Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: a Review

An appreciation of the scale and frequency of climatic oscillations in the past few million years is modifying our views on how evolution proceeds. Such major events caused extinction and repeated changes in the ranges of those taxa that survived. Their spatial effects depend on latitude and topography, with extensive extinction and recolonization in higher latitudes and altitudinal shifts and complex refugia nearer the tropics. The associated population dynamics varied with life history and geography, and the present genetic constitution of the populations and species carry attenuated signals of these past dynamics. Phylogeographic studies with DNA have burgeoned recently and studies are reviewed from the arctic, temperate and tropical regions, seeking commonalities of cause in the resulting genetic patterns. Arctic species show distinct shallow genetic clades with common geographical boundaries. Thus Beringia is distinct phylogeographically, but its role as a refugial source is complex. Arctic taxa do not show the common genetic pattern of southern richness and northern purity in north-temperate species. Temperate refugial regions in Europe and North America show relatively deep DNA divergence for many taxa, indicating their presence over several Ice Ages, and suggesting a mode of speciation by repeated allopatry. DNA evidence indicates temperate species in Europe had different patterns of postglacial colonization across the same area and different ones in previous oscillations, whereas the northwest region of North America was colonized from the north, east and south. Tropical montane regions contain deeply diverged lineages, often in a relatively small geographical area, suggesting their survival there from the Pliocene. Our poor understanding of refugial biodiversity would benefit from further combined fossil and genetic studies.

http://webpages.icav.up.pt/PTDC/BIA-BEC/099915/2008/4.Hewitt%202004%20PhilTransRSocLondB.pdf

Genetic consequences of climatic oscillations in the Quaternary.

OXIDATIVE STRESS . . . . . . . . . . . . . .. . . . . .... . . . . .. . . . . .. . . . ... .. . . . . .... . . .. .. . . . . . ... . 84 RESPONSE OF SOD TO ENVIRONMENTAL STRESS . . . . . . . . . . . . . . . .. . . . .... . . .... . . . . . . 87 Photoinhibition . . . . . . . . . . .. . ... . . .. . . . .. . . . . ..... . . . , ... ", , ... ,' , ... . ,., . . . "" . .. . ,'.' . . ,' . . . . , ., 87 Paraquat and Other Herbicides . . .. , . . .... , ..... , . . . . ... . . . .. . . . . . . . . . . . . ,.. 91 Atmospheric Pollutants . . " .... , .... , " .... " , , . . , .... , ' 94 Waterlogging and Drought .. ", . . ... , . . . . . . , .. "", . . ", . . . . . ", . . . .. ", . . .. , . . . ... """", . . " 97 The Defense Response to Pathogens . ... . . . . "" ... "" .... " ...... " ,."" .... . , 98 The Phenomenon of Cross-Tolerance . . . , , .. . . . . ...... . . , . . . . . . , . . .... , .. . . . . . . . .. .. 101 The Mechanism of SOD Regulation ........ , , ...... , " 102 GENETIC ENGINEERING OF SOD IN PLANTS .. ' ...... ' . . . . . . . . . . . . . . . . . . . . . . . .. . . . , .... ' 104 Cu/ZnSOD and MnSOD Overexpression . . . . . .. . . . . . , . . . . . . .. . . . . . .. . . . . . , .... . . . . .. . . ,.... . . 105 Prospects for Stress Tolerance through Genetic Engineering of SOD . . . . ,,, .. , . . . . . . . 106

Superoxide dismutase and stress tolerance

Water deficits cause a reduction in the rate of photosynthesis. Exposure to mild water deficits, when relative water content (RWC) remains above 70%, primarily causes limitation to carbon dioxide uptake because of stomatal closure. With greater water deficits, direct inhibition of photosynthesis occurs. In both cases limitation of carbon dioxide fixation 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 morphological features which minimize light absorption. The active oxygen species superoxide and singlet oxygen are produced in chloroplasts by photoreduction 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 inactivation of enzymes. They are normally scavenged by a range of antioxidants and enzymes which are present in the chloroplast and other subcellular compartments. When carbon dioxide fixation is limited by water deficit, the rate of active oxygen formation increases in chloroplasts as excess excitation energy, not dissipated fay the photoprotective mechanisms, is used to form superoxide and singlet oxygen. However, photorespiratory hydrogen peroxide production in peroxisomes decreases. Increased superoxide can be detected by EPR (electron paramagnetic resonance) in chloroplasts from droughted plants. Stiperoxide formation leads to changes suggestive of oxidative damage including lipid peroxidation and a decrease in ascorbate. These changes are not, however, apparent until severe water deficits develop, and they could also be interpreted as secondary effects of water deficit-induced senescence or wounding. Non-lethal water deficits often result in increased activity of superoxide dismutase, glutathione reductase and monodehydroascorbate reductase. Increased capacity of these protective enzymes may be part of a general antioxidative response in plants involving regulation of protein synthesis or gene expression. Since the capacity of these enzymes is also increased by other treatments which cause oxidative damage, and which alter the balance between excitation energy input and carbon dioxide fixation such as low temperature and high irradiance, it is suggested that water deficit has the same effect. Light levels that are not normally excessive do become excessive and photoprotective/antioxidative systems are activated. Some of the photoprotective mechanisms themselves could result in active oxygen formation. Photoinhibitory damage also includes a component of oxidative damage. During normally-encountered degrees of water deficit the capacity of the antioxidant systems and their ability to respond to increased active oxygen generation may be sufficient to prevent overt expression of damage. Desiccation-tolerant tissues such as bryophytes, lichens, spores, seeds, some algae and a few vascular plant leaves can survive desiccation to below 30-40% 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 photooxidation. Disruption of membrane-bound electron tranport systems in partially hydrated tissue could lead to reduction of oxygen to superoxide. Oxidation of lipids and sulphydryl groups may also occur in dry tissue. Tolerant cells recover upon rehydration and arc able to reduce their glutathione pool. Non-tolerant species go on to show further oxidative damage including lipid peroxidation. It is difficult to attribute this subsequent damage to the cause or effect of death. Embryos in seeds lose desiccation tolerance soon after imbibition. This is associated with membrane damage that has been attributed to superoxide-mediated deesterification of phospholipids and loss of lipophilic antioxidants. These effects are discussed in relation to other mechanisms involved in desiccation tolerance. Contents Summary 27 I. Introduction 28 II. Generation of active oxygen and defence mechanisms in plant cells 29 III. The effect of water deficit on photosynthesis 31 IV. Mechanisms for active oxygen generation during water deficit 36 V. Evidence for oxidative damage during water deficit 39 VI. Desiccation 47 VII. Conclusions 52 Acknowledgements 53 References 53.

The role of active oxygen in the response of plants to water deficit and desiccation.

The accumulation of dioxygen in Earth's atmosphere allowed for the evolution of aerobic organisms that use O2 as the terminal electron acceptor, thus providing a higher yield of energy compared with fermentation and anaerobic respiration. For example, in aerobic metabolism, the complete breakdown of one molecule of glucose yields a total of 38 molecules of ATP, whereas the anaerobic breakdown of this same glucose molecule to ethanol and CO, yields only 8 ATPs. In its ground state, molecular O2 (dioxygen) is relatively unreactive, yet it is capable of giving rise to lethal reactive ,excited states as free radicals and derivatives. Utilization of O2 proceeds most readily via a complete stepwise, fourelectron reduction to water during which partially reduced reactive intermediates are generated (Fig. 1). The reactive species of reduced dioxygen include the superoxide radical (. 02-), hydrogen peroxide (H202), and the hydroxyl radical (. OH). These and the physiologically energized form of dioxygen, singlet oxygen ('O2), are the biologically most important O2 species. An activation energy of approximately 22 kcal/mol is required to raise molecular O2 from its ground state to its first singlet state. In higher plants, this energy is readily obtained from light quanta via such transfer molecules as Chl (Foote, 1976). A11 of these activated oxygen species are extremely reactive and cytotoxic in a11 organisms. These highly reactive species can react with unsaturated fatty acids to cause peroxidation of essential membrane lipids in the plasmalemma or intracellular organelles. Peroxidation damage of the plasmalemma leads to leakage of cellular contents, rapid desiccation, and cell death. Intracellular membrane damage can affect respiratory activity in mitochondria, cause pigment breakdown, and cause loss of carbon-fixing ability in chloroplasts. Severa1 Calvin-cycle enzymes within chloroplasts are extremely sensitive to H202, and high levels of H202 (the product of superoxide dismutation) directly inhibit C02 fixation (Kaiser, 1979). H202 has also been shown to be active with mixed function oxidases in marking severa1 types of enzymes for proteolytic degradation (Fucci et al., 1983). Superoxide and H202 can react in a \"Haber-Weiss\" reaction to generate the hydroxyl radical ( + OH), which is the most potent oxidant known. The hydroxyl radical indiscriminately and rapidly attacks virtually a11 macromolecules, leading to seri-

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Oxygen Stress and Superoxide Dismutases

The arctic flora is thought to have originated during the late Tertiary, approximately 3 million years ago. Plant migration routes during colonization of the Arctic are currently unknown, and uncertainty remains over where arctic plants survived Pleistocene glaciations. A phylogenetic analysis of chloroplast DNA variation in the purple saxifrage (Saxifraga oppositifolia) indicates that this plant first occurred in the Arctic in western Beringia before it migrated east and west to achieve a circumpolar distribution. The geographical distribution of chloroplast DNA variation in the species supports the hypothesis that, during Pleistocene glaciations, some plant refugia were located in the Arctic as well as at more southern latitudes.

http://science.sciencemag.org/content/sci/289/5483/1343.full.pdf

Molecular Analysis of Plant Migration and Refugia in the Arctic

Past research into flooding tolerance and oxygen shortages in plants has been motivated largely by cultivation problems of arable crops. Unfortunately, such species are unsuitable for investigating the physiological and biochemical basis of anoxia-tolerance as selection has reduced any tolerance of anaerobiosis and anaerobic soil conditions that their wild ancestors might have possessed, Restoration of anoxia-tolerance to species that have lost this property is served better by physiological and molecular studies of the mechanisms that are employed in wild species that still possess long-term anoxia-tolerance. Case studies developing these arguments are presented in relation to a selection of crop and wild species, The flooding sensitivity and metabolism of maize is compared in relation to rice in its capacity for anaerobic germination, The sensitivity of potato to flooding is related to its disturbed energy metabolism and inability to maintain functioning membranes under anoxia and post-inoxia, By contrast, long-term anoxia-tolerance in the American cranberry (Vaccinium macrocarpon) and the arctic grass species Deschampsia beringensis can be related to the provision and utilization of carbohydrate reserves. Among temperate species, the sweet flag (Acorus calamus) shows a remarkable tolerance of anoxia in both shoots and roots and is also able to mobilize carbohydrate and maintain ATP levels during anoxia as well as preserving membrane lipids against anoxic and post-anoxic injury. Phragmites australis and Spartina alterniflora, although anoxia-tolerant, are both sulphide-sensitive species which can pre-dispose them to the phenomenon of die-back in stagnant, nutrient-rich water. Glyceria maxima adapts to flooding through phenological adaptations with a seasonal metabolic tolerance of anoxia confined to winter and spring which, combined with a facility for root aeration and early spring growth, allows rapid colonization of sites with only shallow flooding. The diversity of responses to flooding in wild plants suggests that, depending on the life strategy and habitat of the species, many different mechanisms may be involved in adapting plants to survive periods of inundation and no one mechanism on its own is adequate for ensuring survival.

Oxygen deprivation stress in a changing environment

Publisher Summary From the Arctic to the tropics, the pattern of plant distribution bears the imprint of oxygen as a limiting factor, either directly by acting on plant metabolism or indirectly by altering the environment. This chapter compares the distribution and physiology of plants from a range of habitats. During the life cycle of most species of higher plants there are critical periods when oxygen is a resource that is frequently limiting for germination, growth, and survival. The tolerance of adversity is an important path to survival as resource acquisition and, despite the relative abundance of oxygen in the atmosphere, it too is a resource that frequently limits the survival and competitive ability of many species. The ecological advantages and disadvantages of the various adaptations such as glycolytic rate and alcohol dehydrogenase (ADH) induction and end–products of glycolysis in relation to anoxia tolerance are also discussed. The consequences of oxygen deprivation for survival and metabolism and climatic change for the vegetation of oxygen–deficient habitats are also reviewed. The future prospects for oxygen limitations for plants rooted in upland and oceanic areas are discussed in relation to possible changes in the hydrologic cycle as a consequence of the greenhouse effect.

Oxygen availability as an ecological limit to plant distribution

Although oxygen is vital for all aerobic life forms, excessive levels of oxygen free radical production can lead to potentially lethal oxidative reactions. The role of superoxide dismutase is examined as an integral part of the defence against oxidative injury resulting from various physiological stresses.

Robert M. M. Crawford

Papers

Molecular Analysis of Plant Migration and Refugia in the Arctic

Oxygen deprivation stress in a changing environment

Oxygen availability as an ecological limit to plant distribution

Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress

Studies in Plant Survival.