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Review: abiotic stress sensing and GABA response in plants.


Abiotic plant stresses are common and can have devastating effects on plants. To combat these stresses, plants have developed numerous defenses. Mechanisms of signal perception and subsequent responses to stress are complex and consist of cascades of multiple reactions. These signaling cascades and metabolic responses are of great interest to plant biologists. A better understanding of plant stress responses can lead to improved plant breeding strategies (or transgenics) resulting in better plant performance and increased crop yields under disadvantageous conditions. In this review, changes in cellular cytoplasmic membranes, cytoplasmic calcium, and plant accumulation of gamma-aminobutyric acid (GABA) are discussed in response to abiotic plant stress. GABA, a mammalian neurotransmitter inhibitor, is a metabolite of glutamate that accumulates within the cytoplasm in response to stress. GABA is synthesized in a reaction catalyzed by the calmodulin modulated enzyme glutamate decarboxylase (GAD) that is activated, in part, by stress-induced increases in [Ca.sup.2+.sub.cyt] and has an optimum pH similar to those occurring in response to stress conditions. Accumulations of GABA are known to be large and rapid. However, studies have shown that GABA is then catabolized within the mitochondria of plant cells. Many studies on this phenomenon have been performed, but large areas of stress-induced accumulation of GABA are still unexplored, and the definitive role of GABA in plants has yet to be elucidated.


Abiotic plant stresses cause many major changes in metabolic pathways, plant growth, and productivity and yield (Sabehat et al., 1998; Kaplan et al., 2004; Sakamoto et al., 2004). Some abiotic plant stresses include, but are not limited to: osmotic (water) stress, salt stress, chilling stress, freezing stress, mechanical stress, anaerobic stress, and heat stress. Biological and environmental stresses are major limiting factors to productivity in agricultural settings. These stresses, singly or in combination, are likely to be enhanced due to impending global warming forecasts. Producers lose millions of dollars yearly to these stresses that occur on a daily basis. Studying plants subjected to stressful conditions can help better predict how plants survive inclement environments. A plant stress is generally defined as any external factor that exerts a negative impact upon the plant (Taiz and Zeiger, 1998). Plants have evolved a myriad of responses to alleviate stressful conditions. It has even been suggested that every plant has the encoded capability located within its genome to tolerate stresses (Bohnert et al., 1995). A few plant responses to stress include: osmoregulation (Allard et al., 1998; Kerespi et al., 1998; Kaplan et al., 2004), heat shock protein production (Howarth and Ougham, 1993; Scharf et al., 1998), alterations of metabolic pathways (Knight et al., 1998; van der Luit et al., 1999; Sakamoto et al., 2004), modifications of plant membrane characters (Murata and Los, 1997; Logue et al., 1998), and decreased efficiency of photosynthesis (Loggini et al., 1999; Allakhverdiev et al., 2000). The purpose of this literature review is to familiarize the reader with a plant's: 1) perception of stress, 2) signal transduction, and 3) subsequent responses to stressful conditions.


Plant Membranes and the Recognition of Environmental Stresses

The nature of stress signaling mechanisms has classically been thought of as a cascade effect where the initial signal is perceived by a membrane-bound protein (Horvath et al., 1998). This major triggering protein then somehow stimulates production of other signaling molecules that can turn on/off genes that enable the plant to better cope with the deleterious effects of the stress. This cascade-like effect is an efficient way to quickly initiate many changes within the cell.

One specific example of how this might work was proposed by Murata and Los (1997). They suggested that phase transitions occur in microdomains of the cell membrane upon a shift in temperature. The putative sensor protein would detect such a change within the membrane and could then undergo conformational changes, phosphorylation, or dephosphorylation as an event to begin transduction of the abiotic stress being present.

Another theory proposed in E. coli, as discussed by Van Bogelen and Neidhardt (1990) suggests ribosomal sensing of stresses by virtue of the increased translation of stress proteins. These responses were induced by antibiotic-mimicked heat and chilling stress in E. coli. Whatever the active mechanism is, every plant studied has the ability to sense changes in its environment and can make some adjustments accordingly.

With only the cell wall separating them, biological membranes may act to transmit information from the environment to the plant cell (Horvath et al., 1998). Therefore, it is logical that the primary sensory mechanism for the plant would originate from a stimulus being detected by the membrane. Membranes are composed of a lipid bi-layer with integrated proteins found throughout (Quinn et al., 1989). This lipid bi-layer is a dynamic "fluid" system, and its form can be readily changed (Ohlrogge and Browse, 1995).

In plants, fatty acid synthesis and lipid assembly begin in the chloroplast or endoplasmic reticulum (ER) (Miquel and Browse, 1998). The mechanism of transfer for these fatty acids in order to assemble lipids (and the subsequent integration of lipids into membranes) is unknown (Miquel and Browse, 1998). The overall pathway for fatty acid synthesis in plants is similar to that in other organisms; however, in plants the reactions are all catalyzed by individual proteins rather than a multifunctional peptide and are highly compartmentalized (Somerville and Browse, 1991). The initial saturation level of the fatty acids used to make lipids is controlled by substrate-specific fatty acid desaturases (FAD) found in the cytoplasm (Murata and Los, 1997).

The overall saturation of fatty acids within plant membranes can vary greatly from species to species. It is a crucial factor for survival, and is even specific for the different membranes within the plant (Ohlrogge and Browse, 1995). For example, photosynthetic (thylakoid) membranes of plants are generally more unsaturated than vacuolar, mitochondrial, or other cellular membranes (Hugly et al., 1989).

The importance of the saturation of plant membranes lies in the role it plays in maintaining a proper membrane integrity under adverse conditions. Because of the physical properties of fatty acids, even small differences in the degree of saturation of membranes can contribute largely to the integrity of membranes (Hugly et al., 1989). This is, in part, because of the melting points of the fatty acids contributing to a phase shift from gel to liquid. Unsaturated fatty acids melt at lower temperatures than saturated fatty acids. Therefore, a more saturated membrane would, theoretically, be able to maintain the proper membrane fluidity at high temperatures better than a more unsaturated membrane (Nishida and Murata, 1996). Daniell et al. (1994) showed that cowpea cultures grown at 45[degrees]C had a much higher degree of membrane lipid saturation than those that were grown at 26[degrees]C. It has also been reported that membranes of plants which have been grown at higher temperatures (45[degrees]C) are much less fluid than those grown at lower temperatures (20[degrees]C) because of large amounts of saturated fatty acids found within their membranes (Raison et al., 1982). Much research has been performed correlating cold tolerance and the benefit of unsaturation of plant membranes (Moon et al., 1995; Nishida and Murata, 1996); however, the relatively little information available on the correlation of heat stress and the role of saturation within membranes is not as clear-cut.

Cytoplasmic Signaling Mechanisms to Abiotic Stress

As previously noted, plant response to stress is common. For example, it is well known that plants alter concentrations of ions and solutes in response to osmotic stress. These ions and solutes can have drastic effects on cytoplasmic pH and the signaling mechanisms of the plant. Cytoplasmic calcium levels have also been known to increase in response to environmental signals including: heat stress (Gong et al., 1998; Locy et al., 2000), chilling stress (Knight et al., 1991; Cholewa et al., 1997), osmotic stress (Knight et al., 1997), salt stress, (Kalaji and Pietkiewicz, 1993; Pardo et al., 1998) and mechanical stress (Knight et al., 1991). Cytoplasmic calcium has also been implicated as acting as a messenger (Ling et al., 1994; Carratu, et al., 1996; Cholewa et al., 1997; Gong et al., 1998). With calcium's exact role in response to environmental stimuli signaling pathways still being examined (Arazi et al., 1995; Webb et al., 1996; Knight et al., 1998; Trewavas and Malho, 1998; Romeis et al., 2000), it becomes a crucial focal point in understanding how plants function under less than ideal conditions.

One method by which calcium acts as a signal is through its binding to specific proteins. One such example of this regulatory role is calcium's binding of calmodulin. Once bound with calcium, calmodulin then undergoes a conformational change that leads to its activation and subsequent binding of target proteins (Roberts and Harmon, 1992). This binding of proteins can lead to the activation of certain sets of enzymes and proteins (Roberts and Harmon, 1992).

However, very few plant proteins are known to be modulated by calmodulin. The ones that are known include: an NAD kinase (Anderson and Cormier, 1978), a [Ca.sup.2+] ATPase (Briskin, 1990), a nuclear nucleoside triphosphatase (Matsumoto et al., 1984), a vacuolar ion channel (Bethke and Jones, 1994), a root-expressed glutamate decarboxylase (GAD) enzyme (Ling et al., 1994), and a shoot-expressed GAD enzyme (Zik et al., 1998). Calcium/calmodulin related events will be discussed in greater detail in regard to 4-aminobutyric acid (GABA) accumulation later in this discussion.

A second group of proteins that are activated by calcium are calcium dependent protein kinases (CDPK). Roberts and Harmon (1992) suggested that these proteins contain a calcium binding domain and a kinase domain which could detect changes in calcium levels and translate these changes into the regulation of protein kinase activity. Specifically, CDPK kinase activity has been found to occur in response to osmotic and metabolic stress (Takahashi et al., 1997; Iwata et al., 1998), but strong evidence of its exact role has been elusive. Induction of mRNA has also been found (Tahtiharju et al., 1997), but only recently has clear evidence shown that CDPKs participate in a defense-related signaling mechanism. Romeis et al. (2000) discovered a 68-70 kD CDPK in tomato which was activated after addition of an elicitor and suggested it was involved in plant defense. Much research into CDPKs continues, with exact roles still being investigated.

A much less well-known and understood group of calcium-activated proteins are calcineurin B-like proteins. Found in Arabidopsis, these small calcineurin B-like proteins (AtCBL) have a strong similarity to the calcineurin B subunit and neuronal calcium sensor from animal systems (Kudla et al., 1999; Shi et al., 1999). Possibilities as a player in plant stress responses in signal transduction have been suggested due to upregulated genes in response to osmotic, cold, and mechanical stresses (Kudla et al., 1999).

Specific Stress Response Mechanisms

The saturation/desaturation of membranes is one response that some plants may employ to alleviate environmental stresses (Vigh et al., 1998). As mentioned earlier, a common response to abiotic stresses is the accumulation of solutes. It is well known that plants can accumulate metabolites such as polyols, sucrose, nitrogen-containing compounds (including amino acids), and oligosaccharides (Bohnert et al., 1995). The alterations of biochemical pathways leading to the production of these solutes result in shifts of carbon and nitrogen stores. These shifts can be vital for the survival of a plant undergoing stress.

A few specific examples of solute accumulation in response to abiotic stresses include: accumulation of carbohydrates and glycine betaine in response to chilling stress (Kishitani et al., 1994; Gusta et al., 1996), betaine accumulation in response to freezing stress (Allard et al., 1998), polyol and quaternary ammonium compound accumulation in response to salt stress (Hanson et al., 1994; Bohnert et al., 1995), simple sugars in response to water stress (Mullet and Whitsitt, 1996), and accumulation of amino acids in response to heat, salinity, or osmotic stress (Mayer et al., 1990; Ashraf and Harris, 2004).

The synthesis of some of these solutes appears to have a function which can be easily explained, whereas some pathways (or a particular solute's role) have yet to be explained. The classic example of solute accumulation is proline accumulation in response to water stress. It is known that the accumulation of proline, and solutes in general, will result in a lowering of the water potential within plant cells. This lowering of the water potential, commonly referred to as osmotic adjustment, enables the plant to either take up water from the soil medium or to more efficiently hold on to the water it has already acquired.

Another classic response to stress is the production of heat shock proteins (HSP). Heat shock proteins are produced in all organisms that have been studied and are generally synthesized when organisms are placed at a growth temperature that is 5-10[degrees]C above their normal growth temperature (Howarth and Ougham, 1993). The functions of HSPs are known to include: protein transport, folding of proteins, chaperoning, and providing proteins resistance to denaturing under extreme conditions.

Heat shock proteins are synthesized from newly transcribed mRNA, and their production follows a large reduction of the total proteins being synthesized (Sabehat et al., 1998). Heat shock proteins are known to be synthesized from exposure to water stress, chilling stress, salt stress, heat stress (Grover et al., 1999), anaerobic stress, and heavy metal stress (Sabehat et al., 1998). The synthesis of HSPs, elicited from heat stress, is believed to allow a plant to acclimate to higher temperatures and resume normal growth under conditions that may not be favorable for plant growth (Howarth and Ougham, 1993; Viswanathan and Khanna-Chopra, 1996). Although this phenomenon is not fully understood, it is hypothesized that the accumulation of HSPs in response to a stress other than heat stress also benefits plants by protecting the plant from damage or helping to repair the damage caused by this stress (Sabehat et al., 1998).

Another class of stress-induced proteins is a group known as late embryogenesis abundant (lea) proteins. These genes were first identified as genes that were expressed during maturation and desiccation phases of seed development (Baker et al., 1988). Since then, six classes have been discovered (Dure, 1993) and have been found to be expressed in vegetative tissues during water stress, salt, and chilling stresses (Bray, 1993). Their functions, based on amino acid sequences, have been proposed to include: renaturation of unfolded proteins, protection of proteins from denaturing, protection of membranes, and sequestration of ions (Bray, 1993).

As previously noted, alterations in photosynthetic machinery (which is known to be very heat labile) or physical properties (such as membrane composition) can play an important role in stress tolerance. The photosynthetic machinery of a plant is very sensitive to stressful conditions, becoming less effective or completely shutting down in response to stress. This has been well documented for most stresses, including: osmotic stress (Mullet and Whitsitt, 1996; Allakhverdiev et al., 2000), salt stress (Kalaji and Pietkiewicz, 1993; Delfine et al., 1998; Delfine et al., 1999), chilling stress (Moon et al., 1995; Schneider et al., 1995; Janda, 1998), and heat stress (Chauhan and Senboku, 1996; Srinivasan et al., 1996; Jagtap et al., 1998; Talwar et al., 1999). Plants normally receive light energy and then have the challenge of figuring out what to do with the energy they have captured. Because stresses, particularly heat stress, can perturb membranes, plants may emit the light energy as fluorescence (Srinivasan et al., 1996).

Plants naturally re-emit a small amount of light energy as fluorescence. However, with the plant's photosynthetic machinery being sensitive to stressful conditions, a stress-induced increase in the amount of fluorescence being emitted is an expected response. This re-emission of light energy is believed to originate from the dissociation of the light-harvesting complex (LHC) in photosystem II (Hugly et al., 1989 and references therein). The stability of the LHC, therefore, becomes a critical issue in a plant's ability function in times of stress. Much of this stability lies within the composition of the thylakoid membrane where LHCs are found (Hugly et al., 1989; Kunst et al., 1989; Gombos et al., 1994;). Depending on the plant species in question, it has been reported that thylakoid membranes have been found to contain up to 85% unsaturated fatty acids (Hugly et al., 1989). It has also been reported that the tolerance to some stresses may reside in the particular ratios of saturated versus unsaturated fatty acids within specific plant membranes (Kunst et al., 1989; Somerville, 1995).

Plant membranes can be modified and reorganized when placed in stressful environments (Howarth and Ougham, 1993; Carratu et al., 1996). One modification plants can make lies in the saturation level of the fatty acids composing the membrane (Chen and Burris, 1991; Vigh et al., 1993; Murata and Los, 1997; Logue et al., 1998). Changes to these fatty acids are catalyzed by enzymes known as fatty acid desaturases. These desaturases are part of a biochemical pathway in which the saturation level of fatty acids and the protein:lipid ratio within the membranes of the plant are modified (Quinn et al., 1989). Many studies have been performed where membrane composition and the changes within a cell were analyzed in plants (Behl et al., 1996; Chauhan and Senboku, 1996; Srinivasan et al., 1996). Major differences, such as the overall lipid composition and ratios of saturated to unsaturated fatty acids, in plant lipid profiles of plants grown in different climates have also been shown (Cherry et al., 1985). Plant function under stress also has been studied in regard to maintenance of photosynthetic capabilities and membrane saturation (Hugly et al., 1989; Gombos et al., 1994; Behl et al., 1996). Screening genotypes based on their relative membrane thermostabilities and photosynthesis under stressful conditions is a useful technique and has been explored (Chauhan and Senboku, 1996).

Acclimation to Stresses and Cross-Tolerance To Stresses

An additional facet of the plant stress phenomenon is the acclimation of plants to abiotic stresses. Plants that have previously been subjected to a stress and have undergone some metabolic response will be more resistant to subsequent stresses. Gradual changes in environmental conditions (or a prior acclimation to a stress) induce tolerance to more extreme environments. This acclimation of plants to stress has been linked to the adaptation of signaling molecules and metabolism that respond to stresses (Bohnert et al., 1995; Knight et al., 1998). One specific example of metabolic changes for acclimation was reported in [Ca.sup.2+] signaling responses to environmental stress. Evidence suggests that cellular calcium responses encode a "memory" from previous stresses that allow the plant to better cope with subsequent abiotic stresses. This type of calcium response has been linked to the expression of genes that are protective in nature under stress conditions (Knight et al., 1998). Trewavas (1999) suggests this "memory" is evidence of an unexpected type of cellular intelligence.

Researchers have reported results of acclimation in almost every imaginable scenario. Specific examples include acclimation to chilling stress in cereals crops (Bridger et al., 1994), acclimation of Arabidopsis to chilling stress (Gilmour et al., 1988), adaptation of tomatoes to water stress (Rhodes et al., 1986), and adaptation of Arabidopsis to drought stress (Knight et al., 1998). As mentioned earlier, acclimation to some stresses has also been found to provide cross-tolerance to other stresses. A few specific examples of reported cross tolerance include: salt stress inducing chilling tolerance, mechanical stress inducing chilling tolerance, water stress conferring chilling resistance, and heat stress inducing endurance to heavy metal toxicity, salt stress, water stress, and reducing chilling injury (Sabehat et al., 1998 and references therein). Acclimation and cross-tolerance to stresses are complex physiological features. It has been hypothesized that there exist interconnections or signal crossover between pathways that lead to memory of and cross-tolerance to stresses (Bray, 1993; Sabehat et al., 1998). Isolation of non-acclimating mutants of Arabidopsis have been analyzed at the molecular level to help understand acclimation response in greater detail (Hughes and Dunn, 1996).


The Accumulation of GABA In Response to Plant Stresses

First discovered in plants (potato tubers) (Steward et al., 1949), 4-Aminobutyric (GABA) acid is a four carbon, non-protein amino acid that serves as a major neurotransmitter inhibitor in mammalian systems (Nathan et al., 1994). In plants, it is produced in the cytoplasm through the decarboxylation of glutamate (Cote' and Crutcher, 1991). GABA synthesis is known to occur in many higher plants and is commonly reported as increasing dramatically in response to conditions of environmental stress (Snedden and Fromm, 1999; Bouche and Fromm, 2004). These accumulations of GABA have been reported in many plants and in response to numerous stresses (Bouche and Fromm, 2004). Examples include: 1) rice subjected to anaerobic stress exhibited ten-fold increases in GABA within 24 hours (Aurisano et al., 1995); 2) in asparagus cells subjected to low temperatures, a 100 per cent increase of GABA was reported within 16 minutes (Cholewa et al., 1997); 3) cowpea subjected to heat stress exhibited a doubling of GABA within 15 minutes, quadrupling within an hour, and a 64-fold increase in 24 hours (Mayer et al., 1990); 4) soybean subjected to mechanical stress exhibited a 20-fold increase in GABA (Wallace et al., 1984); 5) soybeans subjected to osmotic stress had a GABA increase of 230% (Serraj et al., 1998).

Accumulations of GABA in response to heat stress are known to be large and rapid with increases up to 40-fold within five minutes (Wallace et al., 1984). These increases are known to occur concomitantly with decreases in glutamate, increases in cytoplasmic calcium ([Ca.sup.2+.sub.cyt]) levels, and decreases in cytoplasmic pH (Bown and Shelp, 1997). Also, studies showing localization of GABA accumulations within different plant tissues such as roots, shoots, germinating seedlings, cultured plant cells, tubers, flowers, fruits, and leaves have been described (Snedden and Fromm, 1999; Kinnersly and Turano, 2000). These findings, and the characterization of two distinct GAD isoforms which are expressed in separate plant tissues, lead to speculation about differences in GABA accumulation within multifarious plant tissues in response to various environmental stresses. Plant tissues of various ages have also been shown to exhibit varying GABA accumulations (Lahdesmaki, 1968). However, GABA accumulations across many environmental stresses, tissue differences, and age differences have not been thoroughly investigated in a single species. Also, comparison across several species of plant tissues has yet to be thoroughly investigated.

The reaction leading to GABA formation is catalyzed by the enzyme glutamate decarboxylase (GAD) (Bown and Shelp, 1997; Fait et al., 2005). GAD is widely distributed in nature, and is found in virtually all organisms including bacteria, fungi, plants, and animals (Satya Narayan and Nair, 1990). In a scenario common to all plants that have been investigated, GADs are modulated by [Ca.sup.2+.sub.cyt] through interaction with calmodulin. Plant GADs are completely inactive in the absence of calcium and calmodulin, and are fully active in the presence of such (Arazi et al., 1995; Baum et al., 1996). In-vitro studies have shown that in the presence of calcium and calmodulin the activity of GAD is greatly stimulated (Johnson et al., 1997).

Abiotic stresses typically lead to an increase in [Ca.sup.2+.sub.cyt] levels (Knight et al., 1998) and a lowering of cytosolic pH (Yoshida et al., 1999). GAD has an acidic pH optimum and is almost completely inactive at a neutral pH in the absence of [Ca.sup.2+.sub.cyt] and calmodulin. Two functional calcium/calmodulin modulated isoforms of GAD are known to exist in some plants (Zik et al., 1998; Snedden and Fromm, 1999). GAD1 is expressed in root tissues only, while GAD2 is expressed in roots, leaves, inflorescence stems, and flowers (Zik et al., 1998). GAD expression has been shown in tissues that accumulate GABA (Bown and Shelp, 1997).

The GABA Shunt

As previously mentioned, GABA is synthesized from a decarboxylation of glutamate in a reaction catalyzed by GAD (Reaction 1, Fig. 1). The synthesis of glutamate can occur through many different pathways in plants including catalysis via glutamine synthetase (Reaction 2, Fig. 1) (followed by subsequent deamination reactions) and glutamate synthase (Reaction 3, Fig. 1). An alternate route is via a transamination reaction of 2-ketoglutarate, from the TCA cycle, with alanine being converted to pyruvate (Reaction 4, Fig. 1). In this GABA shout, the glutamate is then decarboxylated by GAD in a reaction that consumes a cytosolic proton and yields GABA (this has been implicated as a mechanism by which the pH of the cytoplasm may be raised as a result of proton influx due to stress) (Carroll et al., 1994; Crawford et al., 1994). Via this pathway, and in response to abiotic stresses, GABA can be accumulated. Additionally, evidence has shown an increase in the carbon flux through the GABA shunt when glutamate availability was enhanced, suggesting that glutamate levels and availability also influence GAD activity (Scott-Taggart et al., 1999; Fait et al., 2005).

When GABA is catabolized, succinate semialdehyde and alanine are produced via a pyruvate-dependent transaminase (Reaction 5, Fig. 1). This alanine accumulation is thought to be an indicator of GABA degradation in tissues that are rapidly breaking down GABA. In plants, pyruvate-dependent GABA transaminase (Reaction 5, Fig. 1) is an enzyme that is specific to the mitochondria of plants (Breitkreuz and Shelp, 1995). In animal systems a different transaminase exists that utilizes 2-oxoglutarate instead of pyruvate (Kim and Churchich, 1989).

Succinate semialdehyde is toxic to plant cells; therefore, plants must also have an active succinate semialdehyde dehydrogenase (Reaction 6, Fig. 1) to quickly synthesize succinate in tissues that are degrading GABA. It is believed that at this point the succinate would enter the TCA cycle, thereby completing the GABA-shunt off of the TCA cycle.

Proposed Role of GABA Synthesis in Plant Cells

Essentialness for normal plant development, pH regulation, Kreb's cycle bypass, a deterrent for insect herbivory (Bloomquist, 2001; Fait et al., 2005), and its use as a signaling molecule (Coleman et al., 2001) have all been speculated as possible justifications for GABA synthesis (Snedden and Fromm, 1999). Recent analysis has shown that there is a possible requirement of GABA for normal plant development. Plants which had a truncated GAD gene, lacking the calmodulin binding domain, exhibited higher GABA levels, lower glutamate levels, less stem elongation, male sterility, incomplete maturation, and other aberrations (Baum et al., 1996). Coupled with studies showing that GABA promotes root branching and leaf formation (Locy et al., 2000), Snedden and Fromm (1999) go on to state that these findings indicate that GAD is important for glutamate metabolism and postulate a role for GABA in regulation of plant growth and development. This sentiment is echoed in the most recent analysis available as reported by Fait et al., (2005). Possibilities for GABA as a potential modulator of ion transport and amplifier of plant stress via signaling mechanisms have also been proposed (Kinnersly and Lin, 2000). GABA accumulation and the subsequent expulsion of major portions of GABA from cells have also led to speculation that GABA may function as an intercellular signaling molecule (Chung et al., 1992).


pH regulation has been proposed to result from GABA synthesis because of the GAD mediated reaction (L-Glu + [H.sup.+] -> GABA + C[O.sub.2]) which consumes an [H.sup.+] in the production of GABA. This raising of cytoplasmic pH has been confirmed by several researchers using techniques such as fluorescent pH probes (Crawford et al., 1994) and NMR spectroscopy (Carroll et al., 1994) to observe changes in cytosolic pH. In both examples, increases of GABA concentrations coincided with increases in pH.

The formation of GABA as a Kreb's cycle bypass has also been suggested. As discussed by Wiskich and Dry (1985), the possible mechanisms which may prevent succinate from entering the TCA under stressful conditions would be bypassed by the GABA shunt and likely allow succinate to enter the TCA cycle. Consistent with these findings, others have shown that flow through the GABA shunt is increased when mitochondrial electron transport is impeded (Popova et al., 1995). However, metabolism of glutamate through the GABA shunt is less energetically favorable, producing only one NADH instead of NADH and an ATP (Snedden and Fromm, 1999).

GABA has also been discussed as a phytotoxin with the possibility of reducing insect predation. It has been proven to exhibit a myriad of detrimental effects on the growth, development, and survival of insect larvae (Ramputh and Bown, 1996; Bloomquist, 2001). Theoretically, the defensive mechanism for the plant would lie in the rupturing of the cell's vacuole that would lead to a decrease in the cytoplasmic pH and increased calcium levels. This, in turn, would provide conditions suitable for GABA formation/accumulation. If ingested by an insect, GABA, with its neurotransmitter inhibitory properties (Nathan et al., 1994), could be absorbed by the hemolymph of the predator and cause temporary muscle paralysis (Ramputh and Bown, 1996).


While many questions remain unanswered, current knowledge about plant signaling and responses to abiotic stress is becoming clearer. Research involving membranes and cytoplasmic calcium along with "cell memory" of prior stresses is ripe for investigation. With world populations exploding and the need for higher yielding crops in less than ideal agricultural settings, the study of accumulating solutes, such as GABA, is needed for a better understanding of how these metabolic pathways function under stressful conditions. Plants exhibiting a high degree of stress tolerance and an increased yield in stressful environments are highly desirable in both breeding programs and transgenic research.


The authors would like to thank Dr. Narendra Singh and Dr. Joe Cherry for their critical readings of the initial versions of this manuscript. Also, warm thanks are extended to Ms. Lynn Libous-Bailey and Ms. Becky Fagan for their technical assistance throughout the course of preparation of this manuscript.


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T. Wayne Barger*

Alabama Department of Conservation and Natural Resources

State Lands Division, Natural Heritage Section

64 North Union Street

Montgomery, AL 36130


Robert D. Locy

Department of Biological Sciences

Life Sciences Building, Auburn University, AL 38649


* Author to whom correspondence should be directed.
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Title Annotation:gamma-aminobutyric acid
Author:Barger, T. Wayne; Locy, Robert D.
Publication:Journal of the Alabama Academy of Science
Geographic Code:1USA
Date:Jul 1, 2005
Next Article:Scoliosis screening: a review of a legislatively enacted program for the public schools of Alabama.

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