Metabolic Acclimation to Anoxia Induced by Low (2-4 kPa Partial Pressure) Oxygen Pretreatment (Hypoxia) in Root Tips of <i>Zea mays</i>

Saglio, Pierre H.; Drew, M. C.; Pradet, A.

doi:10.1104/pp.86.1.61

Cited by 146 publications

(115 citation statements)

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“…The flooding resistance of a wide range of monocot and dicotyledonous species, both herbaceous and woody, is often associated, in part, with the capacity to develop such aerenchymatous roots (8,9,16,17,19,23). Additionally, metabolic acclimation to low oxygen improves the tolerance of roots to anoxia (29). ' The gaseous plant hormone, ethylene, is associated with a wide variety of responses in higher plant cells (3).…”

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Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.

Drew¹,

He²,

Morgan³

1989

Plant Physiol.

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162

129

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Plants of Zea mays L. cv TX5855 were grown in a complete, well oxygenated nutrient solution then subjected to nutrient starvation by omitting either nitrate and ammonium or phosphate from the solution. These treatments induced the formation of aerenchyma close to the apex of the adventitious roots that subsequently emerged from the base of the shoot, a response similar to that shown earlier to be induced by hypoxia. Compared with control plants supplied with all nutrients throughout, N-or Pstarvation consistently depressed the rates of ethylene release by excised, 25 mm apical segments of adventitious roots. Some enzymes and substrates of the ethylene biosynthetic pathway were examined. The content of 1-amino cyclopropane-1-carboxylic acid (ACC) paralleled the differences in ethylene production rates, being depressed by N or P deficiency, while malonyl-ACC showed a similar trend. Activity of ACC synthase and of ethylene forming enzyme (g-1 fresh weight) was also greater in control roots than in nutrient starved ones. These results indicate that much of the ethylene biosynthetic pathway is slowed under conditions of N-or P-starvation. Thus, by contrast to the effects of hypoxia, the induction of aerenchyma in roots of Zea mays by nutrient starvation is not related to an enhanced biosynthesis and/or accumulation of ethylene in the root tips.Many dryland species are exposed to temporary periods of oxygen deficiency during their growth following heavy rain, irrigation, or flooding, when the soil becomes water saturated (10,17). Some species respond to this situation by forming roots with continuous, gas-filled channels in the roots (19). These channels improve the internal supply of oxygen, the oxygen originating from the atmosphere or photosynthesis and passing from leaves to roots down a concentration gradient (1). The flooding resistance of a wide range of monocot and dicotyledonous species, both herbaceous and woody, is often associated, in part, with the capacity to develop such aerenchymatous roots (8,9,16,17,19,23 The gaseous plant hormone, ethylene, is associated with a wide variety of responses in higher plant cells (3). In earlier reports we showed that aerenchyma formation in adventitious (nodal) roots of maize by cell lysis is induced by a partial oxygen deficiency (hypoxia) and is closely related to enhanced endogenous concentrations of ethylene (1 1). Hypoxia clearly stimulates the biosynthesis of ethylene in growing maize roots (2,11,12,20) as in other responsive plant tissues (4, 5, 7). Low exogenous concentrations of ethylene under aerobic conditions (1-5 uL L-' in air) induce aerenchyma (18) that is structurally indistinguishable from that induced by hypoxia (1 1, 12); furthermore, hypoxically induced aerenchyma formation in the apices of growing roots is blocked by inhibitors of ethylene biosynthesis or ethylene action (12,18,20).However, Konings and Verschuren (21) showed that formation of aerenchyma in the seminal roots of maize was stimulated under fully aerobic conditions by omission o...

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Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.

Drew¹,

He²,

Morgan³

1989

Plant Physiol.

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162

129

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“…Some investigations could not verify any effect of NO 3 -and NR on the energy metabolism in oxygendeficient roots. 22,23 However, other investigations have shown that NO 3 -supply to anaerobic root tissues led to an improved and 0.13 ± 0.03 g, respectively. The changes in the root and shoot dry weights (DW) and in shoot/root ratio were investigated after a three week period of hypoxic treatment.…”

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Prolonged root hypoxia effects on enzymes involved in nitrogen assimilation pathway in tomato plants

Horchani

Aschi‐Smiti²

2010

Plant Signaling & Behavior

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IntroductionPlants grow in a dynamic environment, which frequently imposes constraints on growth and development. Among the adverse environmental factors commonly encountered by land plants, flooding is one of the most significant abiotic stresses. 1 Flooding of the soil can have a tremendous impact on the growth and survival of plants, and thereby on agricultural as well as natural ecosystems. In the last decades considerable progress has been made in our understanding of the mechanisms that enable certain plant species and cultivars to withstand periods with excess soil water or even complete submergence. Much of the research has been carried out with crop plant species, such as Oryza sativa, Zea mays, Trifolium subterraneum and Medicago sativa, 2-5 but wild species originating from wetland habitats have been also used, mostly for comparative studies. 6,7 With transient flooding or irrigation followed by slow drainage, or in natural wetlands, plant roots can become oxygen deficient because of slow transfer of dissolved oxygen in the waterfilled pore space of the soil. The decrease in ambient oxygen may not be, itself or alone, the perceived signal but could trigger metabolic responses, which then initiate the signalling cascade. 8 The immediate consequence of oxygen depletion is the reduction in respiration, thus diminishing ATP generation, and leading to a decrease in the ATP/ADP ratio and the adenylate energy charge. 9 In order to investigate the effects of root hypoxia (1-2% oxygen) on the nitrogen (N) metabolism of tomato plants (Solanum lycopersicum L. cv. Micro-Tom), a range of N compounds and N-assimilating enzymes were performed on roots and leaves of plants submitted to root hypoxia at the second leaf stage for three weeks. Obtained results showed that root hypoxia led to a significant decrease in dry weight (DW) production and nitrate content in roots and leaves. conversely, shoot to root DW ratio and nitrite content were significantly increased. contrary to that in leaves, glutamine synthetase activity was significantly enhanced in roots. The activities of nitrate and nitrite reductase were enhanced in roots as well as leaves. The higher increase in the Nh 4 + content and in the protease activities in roots and leaves of hypoxically treated plants coincide with a greater decrease in soluble protein contents. Taken together, these results suggest that root hypoxia leaded to higher protein degradation. The hypoxia-induced increase in the aminating glutamate dehydrogenase activity may be considered as an alternative N assimilation pathway involved in detoxifying the Nh 4 + , accumulated under hypoxic conditions. With respect to hypoxic stress, the distinct sensitivity of the enzymes involved in N assimilation is discussed. and 0.13 ± 0.03 g, respectively. The changes in the root and shoot dry weights (DW) and in shoot/root ratio were investigated after a three week period of hypoxic treatment. Root hypoxia decreased root and leaf DW production by 34 and 18%, respectively. Shoot to root DW ratio increas...

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“…For maize root tips, hypoxia rather than anoxia induced elevated activity of ADH (Saglio et al, 1988;Johnson et al, 1989). In maize protoplasts Walker et al, 1987), there were severalfold increases in Adhl mRNA with hypoxia (O2 concentra-Plant Physiol.…”

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“…The sudden imposition of anoxia with inhibition of oxidative phosphorylation caused a rapid decline in energy metabolism, and death of the apical meristem occurred in 15 to 20 h (Roberts et al, 1984a(Roberts et al, , 1984bSaglio et al, 1988;Johnson et al, 1989). During that time, there was no incorporation of I4C-labeled amino acids or 35S-labeled Met into proteins (D.J.…”

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“…By contrast, the anoxia tolerance of the root tip is considerably greater if roots are first exposed to a partia1 deficiency of 02, resulting in tissue hypoxia. Following hypoxic pretreatment, the viability of the apical meristem was extended to at least 96 h, ATP concentrations were greater, ADH activity was induced, and the rate of anaerobic respiration was stimulated (Saglio et al, 1988;Johnson et al, 1989;Hole et al, 1992).…”

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Hypoxic and Anoxic Induction of Alcohol Dehydrogenase in Roots and Shoots of Seedlings of Zea mays (Adh Transcripts and Enzyme Activity)

et al. 1993

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Alcohol dehydrogenase (ADH) is one of a number of enzymes of glycolysis and fermentation known to be synthesized preferentially under low O , conditions. We examined levels of Adhl transcripts and of ADH activity in 5-mm root tips, root axes (the remainder of the seminal root), and shoots of maize (Zea mays 1.cv TX 5855) seedlings. Seedlings with roots averaging about 60-mm long were transferred from fully aerobic conditions (solutions sparged with 40% [v/v] O,) to anaerobic (02-free) conditions, or to an intermediate O , concentration. There was no prior acclimation to low O,. In root tips, anoxia induced Adhl transcripts and enzyme activity at 6 h, but this was followed by a rapid decline so that at 12 to 18 h neither were detectable and the root tips were dead. In contrast, higher levels of Adhl transcripts and enzyme activity were maintained for at least 48 h i n root axes and shoots. When induction at 6 h was measured over a wide range of 0, concentrations, a peak i n ADH activity occurred in all tissues at 4% (v/v) O,. Maximum levels of transcripts, however, were i n the range of O to 4% O,, depending on the tissue. The time course of hypoxic induction (at 4% O,) i n root tips showed a peak in transcript levels at 6 h, whereas ADH activity continued to rise throughout the 24-h experiment. These results show that i n root tips, ADH induction by anoxia was small and transient relative to induction by hypoxia.

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Metabolic Acclimation to Anoxia Induced by Low (2-4 kPa Partial Pressure) Oxygen Pretreatment (Hypoxia) in Root Tips of Zea mays

Cited by 146 publications

References 21 publications

Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.

Decreased Ethylene Biosynthesis, and Induction of Aerenchyma, by Nitrogen- or Phosphate-Starvation in Adventitious Roots of Zea mays L.

Prolonged root hypoxia effects on enzymes involved in nitrogen assimilation pathway in tomato plants

Hypoxic and Anoxic Induction of Alcohol Dehydrogenase in Roots and Shoots of Seedlings of Zea mays (Adh Transcripts and Enzyme Activity)

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