Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers

Plants lack specialised organs and circulatory systems, and oxygen can fall to low concentrations in metabolically active, dense or bulky tissues. In animals that tolerate hypoxia or anoxia, low oxygen triggers an adaptive in hibition of respiration and metabolic activity. Growing potato tubers were used to investigate whether an analogous response exists in plants. Oxygen concentrations fall below 5% in the centre of growing potato tubers. This i s accompanied by a decrease of the adenylate energy status, and alterations of metabolites that are indicative of a decreased rate of glycolysis, The response to low oxygen was investigated in more detail by incubating tissue discs from growing tubers for 2 hours at a range of oxygen concentrations. When oxygen was decreased in the range between 21% and 4% there was a part ial inhibition of sucrose breakdown, glycolysis and respiration. The energy status of the adenine, guanine and uridine nucleotides decreased, but pyro phosphate levels remained high, The inhibition of sucrose breakdown and gly colysis was accompanied by a small increase of sucrose, fructose, glycerate -3-phosphate, phosphenolpyruvate, and pyruvate, a decrease of the acetyl-co enymeA:coenzymeA ratio, and a small increase of isocitrate and 2-oxoglutara te. These results indicate that carbon fluxes are inhibited at several site s, but the primary site of action of low oxygen is probably in mitochondria l electron transport. Decreasing the oxygen concentration from 21% to 4% al so resulted in a partial inhibition of sucrose uptake, a strong inhibition of amino acid synthesis, a decrease of the levels of cofactors including th e adenine, guanine and uridine nucleotides and coenzymeA, and attenuated th e wounding-induced increase of respiration and invertase and phenylalanine lyase activity in tissue discs. Starch synthesis was maintained at high rat es in low oxygen. Anoxia led to a diametrically opposed response, in which glycolysis rose P-fold to support fermentation, starch synthesis was strong ly inhibited, and the level of lactate and the lactate: pyruvate ratio and the triose-phosphate:glycerate-3-phosphate ratio increased dramatically. It is concluded that low oxygen triggers (i) a partial inhibition of respirat ion leading to a decrease of the cellular energy status and (ii) a parallel inhibition of a wide range of energy-consuming metabolic processes. These results have general implications for understanding the regulation of glyco lysis, starch synthesis and other biosynthetic pathways in plants, and reve al a potential role for pyrophosphate in conserving energy and decreasing o xygen consumption.