Geigenberger P, Fernie A R, Gibon Y, Christ M, Stitt M
Botanisches Institut, Universität Heidelberg, Germany.
Biol Chem. 2000 Aug;381(8):723-40. doi: 10.1515/BC.2000.093.
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 inhibition 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 is 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 partial inhibition of sucrose breakdown, glycolysis and respiration. The energy status of the adenine, guanine and uridine nucleotides decreased, but pyrophosphate levels remained high. The inhibition of sucrose breakdown and glycolysis was accompanied by a small increase of sucrose, fructose, glycerate-3-phosphate, phosphenolpyruvate, and pyruvate, a decrease of the acetyl-coenzymeA:coenzymeA ratio, and a small increase of isocitrate and 2-oxoglutarate. These results indicate that carbon fluxes are inhibited at several sites, but the primary site of action of low oxygen is probably in mitochondrial electron transport. Decreasing the oxygen concentration from 21% to 4% also resulted in a partial inhibition of sucrose uptake, a strong inhibition of amino acid synthesis, a decrease of the levels of cofactors including the adenine, guanine and uridine nucleotides and coenzymeA, and attenuated the wounding-induced increase of respiration and invertase and phenylalanine lyase activity in tissue discs. Starch synthesis was maintained at high rates in low oxygen. Anoxia led to a diametrically opposed response, in which glycolysis rose 2-fold to support fermentation, starch synthesis was strongly 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 respiration 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 glycolysis, starch synthesis and other biosynthetic pathways in plants, and reveal a potential role for pyrophosphate in conserving energy and decreasing oxygen consumption.
植物缺乏专门的器官和循环系统，在代谢活跃、致密或体积较大的组织中，氧气浓度可能会降至很低水平。在耐受低氧或缺氧的动物中，低氧会触发对呼吸和代谢活动的适应性抑制。本研究利用生长中的马铃薯块茎来探究植物中是否存在类似的反应。生长中的马铃薯块茎中心的氧气浓度会降至5%以下。这伴随着腺苷酸能量状态的降低以及代谢物的变化，这些变化表明糖酵解速率下降。通过在一系列氧气浓度下将生长中的块茎组织圆盘孵育2小时，对低氧反应进行了更详细的研究。当氧气浓度在21%至4%之间降低时，蔗糖分解、糖酵解和呼吸作用受到部分抑制。腺嘌呤、鸟嘌呤和尿苷核苷酸的能量状态下降，但焦磷酸水平仍然很高。蔗糖分解和糖酵解的抑制伴随着蔗糖、果糖、3-磷酸甘油酸、磷酸烯醇丙酮酸和丙酮酸的小幅增加，乙酰辅酶A:辅酶A比值的降低，以及异柠檬酸和2-氧代戊二酸的小幅增加。这些结果表明，碳通量在多个位点受到抑制，但低氧的主要作用位点可能在线粒体电子传递中。将氧气浓度从21%降至4%还导致蔗糖摄取受到部分抑制，氨基酸合成受到强烈抑制，包括腺嘌呤、鸟嘌呤和尿苷核苷酸以及辅酶A在内的辅因子水平降低，并减弱了组织圆盘中伤口诱导的呼吸、转化酶和苯丙氨酸裂解酶活性的增加。在低氧条件下，淀粉合成以高速率维持。缺氧导致完全相反的反应，其中糖酵解增加2倍以支持发酵作用，淀粉合成受到强烈抑制，乳酸水平、乳酸:丙酮酸比值以及磷酸丙糖:3-磷酸甘油酸比值急剧增加。研究得出结论，低氧会触发：（i）对呼吸的部分抑制，导致细胞能量状态下降；（ii）对广泛的耗能代谢过程的平行抑制。这些结果对于理解植物中糖酵解、淀粉合成和其他生物合成途径的调控具有普遍意义，并揭示了焦磷酸在节约能量和降低氧气消耗方面的潜在作用。
