Plant Metabolism in Oxygen-Deficient Environment

Reduction in oxygen level below ambient levels poses a significant threat to the survival of a plant. Such deficiency may be caused by temporary flooding,  water logging or microbial attack. Plant growth is affected by an oxygen-deficient environment. The yield of a crop in such adverse circumstances is reduced drastically. The main reason for reduced yield is low ATP production, resulting from inadequate oxidative phosphorylation. In extreme cases of the total absence of oxygen, the affected plant switches over to alternative pathways leading to fermentation. The latter yields only up to 3 molecules of ATP instead of up to 39 generated under aerobic condition. The fermentation process is also accompanied by the induction of glycolysis and the accumulation of lactate and ethanol.

Equally important is another problem in which oxygen does not reach tissues in the inner parts of the plant body, even though there may be a normal oxygen level in the environment. Lack of intercellular spaces restricts internal oxygen diffusion and slows down oxygen delivery to internal tissues. In such a situation, oxygen supply into internal tissues falls below the rate at which oxygen is consumed by such tissues. The state is called ‘anoxia’, when the oxygen supply is dangerously low and ‘hypoxia’ when the level is low but not threatening. It has been shown that in response to oxygen deficiency, the affected plants cut down their respiration rate to decrease oxygen consumption. Recent studies also indicate that substantial reduction in the concentration of oxygen activates an oxygen-sensing system that adjusts the rate of ATP formation in proportion to oxygen supply.

In the June, 2003 issue of Curr. Opin Plant Biol. (vol. 6:247-256), Peter Geigenberger at the Max Planck Institute of Molecular Plant Physiology, Germany, discusses how plants respond when they are subjected to an oxygen-deficient environment. He also discusses about sensing mechanisms, which detect oxygen deficiency and lead to adaptive responses to avoid or delay the depletion of oxygen to concentrations that would limit oxidative phosphorylation. The author draws our attention to the fact that even in a situation where oxygen supply is abundant in the external atmosphere, the rate of oxygen diffusion into the internal tissue may not keep up with its oxygen consumption rate, adversely affecting metabolic activity.

Low oxygen levels in bulky, dense or metabolically active plant tissues: The author points out, that root meristems and phloem tissue require high rates of oxygen delivery to carry out their metabolic activity. However, small intercellular spaces in these tissues do not allow diffusion of sufficient quantities of oxygen for their normal functioning. Recent study has shown that the oxygen level within the seed coat falls to around 1%, presumably because the seed coat has a cutinized layer of cells, restricting the entry of oxygen. Bulky storage organs such as apples, bananas are characterized by having little airspaces within their cells. In potato tubers, distinct gradients of oxygen concentrations occur during their growth: near the edge typical values are 8–10% as against 2–5% in the center.

Low  internal oxygen level results in a restriction of metabolic activity:
ATP provides energy that drives chemical reactions to take place along biosynthetic pathways. The quantum of force is expressed in terms of adenylate energy state. Short-term depletion of oxygen within the tissue inhibits respiration concomitant with a reduction in ATP/ADP ratio and the adenylate energy. This has been demonstrated in potato tubers, pea and bean seeds, Arabidopsis seeds and the phloem of Ricinus plants. In case of potato tubers, discs from the growing region were used for the study. In the other material, namely, in Ricinus, several sets of phloem exudates derived from a detached hypocotyl stump or stem cuttings served as the experimental material. The results of the three different experimental systems show a high correlation coefficient between oxygen levels and adenylate energy charge.

Low oxygen slows down biosynthetic activities to save ATP. Recent studies have shown that a progressive decrease in oxygen supply down-regulates various biosynthetic processes related to the production of sucrose, starch, amino acids, protein, and lipids. The functional significance of this inhibition is presumably that it allows a concomitant reduction of ATP consumption when respiration rate slows down. The low oxygen content also adversely delays the healing process of injured tissues due to scaling down of metabolic activity. In potato, low oxygen leads to a severe repression of the activity of phenylalanine ammonium lyase (PAL) and to a concomitant inhibition of phenylpropanoid synthesis. When oxygen concentration is reduced from 21% to 8%, phenylpropanoid synthesis goes down by 80% and the synthesis is totally stopped in the absence of oxygen.

Oxygen delivery restricts  energy metabolism and seed development:
When Arabidopsis, rice and rape seeds or siliques are subjected to below normal oxygen supply for two hours, they show progressive decrease in the cellular energy state. As a result, biosynthesis of lipids, protein and cell wall material are adversely affected. It was shown that the low energy state is not due to fermentation because in an environment where the oxygen concentration is 8-12 %,  lactate does not accumulate. It was also shown that a reduction of the external oxygen level down to 5%, stops seed development in a number of species such as rice, soybean, wheat, sorghum, rape and Arabidopsis. The low oxygen concentrations within the phloem of Ricinus plants (around 5–6%) limit phloem energy metabolism, restricting phloem loading and transport of metabolites such as sucrose.

Low internal oxygen supply leads to less consumption of ATP: Two biochemical pathways, differing in their energy requirements,  are involved in sucrose breakdown into hexose phosphates. The pathway that involves the enzymes, invertase and hexokinase consumes two molecules of ATP when one molecule of sucrose is metabolized. The other degradation pathway involving sucrose synthase (SuSy) and UDP-glucose pyrophosphorylase requires no ATP. Instead it uses one molecule of inorganic pyrophosphate (PPi) per sucrose molecule. Another characteristic about the (SuSy) gene is that it is upregulated in an oxygen-deficient environment, whereas low levels of oxygen down-regulate the invertase gene. This switch  indeed provides protection to plants because it saves ATP, conserves oxygen and allows higher oxygen concentrations to be maintained that would  not otherwise be possible and relying on the enzymes which require only PPi for its activity. Under normal growth conditions the activity of invertase is seen early in a development process. SuSytakes over during the later stage of development. Its activity was observed later in the development of potato tubers, and the seed filling process of maize and bean.

Low oxygen leads to complex changes in the pattern of gene expression:  Recent microarray studies have identified well-known transcripts and proteins associated with anoxia but also revealed the presence of hitherto unknown enzymes and signal-transduction components induced in response to low oxygen. A gradual decrease in internal oxygen provides an opportunity for acclimation before anoxic conditions are encountered.One set of  genes induced in maize roots in response to oxygen deprivation, encode enzymes such as Pdc1 (pyruvate decarboxylase 1), Pdc2, adh1 (alcohol dehydrogenase 1) and lactic dehydrogenase. Previous studies with adh1 mutants in maize and Arabidopsis have shown that ADH confers short-term resistance against water-logging.

How do plants sense that oxygen concentration is low? Recent studies have shown that an oxygen-sensing system may operate in higher plants somewhat analogous to that found in bacteria and yeast. In the bacterium, Rhizobium meliloti a 2-component signaling system has been reported. The system consists of a hemoprotein kinase and a transcriptor factor. The kinase is active in the deoxy state, while phosphorylation renders the transcription factor active. On the other hand, in higher plants, non-symbiotic hemoglobins have been indirectly implicated in oxygen sensing. It has been shown that low incidence of oxygen activates the hemoglobin gene GLB1 in Arabidopsis, barley and potato. Overexpression of this gene in transgenic Arabidopsis, induces better growth in a normal environment and prolongs survival in situations where the oxygen supply is depleted.

Conclusions: Plants respond to major oxygen deficiency by adaptive means to prevent tissue damage, resulting from diminished supply of oxygen. These measures are directed to 1) a rapid restriction of metabolism through reduced oxygen consumption,  2) a shift to pathways that use oxygen more efficiently and  (3) long-term morphological changes  to enhance oxygen entry. The author calls attention to some of the challenges that need to be solved. These are:  identification of the oxygen sensing system(s),  its mode of operation via the signal-transduction pathway(s) and  the components that play a key role in fine-tuning responses to low levels of oxygen in internal tissues lacking adequate intercellular space.


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