Those species that live by the water's edge or in seasonally flooded communities are exposed to a double jeopardy in relation to the level of the water table. The first is flooding, and the second is unflooding. The physiological problems that can arise from the first stress include cellular dysfunction due to a reduction in metabolic energy (ATP) and an increase of cytoplasm acidity due to proton pump failure (cytoplasmic acid-osis), which can lead to rapid cell death.
Oxygen deprivation exposes all tissues, irrespective of whether they are plant or animal, to the dangers of anaerobic cytoplasmic acidosis. In the absence of oxygen it is impossible to maintain the ATPase activity of the tonoplast and the functioning of proton pumps. Consequently, there is no proton influx into the vacuoles from the cytoplasm, which results in the immediate onset of cytoplasmic acidosis (Ratcliffe, 1997). In plants the role of cytoplasmic pH in triggering a rapid switch to ethanol production within an hour of the onset of anoxia has been convincingly demonstrated in maize using 31P nuclear magnetic resonance (Fox et al., 1995). In anoxia-tolerant plants basic amino acids (GABA and arginine)
and polyamines are formed to counteract pH decrease (Reggiani et al., 1990). A more gradual loss of viability comes from an increased consumption of carbohydrate reserves, accumulation of toxic waste products of anae-robiosis, and leakage of metabolites leading to pathogenic infections. If the plant has no means of aerating its underground organs, and this is especially the case for large plants such as trees and deep-rooted perennial herbs, then a lack of oxygen can bring all these adverse factors into play.
The second stressful consequence of flooding is unflooding. With the coming of spring plants that have endured a long winter of oxygen deprivation through flooding have to face the additional hazard of post-anoxic injury when the soil profile once again becomes aerated or emerging shoots (or both) restore a pathway for oxygen diffusion to underground organs. Prolonged anaerobiosis, although dangerous in itself creates for the period of unflooding a potentially more dangerous state due to the rapid and often irreversible damage that can be caused when air is re-admitted to tissues that have been deprived of oxygen for a lengthy period. This type of damage, post-anoxic injury, as it is termed in plants, is similar to post-ischaemic injury in animal and human organs which arises when they are suddenly re-exposed to air after interruption of the blood supply, as after a heart attack or a transplant operation.
The return to air generates reactive oxygen species to which the tissues of many plant species become vulnerable after a prolonged absence of oxygen and cessation of aerobic metabolism (see below). Many amphibious plant species, and also those arctic species that face the risk of oxygen deprivation due to prolonged encasement in ice, show a remarkable capacity to survive post-anoxic injury. During flooding, the lack of oxygen causes the transition metals involved in aerobic metabolism (the iron in cytochromes etc.) to become reduced to the ferrous state. The turnover rate of the enzymes needed for aerobic metabolism is also much diminished. Consequently, sudden re-emergence into air as water tables subside presents an aerobic shock to unprepared tissues. Under such conditions many plants are liable to suffer post-anoxic injury. Tissues prone to this type of injury become soft and spongy on return to air, and rapidly lose their cell constituents. In these cases, oxygen exerts a definite toxic effect and membranes are destroyed irreversibly. This type of injury arises from the post-anoxic generation of reactive oxygen species (ROS), typically oxygen (O2~) and hydroxy radicals (*HO2).
Both O2~ and *HO2 can undergo spontaneous dismutation to produce H2O2:
In the post-anoxic state when cytochromes are reduced, the Fenton reaction can be particularly active. This is the iron-salt-dependent decomposition of dihydrogen peroxide, generating the highly reactive hydroxyl radicals:
Fe2+ complex + H2O2 ! Fe3+ complex
Other enzymatic sources include the action of xanthine oxidase on dioxygen:
Ethanol that has accumulated under anoxia is also rapidly oxidized to acetaldehyde by the presence of H2O2
and catalase. The oxidation product, namely acetalde-
hyde, is highly damaging to membranes and therefore probably contributes more to membrane damage at the post-anoxic stage than ethanol during anoxia: Catalase
Other sources of ROS come from the reduced electron chains. In non-green cells the mitochondrial electron transport can give rise to ROS in living cells at any time. However, they are normally detoxified by enzymatic and non-enzymatic systems (SOD, catalase, ascorbate reductase, peroxidase, vitamins C and E, glutathione, and many others).
In stressed cells when these protective mechanisms are not fully developed or no longer equilibrated, ROS become effective agents of cell death. Although these active radicals are capable of reacting with many types of macromolecules, in plants their most deleterious action is in their reaction with lipids (e.g. lipid peroxidation) by initiating membrane damage leading to the destruction of cell organelles. Peroxidation products, such as ethane and malonedialdehyde, appear rapidly in the organs and tissues of non-tolerant plants (Braendle & Crawford, 1999). The inner membrane system of mitochondria seems to be particularly sensitive. The production of ROS is a common feature also for other stresses, including drought, salt injury, and pollution damage. Plants that are able to survive prolonged oxygen deprivation followed by a return to air all have the capacity to withstand both prolonged anoxia and avoid post-anoxic injury to their cell membranes with a protective antioxidant system (Braendle & Crawford, 1999). The highly anoxia-tolerant Acorus calamus (see below) maintains high concentrations of antioxidants, including ascorbate, phenolics and glutathione, throughout the period in which the plant is under anoxia, as well as the enzymes ascorbate reductase, peroxidase and catalase. Iris pseudacorus has a tolerance of anoxia that is only slightly inferior to that of A. calamus. This iris is also notable for the ability while under anoxia to synthesize superoxide dismutase, a key enzyme for active radicle detoxification on return to air (Monk et al., 1987).
The metabolic adaptations associated with surviving low oxygen availability can be summarized as:
(1) anaerobic mobilization of starch reserves
(2) prevention of cytoplasmic acidosis under anoxia
(3) dispersal and excretion of products that transfer hydrogen from anoxic or hypoxic tissues, either to the external environment, or to parts of the plant with access to oxygen
(4) an active antioxidant defence system dependent on (a) antioxidants and (b) enzymatic activity for antioxidant reduction and the destruction of active radicals (e.g. superoxide dismutase).
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