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Lam, H. Amino Acid Transporters and Stress Responses in Plants. Encyclopedia. Available online: https://encyclopedia.pub/entry/20645 (accessed on 07 July 2024).
Lam H. Amino Acid Transporters and Stress Responses in Plants. Encyclopedia. Available at: https://encyclopedia.pub/entry/20645. Accessed July 07, 2024.
Lam, Hon-Ming. "Amino Acid Transporters and Stress Responses in Plants" Encyclopedia, https://encyclopedia.pub/entry/20645 (accessed July 07, 2024).
Lam, H. (2022, March 16). Amino Acid Transporters and Stress Responses in Plants. In Encyclopedia. https://encyclopedia.pub/entry/20645
Lam, Hon-Ming. "Amino Acid Transporters and Stress Responses in Plants." Encyclopedia. Web. 16 March, 2022.
Amino Acid Transporters and Stress Responses in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/ijms23052824

Plants can absorb inorganic and organic nitrogen from the environment via the root system. In soil, inorganic nitrogen is usually found in the forms of nitrate and ammonium, while organic nitrogen usually exists in the forms of free amino acids, urea, and short peptides. The uptake of nitrogen-containing molecules by plants is mediated by the respective transporters of these molecules, especially amino acid transporters, which have been known to play a major role in distributing nitrogen throughout the whole plant. Amino acid accumulation and signaling have been suggested to play important roles in stress responses.

Amino Acid Transporters Plants Stress responses

1. Classification and Structural Properties of Amino Acid Transporters

Amino acid transporters are found in diverse plant species. They are categorized into three major families: the Amino acid Transporter Family (ATF) (which is also known as the [1][2][3][4]. Amino Acid/Auxin Permease (AAAP) family), the Amino acid-Polyamine-organoCation (APC) family and the Usually Multiple Acids Move In and out Transporter family (UMAMIT) The ATF family consists of eight subfamilies: general Amino Acid Permeases (AAPs), Lysine and Histidine Transporters (LHTs), Proline Transporters (ProTs), γ-Aminobutyric acid Transporters (GATs), aromatic and neutral amino acid transporters, indole-3-acetic acid transporters (AUXs), amino acid transporter-like proteins and Vesicular Aminergic-Associated Transporters (VAATs). The APC family consists of three subfamilies: Cationic Amino acid Transporters (CATs), Amino acid/Choline Transporters (ACTs), and Polyamine H+-Symporters (PHSs). Members of the ATF family and the APC family usually share similar transport activities and protein structures. These transporters usually function by one of these mechanisms: solute-cation symport, solute-solute antiport, or facilitated diffusion at the plasma membrane [5] and they have a common protein structure with 10–14 TMDs [5][6]. UMAMITs were more recently identified compared to the ATF and APC families. These transporters belong to the nodulin-like gene family, functioning as the bidirectional facilitator for amino acid transport [4][7].

2. Amino Acid Transporters Are Driven by Proton Motive Force

Amino acid transporters act as secondary active transporters, with the specific amino acid being transported coupled to the proton motive force generated by the primary active H+-pumping complex featuring a proton-pumping ATPase at the membrane [8][2][9][10][11]. The majority of amino acid transporters characterized in plants are proton-amino acid symporters [8][2][9][10][11]. During amino acid import, a transient alkalization of the extracellular medium was observed [9]. In transgenic yeasts expressing Arabidopsis amino acid transporter genes such as AAP3, AAP4, or AAP5, the proline uptake rate was increased when the external pH was made to decrease. In other words, the higher external H+ concentration leads to a stronger transportation driving force for the uptake of the amino acid [11]. The requirement for the driving force provided by the proton gradient was further evidenced by the amino acid transport being abolished upon the addition of the protonophore, CCCP, a compound used for disrupting the proton gradient across the mitochondrial membrane by increasing its permeability to protons [9][11][12][13][14].

3. The Expressions of Amino Acid Transporters Are Stress-Responsive

Changes in the expressions of amino acid transporters were reported under abiotic stresses such as salt and water stress in Arabidopsis, rice, wheat, and barley [15][16][17][18]. Spatiotemporal differences in the induction patterns of different amino acid transporters upon stress were often observed within the same plant species or among their functional homologs. The Hordeum vulgare (barley) proline transporter, HvProT, was suggested to be crucial in transporting proline to the root tip region upon salt stress [18]. The Triticum aestivum (wheat) proline transporter 3, TaProT3, was upregulated in the root under salt stress whereas TaProT1 and TaProT2 were downregulated  [17]. Through genome-wide identification and evolutionary expression analyses on wheat amino acid transporters, numerous stress- and hormone-responsive cis-regulatory elements were found within the promoter regions of the amino acid transporter genes [19]. Similar cis-regulatory element analyses were conducted between Brassica napus (rapeseed) and Arabidopsis, and the results were consistent with previous research [19]. where multiple possible transcription factor recognition sites were discovered in the promoter regions of these transporter genes [20]. Based on the gene expression data, both TaAATs and BnAAPs responded differently to different abiotic stresses, suggesting the involvement of different interconnected regulatory networks of transporters in response to specific stresses [19][20].

4. Amino Acids as Osmolytes and Their Involvement in Ion Transport Mechanisms during Stress Responses

The accumulation of proline is widely known to protect plants from water-related stresses such as salinity, drought, and freezing [21]. The high solubility of proline and low inhibitory effect on seed germination make it a good candidate as a non-toxic osmolyte. One of the toxic effects of salt stress is the mineral nutrient imbalance brought forth by the over-accumulation of Na+ and Cl−, and the reduced levels of other essential ions such as K+ and Ca2+ [22]. In different plant species, including Olea europaea [23] and Cucumis sativus [24]. it was reported that the application of proline promoted salt tolerance. In O. europaea, it was shown that proline treatment reduced the level of Na+ but enhanced the level of Ca2+ in the leaf under salt treatment [23]. In C. sativus, it was shown that proline treatment reduced the level of Cl− in the leaf under salt treatment [24]. Exogenous proline and glycine betaine application were also reported to relieve the inhibition on both root and shoot growth of barley seedlings due to NaCl [25]. These observations suggest a possible involvement of amino acids, such as proline and glycine betaine, in the ion transportation mechanism.

5. Amino Acid Accumulation and Salicylic Acid (SA) Signaling

Plants carry a readily utilizable form of nitrogen. It is conceivable that the amino acid composition in plants was one of the determinants of plant–pathogen interactions. The importance of amino acid transporters in sustaining pathogen growth is not surprising. For example, there are a large number of transporter protein-encoding genes in the Psuedomonas syringae genome [26]. The cellular concentrations of amino acids, the uptake of inorganic nitrogen, and the relocation of amino acids might contribute to the plant’s susceptibility towards the pathogen [27][28]. It has been suggested that amino acid-derived signaling can regulate SA accumulation and signaling [29][30]. A broad-specificity, high-affinity AAP homolog, Lysine Histidine Transporter 1 (LHT1), expressed in the rhizodermis and mesophyll in Arabidopsis [13] was related to the pathogen susceptibility exhibited by the plant. The knockout Arabidopsis mutant lht1 had reduced susceptibility to the hemibiotrophic pathogen, P. syringae [27]. It was hypothesized that the cellular redox status is modulated by nitrogen metabolism, where glutamine deficiency plays an important role in enhancing the defense responses of lht1 plants. By studying the accumulation patterns of H2O2 and NO in the mesophyll and the spatial expression patterns of the pathogen-induced LHT1, it was suggested that LHT1 helped to maintain a low reactive oxygen species (ROS) level by keeping the glutamine level high. As a result, the low ROS level hindered the activation of SA-mediated defense responses [27].
In another study, Arabidopsis overexpressing AtCAT1 (Cation Amino acid Transporter 1) incorporated lysine at a higher rate and was more resistant to P. syringae compared to the wild-type and the cat1 mutant [28]. In the AtCAT1 overexpressor, the resistance to the bacterial pathogen P. syringae was enhanced with an increased SA level in the leaves [28]. Therefore, the expression levels of amino acid transporters might affect biotic stress responses by manipulating the cellular amino acid concentrations [27][28].

6. Amino Acid Transporters Are Involved in the Regulation of Cellular pH and Rhizospheric pH

Although amino acids usually carry charges and their transportation across membranes is often coupled with protons, there was no significant direct correlation among amino acid concentrations, transport, and cellular pH [31][32]. Nevertheless, there have been reports of amino acid assimilation and transportation altering pH homeostasis in plants. Ammonium, nitrogen, and nitrate assimilation produce protons that affect the cellular pH [33]. Aspartic acid and glutamic acid are suggested to be involved in balancing the excessive H+ production during nitrogen assimilation [34]. Moreover, it was reported that the aluminum-activated malate transporter in wheat, TaALMT1, promoted the acidification of an alkaline rhizosphere by facilitating the exudation of both malate and the zwitterionic buffer, gamma-aminobutyric acid (GABA) from the plant root [35]. The expression level of TaALMT1 was positively correlated with the growth performance of the wheat plant in the alkaline environment. The expression pattern of the amino acid transporter SlCAT9 in Solanum lycopersicum was linked to the exchange of GABA for glutamate and aspartate during fruit ripening, and eventually led to changes in the amino acid composition of the developing fruit [34]. The result is a change in the flavor and the nutritional value of the fruit [34]. The correlation between GABA concentration and low cytosolic pH during the early stages of fruit development was demonstrated using nuclear magnetic resonance (NMR) [36]. It was suggested that the export of GABA out of the vacuole in exchange for the import of glutamate or aspartate could serve to counterbalance the proton charges through the ‘reverse’ GABA shunt pathway [34].

7. Protons Are the Unneglectable Regulators of Active Transporters under Stresses

The activities of active transporters have been reported to be pH-dependent. Such property implies the regulation of the transporter activities at biological membranes between various cellular compartments with different pH. An obvious example is the increase in proline uptake by amino acid transporters when the extracellular pH was made to decrease [10]. In addition, the different pH of the vacuole, cytosol, and apoplast further implies the finetune of the transport direction to achieve different purposes. For example, the more acidic vacuole compared to the cytosol favors the storage of toxic nicotine in the vacuole [10] and the influx of Cl− into the vacuole for turgor regulation [37], while the acidification of the rhizosphere favors the exudation of malate and GABA from plant cells to the rhizosphere by TaALMT1 [35]. The pH dependence properties of active transporters even allow bidirectional transport H+. For example, AtSUC4 was demonstrated to have reversible direction of H+ transport when the H+ gradient between the membrane was made to reverse, although the structural basis of such reverse transport direction by the transporter has remained unclear [38]. Reverse transport direction has been observed in other transporters. The possible mechanisms underlying the reverse transport direction include the existence of two discrete conformation states of the transporter protein, which allows the binding of the substrate to either side of the transporter, and the existence of the substrate binding site, which is close to both sides of the transporter protein [39]. For example, based on the protein crystal structure, different conformations of BetP, a betaine transporter, were observed [40]. The existence of both the outward-facing conformation and the inward-facing conformation underlies the possibility of alternating access of the substrate [40]. In another study, it was reported that GltphH7 has the substrate binding site close to both sides of the transporter to allow alternating access of glutamate from either side of the transporter [41].
The pH of different cellular compartments is highly regulated and yet highly dynamic, especially when under stress. The alteration in pH of different cellular compartments under stress implies the regulation of transporter activities. For example, under drought stress, the pH in xylem sap was found to be increased from 6.1 to 6.7 [42], which is closer to pH 7, the optimal pH for the transport activity of AtDTX50 [43]. The significance of such pH-dependent activity lies in the possibility of improving ABA transport activity under stress. In addition, under stress, the deprotonation of phytohormones such as auxin and ABA molecules highlights the necessity of active transporters when the diffusion across membranes is made more difficult. Such reliance on active transporters for phytohormone transportation allows a highly controlled transport of the phytohormones under stresses.
Considering the mechanics of the active transporters under stress, it could be deduced that the altered expression of the transporters under stresses could not fully explain the regulation on the transport capacities. In some cases, the altered transporter activity under stress could be coupled with the altered expression of the gene encoding the transporter to improve the transport efficiency. For example, the pathogen-induced expression of EDS5 is coupled with possible pathogen-induced cytosolic acidification [44][45][46], which favors the SA-exporting activity of EDS5. However, in some cases, the expression of transporters could not sufficiently explain the altered substrate transport under stress. For example, it was found that photosynthetic rate, light level, and CO2 concentration had limited effects on the expressions of SUTs [47]. However, an improved sucrose transport upon the increased photosynthetic rate is expected. In this case, the possible alteration of the sucrose transport efficiency could be the explanation. It is therefore important to understand the mechanics of the active transporters under different situations when the cellular pH fluctuates.
The modulation of the expression of active transporters in plants has been considered a common approach to modulate the accumulation of desired metabolites [48]. Since protons play important roles in regulating active transports in plants, attempts to modulate the transporter activities could be broadened to consider the manipulation of genes that regulate the proton levels in various cellular compartments. Such manipulation allows the finetune of transporter activities under stress when cellular pH fluctuates.
The movement of H+ across the biological membranes results in electrochemical proton gradient, which means the proton gradient as well as the electrical potential gradient across the membrane, to energize the substrate transport. In the above discussion, several proteins, such as AtEDS5 [45][46]. AtSUC4 [38][49][50], and AtLHT1 [27], were reported to have their activities dependent on the proton gradient. Such observations are in line with the suggestion that the active transporters are energized by the electrochemical proton gradient across the biological membranes. In several examples, such as AtDTX50 [43], AtDTX33 [37], AtDTX35 [37], PvSUT1.1 [51], AtPLT5 [52], MdSTP13a [53], and HvProT [18], the transport activities were shown to be different under different pH of the vacuole/medium. However, it is not clear whether such differences of activities are merely a result of the altered electrochemical proton gradient across the membrane or a result of the structural change of the protein under different pH. Detailed studies on the conformation of the proteins under different pH will be needed to address the question.

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