Next Article in Journal
Improving Pepper Inbreds for Resistance to Pepper Yellow Leaf Curl Thailand Virus (PepYLCTHV) through Challenged Inoculations
Previous Article in Journal
The Effect of Humic-Based Biostimulants on the Yield and Quality Parameters of Chili Peppers
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Amino Acid Transporters on Amino Acid Absorption, Transport and Distribution in Crops

State Key Laboratory of Vegetable Biobreeding, The Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Zhongguancun South St, Haidian District, Beijing 100081, China
*
Authors to whom correspondence should be addressed.
Horticulturae 2024, 10(9), 999; https://doi.org/10.3390/horticulturae10090999
Submission received: 24 July 2024 / Revised: 12 September 2024 / Accepted: 20 September 2024 / Published: 21 September 2024
(This article belongs to the Section Vegetable Production Systems)

Abstract

:
Amino acid transporters mediate amino acid transport within and between cells and are the main mediators of nitrogen distribution in plants, which is crucial for maintaining plant growth and development. Many amino acid transporters have been identified in different plant species. In this review, we discuss the functions of amino acid transporters in plant absorption and amino acid transportation from root to shoot, which results in crop yield and quality improvement. Moreover, we summarize the role of amino acid transporters in response to environmental stimuli and the influence of N and C metabolic processes. We also elaborate on potential future research directions.

1. Introduction

Nitrogen (N) is the fundamental nutrient required for plant growth and development [1]. In the soil, there is inorganic and organic N, and amino acids are the main organic N compounds, comprising about 20–100 μM in the surface soil and accounting for 15–60% of the total N content in the soil [2,3]. Amino acids in soil can be directly absorbed by plants [4]. The inorganic N absorbed from the soil is reduced to organic N at the roots and transported through the xylem to the stem and then to the phloem, delivering N to different plant organs for growth and development [5,6]. In plants, amino acids not only provide nutrients but also participate in energy metabolism as carbon (C) skeletons, which is the main form of long-distance N transport [1,7]. Exogenous amino acid application in plants is beneficial for improving plant growth and development and increasing crop yield and quality [8].
Amino acid transporters mediate amino acid transport within and between cells, playing an important role in improving plant N utilization efficiency [5,9,10]. Amino acid transporters can be divided into two families: the amino acid/polyamine/choline (APC) family and the amino acid transporter (ATF) family. The ATF family, also known as the amino acid/auxin permeating enzyme (AAAP) family, has been extensively studied in plants, animals, and fungi [11]. The ATF family is divided into seven subfamilies: the amino acid permeating enzyme (AAP) family, lysine histidine transporter (LHT) family, proline transporter (ProT) family, γ-Aminobutyric acid transporter (GAT) family, aromatic and neutral amino acid transporter (ANT) family, auxin transporter (AUX) family, and usually multiple acids move in and out transporter (UMAMIT) family [5,10,12].
Amino acid transporters generally differ in substrate specificity, affinity, and tissue localization [5,13]. People have extensively studied the functions of amino acid transporters in plants in recent years. They participate in the transport of amino acids within and between cells, transport between the xylem and phloem, and transport from source to sink organs (Figure 1). The role of the AAP family in Arabidopsis has been extensively studied. Frommer and Hummel et al. [14] discovered that AtAAP1 restored proline uptake in yeast mutants. AtAAP1 is located on the cell membranes of the root epidermis, root hairs, and root tips (Figure 1). Glutamate, histidine, and phenylalanine serve as physiological substrates for the AtAAP1 protein, while aspartic acid, lysine, and arginine do not do so [15]. AtAAP2 is expressed in the phloem, in addition to flowers and stamens, and it plays a major role in N transport from the xylem to the phloem [16] (Figure 1). The expression levels of AtAAP1, AtAAP2, AtAAP6, AtAAP7, and AtAAP8 are also expressed higher in flowers and stamens, suggesting that these genes may have similar biological functions [17]. AtAAP5 exhibits a wide range of substrate affinities and can transport anionic, neutral, and cationic amino acids [18]. Few functions of organelle localized amino acid transporters have been identified (Figure 1). For example, AtGABP is identified as a GABA (gamma aminobutyrate) transporter, which mediates the entry of GABA from the cytoplasm into mitochondria [19]. AtCAT2, AtCAT4, and AtCAT8 were found to be localized in the tonoplast [20,21,22]. Tomato CAT9 (SlCAT9) participates in transporting glutamine (Glu) and aspartic acid (Asp) into vacuoles in exchange for GABA, which plays a role in amino acid accumulation during fruit development [19]. The effects of changes in amino acid transporter gene expression on N uptake, distribution, crop yield, and quality have been studied for many years. In this review, we summarized the mechanisms of how amino acid transporters regulate N absorption and distribution, C and N metabolism, and growth and development in vegetables, such as tomato, cucumber, soybean, and pea and model plants, so as to promote the study of amino acid transporters in vegetable crops.

2. Amino Acid Uptake, Transport, and Distribution

2.1. Amino Acid Uptake

Most amino acid transporters are located on the plasma membrane and are involved in amino acid transport. Amino acids and protons are co-transported by amino acid transporters. Many amino acid transporters have been reported to participate in the root absorption of amino acids [23]. LHTs are considered high-affinity transport systems. LHT1 imports neutral and acidic amino acids into the roots [24,25], and LHT1 is expressed in the rhizodermis of Arabidopsis (Figure 1). The capacity for amino acid uptake under limited inorganic N supply is increased several folds by LHT1 overexpression [26]. Moreover, elevated cucumber LHT1 and LHT6 (CsLHT1 and CsLHT6) expression in Arabidopsis significantly improves the uptake of exogenously supplied 15N-glutamate and 15N-glutamine [27]. AAP1 [23], AAP5 [28], and LHT6 [29] have been reported to participate in N uptake (Figure 1). The affinities of Arabidopsis ProTs are similar, while differences in their expression indicate their different roles in plants. AtProT2:GUS (β-glucuronidase) staining has been observed in the root epidermis and cortex, and AtProT1 and AtProT3 are mainly expressed in the phloem and leaves, respectively [30] (Figure 1).
Studies have often found that the knockout of an amino acid transporter gene results in different functions in different environments (such as substrate concentrations) [23,31]. For instance, early studies showed that AAP1 played a role in amino acid acquisition, as Arabidopsis mutants lacking AAP1 expression severely reduced the uptake of neutral amino acids when more than 150 μM of alanine (L-Ala) or glutamic acid (L-Glu) was supplied [23]. However, no significant effect on the absorption rate was found in the aap1 mutant when the maximum concentration of a single amino acid was 50 μM [31]. Further research is needed to determine the impacts of AAP1 and other transporters on amino acid absorption in different soil environments.

2.2. Root-to-Shoot Transport of Amino Acids

Absorbed or synthesized amino acids move from the cortex cells via the endodermis to the vasculature to circumvent the Casparian strip. Xylem elements regulate the flow of nitrates, N assimilates, other nutrients, and water from the root to the shoot [32]. During xylem loading, N is released from the endodermis, pericycle, or xylem parenchyma cells into the apoplast by transporters. N acquired by roots is transported to the stem by xylem transpiration.
Amino acid transport to sinks mainly occurs through the phloem. In general, N compounds synthesized by leaves are loaded into the phloem for the growth and development of sink organs [16]. Amino acids synthesized in the roots are transported to mature leaves via the xylem and then imported into the mesophyll cells for transient storage or loading into the leaf phloem of minor veins [15]. AtAAP8 localized to the plasma membrane has been shown to be expressed in the phloem of the source leaf [33] (Figure 1). When 14C-labeled Glu or glutamine (Gln) was injected into source leaves, the aap8 mutant showed decreased radioactivity in its sink leaves compared with the wild type for both Glu and Gln feeding in both the vegetative and reproductive growth stages, demonstrating the function of AAP8 in xylem-to-phloem transfer. AtAAP6 is localized to the xylem parenchyma in Arabidopsis, and Ataap6 mutants have decreased amino acid content in the phloem [34] (Figure 1). However, this is not sufficient to indicate that AtAAP6 is responsible for amino acid transfer from the xylem to the phloem, as the amino acid content in the xylem is much lower than that of the wild type. Therefore, there may be other functions for this amino acid transporter that need to be explored.

2.3. Amino Acid Transport from Source Leaf to Sink

Generally, N partitioning from source to sink is influenced by N absorption and metabolism in the source organs and the N transfer from source to sink. The increase in N export from the source leaves and the change in N concentration in the leaf may induce a shoot-to-root signal that triggers the upregulation of N uptake and transport in the leaf. Perchlik and Tegeder [35] found that in pea, the increase in the amino acid phloem load positively affected N absorption in the roots, thus affecting N assimilation and utilization effectiveness in the source and sink. Recently, Pereira and Santos et al. [36] found that OsAAP1 knockout resulted in damage to NO3 absorption, with negative effects on N assimilation and C metabolism under low or sufficient N. OsLHT1 is responsible for the long-distance transport of amino acids in rice, and OsLHT1 knockout results in a decrease in N absorption by the roots [37].
The function of amino acid transporters in phloem loading affects not only plant N uptake but also the N distribution from source to sink and the development of vegetative sinks and seeds [33,38,39]. Based on expression and localization studies, several amino acid transporters localize to the leaf vasculature, suggesting an essential role in N supply from source leaves to the sink [37,40,41,42]. Tissue-specific expression analysis has shown GUS activity in the phloem under the LAT5/PUT5 (Arabidopsis L-Type Amino Acid Transporter 5) promoter [40] (Figure 1), and the lat5-1 mutant has reduced leaf growth and altered N content in the seeds. In rice, OsLHT1 localized throughout the roots, including root hairs, epidermis, cortex, and stele, and to the leaf vasculature, and OsLHT1 knockout reduced the root uptake of amino acids. The delivery of root-synthesized amino acids to Oslht1 shoots was also significantly decreased, indicating that the elimination of OsLHT1 seriously affected N absorption and distribution [37]. Therefore, the yield of the Oslht1 mutant decreased significantly compared with the wide type [41,43].
Amino acids are produced by N assimilation, which typically occurs in the source organs (leaves); they are transported via the vascular system, xylem and phloem, into the seeds, the sink organs, where they are stored or consumed. In seeds, amino acids must be exported from the cell into the apoplast and imported into the cell many times to support seed development [44]. Several members of the UMAMIT family have been reported to function as bidirectional amino acid transporters in the last decade. AtUMAMIT11, 14, 18, 28, and 29 play important roles in seed development [44,45] (Figure 1). AtUMAMIT11, AtUMAMIT14, and AtUMAMIT18 are expressed in the unloading domain; therefore, they may mediate amino acid release (Figure 1). AtUMAMIT 28 is later found only in the innermost layer, and AtUMAMIT 29 is localized in the middle layer of the inner integument, suggesting its crucial role in amino acid export from different symplasmic domains of the developing seed. UMAMITs may be very interesting in many vegetable crops, as they can improve the amino acid levels and compositions of fruits, thereby increasing yield and quality.
Figure 1. An overview of the function and site of action of amino acid transporters identified in plants. Amino acid transporters play roles in root uptake, xylem–phloem transfer, phloem loading, intracellular transport, and seed loading and unloading. Each amino acid transporter highlighted here is mentioned in the text. LHT: lysine histidine transport family; AAP: amino acid permeating enzyme family; ProT: proline transporter family; UMAMIT: usually multiple acids move in and out transporter family; CAT: cationic amino acid transporter; AtGABP: gamma aminobutyrate transporter, which mediates the entry of GABA from the cytoplasm into mitochondria [19]; AtAVT3: homologs of AtANT1, which functions as a vacuolar amino acid exporter in Arabidopsis [46]. Blue arrows represent the direction of amino acid transport. Black arrows indicate the transport directions when known. Xy, xylem; Ph, phloem; CC, companion cell; SE, sieve tube.
Figure 1. An overview of the function and site of action of amino acid transporters identified in plants. Amino acid transporters play roles in root uptake, xylem–phloem transfer, phloem loading, intracellular transport, and seed loading and unloading. Each amino acid transporter highlighted here is mentioned in the text. LHT: lysine histidine transport family; AAP: amino acid permeating enzyme family; ProT: proline transporter family; UMAMIT: usually multiple acids move in and out transporter family; CAT: cationic amino acid transporter; AtGABP: gamma aminobutyrate transporter, which mediates the entry of GABA from the cytoplasm into mitochondria [19]; AtAVT3: homologs of AtANT1, which functions as a vacuolar amino acid exporter in Arabidopsis [46]. Blue arrows represent the direction of amino acid transport. Black arrows indicate the transport directions when known. Xy, xylem; Ph, phloem; CC, companion cell; SE, sieve tube.
Horticulturae 10 00999 g001

3. Amino Acid Transporter Functions in N and C Metabolism

N plays a number of vital roles in the central metabolism of plants. The N distribution between source and sink organs balances N absorption and metabolism, as well as the transport potential from source to sink organs [32]. Amino acids are essential N forms for long-distance transport, serving as intermediates of final metabolites in certain metabolic pathways, participating in the regulation of multiple metabolic, physiological, and biochemical pathways, thereby affecting many physiological processes in plants [32,47]. Their uptake, allocation, and remobilization are mediated by multiple amino acid transporters belonging to several subfamilies, as mentioned previously.
Guo and Qu et al. [48] showed that OsLHT1 knocked out altered the transport and metabolism of multiple amino acids, including Ala, serine (Ser), and threonine (Thr), which represented sustained rusty red spots on fully mature leaf blades and premature leaf senescence at the vegetative growth stage. OsLHT1 is a key transporter, and the alternation of OsLHT1 expression has a significant impact on growth and development, yield, and grain quality in rice [43,48]. Current related research involves N nutrition and metabolism, whether knocking out OsLHT1 has certain effects on C metabolism, such as the photosynthetic rate and sucrose and starch contents in leaves that have not been shown.
Numerous studies have shown that N and C metabolism are regulated in a coordinated manner [49,50,51]. The manipulation of N transport processes can affect primary metabolism, including N and/or C assimilation [7,17,52]. In Arabidopsis, AAP8 plays an important role in source-to-sink N partitioning [33], and aap8 mutant lines resolve the consequences of reduced amino acid phloem loading for source leaf C metabolism, sucrose phloem transport, and sink development during vegetative and reproductive growth phases. C fixation and assimilation and sucrose partitioning to siliques strongly decreased during the reproductive stage in aap8 mutants [38]. During the reproductive growth stage, changes in N metabolism or the N pool in leaves may affect C metabolism and allocation pathways through transcriptional inhibition, as a strong reduction in amino acid synthesis requires less input of C assimilates [38,53].
The target of rapamycin (TOR) kinase functions as a central regulator of fundamental cellular processes including amino acid transport [54]. Previous studies have shown that plant productivity is regulated by a TOR-mediated network that coordinates nutrient and stress responses to maintain growth and energy redistribution. For example, higher TOR activity promoted growth height and tillering and resulted higher yields and biomass of rice [55]. Previous ribosome profiling studies have shown that TOR controls the translation of various transcripts [56,57]. The impact of TOR on plant growth and metabolism may be based on two mechanisms: (1) The increase in TOR activity may lead to changes in the translation levels of certain amino acid transporters or N related transporters, ultimately resulting in an increase in crop yield. For example, the latest research has found that elevated TOR activity significantly increased the translation level of ammonium transporter AMT1;1 and amino acid transporter AAP1, which enhanced N uptake and allocation, improving plant growth and development [55]. (2) Knocking out or overexpressing certain key amino acid transporter genes may also cause changes in TOR levels, thereby altering the synthesis and metabolism processes in plants and affecting growth. For example, knocking out OsLHT1 affects TOR signaling transduction, inhibiting rice growth. However, the mechanism of interaction between TOR and amino acid transporters is still unclear, so it requires further research in the future, especially in vegetable crops.

4. Regulation of Amino Acid Transporters in Response to Environmental Stimuli

Amino acids are a key form of N transport that can be directly absorbed from the soil through specific root amino acid transporters; however, pathogenic microorganisms can invade plant tissues and feed on different plant amino acid pools. Plants may initiate immune response programs to limit this invasion, utilizing various amino acid transporters to modify the amino acid pool at the site of pathogen attack [58]. Disease-causing plant pathogens are considered major yield-limiting factors, resulting in billions of US dollars in lost crop yields each year [59]. Plants will transfer signals quickly in their bodies to establish defense mechanisms after perceiving various biotic and abiotic stress factors. Many amino acid transporters also play significant roles in plant defense responses, in addition to functioning in amino acid absorption, long-distance amino acid transport, and root and reproductive organ development, which is referred to in Figure 2. For example, cationic amino acid transporter 1 (CAT1) overexpression enhances resistance to Pseudomonas aeruginosa and upregulates genes related to systemic acquired resistance [60]. Similarly, the elevated expression of UMAMIT transporters induces stress phenotypes and pathogen resistance [61]. In the LHT family, AtLHT1 knockout increases resistance to a broad spectrum of pathogens [62], similar to its homologous gene OsLHT1 in rice. The disruption of OsLHT1 significantly prevents leaf invasion by Magnaporthe oryzae, a hemibiotrophic ascomycete fungus. OsLHT1 knockout alters the transportation and metabolism of amino acids, enhancing the expression of jasmonic acid- and salicylic acid-related defense genes [48]. However, further exploration is needed to determine whether and how hormones are involved in resisting external pathogens.
Proline is involved in multiple mechanisms to avoid the adverse effects of abiotic stress on plants. These mechanisms range from regulating osmotic balance to forming reactive oxygen species (ROS) according to the stressor [63]. Salt and drought stress promote proline production and inhibit its degradation [64]. Several amino acid transporters, such as ProTs, AAPs, and LHTs, transport proline, which can enhance plant stress resistance [26,65,66,67,68] (Figure 2). For example, the HvProT genes are highly expressed in root cap cells under salt stress in barley [69]. In soybean, the GmProT1 and GmProT2 genes are strongly induced by salt, drought, and abscisic acid (ABA) treatments. Overexpressing GmProT1 or GmProT2 in Arabidopsis results in more proline accumulation, elevated stress-related gene expression, and higher salt and drought resistance than wild-type plants under salt and drought stress [66]. Moreover, GmAAP6 encodes ay N deficiency-responsive amino acid permease in soybean, and its overexpression in Arabidopsis and soybean results in elevated tolerance to N limitation [39].

5. Amino Acid Transporter Functions for Improving Crop Yield and Quality

5.1. Crop Yield Improvement

Increasing crop yields can alleviate global food shortages and ensure that people around the world have access to a sufficient food supply. There have also been many reports on the molecular mechanisms that enhance the yields of different crops. For cereal crops, such as rice, they generally affect nutrient absorption and distribution, ultimately affecting plant growth and development or tillering and leading to an increase or decrease in yield. For example, in recent years, studies have shown that knocking out the amino acid transporter gene LHT1 in rice reduces the seed germination rate and N absorption and utilization efficiency by 55 and 72%, respectively, leading to significant growth inhibition [41,43]. This indicates that LHT1 is a key functional transporter that plays a crucial role in rice growth and development. However, in the AAP family, disrupting OsAAP3, OsAAP5, or OsAAP7, whose functions seem to be opposite to LHT1, promotes tillering, increasing grain yield [70,71,72]. This indicates that the functions of many amino acid transporters in plants differ, and they complement each other to jointly cast a regulatory network that affects plant growth and development.
The mechanism by which amino acid transporters affect plant growth and development has been widely studied in Arabidopsis. AtLHT1 is strongly expressed on the surfaces of roots, young leaves, flowers, and leaf sheaths and is involved in amino acid absorption and input into mesophyll cells [24,26]. AtLHT1 overexpression improves N utilization efficiency, while its destruction reduces aboveground biomass and seed yield under restricted N application conditions [26]. AtAAP1 is involved in the growth and seed development of Arabidopsis, which can also affect seed protein storage and yield [73]. AtAAP2 is expressed in the phloem and participates in the transmission process from the xylem to the phloem. The increased allocation of amino acids to the leaves in the aap2 mutant leads to an increase in seed yield [17,74]. AtAAP8 is expressed in the leaf phloem and petiole, and its function is to load amino acids into the phloem and input them into the seeds. In the aap8 mutant, amino acid loading in the phloem and allocation to the sink is reduced, decreasing the number of plants and seeds [33,75].
Changes in the expression of amino acid transporter genes may affect plant growth and development through N absorption and assimilation [37,41,43] or other factors such as hormone levels, thereby regulating plant growth, such as rice tiller number, and yield [71]. The mechanism by which amino acid transporters regulate plant growth and development is complex; plants contain different types of amino acid transporters. Typically, studies have evaluated the molecular and physiological functions of amino acid transporters by creating a single mutant, while different genes in plants have functional redundancy. However, knocking out one gene may not show obvious differences in plant absorption and other aspects. Therefore, double or even triple mutants need to be generated to further discuss and clarify their functions.

5.2. Crop Quality Improvement

Fruit quality has been a hot research topic in recent years. Fruit quality improvement not only increases the incomes of farmers but also relates to human health. As a sink in plants, fruit requires the continuous input of nutrients and other substances from the source to the sink to ensure normal fruit growth and development and nutritional quality. The overexpression of the sugar transporter SUT1 and amino acid transporter AAP1 in peas increases the flux of sucrose and amino acids from source to sink, enhances the interaction between cytokinin and cell wall-converting enzymes during seed coat development, and leads to enhanced sink activity, increasing the sucrose content in the leaves during pea harvest and increasing the seed quantity and protein content at maturity [76].
There may be a complex balance between fruit yield and N content, as knocking out OsLHT1 significantly reduces grain yield, and Oslht1 mutants have higher protein contents and contain most essential free amino acids in seeds [41,43]. The amino acid transporter OsAAP6 is a necessary regulatory factor for grain protein content and nutritional quality; however, changes in OsAAP6 expression have no significant effect on grain yield, while transgenic plants with higher OsAAP6 expression levels produce more stored grain proteins [77]. The changes in seed quantity and N content may be caused by the species or other unknown complex mechanisms [73,78,79], and further research and exploration are needed in the future.

6. Conclusions

With the rapid development of genome sequencing, many amino acid transporters have been discovered in different species. However, there is too much complexity and uncertainty in plants due to the functional redundancy of different amino acid transporters. Thus, the specific functions of amino acid transporters need to be further explored. The knockout or overexpression of one or more amino acid transporter genes can effectively improve plant yield or quality, enhance crop N utilization efficiency, and maximize plant growth under a limited N supply, which is very important and meaningful.
However, current studies in this field mainly focus on model plants, such as Arabidopsis and rice, and there is little research on the impacts of amino acid transporters on vegetable crop yield and quality, which need to be extensively and deeply studied in the future. Moreover, amino acid transporters may have other functions in addition to playing a major role in amino acid absorption and distribution, such as resistance to external bacterial invasion and various environmental stimuli. Currently, research in this area is limited and requires further exploration.

Author Contributions

Conceptualization, L.L. and M.S.; methodology, Y.L.; software, L.L. and M.S.; validation, Y.L. and M.S.; writing—original draft preparation, L.L.; writing—review and editing, L.L and M.S.; supervision, X.Y., Y.Y., C.H. and J.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research acknowledged the support of the National Natural Science Foundation of China (No. 31972480 and No. 32260800), the Earmarked Fund for CARS (CARS-23-B05; CARS-24-B-04), the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS), and the National Key Research and Development Program of China (2023YFD2300704). This research acknowledged the support of the Key Laboratory of Horticultural Crop Biology and Germplasm Innovation, the Ministry of Agriculture, China.

Data Availability Statement

The original contributions presented in this study are included in the article; further inquiries can be directed to the corresponding authors.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Bloom, A.J. The increasing importance of distinguishing among plant nitrogen sources. Curr. Opin. Plant Biol. 2015, 25, 10–16. [Google Scholar] [CrossRef] [PubMed]
  2. Lipson, D.; Näsholm, T. The unexpected versatility of plants: Organic nitrogen use and availability in terrestrial ecosystems. Oecologia 2001, 128, 305–316. [Google Scholar] [CrossRef]
  3. Jämtgård, S.; Näsholm, T.; Huss-Danell, K. Nitrogen compounds in soil solutions of agricultural land. Soil Biol. Biochem. 2010, 42, 2325–2330. [Google Scholar] [CrossRef]
  4. Herdiansyah, G.; Farid, M.; Aziz, M.; Sari Dewi, F.; Rahayu, A.S. Nitrogen uptake in fully organic, semi-organic and conventional rice fields in Madiun Regency. IOP Conf. Ser. Earth Environ. Sci. 2022, 1016, 012011. [Google Scholar] [CrossRef]
  5. Yang, G.; Wei, Q.; Huang, H.; Xia, J. Amino acid transporters in plant cells: A brief review. Plants 2020, 9, 967. [Google Scholar] [CrossRef] [PubMed]
  6. Li, F.; Lv, C.; Zou, Z.; Duan, Y.; Zhou, J.; Zhu, X.; Ma, Y.; Zhang, Z.; Fang, W. CsAAP7.2 is involved in the uptake of amino acids from soil and the long-distance transport of theanine in tea plants (Camellia sinensis L.). Tree Physiol. 2022, 42, 2369–2381. [Google Scholar] [CrossRef] [PubMed]
  7. Zhang, L.; Garneau, M.G.; Majumdar, R.; Grant, J.; Tegeder, M. Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids. Plant J. Cell Mol. Biol. 2015, 81, 134–146. [Google Scholar] [CrossRef] [PubMed]
  8. Forsum, O.; Svennerstam, H.; Ganeteg, U.; Näsholm, T. Capacities and constraints of amino acid utilization in Arabidopsis. New Phytol. 2008, 179, 1058–1069. [Google Scholar] [CrossRef]
  9. Ortiz-Lopez, A.; Chang, H.C.; Bush, D.R. Amino acid transporters in plants. Biochim. Biophys. Acta-Biomembr. 2000, 1465, 275–280. [Google Scholar] [CrossRef]
  10. Yao, X.; Nie, J.; Bai, R.; Sui, X. Amino Acid Transporters in Plants: Identification and Function. Plants 2020, 9, 972. [Google Scholar] [CrossRef]
  11. Chang, A.B.; Lin, R.; Studley, W.K.; Tran, C.V.; Saier, M.H., Jr. Phylogeny as a guide to structure and function of membrane transport proteins. Mol. Membr. Biol. 2004, 21, 171–181. [Google Scholar] [CrossRef] [PubMed]
  12. 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. [Google Scholar] [CrossRef]
  13. Wan, Y.; Wang, Y.; Shi, Z.; Rentsch, D.; Ward, J.L.; Hassall, K.; Sparks, C.A.; Huttly, A.K.; Buchner, P.; Powers, S.; et al. Wheat amino acid transporters highly expressed in grain cells regulate amino acid accumulation in grain. PLoS ONE 2021, 16, e0246763. [Google Scholar] [CrossRef]
  14. Frommer, W.B.; Hummel, S.; Riesmeier, J.W. Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 1993, 90, 5944–5948. [Google Scholar] [CrossRef] [PubMed]
  15. Rentsch, D.; Schmidt, S.; Tegeder, M. Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett. 2007, 581, 2281–2289. [Google Scholar] [CrossRef]
  16. Zhang, L.; Tan, Q.; Lee, R.; Trethewy, A.; Lee, Y.H.; Tegeder, M. Altered xylem-phloem transfer of amino acids affects metabolism and leads to increased seed yield and oil content in Arabidopsis. Plant Cell 2010, 22, 3603–3620. [Google Scholar] [CrossRef] [PubMed]
  17. Chen, Z.; Zhang, Y.; Zhang, J.; Fan, B.; Zhou, Y.; Cui, X. Expression of AtAAP gene family and endosperm-specific expression of AtAAP1 gene promotes amino acid absorption in Arabidopsis thaliana and maize. Agronomy 2021, 11, 1668. [Google Scholar] [CrossRef]
  18. Fischer, W.N.; Kwart, M.; Hummel, S.; Frommer, W.B. Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 1995, 270, 16315–16320. [Google Scholar] [CrossRef]
  19. Snowden, C.J.; Thomas, B.; Baxter, C.J.; Smith, J.A.C.; Sweetlove, L.J. A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition. Plant J. 2015, 81, 651–660. [Google Scholar] [CrossRef]
  20. Yang, H.; Krebs, M.; Stierhof, Y.D.; Ludewig, U. Characterization of the putative amino acid transporter genes AtCAT2, 3 & 4: The tonoplast localized AtCAT2 regulates soluble leaf amino acids. J. Plant Physiol. 2014, 171, 594–601. [Google Scholar] [PubMed]
  21. Su, Y.H.; Frommer, W.B.; Ludewig, U. Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol. 2004, 136, 3104–3113. [Google Scholar] [CrossRef] [PubMed]
  22. Yang, H.; Bogner, M.; Stierhof, Y.D.; Ludewig, U. H+-Independent glutamine transport in plant root tips. PLoS ONE 2010, 5, e8917. [Google Scholar] [CrossRef]
  23. Lee, Y.H.; Foster, J.; Chen, J.; Voll, L.M.; Weber, A.P.; Tegeder, M. AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J. 2007, 50, 305–319. [Google Scholar] [CrossRef]
  24. Chen, L.; Bush, D.R. LHT1, a lysine-and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol. 1997, 115, 1127–1134. [Google Scholar] [CrossRef] [PubMed]
  25. Ganeteg, U.; Ahmad, I.; Jämtgård, S.; Aguetoni-Cambui, C.; Inselsbacher, E.; Svennerstam, H.; Schmidt, S.; Näsholm, T. Amino acid transporter mutants of Arabidopsis provides evidence that a non-mycorrhizal plant acquires organic nitrogen from agricultural soil. Plant Cell Environ. 2017, 40, 413–423. [Google Scholar] [CrossRef] [PubMed]
  26. Hirner, A.; Ladwig, F.; Stransky, H.; Okumoto, S.; Keinath, M.; Harms, A.; Frommer, W.B.; Koch, W. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 2006, 18, 1931–1946. [Google Scholar] [CrossRef] [PubMed]
  27. Li, F.; Dong, C.; Yang, T.; Bao, S.; Fang, W.; Lucas, W.J.; Zhang, Z. The tea plant CsLHT1 and CsLHT6 transporters take up amino acids, as a nitrogen source, from the soil of organic tea plantations. Hortic. Res. 2021, 8, 178. [Google Scholar] [CrossRef] [PubMed]
  28. Svennerstam, H.; Ganeteg, U.; Näsholm, T. Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. New Phytol. 2008, 180, 620–630. [Google Scholar] [CrossRef]
  29. Perchlik, M.; Foster, J.; Tegeder, M. Different and overlapping functions of Arabidopsis LHT6 and AAP1 transporters in root amino acid uptake. J. Exp. Bot. 2014, 65, 5193–5204. [Google Scholar] [CrossRef]
  30. Grallath, S.; Weimar, T.; Meyer, A.; Gumy, C.; Suter-Grotemeyer, M.; Neuhaus, J.M.; Rentsch, D. The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol. 2005, 137, 117–126. [Google Scholar] [CrossRef]
  31. Svennerstam, H.; Jämtgård, S.; Ahmad, I.; Huss-Danell, K.; Näsholm, T.; Ganeteg, U. Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytol. 2011, 191, 459–467. [Google Scholar] [CrossRef] [PubMed]
  32. Tegeder, M.; Masclaux-Daubresse, C. Source and sink mechanisms of nitrogen transport and use. New Phytol. 2018, 217, 35–53. [Google Scholar] [CrossRef] [PubMed]
  33. Santiago, J.P.; Tegeder, M. Connecting source with sink: The role of Arabidopsis AAP8 in phloem loading of amino acids. Plant Physiol. 2016, 171, 508–521. [Google Scholar] [CrossRef] [PubMed]
  34. Hunt, E.; Gattolin, S.; Newbury, H.J.; Bale, J.S.; Tseng, H.M.; Barrett, D.A.; Pritchard, J. A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J. Exp. Bot. 2010, 61, 55–64. [Google Scholar] [CrossRef]
  35. Perchlik, M.; Tegeder, M. Improving Plant Nitrogen Use Efficiency through Alteration of Amino Acid Transport Processes. Plant Physiol. 2017, 175, 235–247. [Google Scholar] [CrossRef]
  36. Pereira, E.G.; Santos, L.A.; Chapeta, A.C.O.; de Souza Ribeiro, Y.R.; Santa-Catarina, C.; Bucher, C.P.C.; Bucher, C.A.; García, A.C.; Fernandes, M.S. Disruption of Amino Acid Transporter OsAAP1 Impairs Rice Seedling Establishment and Nitrate Uptake and Assimilation. J. Plant Growth Regul. 2024, 43, 2841–2854. [Google Scholar] [CrossRef]
  37. Guo, N.; Hu, J.; Yan, M.; Qu, H.; Luo, L.; Tegeder, M. Oryza sativa Lysine-Histidine-type Transporter 1 functions in root uptake and root-to-shoot allocation of amino acids in rice. Plant J. Cell Mol. Biol. 2020, 103, 395–411. [Google Scholar] [CrossRef]
  38. Santiago, J.P.; Tegeder, M. Implications of nitrogen phloem loading for carbon metabolism and transport during Arabidopsis development. J. Integr. Plant Biol. 2017, 59, 409–421. [Google Scholar] [CrossRef]
  39. Liu, S.; Wang, D.; Mei, Y.; Xia, T.; Xu, W.; Zhang, Y.; You, X.; Zhang, X.; Li, L.; Wang, N.N. Overexpression of GmAAP6a enhances tolerance to low nitrogen and improves seed nitrogen status by optimizing amino acid partitioning in soybean. Plant Biotechnol. J. 2020, 18, 1749–1762. [Google Scholar] [CrossRef]
  40. Begam, R.A.; D’Entremont, J.; Good, A. The Arabidopsis L-Type Amino Acid Transporter 5 (LAT5/PUT5) Is Expressed in the Phloem and Alters Seed Nitrogen Content When Knocked Out. Plants 2020, 9, 1519. [Google Scholar] [CrossRef]
  41. Guo, N.; Gu, M.; Hu, J.; Qu, H.; Xu, G. Rice OsLHT1 Functions in Leaf-to-Panicle Nitrogen Allocation for Grain Yield and Quality. Front. Plant Sci. 2020, 11, 1150. [Google Scholar] [CrossRef] [PubMed]
  42. Yang, X.; Yang, G.; Wei, X.; Huang, W.; Fang, Z. OsAAP15, an amino acid transporter in response to nitrogen concentration, mediates panicle branching and grain yield in rice. Plant Sci. 2023, 330, 111640. [Google Scholar] [CrossRef] [PubMed]
  43. Wang, X.; Yang, G.; Shi, M.; Hao, D.; Wei, Q.; Wang, Z.; Fu, S.; Su, Y.; Xia, J. Disruption of an amino acid transporter LHT1 leads to growth inhibition and low yields in rice. BMC Plant Biol. 2019, 19, 268. [Google Scholar] [CrossRef] [PubMed]
  44. Müller, B.; Fastner, A.; Karmann, J.; Mansch, V.; Hoffmann, T.K.; Schwab, W.; Suter-Grotemeyer, M.; Rentsch, D.; Truernit, E.; Ladwig, F. Amino acid export in developing Arabidopsis seeds depends on umamit facilitators. Curr. Biol. 2015, 25, 3126–3131. [Google Scholar] [CrossRef] [PubMed]
  45. Ladwig, F.; Stahl, M.; Ludewig, U.; Hirner, A.A.; Hammes, U.Z.; Stadler, R.; Harter, K.; Koch, W. Siliques Are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol. 2012, 158, 1643–1655. [Google Scholar] [CrossRef]
  46. Fujiki, Y.; Teshima, H.; Kashiwao, S.; Kawano-Kawada, M.; Ohsumi, Y.; Kakinuma, Y.; Sekito, T. Functional identification of AtAVT3, a family of vacuolar amino acid transporters, in Arabidopsis. FEBS Lett. 2017, 591, 5–15. [Google Scholar] [CrossRef]
  47. Amir, R.; Galili, G.; Cohen, H. The metabolic roles of free amino acids during seed development. Plant Sci. 2018, 275, 11–18. [Google Scholar] [CrossRef]
  48. Guo, N.; Qu, H.; Zhi, Y.; Zhang, Y.; Cheng, S.; Chu, J.; Zhang, Z.; Xu, G. Knock out of amino acid transporter gene OsLHT1 accelerates leaf senescence and enhances resistance to rice blast fungus. J. Exp. Bot. 2023, 74, 4143–4157. [Google Scholar] [CrossRef]
  49. Wang, R.; Okamoto, M.; Xing, X.; Crawford, N.M. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 2003, 132, 556–567. [Google Scholar] [CrossRef]
  50. Nunes-Nesi, A.; Fernie, A.R.; Stitt, M. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant 2010, 3, 973–996. [Google Scholar] [CrossRef]
  51. Sahrawy, M.; Avila, C.; Chueca, A.; Cánovas, F.M.; Lopez-Gorgé, J. Increased sucrose level and altered nitrogen metabolism in Arabidopsis thaliana transgenic plants expressing antisense chloroplastic fructose-1,6-bis phosphatase. J. Exp. Bot. 2004, 55, 2495–2503. [Google Scholar] [CrossRef] [PubMed]
  52. Carter, A.M.; Tegeder, M. Increasing nitrogen fixation and seed development in soybean requires complex adjustments of nodule nitrogen metabolism and partitioning processes. Curr. Biol. 2006, 26, 2044–2051. [Google Scholar] [CrossRef]
  53. De Groot, C.C.; Marcelis, L.F.; van den Boogaard, R.; Kaiser, W.M.; Lambers, H. Interaction of nitrogen and phosphorus nutrition in determining growth. Plant Soil 2003, 248, 257–268. [Google Scholar] [CrossRef]
  54. Awasthi, A.; Nain, V.; Srikanth, C.V.; Puria, R. A regulatory circuit between lncRNA and TOR directs amino acid uptake in yeast. Biochim. Biophys. Acta-Mol. Cell Res. 2020, 1867, 118680. [Google Scholar] [CrossRef] [PubMed]
  55. Li, W.; Liu, J.; Li, Z.; Ye, R.; Chen, W.; Huang, Y.; Yuan, Y.; Zhang, Y.; Hu, H.; Zheng, P.; et al. Mitigating growth-stress trade offs via elevated tor signaling in rice. Mol. Plant 2024, 17, 240–257. [Google Scholar] [CrossRef] [PubMed]
  56. Lee, D.H.; Park, S.J.; Ahn, C.S.; Pai, H.S. MRF Family Genes Are Involved in Translation Control, Especially under Energy-Deficient Conditions, and Their Expression and Functions Are Modulated by the TOR Signaling Pathway. Plant Cell 2017, 29, 2895–2920. [Google Scholar] [CrossRef] [PubMed]
  57. Scarpin, M.R.; Leiboff, S.; Brunkard, J.O. Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation. eLife Sci. 2020, 9, e58795. [Google Scholar] [CrossRef]
  58. Tünnermann, L.; Colou, J.; Näsholm, T.; Gratz, R. To have or not to have: Expression of amino acid transporters during pathogen infection. Plant Mol. Biol. 2022, 109, 413–425. [Google Scholar] [CrossRef]
  59. Ding, S.; Shao, X.; Li, J.; Ahammed, G.J.; Yao, Y.; Ding, J.; Hu, Z.; Yu, J.; Shi, K. Nitrogen forms and metabolism affect plant defence to foliar and root pathogens in tomato. Plant Cell Environ. 2021, 44, 1596–1610. [Google Scholar] [CrossRef] [PubMed]
  60. Yang, H.; Postel, S.; Kemmerling, B.; Ludewig, U.W.E. Altered growth and improved resistance of A rabidopsis against P seudomonas syringae by overexpression of the basic amino acid transporter AtCAT1. Plant Cell Environ. 2014, 37, 1404–1414. [Google Scholar] [CrossRef]
  61. Besnard, J.; Sonawala, U.; Maharjan, B.; Collakova, E.; Finlayson, S.A.; Pilot, G.; McDowell, J.; Okumoto, S. Increased Expression of UMAMIT Amino Acid Transporters Results in Activation of Salicylic Acid Dependent Stress Response. Front. Plant Sci. 2021, 11, 606386. [Google Scholar] [CrossRef] [PubMed]
  62. Liu, G.; Ji, Y.; Bhuiyan, N.H.; Pilot, G.; Selvaraj, G.; Zou, J.; Wei, Y. Amino acid homeostasis modulates salicylic acid–associated redox status and defense responses in Arabidopsis. Plant Cell 2010, 22, 3845–3863. [Google Scholar] [CrossRef]
  63. Furlan, A.L.; Bianucci, E.; Giordano, W.; Castro, S.; Becker, D.F. Proline metabolic dynamics and implications in drought tolerance of peanut plants. Plant Physiol. Biochem. 2020, 151, 566–578. [Google Scholar] [CrossRef] [PubMed]
  64. Ren, Y.; Miao, M.; Meng, Y.; Cao, J.; Fan, T.; Yue, J.; Xiao, F.; Liu, Y.; Cao, S. DFR1-Mediated Inhibition of Proline Degradation Pathway Regulates Drought and Freezing Tolerance in Arabidopsis. Cell Rep. 2018, 23, 3960–3974. [Google Scholar] [CrossRef] [PubMed]
  65. 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. [Google Scholar] [CrossRef]
  66. Na, G.; Dong, X.; Zhang, W.; Zhao, J.M.; Xue, C.C.; Qiang, Y.; Xue, J.Y.; Wang, H.T.; Zhang, Y.M.; Han, X. Overexpression of GmProT1 and GmProT2 increases tolerance to drought and salt stresses in transgenic Arabidopsis. J. Integr. Agric. 2016, 15, 1727–1743. [Google Scholar]
  67. Wang, T.; Chen, Y.; Zhang, M.; Chen, J.; Liu, J.; Han, H.; Hua, X. Arabidopsis AMINO ACID PERMEASE1 contributes to salt stress-induced proline uptake from exogenous sources. Front. Plant Sci. 2017, 8, 2182. [Google Scholar] [CrossRef] [PubMed]
  68. Akbudak, M.A.; Filiz, E. Genome-wide investigation of proline transporter (ProT) gene family in tomato: Bioinformatics and expression analyses in response to drought stress—ScienceDirect. Plant Physiol. Biochem. 2020, 157, 13–22. [Google Scholar] [CrossRef]
  69. Ueda, A.; Shi, W.; Sanmiya, K.; Shono, M.; Takabe, T. Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol. 2001, 42, 1282–1289. [Google Scholar] [CrossRef]
  70. Lu, K.; Wu, B.; Wang, J.; Zhu, W.; Nie, H.; Qian, J.; Huang, W.; Fang, Z. Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol. J. 2018, 16, 1710–1722. [Google Scholar] [CrossRef] [PubMed]
  71. Wang, J.; Wu, B.; Lu, K.; Wei, Q.; Qian, J.; Chen, Y.; Fang, Z. The Amino Acid Permease 5 (OsAAP5) Regulates Tiller Number and Grain Yield in Rice. Plant Physiol. 2019, 180, 1031–1045. [Google Scholar] [CrossRef]
  72. Jin, F.; Xie, P.; Li, Z.; Wu, B.; Huang, W.; Fang, Z. Blocking of amino acid transporter OsAAP7 promoted tillering and yield by determining basic and neutral amino acids accumulation in rice. BMC Plant Biol. 2024, 24, 447. [Google Scholar] [CrossRef] [PubMed]
  73. Sanders, A.; Collier, R.; Trethewy, A.; Gould, G.; Sieker, R.; Tegeder, M. AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 2009, 59, 540–552. [Google Scholar] [CrossRef] [PubMed]
  74. Perchlik, M.; Tegeder, M. Leaf amino acid supply affects photosynthetic and plant nitrogen use efficiency under nitrogen stress. Plant Physiol. 2018, 178, 174–188. [Google Scholar] [CrossRef] [PubMed]
  75. Schmidt, R.; Stransky, H.; Koch, W. The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 2007, 226, 805–813. [Google Scholar] [CrossRef]
  76. Grant, J.E.; Ninan, A.; Cripps-Guazzone, N.; Shaw, M.; Song, J.; Petřík, I.; Novák, O.; Tegeder, M.; Jameson, P.E. Concurrent overexpression of amino acid permease AAP1 (3a) and SUT1 sucrose transporter in pea resulted in increased seed number and changed cytokinin and protein levels. Funct. Plant Biol. 2021, 48, 889–904. [Google Scholar] [CrossRef] [PubMed]
  77. Peng, B.; Kong, H.; Li, Y.; Wang, L.; Zhong, M.; Sun, L.; Gao, G.; Zhang, Q.; Luo, L.; Wang, G.; et al. OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice. Nat. Commun. 2014, 5, 4847. [Google Scholar] [CrossRef]
  78. Fageria, N.K.; Baligar, V.C. Enhancing nitrogen use efficiency in crop plants. Adv. Agron. 2005, 88, 97–185. [Google Scholar]
  79. Hirel, B.; Le Gouis, J.; Ney, B.; Gallais, A. The challenge of improving nitrogen use efficiency in crop plants: Towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 2007, 58, 2369–2387. [Google Scholar] [CrossRef]
Figure 2. A schematic diagram of the role of amino acid transporters in response to external stimuli. Amino acid transporters known to be involved in resisting external stress have been mentioned in the text. OsLHT1: the members of lysine histidine transport family in rice; HvProTs: the members of proline transporter family in barley; GmProTs: the members of proline transporter family in soybean; GmAAP6: the members of the amino acid permeating enzyme family in soybean. Black arrows indicate the sequential responses used of plants to cope with changes in their physical environments.
Figure 2. A schematic diagram of the role of amino acid transporters in response to external stimuli. Amino acid transporters known to be involved in resisting external stress have been mentioned in the text. OsLHT1: the members of lysine histidine transport family in rice; HvProTs: the members of proline transporter family in barley; GmProTs: the members of proline transporter family in soybean; GmAAP6: the members of the amino acid permeating enzyme family in soybean. Black arrows indicate the sequential responses used of plants to cope with changes in their physical environments.
Horticulturae 10 00999 g002
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Liu, L.; Yu, X.; Yan, Y.; He, C.; Wang, J.; Sun, M.; Li, Y. Amino Acid Transporters on Amino Acid Absorption, Transport and Distribution in Crops. Horticulturae 2024, 10, 999. https://doi.org/10.3390/horticulturae10090999

AMA Style

Liu L, Yu X, Yan Y, He C, Wang J, Sun M, Li Y. Amino Acid Transporters on Amino Acid Absorption, Transport and Distribution in Crops. Horticulturae. 2024; 10(9):999. https://doi.org/10.3390/horticulturae10090999

Chicago/Turabian Style

Liu, Lu, Xianchang Yu, Yan Yan, Chaoxing He, Jun Wang, Mintao Sun, and Yansu Li. 2024. "Amino Acid Transporters on Amino Acid Absorption, Transport and Distribution in Crops" Horticulturae 10, no. 9: 999. https://doi.org/10.3390/horticulturae10090999

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop