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Published on December 19, 2008; 10.1104/pp.108.129288

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Received September 3, 2008
Accepted December 15, 2008

REGULATION OF RESPIRATION AND FERMENTATION TO CONTROL THE PLANT INTERNAL OXYGEN CONCENTRATION

Ana Zabalza , Joost T. van Dongen *, Anja Froehlich , Sandra Oliver , Benjamin Faix , Jagadis Gupta Kapuganti , Elmar Schmalzlin , Maria Igal , Luis Orcaray , Mercedes Royuela , and Peter Geigenberger

Max-Planck-Institute of Molecular Plant Physiology, Am Muhlenberg 1, D-14476 Golm-Potsdam, Germany; Dpto. Ciencias Medio Natural, Universidad Publica de Navarra, Campus Arrosadia, E-31006 Pamplona, Spain; University of Potsdam, Institute of Chemistry / Physical Chemistry & Interdisciplinary Center of Photonics, D-14476 Potsdam-Golm, Germany; Leibniz-Institute of Vegetable and Ornamental Crops, Theodor-Echtermeyer-Weg 1, D-14979 Grossbeeren, Germany

* Corresponding author; email: dongen{at}mpimp-golm.mpg.de.

Plant internal oxygen concentrations can drop well below ambient even when the plant grows under optimal conditions. Using pea (Pisum sativum L.) roots, we show how amenable respiration adapts to hypoxia in order to save oxygen when the oxygen availability decreases. The data cannot simply be explained by oxygen being limiting as substrate but indicate the existence of a regulatory mechanism, because the oxygen concentration at which the adaptive response is initiated is independent of the actual respiratory rate. Two phases can be discerned during the adaptive reaction: an initial linear decline of respiration is followed by a non-linear inhibition in which the respiratory rate decreased progressively faster upon decreasing oxygen availability. In contrast to the cytochrome-c pathway, the inhibition of the AOX pathway shows only the linear component of the adaptive response. Feeding pyruvate to the roots led to an increase of the oxygen consumption rate, which ultimately led to anoxia. This is explained by the increase of respiratory substrate and by a specific increase of the protein level of cytochrome-c oxidase and alternative oxidase after feeding pyruvate. The importance of balancing the in vivo pyruvate availability in the tissue was further investigated. Using various ADH knock-out lines of Arabidopsis, it was shown that even under aerobic conditions alcohol fermentation plays an important role in the control of the level of pyruvate in the tissue. Interestingly, alcohol fermentation appeared to be primarily induced by a drop in the energy status of the tissue rather than by a low oxygen concentration, indicating that sensing the energy status is an important component of optimizing plant metabolism to changes in the oxygen availability.




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