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How and why does tomato accumulate a large amount of GABA in the fruit?

Takayama M, Ezura H - Front Plant Sci (2015)

Bottom Line: The GABA levels in tomato fruits dramatically change during fruit development; the GABA levels increase from flowering to the mature green stage and then rapidly decrease during the ripening stage.Although GABA constitutes up to 50% of the free amino acids at the mature green stage, the molecular mechanism of GABA accumulation and the physiological function of GABA during tomato fruit development remain unclear.In this review, we summarize recent studies of GABA accumulation in tomato fruits and discuss the potential biological roles of GABA in tomato fruit development.

View Article: PubMed Central - PubMed

Affiliation: The Ezura Laboratory, Graduate School of Life and Environmental Sciences, University of Tsukuba , Tsukuba, Japan.

ABSTRACT
Gamma-aminobutyric acid (GABA) has received much attention as a health-promoting functional compound, and several GABA-enriched foods have been commercialized. In higher plants, GABA is primarily metabolized via a short pathway called the GABA shunt. The GABA shunt bypasses two steps (the oxidation of α-ketoglutarate to succinate) of the tricarboxylic acid (TCA) cycle via reactions catalyzed by three enzymes: glutamate decarboxylase, GABA transaminase, and succinic semialdehyde dehydrogenase. The GABA shunt plays a major role in primary carbon and nitrogen metabolism and is an integral part of the TCA cycle under stress and non-stress conditions. Tomato is one of the major crops that accumulate a relatively high level of GABA in its fruits. The GABA levels in tomato fruits dramatically change during fruit development; the GABA levels increase from flowering to the mature green stage and then rapidly decrease during the ripening stage. Although GABA constitutes up to 50% of the free amino acids at the mature green stage, the molecular mechanism of GABA accumulation and the physiological function of GABA during tomato fruit development remain unclear. In this review, we summarize recent studies of GABA accumulation in tomato fruits and discuss the potential biological roles of GABA in tomato fruit development.

No MeSH data available.


Related in: MedlinePlus

Potential roles of GABA in tomato fruits. (A) Fruits at the early developmental (green) stage when GABA is biosynthesized. (B) Fruits at the ripening stage when GABA is catabolized. MG, mature green; Br, breaker; GAD, glutamate decarboxylase; GABA-T (K), (α-ketoglutarate-dependent) GABA transaminase; SSADH, succinic semialdehyde dehydrogenase; Asp-AT, aspartate aminotransferase; Glu, glutamate; Asp, aspartate.
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Figure 2: Potential roles of GABA in tomato fruits. (A) Fruits at the early developmental (green) stage when GABA is biosynthesized. (B) Fruits at the ripening stage when GABA is catabolized. MG, mature green; Br, breaker; GAD, glutamate decarboxylase; GABA-T (K), (α-ketoglutarate-dependent) GABA transaminase; SSADH, succinic semialdehyde dehydrogenase; Asp-AT, aspartate aminotransferase; Glu, glutamate; Asp, aspartate.

Mentions: As described above, effects of impaired GABA metabolism on tomato plants have been increasingly reported. However, little is known about the function of GABA and the metabolism of this amino acid in fruits. Previous studies have suggested that GABA production during fruit development might contribute to the regulation of cellular pH (Rolin et al., 2000). During tomato fruit development, organic acids are continuously synthesized from unloaded sucrose, coupled with proton production. Overaccumulation of protons would cause an intracellular acidification, but the intracellular pH is probably regulated by ATP-driven proton pumps that extrude intracellular protons out of the cytoplasm, or by the proton-consuming decarboxylation of organic acids. Because GAD reaction requires protons, it might act as a sink for excess protons, preventing intracellular acidification (Rolin et al., 2000; Figure 2A). Moreover, the GAD reaction also promotes glutamate transport. In cherry tomatoes, glutamate is translocated through phloem sap and unloaded in fruits. The unloaded glutamate is subsequently transported symplastically or taken up through a proton symport mechanism across the membrane. In the latter transport mechanism, glutamate and protons are cotransported into the cytosol, thereby promoting cytoplasmic acidosis and the depolarization of the plasma membrane. Thus, continuous GABA accumulation during fruit development reflects the continuous GAD reaction, which potentially maintains glutamate transport through the consumption of excess protons (Snedden et al., 1992; Rolin et al., 2000). In addition, accumulated GABA in tomato fruits functions as an energy source, as 14C-labeled CO2 was discharged from fruits fed 14C-labeled GABA, indicating that GABA is utilized as a substrate for respiration (Yin et al., 2010; Figure 2B). Indeed, GABA shunt also functions as an alternative pathway for the production of succinate (the substrate for respiration) in tomato leaves when the enzyme of the TCA cycle is impaired (Studart-Guimarães et al., 2007). However, recent findings suggest that GABA metabolism has little effect on tomato fruit development under normal conditions, as the fruits of RNAi transgenic plants targeting the three SlGADs exhibited normal development, although the enzymatic activity of GAD and the GABA content in fruits were dramatically decreased (Takayama et al., 2015). Similarly, RNAi transgenic plants targeting SlGABA-T also produced normal fruits, although the GABA levels in red fruits were 6.8–9.2 times higher than those in wild-type controls (Koike et al., 2013). Therefore, GABA metabolism in tomato fruits might be involved in stress tolerance, similar to other plants. Another possibility is that GABA contributes to tomato seed dispersal through changes in the amino acid composition during fruit development. Because GABA functions in defense against pests and pathogens (Bown et al., 2006; Seifi et al., 2013), GABA accumulation in fruits at the early developmental stage might protect immature seeds (Figure 2A). However, the GABA levels in fruits rapidly decline during the ripening stage, when seeds have already matured. In parallel, the levels of glutamate and/or aspartate, which provide the “Umami taste,” dramatically increase during the ripening stage. These changes in the amino acid composition might attract insects and animals, resulting in successful seed dispersal (Figure 2B). The increases in glutamate and/or aspartate during fruit ripening have been well characterized in various cultivars (Rolin et al., 2000; Akihiro et al., 2008; Koike et al., 2013). The increase in glutamate probably reflects the increase in glutamate dehydrogenase (GDH) and GABA-TK activities during the ripening stage and the decreased consumption of glutamate through GAD, which is almost undetectable in ripe fruits (Sorrequieta et al., 2010; Ferraro et al., 2015; Figure 1). On the other hand, aspartate is synthesized from glutamate through aspartate aminotransferase (Figure 1). In GABA-rich cultivars, lower levels of glutamate and aspartate have been observed in ripening fruits (Akihiro et al., 2008), suggesting that GABA catabolism contributes to the accumulation of glutamate and glutamate-derived aspartate in ripening fruits. Furthermore, Snowden et al. (2015) recently identified a tonoplast-localized glutamate/aspartate/GABA exchanger (SlCAT9) in tomato fruits. As overexpression of the SlCAT9 gene strongly influences the accumulation of glutamate, aspartate, and GABA during tomato fruit development, it is suggested that the intracellular transport of amino acids between vacuole and cytosol is also a major determinant of their accumulation in ripening fruits (Snowden et al., 2015). Although the pathway involving the conversion from GABA to glutamate remains uncertain, GABA catabolism might play a crucial role in the determination of tomato fruit taste during ripening.


How and why does tomato accumulate a large amount of GABA in the fruit?

Takayama M, Ezura H - Front Plant Sci (2015)

Potential roles of GABA in tomato fruits. (A) Fruits at the early developmental (green) stage when GABA is biosynthesized. (B) Fruits at the ripening stage when GABA is catabolized. MG, mature green; Br, breaker; GAD, glutamate decarboxylase; GABA-T (K), (α-ketoglutarate-dependent) GABA transaminase; SSADH, succinic semialdehyde dehydrogenase; Asp-AT, aspartate aminotransferase; Glu, glutamate; Asp, aspartate.
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Figure 2: Potential roles of GABA in tomato fruits. (A) Fruits at the early developmental (green) stage when GABA is biosynthesized. (B) Fruits at the ripening stage when GABA is catabolized. MG, mature green; Br, breaker; GAD, glutamate decarboxylase; GABA-T (K), (α-ketoglutarate-dependent) GABA transaminase; SSADH, succinic semialdehyde dehydrogenase; Asp-AT, aspartate aminotransferase; Glu, glutamate; Asp, aspartate.
Mentions: As described above, effects of impaired GABA metabolism on tomato plants have been increasingly reported. However, little is known about the function of GABA and the metabolism of this amino acid in fruits. Previous studies have suggested that GABA production during fruit development might contribute to the regulation of cellular pH (Rolin et al., 2000). During tomato fruit development, organic acids are continuously synthesized from unloaded sucrose, coupled with proton production. Overaccumulation of protons would cause an intracellular acidification, but the intracellular pH is probably regulated by ATP-driven proton pumps that extrude intracellular protons out of the cytoplasm, or by the proton-consuming decarboxylation of organic acids. Because GAD reaction requires protons, it might act as a sink for excess protons, preventing intracellular acidification (Rolin et al., 2000; Figure 2A). Moreover, the GAD reaction also promotes glutamate transport. In cherry tomatoes, glutamate is translocated through phloem sap and unloaded in fruits. The unloaded glutamate is subsequently transported symplastically or taken up through a proton symport mechanism across the membrane. In the latter transport mechanism, glutamate and protons are cotransported into the cytosol, thereby promoting cytoplasmic acidosis and the depolarization of the plasma membrane. Thus, continuous GABA accumulation during fruit development reflects the continuous GAD reaction, which potentially maintains glutamate transport through the consumption of excess protons (Snedden et al., 1992; Rolin et al., 2000). In addition, accumulated GABA in tomato fruits functions as an energy source, as 14C-labeled CO2 was discharged from fruits fed 14C-labeled GABA, indicating that GABA is utilized as a substrate for respiration (Yin et al., 2010; Figure 2B). Indeed, GABA shunt also functions as an alternative pathway for the production of succinate (the substrate for respiration) in tomato leaves when the enzyme of the TCA cycle is impaired (Studart-Guimarães et al., 2007). However, recent findings suggest that GABA metabolism has little effect on tomato fruit development under normal conditions, as the fruits of RNAi transgenic plants targeting the three SlGADs exhibited normal development, although the enzymatic activity of GAD and the GABA content in fruits were dramatically decreased (Takayama et al., 2015). Similarly, RNAi transgenic plants targeting SlGABA-T also produced normal fruits, although the GABA levels in red fruits were 6.8–9.2 times higher than those in wild-type controls (Koike et al., 2013). Therefore, GABA metabolism in tomato fruits might be involved in stress tolerance, similar to other plants. Another possibility is that GABA contributes to tomato seed dispersal through changes in the amino acid composition during fruit development. Because GABA functions in defense against pests and pathogens (Bown et al., 2006; Seifi et al., 2013), GABA accumulation in fruits at the early developmental stage might protect immature seeds (Figure 2A). However, the GABA levels in fruits rapidly decline during the ripening stage, when seeds have already matured. In parallel, the levels of glutamate and/or aspartate, which provide the “Umami taste,” dramatically increase during the ripening stage. These changes in the amino acid composition might attract insects and animals, resulting in successful seed dispersal (Figure 2B). The increases in glutamate and/or aspartate during fruit ripening have been well characterized in various cultivars (Rolin et al., 2000; Akihiro et al., 2008; Koike et al., 2013). The increase in glutamate probably reflects the increase in glutamate dehydrogenase (GDH) and GABA-TK activities during the ripening stage and the decreased consumption of glutamate through GAD, which is almost undetectable in ripe fruits (Sorrequieta et al., 2010; Ferraro et al., 2015; Figure 1). On the other hand, aspartate is synthesized from glutamate through aspartate aminotransferase (Figure 1). In GABA-rich cultivars, lower levels of glutamate and aspartate have been observed in ripening fruits (Akihiro et al., 2008), suggesting that GABA catabolism contributes to the accumulation of glutamate and glutamate-derived aspartate in ripening fruits. Furthermore, Snowden et al. (2015) recently identified a tonoplast-localized glutamate/aspartate/GABA exchanger (SlCAT9) in tomato fruits. As overexpression of the SlCAT9 gene strongly influences the accumulation of glutamate, aspartate, and GABA during tomato fruit development, it is suggested that the intracellular transport of amino acids between vacuole and cytosol is also a major determinant of their accumulation in ripening fruits (Snowden et al., 2015). Although the pathway involving the conversion from GABA to glutamate remains uncertain, GABA catabolism might play a crucial role in the determination of tomato fruit taste during ripening.

Bottom Line: The GABA levels in tomato fruits dramatically change during fruit development; the GABA levels increase from flowering to the mature green stage and then rapidly decrease during the ripening stage.Although GABA constitutes up to 50% of the free amino acids at the mature green stage, the molecular mechanism of GABA accumulation and the physiological function of GABA during tomato fruit development remain unclear.In this review, we summarize recent studies of GABA accumulation in tomato fruits and discuss the potential biological roles of GABA in tomato fruit development.

View Article: PubMed Central - PubMed

Affiliation: The Ezura Laboratory, Graduate School of Life and Environmental Sciences, University of Tsukuba , Tsukuba, Japan.

ABSTRACT
Gamma-aminobutyric acid (GABA) has received much attention as a health-promoting functional compound, and several GABA-enriched foods have been commercialized. In higher plants, GABA is primarily metabolized via a short pathway called the GABA shunt. The GABA shunt bypasses two steps (the oxidation of α-ketoglutarate to succinate) of the tricarboxylic acid (TCA) cycle via reactions catalyzed by three enzymes: glutamate decarboxylase, GABA transaminase, and succinic semialdehyde dehydrogenase. The GABA shunt plays a major role in primary carbon and nitrogen metabolism and is an integral part of the TCA cycle under stress and non-stress conditions. Tomato is one of the major crops that accumulate a relatively high level of GABA in its fruits. The GABA levels in tomato fruits dramatically change during fruit development; the GABA levels increase from flowering to the mature green stage and then rapidly decrease during the ripening stage. Although GABA constitutes up to 50% of the free amino acids at the mature green stage, the molecular mechanism of GABA accumulation and the physiological function of GABA during tomato fruit development remain unclear. In this review, we summarize recent studies of GABA accumulation in tomato fruits and discuss the potential biological roles of GABA in tomato fruit development.

No MeSH data available.


Related in: MedlinePlus