Hypoxia-Induced Damage: Energy Metabolism of Plants Under Oxygen Deficiency

Root cells need to produce ATP via respiration in order to support transport processes and iosynthesis—for example, the uptake of nutrient anions from the soil solution against a negative membrane potential or the activation of sugars to build cell wall polysaccharides, respectively. The daily oxygen demands of soils during the growth period of plants are in the range of 10-20 L/m², depending on the density of the roots and the activity of soil microbes. There is a direct positive correlation between O2 partial pressure and root growth.

The minimum oxygen partial pressure in the soil for the growth of flooding-sensitive plants is 2-3% (about 5 kPa). Inhibition of growth under hypoxic conditions is a multifactorial phenomenon, which is basically caused by the very low efficiency of the energy metabolism. During inhibition of mitochondrial respiration, many heterotrophic organisms and plant tissues are able to switch to fermentative metabolism, which can be regarded as an accli- mative response to oxygen deficiency. This type of metabolism, however, requires increased throughput of energy carriers such as glucose because of the much lower energy yield (2 moles of ATP per mole of glucose via glycolysis, compared with 34-36 moles of ATP per mole of glucose via oxidative phosphorylation).

Under these conditions, reserve material is quickly consumed. Despite stimulation of glycolysis and fermentation—the so-called Pasteur effect—the energy charge of cells remains low, so during extended periods of hypoxia, or even short-term anoxia, values below 0.5 result (Fig. 5.4). These values are too low for anabolic metabolism (i.e. for growth). Inhibition of phloem transport and phloem unloading is another consequence of the low energy charge of the plant tissues. Thus, cells are depleted not only because of the faster turnover of storage material but also because of a drop in supply of photosynthates.

Fig. 5.4. Energy charge (EC) of lettuce seeds a or rice grains b during germination in air or under nitrogen. The energy charge of cells is usually determined by the degree of phosphorylation of the adenylate system. The following formula is applied: EC = ([ATP] + 0.5[ADP])/([ATP] + [ADP] + [AMP]). By definition, the maximum EC equals 1. Since ADP possesses only one energy-rich phosphate bond, its concentration has to be multiplied by the factor 0.5. A cell supplied with sufficient oxygen has an EC between 0.8 and 0.95. Under anaerobic conditions the energy charge may drop to 0.2. (After Pradet et al. (1985))

In addition to the energy deficit caused by hypoxia and anaerobiosis, fermentation leads to the accumulation of toxic metabolic products. The first product is lactate, produced by lactate dehydrogenase (LDH), which is rapidly activated upon O2 deficiency. A rise in lactate concentrations causes acidification of the cytosol, with potentially detrimental effects on metabolism. The next acclimative response, therefore, is inactivation of LDH by acidic pH. As the pH optimum of LDH is in the neutral range, it inhibits itself upon acidification of the cytosol. Pyruvate decarboxylase is less susceptible to acidity and therefore takes over, producing acetaldehyde, which is converted to ethanol by alcohol dehydrogenase.

Higher concentrations of this poisonous compound destroy the selective permeability of membranes and prevent formation of proton gradients and, in turn, the gain of energy. On the other hand, ethanol easily permeates through cellular membranes and cell walls and thus only rarely reaches damaging concentrations of 50-100 nM in the cell. This limits toxicity but results in a loss of reduced carbon. Acetaldehyde, the biochemical precursor of ethanol, is much more toxic than ethanol but is usually reduced immediately. It accumulates only when alcohol dehydrogenase is nonfunctional or switched off by mutation or regulation, respectively.

Fine root systems and root meristems are particularly sensitive to oxygen deficiency. In species not tolerant of flooding, those parts of the root system used for water and ion uptake die off at oxygen partial pressures below 0.5-5 kPa and, as a consequence, the plant becomes stressed as if exposed to drought even though it is standing in water. This is indicated by stomatal closure. The rates of photosynthesis and growth decrease.

Finally, the plants become stunted, while their leaves show strong epinasty (downward bending of the leaves and petioles because of increased relative growth of the upper side; this response is hypothesised to limit transpirational water loss because exposure to light is reduced). Such phenomena are often observed in indoor plants that are watered too much. Hypoxia in the water- saturated soil leads to death of the root system and withering of the shoot. In fact, most plants are more sensitive to flooding than to desiccation.