TANSLEY REVIEW .52. THE ROLE OF ACTIVE OXYGEN IN THE RESPONSE OF PLANTS TO WATER-DEFICIT AND DESICCATION

Water deficits cause a reduction in the rate of photosynthesis. Exposu re to mild water deficits, when relative water content (RWC) remains a bove 70%, primarily causes limitation to carbon dioxide uptake because of stomatal closure. With greater water deficits, direct inhibition o f photosynthesis occurs. In both cases limitation of carbon dioxide fi xation results in exposure of chloroplasts to excess excitation energy . Much of this can be dissipated by various photoprotective mechanisms . These include dissipation as heat via carotenoids, photorespiration, CAM idling and, in some species, leaf movements and other morphologic al features which minimize light absorption. The active oxygen species superoxide and singlet oxygen are produced in chloroplasts by photore duction of oxygen and energy transfer from triplet excited chlorophyll to oxygen, respectively. Hydrogen peroxide and hydroxyl radicals can form as a result of the reactions of superoxide. All these species are reactive and potentially damaging, causing lipid peroxidation and ina ctivation of enzymes. They are normally scavenged by a range of antiox idants and enzymes which are present in the chloroplast and other subc ellular compartments. When carbon dioxide fixation is limited by water deficit, the rate of active oxygen formation increases in chloroplast s as excess excitation energy, not dissipated by the photoprotective m echanisms, is used to form superoxide and singlet oxygen. However, pho torespiratory hydrogen peroxide production in peroxisomes decreases. I ncreased superoxide can be detected by EPR (electron paramagnetic reso nance) in chloroplasts from droughted plants. Superoxide formation lea ds to changes suggestive of oxidative damage including lipid peroxidat ion and a decrease in ascorbate. These changes are not, however, appar ent until severe water deficits develop, and they could also be interp reted as secondary effects of water deficit-induced senescence or woun ding. Non-lethal water deficits often result in increased activity of superoxide dismutase, glutathione reductase and monodehydroascorbate r eductase. Increased capacity of these protective enzymes may be part o f a general antioxidative response in plants involving regulation of p rotein synthesis or gene expression. Since the capacity of these enzym es is also increased by other treatments which cause oxidative damage, and which alter the balance between excitation energy input and carbo n dioxide fixation such as low temperature and high irradiance, it is suggested that water deficit has the same effect. Light levels that ar e not normally excessive do become excessive and photoprotective/antio xidative systems are activated. Some of the photoprotective mechanisms themselves could result in active oxygen formation. Photoinhibitory d amage also includes a component of oxidative damage. During normally-e ncountered degrees of water deficit the capacity of the antioxidant sy stems and their ability to respond to increased active oxygen generati on may be sufficient to prevent overt expression of damage. Desiccatio n-tolerant tissues such as bryophytes, lichens, spores, seeds, some al gae and a few vascular plant leaves can survive desiccation to below 3 0-40% RWC. A component of desiccation damage in seeds and bacteria is oxygen-dependent. Desiccation causes oxidation of glutathione, a major antioxidant, and appearance of a free radical signal detected by EPR in a number of tissues suggesting that oxidative damage has occurred. In photosynthetic cells damage may arise from photo-oxidation. Disrupt ion of membrane-bound electron tranport systems in partially hydrated tissue could lead to reduction of oxygen to superoxide. Oxidation of l ipids and sulphydryl groups may also occur in dry tissue. Tolerant cel ls recover upon rehydration and are able to reduce their glutathione p ool. Non-tolerant species go on to show further oxidative damage inclu ding lipid peroxidation. It is difficult to attribute this subsequent damage to the cause or effect of death. Embryos in seeds lose desiccat ion tolerance soon after imbibition. This is associated with membrane damage that has been attributed to superoxide-mediated deesterificatio n of phospholipids and loss of lipophilic antioxidants. These effects are discussed in relation to other mechanisms involved in desiccation tolerance.