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Yuan, D.; Wu, X.; Gong, B.; Huo, R.; Zhao, L.; Li, J.; Lü, G.; Gao, H. Transport of Exogenous GABA in Plants. Encyclopedia. Available online: https://encyclopedia.pub/entry/43187 (accessed on 18 May 2024).
Yuan D, Wu X, Gong B, Huo R, Zhao L, Li J, et al. Transport of Exogenous GABA in Plants. Encyclopedia. Available at: https://encyclopedia.pub/entry/43187. Accessed May 18, 2024.
Yuan, Ding, Xiaolei Wu, Binbin Gong, Ruixiao Huo, Liran Zhao, Jingrui Li, Guiyun Lü, Hongbo Gao. "Transport of Exogenous GABA in Plants" Encyclopedia, https://encyclopedia.pub/entry/43187 (accessed May 18, 2024).
Yuan, D., Wu, X., Gong, B., Huo, R., Zhao, L., Li, J., Lü, G., & Gao, H. (2023, April 18). Transport of Exogenous GABA in Plants. In Encyclopedia. https://encyclopedia.pub/entry/43187
Yuan, Ding, et al. "Transport of Exogenous GABA in Plants." Encyclopedia. Web. 18 April, 2023.
Transport of Exogenous GABA in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/metabo13030347

γ- Aminobutyric acid (GABA) is a ubiquitous four-carbon non-protein amino acid. In plants, GABA is found in different cell compartments and performs different metabolic functions. As a signalling molecule, GABA participates in the regulation of tolerance to various abiotic stresses.  GABA transporters were identified for the first time in 1999. Arabidopsis can grow efficiently on media in which GABA is the only nitrogen source, which shows that exogenous GABA can be taken up by plants and verifies the existence of GABA transporters. The transport of GABA in plants includes the transport of GABA between membranes, as well as into the cell membrane to various organelles. This process is affected by many transporters, such as aluminium activated malate transporters (ALMTs), GABA transporters (GATs), bidirectional amino acid transporters (BATs) and cationic amino acid transporters (CATs). These transporters are located on the cell membrane or organelle membrane and control the transport of GABA to the intracellular space and various organelles.

γ- aminobutyric acid distribution biosynthesis and catabolism

1. Transcell Membrane GABA Transporters

1.1. ALMT1

Aluminium-activated malic acid transporters (ALMTs) are bidirectional transmembrane anion transporters [1]. Twelve ALMT homologous genes have been found in plants [2]. In previous studies, this protein family was shown to mainly control the transmembrane transport of malate and anions in cells. In 2018, Ramesh et al. [1] discovered that GABA can be transported across the cell membrane at a high rate under the action of ALMT1 located on the cell membrane. ALMT1 has been found in Arabidopsis, wheat, rice, rape and other plant species, and the transport of TaALMT1 to GABA has mainly been studied in wheat. AtALMT1 and TaALMT1 are highly homologous [3], but there has been no experiment in Arabidopsis that clearly shows that AtALMT1 transports GABA. The mechanism by which ALMT1 transports GABA is also a research hotspot at present. The function of ALMT1 in transporting GABA is closely related to the activity of anion channels. A study of GABA and malate showed that anions can activate ALMT1 [4]. Thus, there is a potential difference inside and outside the membrane, which promotes the transport of GABA [5]. Bush et al. [6][7] found that the protons generated by H+-ATPase passing through the plasma membrane input amino acids into the cell, while Ramesh proposed that the increased activity of ALMT can avoid the inactivation of H+-ATPase at the extreme hyperpolarized membrane potential, which ensures the transport of GABA and provides necessary energy [1]. Under low pH conditions, aluminium ions (Al3+) can promote the efflux of GABA from wheat via TaALMT1. In the case of apoplast acidification, GABA can also influx through TaALMT1. These studies suggest that pH may be the factor influencing of GABA transport [1].
Many homologous genes of the ALMT family have also been cloned and identified, and related protein sequences have been studied. In the process of studying related transporters, it was also found that ALMT activity decreased with increasing GABA content, indicating that GABA may negatively regulate ALMT [5]. In previous studies, Yu Long confirmed that GABA inhibits the transport of anions in wheat by changing the active structure of ALMT1 [5]. The molecular mechanism of this conformational transformation is similar to Stefano’s research on the conformational transformation of GabR combined with aspartate aminotransferase (AAT) and GABA [8]. The interaction between GABA and ALMT can be used as a plant signal to participate in the regulation of ALMT1-mediated GABA transmembrane transport.

1.2. GAT1

GATs are a class of transcell membrane transport proteins [9][10]. The GAT gene belongs to the AAAP gene family [2]. Four homologous genes (GAT1, GAT2, GAT3 and GAT4) have been identified in plants. GAT1 located on the cell membrane can transport GABA across the membrane and transport GABA from the apoplast to the cytoplasm. Compared with the transport of GABA by ALMT1, Al3+ can block the influx of GABA from the apoplast to the cytoplasm during the transport of ALMT1 [5] but has no effect on the transport of GABA by GAT1. To date, genes encoding the GAT1 protein have been identified in Arabidopsis, rice, potato and other species, and the study of AtGAT1 transporting GABA has been carried out in Arabidopsis. Andreas et al. [9] studied AtGAT1 using Saccharomyces cerevisiae and Xenopus laevis oocytes as heterologous expression systems and found that AtGAT1 is an H+-driven transport protein that transports GABA through proton coupling. AtGAT1 has a very high affinity for GABA (Km10 ± 3 μM), which is the key factor in the transport of GABA.
Many studies on Arabidopsis have also verified the transport of GABA by GAT1 from other perspectives. The transient expression of AtGAT1-GFP in tobacco protoplasts showed that it localizes to the cytoplasmic membrane, which is consistent with the characteristics of GABA transport [9]. In the AtGAT1 mutant, endogenous GABA was not affected by exogenous GABA, which compared with the WT, verifies the role of AtGAT1 in the transmembrane influx of GABA [9]. However, studies on GAT gene transport function in species other than Arabidopsis have not been reported, which is a valuable research direction in the future.

1.3. AAP3 and ProT2

In the GAT1 mutant, other quaternary transporters can partially compensate for the loss of the GAT1 transporter. Two low-affinity GABA transporters located on the cell membrane were identified by heterologous recombination in yeast, namely, amino acid permease (AAP3) and proline transporter 2 (ProT2) [11][12]. Both of these transporters are located on the cell membrane and can potentially transport GABA [13]. Genes related to these two transporters have been identified in Arabidopsis, potato, rice and other crops [14]. AAP3 belongs to the amino acid/auxin permease (AAAP) family, and ProT2 belongs to the amino acid transporter (ATF) superfamily [15][16]. In Arabidopsis, AtAAP3 has higher affinity for other amino acids, such as lysine, than for GABA [17]. AtProT2 has higher affinity for compatible solutions of proline and glycine betaine than GABA [13][18]. Therefore, these two low-affinity transporters can transport GABA, but the effect is not very significant.

2. Transorganelle Membrane GABA Transporter

2.1. BAT1

BATs are bidirectional transmembrane transport proteins located on the mitochondrial membrane [19][20]. To date, seven homologous BAT genes have been found in Arabidopsis, potato, rice and other crop species [2][14], of which BAT1 can transport amino acids [21]. Research on the transfer of the BAT1 gene has only been carried out in Arabidopsis, and the gene encoding this protein in Arabidopsis (AtBAT1) exists as only a single copy. In the study by Bush et al., AtBAT1 had high transport activity for arginine, glutamate, lysine and other amino acids but no transport activity for GABA [19]. Michaeli found that AtGABP (At2g01170.1) is a splicing variant of AtBAT1 (At2g01170) belonging to the APC gene family, mainly responsible for the transmembrane transport of GABA on the mitochondrial membrane [22]. A 3H-GABA experiment showed that after incubation with GABA for 10 min, the GABA divergence between the AtGABP mutant and WT reached 1.72 times in mitochondria, which indicated that GABP played a transport role as a mitochondrial GABA carrier. In contrast to the two low affinity GABA transporters AAP3 and ProT2 mentioned above, GABP can transport GABA but not proline with highly similar sequence structures [22]. In a study of GABP transport of GABA, it was also found that coexpression of the GABP gene was very highly correlated with the SSADH gene encoding succinate semialdehyde dehydrogenase [22], indicating that GABP may be related to GABA metabolic reactions, such as the GABA shunt and TCA cycle (Table 1).
Table 1. GABA transport protein in plants.
Type Transporter Species Description
Cell membrane ALMT1 [5] Arabidopsis, Wheat, Barley, Rice Trans-cell membrane transport of GABA between apoplast and cytoplasm. Anions can activate its activity, and Al3+ can promote GABA efflux through it. GABA inhibits the transport of anions in wheat by changing the active structure of ALMT1
GAT1 [10] Arabidopsis, Rice, Potato A high-affinity GABA transporter protein, which transports GABA from the apoplast to the cytoplasm; the GAT1 gene belongs to the AAAP gene family
AAP3 [15] Arabidopsis, Rice, Potato The affinity for GABA is lower than other amino acids, such as lysine; the AAP3 gene belongs to the AAAP family
ProT2 [18] Arabidopsis, Rice, Potato Having higher affinity for compatible solutions of proline and glycine betaine than GABA; the ProT2 gene belongs to the ATF superfamily
Organelle membrane CAT9 [23] Arabidopsis, Tomato, Rice, Potato Experimental verification of GABA transport function of related gene (SlCAT9) in tomato; the CAT9 gene belongs to the APC gene family; transport through gradient concentration of substrate and driving force of vacuolar membrane proton pump
GABP [22] Arabidopsis AtGABP (At2g01170.1) is a splicing variant of AtBAT1 (At2g01170) belonging to the APC gene family; coexpression of GABP and SSADH

2.2. CAT9

Cationic amino acid transporters (CATs) are located on the vacuolar membrane, and the CAT gene belongs to the APC gene family [23][24][25]. To date, nine homologous CAT genes have been found in plants, of which CAT9 is mainly responsible for the two-way transport of GABA between the cytoplasm and vacuole. CAT9 has been identified in tomato, potato, Arabidopsis and rice, and experimental verification of the involvement of a related gene (SlCAT9) in GABA transport has been carried out in tomato [23][26]. The transport of GABA by SlCAT9 is mainly realized in two ways: through the gradient concentration of the transport substrate and by the driving force of the tonoplast proton pumps on the charge exchange system. Notably, the vacuole is a special organelle, and changes in the content of amino acid components in the vacuole do not affect the osmotic pressure of the vacuole [27][28]. Therefore, all transport processes must be carried out under strict conditions. In previous research, SlCAT9 was found to also transport Glu/Asp and may be involved in the conversion of GABA [29], thus affecting the metabolic pathway of GABA in plants.

References

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  2. Ma, H.; Cao, X.; Shi, S.; Li, S.; Gao, J.; Ma, Y.; Zhao, Q.; Chen, Q. Genome-wide survey and expression analysis of the amino acid transporter superfamily in potato (Solanum tuberosum L.). Plant Physiol. Biochem. 2016, 107, 164–177.
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  11. Young, G.B.; Jack, D.L.; Smith, D.W.; Saier, M.H. The amino acidauxinproton symport permease family. Biochim. Biophys. Acta 1999, 1415, 306–322.
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  13. Dinkeloo, K.; Boyd, S.; Pilot, G. Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Semin. Cell Dev. Biol. 2018, 74, 105–113.
  14. Tian, R.; Yang, Y.; Chen, M. Genome-wide survey of the amino acid transporter gene family in wheat (Triticum aestivum L.): Identification, expression analysis and response to abiotic stress. Int. J. Biol. Macromol. 2020, 162, 1372–1387.
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  16. Schwacke, R.; Grallath, S.; Breitkreuz, K.E.; Stransky, E.; Stransky, H.; Frommer, W.B.; Rentsch, D. LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 1999, 11, 377–391.
  17. Fischer, W.N.; Loo, D.D.; Koch, W.; Ludewig, U.; Boorer, K.J.; Tegeder, M.; Rentsch, D.; Wright, E.M.; Frommer, W.B. Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J. 2002, 29, 717–731.
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  26. Whiteman, S.A.; Serazetdinova, L.; Jones, A.M.; Sanders, D.; Rathjen, J.; Peck, S.C.; Maathuis, F.J. Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Wiley-VCH Verlag GMBH 2008, 8, 3536–3547.
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  28. Tsai, M.F.; McCarthy, P.; Miller, C. Substrate selectivity in glutamate-dependent acid resistance in enteric bacteria. Proc. Natl. Acad. Sci. USA 2013, 110, 5898–5902.
  29. Koike, S.; Matsukura, C.; Takayama, M.; Asamizu, E.; Ezura, H. Suppression of gamma -aminobutyric acid (GABA) transaminases induces prominent GABA accumulation, dwarfism and infertility in the tomato (Solanum lycopersicum L.). Plant Cell Physiol. 2013, 54, 793–807.
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Subjects: Horticulture
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Ding Yuan
,
Xiaolei Wu
,
Binbin Gong
,
Ruixiao Huo
,
Liran Zhao
,
Jingrui Li
,
Guiyun Lü
,
Hongbo Gao
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Revisions: 2 times (View History)
Update Date: 19 Apr 2023
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