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

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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 (pH(cyt)). 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 pH(cyt) 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 pH(cyt) 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 (pH(vac)), 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-PP(i)ases, over that of V-ATPases, may direct energy flow at the tonoplast to maintain pH(cyt).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 pH(cyt) 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.
Original languageEnglish
Pages (from-to)999-1036
JournalFunctional Plant Biology
Volume30
DOIs
Publication statusPublished - 2003

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