Plant Physiol. (1998) 118: 1403-1409

Changes in Hexokinase Activity in Echinochloa phyllopogon and Echinochloa crus-pavonis in Response to Abiotic Stress¹

Theodore C. Fox, Brian J. Green, Robert A. Kennedy, and Mary E. Rumpho^*

Program in Plant Physiology and Plant Biotechnology and Departments of Horticultural Sciences (T.C.F., B.J.G., M.E.R.), and Biology (R.A.K.), Texas A&M University, College Station, Texas 77843

	ABSTRACT

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Hexokinase (HXK; EC 2.7.1.1) regulates carbohydrate entry into glycolysis and is known to be a sensor for sugar-responsive gene expression. The effect of abiotic stresses on HXK activity was determined in seedlings of the flood-tolerant plant Echinochloa phyllopogon (Stev.) Koss and the flood-intolerant plant Echinochloa crus-pavonis (H.B.K.) Schult grown aerobically for 5 d before being subjected to anaerobic, chilling, heat, or salt stress. HXK activity was stimulated in shoots of E. phyllopogon only by anaerobic stress. HXK activity was only transiently elevated in E. crus-pavonis shoots during anaerobiosis. In roots of both species, anoxia and chilling stimulated HXK activity. Thus, HXK is not a general stress protein but is specifically induced by anoxia and chilling in E. phyllopogon and E. crus-pavonis. In both species HXK exhibited an optimum pH between 8.5 and 9.0, but the range was extended to pH 7.0 in air-grown E. phyllopogon to 6.5 in N₂-grown E. phyllopogon. At physiologically relevant pHs (6.8 and 7.3, N₂ and O₂ conditions, respectively), N₂-grown seedlings retained greater HXK activity at the lower pH. The pH response suggests that in N₂-grown seedlings HXK can function in a more acidic environment and that a specific isozyme may be important for regulating glycolytic activity during anaerobic metabolism in E. phyllopogon.

	INTRODUCTION

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HXKs (EC 2.7.1.1) are ubiquitous, constitutive enzymes found in all organisms and have been localized within the cytosol, mitochondria, and plastids of higher plants (Miernyk and Dennis, 1983; Schnarrenberger, 1990; Galina et al., 1995). The enzymes catalyze the phosphorylation of hexose sugars, typically Glc and Fru, that are produced during catabolism of Suc. Phosphorylation of hexoses by HXKs is essentially an irreversible metabolic step regulating the entry of Glc into glycolysis. Several studies have shown that plants typically contain an array of three to five HXKs that differ in their chromatographic and kinetic properties (Kruger, 1990). The native molecular masses of HXKs vary considerably, from 38 kD in castor oil seeds (Miernyk and Dennis, 1983) to 118 kD in potato tubers (Renz et al., 1993). Even within the same species the apparent native molecular masses of the HXKs are variable: 39 and 59 kD in maize kernels (Doehlert, 1989); 66, 102, 105, and 118 kD in potato tubers (Renz et al., 1993); and 50 and 100 kD in wheat germ (Higgins and Easterby, 1974). In those cases in which the subunit molecular masses have been determined (i.e. wheat germ [Higgins and Easterby, 1974], pea [Copeland et al., 1978], and mammals [Colowick, 1973]), HXKs are monomeric and the smaller isozymes do not appear to be subunits of the larger isoforms. Only in yeast has the native form of HXK been reported to be a dimer (Schmidt and Colowick, 1973).

The physiological significance of multiple forms of HXKs is not clear. Some HXKs are specific for Glc (i.e. GLKs) or Fru (i.e. FKs), although other forms can utilize either sugar as a substrate (Kruger, 1990). Part of the variation among HXK isozymes may reflect this specificity for a sugar substrate. HXKs generally utilize ATP as the nucleoside substrate, and Suc metabolism proceeds through the action of invertase and HXKs. However, some FKs utilize UTP as the phosphoryl donor (Huber and Akazawa, 1986; Baysdorfer et al., 1989; Xu et al., 1989; Schnarrenberger, 1990). Mobilization of Suc occurs through the concerted action of Susy, UDP-Glc pyrophosphorylase, and FK via a uridine-nucleotide- and PPi-dependent pathway (Huber and Akazawa, 1986; Xu et al., 1989). Thus, the relative abundance of FKs and GLKs correlates with the pathway of Suc catabolism that operates in a particular tissue.

Although control of glycolytic flux is usually shared among all enzymes of the pathway (Kaczer and Burns, 1973; Rapoport et al., 1974), stress conditions may permit certain enzymes to exert a greater proportion of control. HXKs are reported to regulate glycolytic flux in human erythrocytes (Rapoport et al., 1974), perfused rat hearts (Kashiway et al., 1994), and pancreatic islet beta cells (German, 1993) during anaerobic stress, and in the red blood cells of rabbits during exposure to oxygen-free radicals (Stocchi et al., 1994). In potato tubers HXKs are subject to product inhibition by ADP, leading to the proposal that HXKs control glycolytic flux during anoxia in higher plants (Renz and Stitt, 1993). Under conditions that decrease the ATP-to-ADP ratio, such as anaerobic stress, ADP would inhibit HXK activity. Presumably, the reduction in HXK activity prevents depletion of cytosolic Pi so that sufficient Pi is present for ATP synthesis.

In maize root tips (Bouny and Saglio, 1996) and tomato roots (Germain et al., 1997), HXK activity is stimulated by hypoxia but does not increase during anoxia, whether or not the root tips are hypoxically pretreated to enhance their survival. Native-PAGE activity gels revealed one HXK, one GLK, and two FK isozymes in maize. No new isoforms were detected, although the resolution obtained with this technique is insufficient to definitively exclude this possibility. The low HXK activity, however, accounts for most of the reduction in glycolytic flux in anaerobically treated maize root tips, and both HXK induction and glycolytic flux recover when the stress is removed, suggesting that HXK regulates glycolytic activity (Bouny and Saglio, 1996).

In the present study we examined HXK activity in response to several abiotic stresses, characterized its enzymatic activity under anaerobic conditions, and determined the influence of pH on its activity in two barnyard grass species of Echinochloa. The Echinochloa genus, with several flood-tolerant and -intolerant species, has been well characterized with regard to its metabolic adaptations to anoxia and is an excellent model system to investigate differences in the environmental regulation of gene expression and metabolism. The tolerant species Echinochloa phyllopogon has been extensively characterized because of its ability to germinate and grow under anoxia, whereas the intolerant species Echinochloa crus-pavonis has been studied for its inability to germinate under anoxia (Kennedy et al., 1992). In E. phyllopogon, anaerobic germination and growth occur solely by emergence and elongation of the coleoptile; the radicle does not emerge from the seed in the absence of O₂ (VanderZee and Kennedy, 1981). Unlike the flood-intolerant species, E. phyllopogon maintains an active carbohydrate and lipid metabolism high ATP levels, and energy charge during long exposures to anaerobic conditions (Kennedy et al., 1987, 1992; Fox et al., 1988). This coordinated metabolic activity by the tolerant species is a product of both differential gene expression and posttranslational regulation of metabolic activity during anoxia. HXK is postulated to serve a dual role in this regard by regulating entry of Glc into glycolysis and as part of the mechanism regulating the expression of sugar-responsive genes (Koch, 1996; Lang et al., 1997).

	MATERIALS AND METHODS

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Plant Materials

HXK Assay

	RESULTS

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Anaerobic stress stimulated HXK activity in both shoots (Fig. 1A) and roots (Fig. 1B) of the flood-tolerant species E. phyllopogon, whereas chilling stress elevated HXK activity only in roots. Heat shock and salt stress inhibited HXK in both shoots and roots. In contrast, in the flood-intolerant species E. crus-pavonis, shoot HXK activity was unaffected or inhibited by the four stresses (Fig. 1D), but in roots it was stimulated to varying degrees by each of the stresses (Fig. 1E). In seeds of both species (Fig. 1, C and F), abiotic stresses generally inhibited HXK activity, except for chilling stress in E. crus-pavonis, which did not affect its activity.

View larger version (50K): [in this window] [in a new window]   Figure 1. Relative hexokinase (HK) activity in shoots (A and D), roots (B and E), and seeds (C and F) of E. phyllopogon (A-C) and E. crus-pavonis (D-F) in response to abiotic stresses. Seedlings were grown aerobically for 5 d and harvested immediately (Control 1), continued in air for 2 d (Control 2), or subjected to the indicated stresses. Activities are expressed relative to Control 1. Absolute activities of the Control 1 plants were 217, 87, and 332 nmol min1 g1 fresh weight for shoots, roots, and seeds, respectively, of E. phyllopogon, and 106, 21, and 88 nmol min1 g1 fresh weight for shoots, roots, and seeds, respectively, of E. crus-pavonis. Values are means ± SD of three replicates.

The anaerobic stimulation of HXK activity in shoots of E. phyllopogon occurred within 3 h and to a higher level (4-fold) than in roots, in which the response was apparent only after 9 h and was ultimately stimulated only 2.5-fold after 24 h of anoxia (Fig. 2, A and B). In seeds (Fig. 2C), inhibition of HXK activity occurred after 9 h of anoxia and continued for the duration of the experiment.

View larger version (48K): [in this window] [in a new window]   Figure 2. HXK activity in shoots (A and D), roots (B and E), and seeds (C and F) of E. phyllopogon (A-C) and E. crus-pavonis (D-F) during anaerobic stress. Seedlings were grown for 5 d in air and HXK activities were determined during the subsequent 24-h period in seedlings that were maintained in air () or transferred into an anaerobic chamber (). Values are means ± SD of three replicates. gfw, Grams fresh weight.

Shoots of E. crus-pavonis exhibited a 2-fold stimulation of HXK activity by 18 h of anoxia, but activity declined to nearly initial levels after 24 h in N₂ (Fig. 2D). In roots, however, HXK activity was elevated within 3 h and the activity was stimulated 8-fold by 18 h in N₂ (Fig. 2E). Anoxia did not affect HXK activity in seeds (Fig. 2F). The comparatively low and transient nature of HXK activity in the shoots may be one factor that limits the ability of E. crus-pavonis to withstand flooding in contrast to E. phyllopogon.

Having identified that HXK activity was stimulated to a larger extent in shoots of E. phyllopogon and roots of E. crus-pavonis, we proceeded to characterize the enzyme in these respective organs. To assess how changes in cytoplasmic pH affect HXK activity, crude extracts from shoots of E. phyllopogon and roots of E. crus-pavonis (grown in air or transferred to N₂ for 2 d) were assayed for activity at several pHs (Fig. 3). In E. phyllopogon HXK from shoots of aerobically grown seedlings exhibited a broad pH optima peak between 8.0 and 8.5, whereas those subjected to anoxia exhibited significantly higher activities, with a sharp pH optimum at approximately 8.75 and a distinct shoulder below 7.5 (Fig. 3A). HXK from both aerobically and anaerobically grown roots of E. crus-pavonis, however, exhibited a broad curve, "peaking" at pH 9.0 with only a slight shoulder below 7.5 (Fig. 3B).

View larger version (25K): [in this window] [in a new window]   Figure 3. HXK activity as a function of pH in E. phyllopogon (A) and E. crus-pavonis (B). Crude protein extracts were prepared from shoots of E. phyllopogon and roots of E. crus-pavonis grown in air (, ) or transferred to N2 for 2 d (, ) and assayed for HXK activity at the indicated pH using Hepes-KOH (, ) or Tris-HCl (, ) buffer systems. Values are means ± SD of three replicates. gfw, Grams fresh weight.

In vivo measurements of cytoplasmic pH in maize root tips have demonstrated that the pH rapidly declines from approximately 7.4 in air to approximately 6.8 under hypoxic conditions (Roberts et al., 1984). Although differences in HXK activity between aerobically and anaerobically grown seedlings as a function of pH were more pronounced at higher pHs (Fig. 3), we more closely examined the effect of pH on HXK activity within a physiologically relevant range for the two species of Echinochloa. In addition to extracting and assaying HXK near its pH optimum (8.0), the enzyme was extracted from shoots of E. phyllopogon and its activity was determined at pH 7.3 and 6.8 to assess its activity at the approximate pH of the cytoplasm during aerobic and anaerobic conditions, respectively (Fig. 4, A-C). At a pH of less than optimum (i.e. <8.75), HXK activity was significantly reduced.

View larger version (27K): [in this window] [in a new window]   Figure 4. HXK activity in shoots of E. phyllopogon (A-C) and E. crus-pavonis (D-F) as a function of extraction and assay buffer pH. Five-day-old seedlings grown aerobically () or anaerobically () were extracted at pH 8.0, 7.3, or 6.8 and assayed at pH 8.0 (A and D), 7.3 (B and E), or 6.8 (C and F). The pH values were selected for being near optimum for HXK activity and for physiological relevance. Values are means ± SD of three replicates.

It is interesting that the slopes of the activity- versus extraction-pH curves of shoots from anaerobically grown seedlings (143, 104, and 76 at assay pH 8.0, 7.3, and 6.8, respectively), were 3- to 8-fold greater than the corresponding slopes of aerobically grown seedlings (18, 12, and 22 at assay pH 8.0, 7.3, and 6.8, respectively; Fig. 4, A-C). The different responses of HXK activity- versus extraction-pH curves in shoots of aerobically and anaerobically grown seedlings demonstrate that HXK activity in shoots of anaerobically grown seedlings of E. phyllopogon was more responsive to subtle changes in pH than in those grown in air, suggesting that different isozymes may predominate under these two growth conditions. In similar experiments with roots of 5-d-old seedlings of E. crus-pavonis, the slopes of the activity- versus extraction-pH curves in roots of anaerobically grown seedlings (92, 87 and 52 at assay pH 8.0, 7.3, and 6.8, respectively) were less than 2-fold greater than the corresponding slopes of aerobically grown seedlings (41, 51, and 42, respectively; Fig. 4, D-F).

	DISCUSSION

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Stimulation of HXK Activity by Abiotic Stress

In maize, however, inhibition of HXK activity, low levels of hexose phosphates (Bouny and Saglio, 1996), and induction of Susy by anoxia (Talercio and Chourey, 1989) led to the conclusion that metabolism of Suc occurs predominately via the Susy pathway. Experiments with a Susy double mutant confirmed that aerobic growth is not dependent on Susy activity but is required for anaerobic growth in maize (Ricard et al., 1998). Induction of Susy by low O₂ conditions in tomato (Germain et al., 1997, wheat (Marana et al., 1990), and rice (Ricard et al., 1991) suggests that anaerobic metabolism of Suc via Susy is a general plant response. In the present study it is reasonable to infer from the transient induction of HXK activity (Fig. 2) that E. crus-pavonis responds to anoxia in a manner analogous to maize. In contrast, E. phyllopogon appears to retain the hexose-phosphorylating pathway; HXK activity is strongly induced (Fig. 2) and increased incorporation of ¹⁴C into sugar-monophosphates from Suc occurs during anoxia (Rumpho and Kennedy, 1983).

The appearance and abundance of specific HXKs have been found to depend on the organ and developmental state of the tissue in potato. FK3 is present in leaves, whereas FK1 and FK2 are the major forms in growing tubers (Renz et al., 1993). The high levels of FKs in tubers correspond with Suc utilization via Susy and UDP-Glc pyrophosphorylase. In stored tubers elevated levels of HXK1 and HXK2 activities (Renz et al., 1993) correspond to a decline in Suc utilization via Susy (Geigenberger and Stitt, 1993) and elevation of invertase levels (Richardson et al., 1990). In sprouting tubers HXK1 is the predominant form of HXK, possibly because starch is the major carbohydrate source (Renz et al., 1993). Thus, changes in the specific forms of FKs and GLKs appear to regulate carbon flow through Fru and Glc pools at different stages of development.

Localization of HXKs may be important for directing Glc to specific subcellular compartments at critical times during development to supply carbon skeletons for various anabolic pathways. For instance, high levels of HXK activity in plastids of castor oil seed endosperm may be necessary to provide substrates for fatty acid biosynthesis (Miernyk and Dennis, 1983). HXKs have been reported on the outer membranes of mitochondria of spinach leaves (Baldus et al., 1981) and avocado (Copeland and Tanner, 1988), the outer membranes of spinach leaf chloroplasts (Stitt et al., 1978), in spinach chloroplasts (Schnarrenberger, 1990), and in the plastids and mitochondria of castor oil seed endosperm (Miernyk and Dennis, 1983).

HXK-Regulated Gene Expression

HXK has also been shown to repress the expression of mannitol dehydrogenase in celery cell-suspension cultures (Prata et al., 1997) and -amylase rice embryos (Yamaguchi et al., 1997) when sugars were present in the culture media. In both cases, the repression of gene expression was relieved during sugar starvation. The use of mannoheptulose, a competitive inhibitor of HXK, and 2-deoxyglucose, a sugar analog that is phosphorylated by HXK but not metabolized further, mimics the effects of sugar starvation, indicating that HXK regulates the expression of these two genes.

An analogous mechanism may be important for signaling anaerobic stress and regulating the associated changes in gene expression in Echinochloa spp. In addition to changes in sugar status and metabolic flux (Fox et al., 1994), anaerobiosis influences the overall adenylate energy charge of the seedlings and the synthesis of adenylates (Kennedy et al., 1987). Since ATP is a substrate for HXK, fluctuations in ATP-to-ADP ratios would also be expected to modulate HXK activity. Renz and Stitt (1993) have shown that ATP-to-ADP ratios regulate HXK activity in potato. Under anaerobic conditions availability of ATP may be an additional determinant of HXK activity and its associated feedback on gene expression.

Cytoplasmic acidification is an early consequence of anaerobiosis and has pleiotropic effects on cellular metabolism (Roberts et al., 1984). One effect is to modulate HXK activity. Results of in vitro experiments with crude extracts suggest that shoots of anaerobically grown E. phyllopogon seedlings retain partial HXK activity at pH 6.8 but aerobically grown seedlings do not (Fig. 3). An HXK with an acidic pH optimum would maintain carbohydrate entry into glycolysis, fatty acid biosynthesis, and other metabolic pathways during anaerobiosis. Since the rate of hexose phosphorylation is more important than the concentration of hexose phosphates in signaling the sugar status of the cell to the nucleus, the combined effects of sugar supply, ATP concentration, and cytoplasmic pH in modulating HXK activity may permit one HXK isozyme in Echinochloa spp. to serve as a sensor of the aeration state of the cell.

Whereas several HXK genes have been cloned from yeast and animals, only two HXKs have been cloned and characterized in plants. Smith et al. (1993) cloned an FK gene from potato and found the sequence homology to yeast and animal HXKs to be low. A HXK has also been cloned from an Arabidopsis cDNA library by functional complementation of a yeast triple mutant (Dai et al., 1995). This gene encodes a 47-kD protein that preferentially utilizes Glc over Fru. Jang and Sheen (1994) cloned and are characterizing two additional plant HXK genes. Isolation and characterization of additional HXK genes in plants will be important for analyzing the expression of specific isozymes and their significance during Glc metabolism in relation to environmental stress and regulation of homeostasis in plant cells. Studies in yeast indicate that GLKs do not have the same sugar-sensing capabilities as HXKs (Rose et al., 1991). Variability among HXKs, GLKs, and FKs in plants may be one level of complexity in regulating expression of sugar-responsive genes.

	Conclusion

In Echinochloa spp. HXK is not a general stress protein but is specifically induced by anoxia and chilling in an organ-dependent manner. Furthermore, the two Echinochloa spp. exhibit different patterns of HXK activity that correlate with their ability to withstand flooding. The flood-intolerant E. crus-pavonis exhibits a weak, transient elevation of HXK activity in shoots during anaerobiosis, whereas a strong, persistent stimulation occurs in the shoots of the flood-tolerant species. The decline in HXK activity in E. crus-pavonis is consistent with results from other species (e.g. maize, tomato, wheat, and rice), in which metabolism of Suc occurs primarily via Susy rather than by invertase under low-O₂ conditions. In contrast, E. phyllopogon increases its capacity to phosphorylate hexoses arising from Suc hydrolysis via invertase. The invertase-HXK pathway for Suc catabolism is not an absolute requirement for flood tolerance, however, because rice induces the Susy pathway under anoxia. Instead, E. phyllopogon has adopted an alternative strategy for metabolizing carbohydrates during anaerobic stress. The occurrence of this adaptation in other species and the expression of HXK at the isozyme and molecular levels need to be explored further in the context of improving flood tolerance in commercially important crop plants.

	FOOTNOTES

   Received May 29, 1998; accepted September 17, 1998.

	ABBREVIATIONS

Abbreviations: FK, fructokinase. GLK, glucokinase. HXK, hexokinase. Susy, Suc synthase.

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