Lactic Acid Efflux as a Mechanism of Hypoxic Acclimation of Maize Root Tips to Anoxia

Abstract

Hypoxic pretreatment (3 kPa oxygen) of maize (Zea mays L.) root tips improved their survival time in a subsequent anoxic incubation from 10 h to more than 3 d, provided that glucose was added to the medium to sustain metabolism. The glycolytic flux (lactate + ethanol) was the same in both pretreated and untreated root tips during the 1st h after transfer to anoxia. It was only after 2 h that it declined sharply in untreated tips, but was sustained in pretreated ones. Right after the transition from normoxia to anoxia of untreated root tips, the only fermentative product detected was lactic acid, which accumulated in a 7:1 proportion after 30 min in tissue and medium, respectively. It took 10 min before ethanol could be detected and 20 min for it to be produced at its maximum rate at the expense of lactate production, which slowed down. In contrast, in hypoxically pretreated root tips, ethanol was produced at a maximum rate right after the transfer to anoxia. Concurrently, low amounts of lactic acid were produced that accumulated in a 1:1 proportion after 30 min in tissue and medium, respectively. This large efflux of lactic acid could account for the higher cytoplasmic pH values always found in pretreated tissues. The presence of cycloheximide during pretreatment abolished this difference, suggesting that the greater efficiency of lactate efflux was linked to protein synthesis. The role of lactate in cytosolic pH regulation and in sensitivity to anoxia is discussed.Most mesophytes, including maize, are intolerant to anoxic conditions. However, pretreatment at low oxygen pressure induces mechanisms that improve their survival capacity under subsequent anoxic conditions. These mechanisms lead to two kinds of survival strategies. One consists of the formation of lysigenous cortical aerenchymas, helping to maintain a high respiration rate in the tissues by improving internal oxygen transport (5). This is a slow (days) and nonreversible mechanism induced by ethylene (4). The second strategy consists of the metabolic acclimation that apparently improves the energy relationships of anoxic tissues and contributes to a more prolonged survival in the absence of oxygen (9,25). This response is fast (hours) and involves the induction of a limited number of 'anaerobic polypeptides' (23). These polypeptides are different from the 'heat shock proteins ' (14), and those that have been identified are enzymes involved in the glycolytic and fermentative pathways (18,19,24). However, the significance of these proteins in tolerance to anoxia has rarely been examined and remains unclear. The results obtained by Hanson and colleagues (6, 7) on hypoxically inducible LDH' in barley roots and aleurone tissues imply some unrecognized function for this enzyme. Furthermore, there is evidence that ADH levels, which are known to increase dramatically during hypoxic acclimation, are not correlated with the better survival capacity of acclimated maize root tips in anoxia (22).Metabolic studies of survival of plant tissues in the absence...

The control of carbon acquisition by roots

“…The gating of this channel appears to be directly regulated by external Al concentration, is cell-specific and is under the control of a single gene (Kochian, 1995). Similar mechanisms have been proposed for lactate efflux under anaerobiosis, and organic acid efflux under P and Fe deficiency (Hoffland, 1992 ;Xia & Saglio, 1992 ;Xia & Roberts, 1994).…”

Effects of Short-term Exposure to Low Oxygen Atmospheres on Phsyiological Responses of Sweetpotato Roots

“…The extent of cytoplasmic acidification in plants under low oxygen has been shown to correlate with their intolerance of stress (Xia and Roberts, 1996). Xia and Saglio (1992) found that hypoxia-acclimated maize root tips have a higher cytoplasmic pH under anoxia than in the case of non-acclimated maize root tips. In addition, the acidification of cell sap has been induced by anoxia in non-resistant plants like wheat and barley.…”

“…2), ADH was not likely to be the factor that limited ethanol production. Xia and Saglio (1992) also suggested that the activity of ADH was not the limiting factor for the accumulation of ethanol in some plant tissues. On the other hand, PDC was reported to be an allosteric enzyme, as indicated by the sigmoidal relationship between activity and pyruvate concentrations (Rivoal et al, 1990).…”

“…Roberts et al (1989) reported that ethanol production rates in hypoxic maize root tips were correlated with ADH activity when the enzyme level was very low, but at high levels of ADH activity, ethanol production was independent of this activity. Xia and Saglio (1992) also suggested that the activities of ADH and lactate dehydrogenase (LDH) were not ratelimiting factors in the accumulation of ethanol and lactate in some plant tissues if the activities of these enzymes were high. Ke et al (1995) proposed that fermentative metabolism can be regulated by two mechanisms in avocado fruit: (1) molecular control of PDC and ADH, and (2) metabolic control of these enzymes in plant tissue under low-O 2 stresses.…”

Rhizosphere properties of rice genotypes as influenced by anoxia and availability of zinc and iron

“…Anoxic conditions showed no considerable effect on ADH and LDH activity. A direct involvement of ADH and LDH in the resistance of maize plants to anoxia has not been confirmed (Xia & Saglio, 1992).…”