceae. The Trustees, Royal Botanic Gardens. Kew, London
Moore AL, Albury MS (2008) Further insights into the structure of the alternative oxidase: from plants to parasites. Biochem Soc Trans 36:1022–1026
Nie ZL, Sun H, Li H, Wen J (2006) Intercontinental biogeography of subfamily Orontioideae (Symplocarpus, Lysichiton, and Orontium) of Araceae in Eastern Asia and North America. Mol Phylogenet Evol 40:155–165
Onda Y, Kato Y, Abe Y, Ito T, Ito-Inaba Y, Morohashi M, Ito Y, Ichikawa M, Matsukawa K, Otsuka M, Koiwa H, Ito K (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
Seymour RS (2004) Dynamics and precision of thermoregulatory responses of eastern skunk cabbage Symplocarpus foetidus. Plant Cell Environ 27:1014–1022
Seymour RS, Blaylock AJ (1999) Switching off the heater: influence of ambient temperature on thermoregulation by eastern skunk cabbage Symplocarpus foetidus. J Exp Bot 50:1525–1532
Seymour RS, Schultze-Motel P (1998) Physiological temperature regulation by flowers of the sacred lotus. Philos Trans R Soc London B 353:935–943
Seymour RS, Bartholomew GA, Christopher Barnhart M (1983) Respiration and heat production by the inflorescence of Philodendron selloum Koch. Planta 157:336–343
Siedow JN, Umbach AL (2000) The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta 1459:432–439
Tam SM, Boyce PC, Upson TM, Barabe D, Brunear A, Forest F, Parker JS (2004) Intergeneric and infrafamilial phylogeny of subfamily Monsteroideae (Araceae) revealed by chloroplast trnL-F sequences. Am J Bot 91:490–498
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Uemura S, Ohkawara K, Kudo G, Wada N, Higashi S (1993) Heat-production and cross-pollination of the Asian skunk cabbage Symplocarpus renifolius. Am J Bot 80:635–640
Umbach AL, Ng VS, Siedow JN (2006) Regulation of plant alternative oxidase activity: a tale of two cysteines. Biochim Biophys Acta 1757:135–142
Vercesi AE, Borecky J, Maia Ide G, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 57:383–404
Acknowledgments
We thank Mrs. Hitomi Ito (Iwate University) for her technical support. This work was supported by grant-in-aid for Young Investigator (nos. 20780070 and 20780236), and the New Energy and Industrial Technology Development Organization (NEDO).
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The nucleotide sequence reported in this paper has been submitted to the DDBJ with accession number (AB515348 for SrUCPA, AB515349 for LcUCP and AB515350 for LcAOX).
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Ito-Inaba, Y., Hida, Y. & Inaba, T. What is critical for plant thermogenesis? Differences in mitochondrial activity and protein expression between thermogenic and non-thermogenic skunk cabbages. Planta 231, 121–130 (2009). https://doi.org/10.1007/s00425-009-1034-z
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DOI: https://doi.org/10.1007/s00425-009-1034-z