H<sup>+</sup> Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tips

Xia, Jianrong; Saglio, Pierre H.

doi:10.1104/pp.93.2.453

Cited by 25 publications

(22 citation statements)

References 25 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Thus, the efflux of lactate would only occur in conjunction with a proton, lowering the acidity of the cytosol in the process. In addition, the rapid time course of expression is consistent with the rapid onset of lactic acid fermentation and accompanying lactic acid release from hypoxic roots, which is detectable within the 1st h after oxygen deprivation (49).…”

Section: Discussionmentioning

confidence: 66%

“…Consistent with this observation, lactic acid efflux is observed in hypoxiachallenged roots of certain plant species (49 -51). Moreover, this induction of lactic acid secretion is correlated with an increased ability to survive anoxic conditions (49,50) and presumably mitigates the cytosolic acid load during flooding-induced fermentation (38).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Choi

Roberts

2007

Journal of Biological Chemistry

161

128

View full text Add to dashboard Cite

Nodulin 26 intrinsic proteins (NIPs) are plant-specific, highly conserved water and solute transport proteins with structural and functional homology to soybean nodulin 26. Arabidopsis thaliana contains nine NIP genes. In this study, it is shown that one of these, AtNIP2;1, is exquisitely sensitive to water logging and anoxia stress. Based on quantitative PCR and promoter::GUS experiments, AtNIP2;1 is expressed at a low basal level in the root tips and the vascular bundle of differentiated roots. Transcript levels are elevated acutely and rapidly upon water logging of root or leaf tissues, increasing 70-fold in roots within the 1st h of submersion. After this large initial increase, mRNA levels decline to steady state levels that remain over 10-fold higher by 6 h post-submersion. An even greater induction of AtNIP2;1 expression was observed upon anoxia challenge of Arabidopsis seedlings, with a 300-fold increase in AtNIP2;1 transcript observed by 2 h after the initiation of oxygen deprivation. Functional analysis of AtNIP2;1 expressed in Xenopus oocytes shows that the protein differs from soybean nodulin 26, showing minimal water and glycerol transport. Instead, AtNIP2;1 displays transport of lactic acid, with a preference for the protonated acidic form of this weak acid. Overall, the data suggest that AtNIP2;1 is an anaerobic-induced gene that encodes a lactic acid transporter and may play a role in adaptation to lactic fermentation under anaerobic stress.Major intrinsic proteins (MIPs) 2 are an ancient integral membrane channel protein family of water and uncharged solute transporters that have been found in nearly all living organisms. MIPs are especially prevalent and diverse in higher plants and have been classified into four monophyletic groups as follows: the plasma membrane intrinsic proteins (PIPs), the tonoplast intrinsic proteins, the nodulin 26-like intrinsic proteins (NIPs), and the small basic intrinsic proteins (1).NIPs are named for soybean nodulin 26 (Nod26) (2), which is the major protein component of the symbiosome membrane from nitrogen-fixing soybean root nodules (3, 4). Functional analyses indicate that Nod26 is an aquaglyceroporin with a low intrinsic water permeability and the ability to transport uncharged metabolites such as glycerol (4, 5) and has also been implicated in ammonia transport (6). It has become clear that NIPs represent a large, diverse family of aquaglyceroporins, with multiple members found in every sequenced higher plant genome (1,7,8). For example, among the 35 MIP genes in Arabidopsis thaliana (1), there are nine members of the NIP subfamily. Based on molecular modeling of the pore selectivity sequences, these nine NIPs are subdivided into the following two groups: NIP subgroup I proteins are encoded by NIP1;1, NIP1;2, NIP2;1, NIP3;1, NIP4;1, and NIP4;2, and NIP subgroup II proteins are encoded by NIP5;1, NIP6;1, and NIP7;1 (9).Analysis of NIP subgroup I proteins shows that they are more similar to soybean nodulin 26 in structure and function, with several showing aqu...

show abstract

Section: Discussionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Choi

Roberts

2007

Journal of Biological Chemistry

161

128

View full text Add to dashboard Cite

show abstract

“…This limitation cannot be explained by decreased sugar penetration in anoxia. According to Xia and Saglio (1990), sugar influx in the absence of O, is proportional to the sugar concentration and should allow the penetration of 100 and 35 nmol tip-' h-l for 100 mM Glc or Fru, respectively. A simple calculation using the penetration of labeled dGlc presented in this paper gives similar values (50 nmol tip-' h-l for NHPT root tips).…”

Section: Discussionmentioning

confidence: 99%

Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment

1996

View full text Add to dashboard Cite

Severa1 enzyme activities were measured in extracts from acclimated and nonacclimated maize (Zea mays) root tips at pH 6.5 and 7.5, corresponding to cytoplasmic pH in anaerobiosis or aerobiosis, respectively, to determine what causes the decline of the glycolytic flux observed in anoxia in nonacclimated tips. We found that phosphorylation of hexoses by kinases was a major limiting step of glycolysis in anoxia. When fructose was substituted for glucose, glycolysis was slightly enhanced and survival improved, but neither matched that of acclimated tips. Decrease of kinase activities was not the result of proteolytic degradation but was more likely the result of inhibition by interna1 factors (low pH and low ATP). There was no evidence of induction during the hypoxic pretreatment of isoenzymes better adapted to the anoxic cellular environment. A preacclimation in hypoxia allows excised maize (Zea nzays) root tips supplemented with externa1 Glc to survive severa1 days in strict anoxia instead of less than 10 h in the absence of pretreatment Xia and Saglio, 1992). However, in the absence of exogenous Glc, they do not survive significantly longer than nonacclimated tips. We have shown that, below a critica1 threshold of glycolytic flux, survival was compromised (Xia et al., 1995). An hypoxic pretreatment induces an increase of maximal in vitro catalytic activities of many enzymes involved in sugar metabolism, a higher ATP level correlated with a higher energy charge (reviewed by Ricard et al., 1994), and a better regulation of cytoplasmic pH linked to an efficient efflux of lactic acid (Xia and Roberts, 1994;Xia et al., 1995;Xia and Saglio, 1992). However, the role of these modifications in the subsequent survival of tissues in anoxia is not obvious. For example, we have shown that in HPT root tips the level of ATP is not critica1 for survival or for cytosolic pH regulation in anoxia (Xia et al., 1995), and the increase in glycolytic enzyme activities is not correlated with a higher glycolytic rate during the 90 min after the transfer of tissues from air to strictly anoxic conditions. During this period, the glycolytic rate (measured as the sum of ethanol plus lactate) remains strictly identical in HPT and NHPT * Corresponding author; e-mail saglio@bordeaux.inra.fr; fax 56-84-32-45. root tips. It is only after 60 to 90 min that the glycolytic flux declines and then almost stops in NHPT root tips even in the presence of added Glc, whereas it remains sustained in HPT tips (Xia and Saglio, 1992). Such a decline of ethanol production during the hours or days after the transfer to anoxia appears to be common to many plants (Smith and ap Rees, 1979;Raymond et al., 1985; Kimmerer and Mac Donald, 1987). Exceptions are rice seeds and seedlings, which are resistant to anoxia and in which the rate of ethanol production increases during at least the first 2 d in the absence of O, (Raymond et al., 1985).How glycolytic flux is modified in HPT and NHPT root tips and what is responsible for its decline in NHPT tips early in anoxia (...

show abstract

“…For each condition tested at pH, 4.5, net H+ influx was lower during anoxia than normoxia. This result could reflect either activation of H+ extrusion (via mechanisms such as the plasma membrane H' -ATPase) or reduced H+ influx via secondary transport systems (Kurkdjian and Guern, 1989;Xia and Saglio 1990) under anoxia. Evidence in support of the first alternative is provided by the observation that fluoride caused increased influx under anoxia at pH, 4.5 but not significantly at pH, 6.1, where the net H+ influx was very low (Fig.…”

Section: Net Movement Of H+ Into Root Tips From Acidic Media and Consmentioning

confidence: 99%

Regulation of H+ Extrusion and Cytoplasmic pH in Maize Root Tips Acclimated to a Low-Oxygen Environment

Xia

Roberts

1996

Plant Physiology

View full text Add to dashboard Cite

We tested the hypothesis that H+ extrusion contributes to cytoplasmic pH regulation and tolerance of anoxia in maize (Zea mays) root tips. We studied root tips of whole seedlings that were acclimated to a low-oxygen environment by pretreatment in 3% (v/v) O,. Acclimated root tips characteristically regolate cytoplasmic pH near neutrality and survive prolonged anoxia, whereas nonacclimated tips undergo severe cytoplasmic acidosis and die much more quickly. We show that the plasma membrane H+-AlPase can operate under anoxia and that net H+ extrusion increases when cytoplasmic pH falls. However, at an external pH near 6.0, H+ extrusion contributes little to cytoplasmic pH regulation. At more acidic external p H values, net H+ flux into root tips increases dramatically, leading to a decrease in cytoplasmic pH and reduced tolerante of anoxia. We present evidence that, under these conditions, H+ pumps are activated to partly offset acidosis due to H+ influx and, thereby, contribute to cytoplasmic pH regulation and tolerante of anoxia. l h e regulation of H+ extrusion under anoxia is discussed with respect to the acclimation response and mechanisms of intracellular p H regulation in aerobic plant cells.Root tips of whole maize (Zea mays) seedlings subjected to HPT with 3% (v/v) O, in N, survive longer under anoxia than NHPT tips (Saglio et al., 1988;Johnson et al., 1989). HPT root tips regulate cytoplasmic pH near neutrality for many hours, in contrast to NHPT root tips, which exhibit severe cytoplasmic acidosis early in anoxia (Xia and Roberts, 1994;Xia et al., 1995). Cytoplasmic acidosis can cause early death in hypoxic maize root tips (Roberts et al., 1984), and the extent of cytoplasmic acidosis in plants under low oxygen has been widely shown to correlate with their intolerance of this stress (reviewed by Kennedy et al., 1992 andRicard et al., 1994). It is therefore important to understand the factors and mechanisms contributing to intracellular pH regulation in plant cells under anoxia.One phenomenon that may be valuable in preventing cytoplasmic acidosis during anoxic stress is lactate efflux, which has been observed to be induced in maize roots during acclimation in 3% O, (Xia and Saglio, 1992;Xia and Roberts, 1994) and also in certain Limonium sp. (Rivoal and Hanson, 1993). Fermentation to cytoplasmic lactate leads to significant cytoplasmic acidosis (reviewed by Ricard et al., 1994). Therefore, it is possible that remova1 of cytoplasmic lactate by efflux might serve to limit acidosis. Such a pos- sibility depends in part on the fate of H+ generated during fermentation of Glc to lactate; H+ generation is stoichiometric with lactate at constant ATP (Hochachka and Mommsen, 1983). It is not currently known if HPT root tips excrete lactate anion or lactic acid or if cytoplasmic H+ produced during fermentation to lactate is pumped into the extracellular space or the vacuole.Saint-Ges et al. (1991) observed a correlation between cytoplasmic pH and ATP levels after the onset of anoxia in excised NHPT maize root tips....

show abstract

H⁺ Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tips

Cited by 25 publications

References 25 publications

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment

Regulation of H+ Extrusion and Cytoplasmic pH in Maize Root Tips Acclimated to a Low-Oxygen Environment

Contact Info

Product

Resources

About

H+ Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tips

Cited by 25 publications

References 25 publications

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment

Regulation of H+ Extrusion and Cytoplasmic pH in Maize Root Tips Acclimated to a Low-Oxygen Environment

Contact Info

Product

Resources

About

H⁺ Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tips