Skip to main content

Plant Respiratory Metabolism: A Special Focus on the Physiology of Beetroot (Beta Vulgaris L.) Mitochondria

  • Chapter
  • First Online:
Red Beet Biotechnology

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Borisjuk L, Rolletschek H 2009.The oxygen status of the developing seed. New Phytol. 182(1):17–30

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Geigenberger, P. 2003. Response of plant metabolism to too little oxygen. Current Opinion in Plant Biology 6: 247–56.

    Article  CAS  Google Scholar 

  • Geigenberger, P., D. Riewe, and A.R. Fernie. 2010. The central regulation of plant physiology by adenylates. Trends in Plant Science 15: 98–105.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gupta, K.J., A. Zabalza, and J.T. van Dongen. 2009. Regulation of respiration when the oxygen availability changes. Physiologia Plantarum 137: 383–391.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Krömer, S. 1995. Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46: 45–70.

    Article  Google Scholar 

  • Lambers, H. 1982. Cyanide resistant respiration: A nonphosphorylating electron transport pathway acting as an energy overflow. Plant Physiology 55: 478–485.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Mackenzie, S., and L. McIntosh. 1999. Higher plant mitochondria. The Plant Cell 11: 571–585.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Moller, I.M., and A.G. Rasmusson. 1998. The role of NADP in the mitochondrial matrix. Trends in Plant Science 3: 21–27.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rasmusson, A.G., A.R. Fernie, and J.T. van Dongen. 2009. Alternative oxidase: A defence against metabolic fluctuations? Physiologia Plantarum 137: 371–82.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.).

    CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Kapuganti J. Gupta .

Editor information

Editors and Affiliations

Rights and permissions

Reprints 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

Publish with us

Policies and ethics