Response of plant metabolism to too little oxygen Peter Geigenberger Oxygen can fall to low concentrations within plant tissues, either because of environmental factors that decrease the external oxygen concentration or because the movement of oxygen through the plant tissues cannot keep pace with the rate of oxygen consumption. Recent studies document that plants can decrease their oxygen consumption in response to low oxygen concentrations to avoid internal anoxia. This adaptive response involves a restriction of respiration and a concomitant decrease in ATP consumption that results from the inhibition of a wide range of biosynthetic processes. The inhibition of respiration is rapid and occurs at oxygen concentrations well above the K m (oxygen) of cytochrome oxidase, indicating that an oxygen-sensing system triggers a coordinated inhibition of ATP formation and consumption. In addition to this, low oxygen concentrations lead to the induction of a plant-specific and energy-conserving pathway of sucrose degradation, which decreases oxygen consumption and improves plant performance. Low oxygen concentrations also lead to long-term morphological adaptations, which allow respiration per volume tissue to be decreased and oxygen entry to be increased. Recently, advances have been made in elucidating possible oxygen-sensing systems and regulatory components that are involved in these responses. Addresses Max Planck Institute of Molecular Plant Physiology, Am Mu ¨ hlenberg 1, 14476 Golm, Germany e-mail: geigenberger@mpimp-golm.mpg.de Current Opinion in Plant Biology 2003, 6:247–256 This review comes from a themed issue on Physiology and metabolism Edited by Alison Smith and Mary Lou Guerinot 1369-5266/03/$ – see front matter ß 2003 Elsevier Science Ltd. All rights reserved. DOI 10.1016/S1369-5266(03)00038-4 Abbreviations ADH alcohol dehydrogenase LDH lactate dehydrogenase Pdc1 pyruvate decarboxylase1 PPi inorganic pyrophosphate SNF1 SUCROSE NON-FERMENTING1 SuSy sucrose synthase Introduction Like animals, plants are obligate aerobic organisms. Oxygen is essential as the terminal electron acceptor in the oxidative phosphorylation pathway, which provides the vast majority of ATP for cellular metabolism by regenerating NAD þ from NADH. Oxygen is also required in several important cellular pathways, includ- ing haem, sterol and fatty-acid biosynthesis. The pro- vision of sufficient oxygen to internal tissues is a fundamental physiological challenge in multicellular organisms. Animals have evolved specialized respiratory organs, circulation systems, and oxygen-carrying pig- ments to allow the efficient delivery of oxygen to meta- bolically active tissues, and to buffer against rapid changes in the rate of oxygen use and resulting changes in the internal oxygen tension. In contrast, plants lack efficient systems for oxygen delivery. Transient flood- ing, water logging or microbial activity in the soil can rapidly lead to oxygen deprivation within the roots, affecting the growth and distribution of terrestrial plants and leading to major reductions in crop yield [1,2]. Under anoxic conditions when cytochrome oxidase activity becomes oxygen limited (K m ½O 2 ¼ 14 mM, equivalent to 0.013% oxygen; [2]), ATP formation through oxidative phosphorylation is inhibited and ATP has to be pro- duced by fermentation [3]. This impairs cellular meta- bolism and function because the efficiency of ATP formation is sharply reduced. The respiration of one molecule of hexose equivalent produces up to 39 mole- cules of ATP, whereas the fermentation of such a mole- cule provides a maximum of just three molecules of ATP. In addition, fermentation results in falling cyto- solic pH, the induction of glycolysis, and the accumula- tion of lactate and ethanol [2]. Re-entry of oxygen into highly reduced anoxic tissues during the post-anoxic phase leads to the formation of harmful oxygen radicals and toxic oxidative products, resulting in rapid perox- idative damage [4,5]. In this review, I discuss the adaptive responses of plant metabolism to a fall in internal oxygen concentration and possible oxygen-sensing mechanisms that trigger these responses. In particular, I focus on a crucial aspect of low oxygen responses that has been largely ignored in the past: even when external oxygen is high, oxygen in plant tissues may fall to low concentrations because a large diffusion gradient is required to drive oxygen through the tissue at a fast enough rate to keep up with the rate of oxygen consumption. Plant tissues actually have a pro- pensity to drive themselves into anoxia, which could have serious consequences for growth and fitness when exter- nal oxygen is freely available and will exacerbate the impact of falling external oxygen. However, plants have evolved metabolic strategies to avoid or delay the deple- tion of oxygen to concentrations that would limit oxida- tive phosphorylation. 247 www.current-opinion.com Current Opinion in Plant Biology 2003, 6:247–256