Abstract
Mitochondria are important organelles for cellular energy. Apart from orchestrating cellular energy balance, mitochondria involve themselves in various processes such as synthesis of vitamins and lipids and production of reactive oxygen and nitrogen species. Understanding mitochondrial metabolism is crucial for understanding complete cellular metabolism, which is directly or indirectly involved in the biosynthesis of food and pharmaceutical products. Respiration, the chief function occurring in mitochondria, is divided into glycolysis, tricarboxylic acid (TCA) cycle, and electron transport chain. In addition to the classic operation of the pathways, mitochondria have various alternative pathways that are involved in plant responses to various stresses. Respiratory metabolism in green tissues is different from that occurring in roots, and more so in bulky tissues such as beetroots, because such storage organs have to cope with very low cellular oxygen concentrations. Bulky tissue organs like beetroots store sucrose as their storage carbohydrate. Therefore the cellular respiration in beetroots is different, especially during the storage period and sprouting period in comparison with the normal roots. Here respiratory metabolism and its association with various other metabolic pathways are described, with a special focus on beetroot, in which various alternative pathways such as NAD(P)H dehydrogenases or alternative oxidase pathways are discussed. Understanding respiratory metabolism has bearing on engineering beetroot for higher yields as well as prevention of storage losses.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Benamar, A., H. Rolletschek, L. Borisjuk, M.H. Avelange-Macherel, G. Curien, A. Mostefai, R. Andriantsitohaina, and D. Macherel. 2008. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochimica et Biophysica Acta 1777: 1268–1275.
Borisjuk, L., D. Macherel, A. Benamar, U. Wobus, and H. Rolletschek. 2007. Low oxygen sensing and balancing in plant seeds – A role for nitric oxide. The New Phytologist 176: 813–823.
Borisjuk L, Rolletschek H 2009.The oxygen status of the developing seed. New Phytol. 182(1):17–30
Chaudhuri, M., and G.C. Hill. 1996. Cloning, sequencing and functional activity of the Trypanosoma brucei brucei alternative oxidase. Molecular and Biochemical Parasitology 83: 125–129.
Considine, M.J., R.C. Holtzapffel, D.A. Day, J. Whelan, and A.H. Millar. 2002. Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiology 129: 949–953.
Fernie, A.R., A. Tiessen, M. Stitt, L. Willmitzer, and P. Geigenberger. 2002. Altered metabolic fluxes result from shifts in metabolite levels in sucrose phosphorylase-expressing potato tubers. Plant, Cell & Environment 25: 1219–32.
Fredlund, K.M., A.G. Rasmusson, and I.M. Møller. 1991. The effects of aging on the oxidation of external NAD(P)H in purified red beetroot (Beta vulgaris L.) mitochondria. Plant Physiology 97: 99–103.
Geigenberger, P. 2003. Response of plant metabolism to too little oxygen. Current Opinion in Plant Biology 6: 247–56.
Geigenberger, P., D. Riewe, and A.R. Fernie. 2010. The central regulation of plant physiology by adenylates. Trends in Plant Science 15: 98–105.
Giege, P., J.L. Heazlewood, U. Roessner-Tunali, A.H. Millar, A.R. Fernie, C.J. Leaver, and L.J. Sweetlove. 2003. Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. The Plant Cell 15(9): 2140–2151.
Gupta, K.J., A. Zabalza, and J.T. van Dongen. 2009. Regulation of respiration when the oxygen availability changes. Physiologia Plantarum 137: 383–391.
Karpova, O.V., E.V. Kuzmin, T.E. Elthon, and K.J. Newton. 2002. Differential expression of alternative oxidase genes in maize mitochondrial mutants. The Plant Cell 14: 3271–3284.
Klok, E.J., I.W. Wilson, D. Wilson, S.C. Chapman, R.M. Ewing, S.C. Somerville, W.J. Peacock, R. Dolferus, and E.S. Dennis. 2002. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. The Plant Cell 14: 2481–2494.
Klotz, K.L., F.L. Finger, and M.D. Anderson. 2008. Respiration in postharvest sugar beet roots is not limited by respiratory capacity or adenylates. Journal of Plant Physiology 165: 1500–1510.
Krömer, S. 1995. Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46: 45–70.
Lambers, H. 1982. Cyanide resistant respiration: A nonphosphorylating electron transport pathway acting as an energy overflow. Plant Physiology 55: 478–485.
Liu, F., T. VanToai, L.P. Moy, G. Bock, L. Linford, and J. Quackenbush. 2005. Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiology 137: 1115–1129.
Luethy, M.H., J.J. Thelen, A.F. Knudten, and T.E. Elthon. 1995. Purification, characterization, and submitochondrial localization of a 58-kilodalton NAD(P)H dehydrogenase. Plant Physiology 107: 443–50.
Mackenzie, S., and L. McIntosh. 1999. Higher plant mitochondria. The Plant Cell 11: 571–585.
Maxwell, D.P., Y. Wang, and L. McIntosh. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences of the United States of America 96: 8271–76.
McDonald, A.E. 2008. Alternative oxidase: An inter-kingdom perspective on the function and regulation of this broadly distributed ‘cyanide resistant’ terminal oxidase. Functional Plant Biology 35: 535–552.
McDonald, A.E., and G.C. Vanlerberghe. 2006. Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comparative Biochemistry and Physiology 1: 357–364.
Menz, R.I., and D.A. Day. 1996. Purification and characterisation of a 43-kDa rotenone-insensitive NADH dehydrogenase from plant mitochondria. Journal of Biological Chemistry 271: 23117–20.
Millar, A.H., F.J. Bergersen, and D.A. Day. 1994. Oxygen affinity of terminal oxidases in soybean mitochondria. Plant Physiology and Biochemistry 32: 847–852.
Millar, A.H., J. Whelan, K.L. Soole, and D.A. Day. 2011. Organization and regulation mitochondrial respiration in plants. Annual Review of Plant Biology 62: 79–104.
Møller, I.M. 2001. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Biology and Plant Molecular Biology 52: 561–91.
Moller, I.M., and A.G. Rasmusson. 1998. The role of NADP in the mitochondrial matrix. Trends in Plant Science 3: 21–27.
Podestá, F.E., and W.C. Plaxton. 1991. Association of phosphoenolpyruvate phosphatase activity with the cytosolic pyruvate kinase of germinating mung beans. Plant Physiology 97: 1329–1333.
Rasmusson, A.G., and I.M. Møller. 1991. NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial membrane studied using inside-out submitochondrial particles. Physiologia Plantarum 83: 357–365.
Rasmusson, A.G., K.M. Fredlund, and I.M. Møller. 1993. Purification of a rotenone-insensitive NAD(P)H dehydrogenase from the inner surface of the inner mitochondrial membrane of red beetroot mitochondria. Biochimica et Biophysica Acta 1141: 107–10.
Rasmusson, A.G., D.A. Geisler, and I.M. Møller. 2008. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47–60.
Rasmusson, A.G., A.R. Fernie, and J.T. van Dongen. 2009. Alternative oxidase: A defence against metabolic fluctuations? Physiologia Plantarum 137: 371–82.
Rayner, J.R., and J.T. Wiskich. 1983. Development of NADH oxidation by red beet mitochondria on slicing and aging of the tissues. Australian Journal of Plant Physiology 10: 55–63.
Ribas-Carbo, M., J.A. Berry, D. Yakir, L. Giles, S.A. Robinson, A.M. Lennon, and J.N. Siedow. 1995. Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiology 109: 829–837.
Rocha, M., F. Licausi, W.L. Araújo, A. Nunes-Nesi, L. Sodek, A.R. Fernie, and J.T. van Dongen. 2010. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152: 1501–1513.
Rolletschek, H., L. Borisjuk, M. Koschorreck, U. Wobus, and H. Weber. 2002. Legume embryos develop in a hypoxic environment. Journal of Experimental Botany 53: 1099–110.
Rolletschek, H., K. Koch, U. Wobus, and L. Borisjuk. 2005a. Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. The Plant Journal 42: 69–83.
Rolletschek, H., R. Radchuk, C. Klukas, F. Schreiber, U. Wobus, and L. Borisjuk. 2005b. Evidence of a key role for photosynthetic oxygen release in oil storage in developing soybean seeds. The New Phytologist 167: 777–786.
Rolletschek, H., L. Borisjuk, A. Sánchez-García, C. Romero, L. Gotor, J. Rivas, and M. Mancha. 2007. Temperature-dependent endogenous oxygen concentration regulates microsomal oleate desaturase in developing sunflower seeds. Journal of Experimental Botany 58: 3171–3181.
Shugaev, A.G., and E.I. Vyskrebentseva. 1985. Developmental changes in the functional activity of mitochondria in sugar beet roots. Fiziologiya Rastenii (Moscow) 32: 259–267 (Sov. Plant Physiology, Engl. Transl.).
Shugaev A.G., D.A. Lashtabega, N.A. Shugaeva, and E.I. Vyskrebentseva. 2011. Activities of antioxidant enzymes in mitochondria of growing and dormant sugar beet roots. Russian Journal of Plant Physiology 58: 387–393.
Skutnik, M., and A.M. Rychter. 2009. Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. Journal of Plant Physiology 166: 926–937.
Soole, K.L., I.B. Dry, and J.T. Wiskich. 1986. The responses of isolated plant mitochondria to external nicotinamide adenine dinucleotide. Plant Physiology 81: 587–592.
Soole, K.L., I.B. Dry, A.T. James, and J.T. Wiskich. 1990. The kinetics of NADH oxidation by complex I of isolated plant mitochondria. Physiologia Plantarum 80: 75–82.
Sugie, A., N. Naydenov, N. Mizuno, C. Nakamura, and S. Takumi. 2006. Over expression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes & Genetic Systems 81: 349–54.
Sweetlove, L.J., K.F.M. Beard, A. Nunes-Nesi, A.R. Fernie, and R.G. Ratcliffe. 2010. Not just a circle: Flux modes in the plant TCA cycle. Trends in Plant Science 15: 462–470.
Thiel, J., H. Rolletschek, S. Friedel, J.E. Lunn, T.H. Nguyen, R. Feil, H. Tschiersch, M. Müller, and L. Borisjuk. 2011. Seed-specific elevation of non-symbiotic hemoglobin AtHb1: Beneficial effects and underlying molecular networks in Arabidopsis thaliana. BMC Plant Biology 11: 48.
Tobin, A., B. Djerdjour, E. Journet, M. Neuburger, and R. Douce. 1980. Effect of NAD on the malate oxidation in intact plant mitochondria. Plant Physiology 66: 225–229.
Trost, P., P. Bonora, S. Scagliarini, and P. Pupillo. 1995. Purification and properties of NAD(P)H:(quinone-acceptor) oxidoreductase of sugar beet cells. European Journal of Biochemistry 234: 452–58.
Urbanczyk-Wochniak, E., B. Usadel, O. Thimm, A. Nunes-Nesi, F. Carrari, M. Davy, O. Blasing, M. Kowalczyk, D. Weicht, A. Polinceusz, S. Meyer, M. Stitt, and A.R. Fernie. 2006. Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: Effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Molecular Biology 60: 773–92.
van Dongen, J.T., U. Schurr, M. Pfister, and P. Geigenberger. 2003. Phloem metabolism and function have to cope with low internal oxygen. Plant Physiology 131: 1529–1543.
van Dongen, J.T., K.J. Gupta, S.J. Ramírez-Aguilar, W.J. Araujo, A. Nunes-Nesi, A.R. Fernie. 2011. Regulation of respiration in plants: A role for alternative metabolic pathways. Journal of Plant Physiology 168: 1434–1443.
Vanlerberghe, G.C., and L. McIntosh. 1992. Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiology 100: 115–119.
Vanlerberghe, G.C., L. McLntosh. 1996. Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiology 111(2): 589–595.
Vanlerberghe, G.C., M. Cvetkovska, and J. Wang. 2009. Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiologia Plantarum 137: 392–406.
Zabalza, A., J.T. van Dongen, A. Froehlich, S.N. Oliver, B. Faix, K.J. Gupta, E. Schma lzlin, M. Igal, L. Orcaray, M. Royuela, et al. 2009. Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiology 149: 1087–1098.
Zottini, M., G. Mandolino, and D. Zannoni. 1993. Oxidation of external NAD(P)H by mitochondria from taproots and tissue cultures of sugar beet (Beta vulgaris). Plant Physiology 102: 579–85.
Acknowledgements
This work was supported by Deutsche Forschungsgemeinschaft (BA 1177/8-1) (KJG, HB). I thank Ian Max Møller, Aarhus University, Denmark, for valuable suggestions on this book chapter. I thank Shruthi Segu for editorial help.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Gupta, K.J., Rolletschek, H. (2013). Plant Respiratory Metabolism: A Special Focus on the Physiology of Beetroot (Beta Vulgaris L.) Mitochondria. In: Neelwarne, B. (eds) Red Beet Biotechnology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-3458-0_5
Download citation
DOI: https://doi.org/10.1007/978-1-4614-3458-0_5
Published:
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4614-3457-3
Online ISBN: 978-1-4614-3458-0
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)