Review: Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes

Abstract

Anoxia in plant tissues results in an energy crisis (Gibbs and Greenway 2003). How anoxia-tolerant tissues cope with such an energy crisis is relevant not only to anoxia tolerance, but also to adverse conditions in air that cause an energy crisis.To survive an energy crisis, plant cells need to reduce their energy requirements for maintenance, and also direct the limited amount of energy produced during anaerobic catabolism to the energy-consuming processes that are critical to survival.We postulate that during anoxia, reductions in ion fluxes and protein turnover achieve economies in energy consumption. Processes receiving energy from the limited supply available under anoxia include synthesis of anaerobic proteins and energy-dependent substrate transport. Energy would also be required for maintenance of membrane integrity and for regulation of cytoplasmic pH (pHcyt). We suggest that a moderate decrease in the set point of pHcyt, from approximately 7.5 to approximately 7.0 is an acclimation to the energy crisis in anoxia-tolerant tissues. This decrease in the set point of pHcyt would favour metabolism of acclimative value, such as reduction in protein synthesis and stimulation of ethanolic fermentation. During anoxia lasting several days, a proportion of the scarce energy produced may need to be spent to mitigate the acidifying effect on pHcyt arising from fluxes of undissociated organic acids across the tonoplast as a consequence of high concentrations of organic acids in the vacuole. Increases in vacuolar pH (pHvac), with concomitant decreases in the vacuolar concentrations of undissociated acids, would mitigate such an 'acid load' on the cytoplasm. We present evidence that a preferential engagement of V-PPiases, over that of V-ATPases, may direct energy flow at the tonoplast to maintain pHcyt.We conclude that the likely causes of death under anoxia are firstly, a decrease in pHcyt below 7.0. Cytoplasmic acidosis occurs in several anoxia-intolerant tissues and may contribute to their death. Such adverse decreases in pHcyt can be mitigated by the biochemical pH stat. Secondly, deterioration in membrane selectivity culminating in loss of membrane integrity would be fatal. We suggest these two causes are not mutually exclusive but may act in concert.

Nitrogen metabolism in plants under low oxygen stress

“…Decarboxylation of glutamate by GDC is part of the GABA shunt that involves the reactions catalyzed by the enzymes GABA-Transaminase (GABA-T) and succinic semialdehyde dehydrogenase (SSADH). The GABA shunt contributes to cellular pH-stat since glutamate decarboxylation is a proton consuming reaction that increases the pH (Drew 1997;Greenway and Gibbs 2003). In the freshwater crayfish Orconectes virilis, GDH was shown to be phosphorylated under oxygen-limiting conditions leading to a reduction of the enzyme activity to cut the bridge between C and N assimilatory pathways until the fish return to normoxia (Dawson and Storey 2012).…”

“…Major disorders caused by low oxygen stress are related to energy crisis caused by the inhibition of mitochondrial oxidative phosphorylation and subsequent reduction in ATP production. Thus, available energy becomes insufficient to meet the needs of energy-demanding biological processes (Greenway and Gibbs 2003). One of the major consequences of the shortage in ATP is an impaired functioning of the plasma membrane H + pumping ATPase that contributes to hypoxiainduced acidification of the cytoplasm (Felle 2006).…”

Plant respiration under low oxygen

“…Under some conditions, when the availability of O 2 in roots is decreased, adaptation to stress may occur through two strategies; the first is a decrease in ATP consumption which leads to a metabolic crisis at the cellular level , and the second is an increase in the glycolytic flux (Mancuso and Marras, 2006). The latter is called the "Pasteur effect" (Gibbs et al, 2000), consisting of a progressive acceleration in carbohydrate metabolism that allows the plants to maintain their energy level, especially during the early phase of acclimation to oxygen deficiency (Turner, 1951;Greenway and Gibbs, 2003;Camacho-Pereira et al, 2009;Wegner, 2010).…”

“…The O 2 is a molecule that participates as a final electron acceptor in the transport chain complexes ; therefore, when oxygen availability decreases dramatically in the rhizosphere (anoxia, Table 1), OXPHOS is inactivated (Moller, 2001) and terminal oxidase (COX) is inhibited (Liao and Lin, 2001;Greenway and Gibbs, 2003;Mancuso and Marras, 2006;Mailloux et al, 2007). Under these conditions, plants have developed alternative pathways to aerobic respiration in order to maintain glycolysis through the regeneration of NAD + and thus obtain the energy needed to maintain key processes of metabolism such as membrane integrity and thus ion selectivity (Tadege et al, 1999), protein synthesis and turnover and regulation of cytosolic pH, among others (Blokhina et al, 2003).…”

Effects of waterlogging on the soil structure of some Italian soils in relation to the GAEC cross-compliance standard Maintenance of farm channel networks and field convexity

“…They are mainly due to a decreased availability of O2 and an accumulation of phytotoxins (Armstrong and Armstrong, 2001). Oxygen deficiency inhibits aerobic respiration, resulting in severe energy deficiency and eventually death (Greenway and Gibbs, 2003). In addition, waterlogging can also reduce the availability of some essential nutrients, such as nitrogen, and increase the availability of nutrients, such as iron (Fe) and manganese (Mn) (Ponnamperuma, 1972).…”