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Nitrogen Assimilation and Translocation in Arabidopsis Seeds

Written By

Rowshon A. Begam and Michael Deyholos

Submitted: 11 June 2023 Reviewed: 08 July 2023 Published: 09 August 2023

DOI: 10.5772/intechopen.1002410

Seed Biology IntechOpen
Seed Biology New Advances Edited by Ertan Yildirim

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Seed Biology - New Advances

Ertan Yıldırım, Sıtkı Ermiş and Eren Özden

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Abstract

In plants, assimilated nitrogen travels mostly as amino acids. Amino acids travel from sources to sink tissues through cellular and organelle membranes such as plasma membrane, chloroplast membrane, mitochondrial membrane, and tonoplast membrane via facilitated or active transport. Membrane transporter proteins such as amino acid transporters mediate the transport. These transporters, as they facilitate the movement of amino acids through membranes, also regulate the distribution of amino nitrogen. Understanding the organ and tissue-specific distribution of amino acid transporters, their substrate affinity, and transport mechanism can help us understand the source-sink distribution of amino nitrogen in plants. With advancements in plant science research, we understand the amino acid distribution route in theory, but we have yet to identify many of the necessary amino acid transporters that enable this route. This chapter discusses the source-sink distribution of amino acids with a specific focus on seeds and lists the amino acid transporters in this route, characterized to date, in the model plant system, Arabidopsis thaliana.

Keywords

  • amino acids
  • amino nitrogen
  • seed nitrogen
  • amino acid distribution
  • seed nitrogen
  • seed storage nitrogen
  • Arabidopsis
  • amino acid transporter

1. Introduction

Plants take up organic nitrogen in the form of amino acids and peptides. However, the predominant forms of nitrogen taken up by plants are nitrate (NO3−) and ammonium (NH4+). Nitrogen, taken up as nitrate or ammonium, is assimilated into amino acids glutamine or glutamate [1]. When nitrogen is taken up as nitrate, it is reduced to ammonium before being assimilated into amino acids. Assimilated nitrogen travels as amino acids from the source to sink tissues.

The movement of amino acids from sources and sinks requires them to cross cellular and organelle membranes such as plasma membrane, chloroplast membrane, mitochondrial membrane, tonoplast membrane, and peroxisome membrane. Amino acids do not cross membranes through passive diffusion. When crossing a membrane, they require facilitated or active transport by membrane transporter proteins. These transporter proteins are known as amino acid transporters. Higher plants, or angiosperms, are complex organisms that have specialized organs and tissues for the uptake, transport, and storage of amino acids. This complex arrangement of sources and sink tissues requires a complex transport system involving amino acid export, import, antiport, or homeostasis mechanisms.

Additionally, amino acid transporters exhibit a preference for some amino acids over others. We explain this preference with terminologies such as “substrate affinity” and “substrate specificity.” Amino acids of various charges and sizes such as acidic, basic, small neutral, or large neutral may require amino acid transporters with substrate affinity and substrate specificity for each kind to transport them across membranes. There are 20 common amino acids that are found in both plants and animals. These amino acids mainly function as building blocks for protein synthesis. In addition to the 20 common amino acids, plants produce several other nonproteinogenic amino acids for specialized functions.

The complexity of the amino acid transport process and the diversity in the types of amino acids require plants to have many amino acid transporters. Table 1 shows the number of annotated amino acid transporters identified to date in selected monocot and dicot plant species that are fully sequenced. These numbers continue to evolve as more plant genomes are sequenced and the tools for phylogenetic analysis of gene sequences advance.

Plant speciesTotal number of annotated amino acid transportersReference(s)
Arabidopsis thaliana85–100[2, 3]
Wheat (Triticum aestivum)283[4]
Rice (Oryza sativa L.)85[5]
Soybean (Glycine max)189[6]
Tomato (Solanum lycopersicum)88[7]
Potato (Solanum tuberosum L)72[8]

Table 1.

Annotated amino acid transporters in Arabidopsis thaliana and selected crop species.

Arabidopsis thaliana, a dicotyledonous model plant species, has 85 to over 100 putative amino acid transporters [2, 3]. While these transporters facilitate the movement of amino acids through membranes, they also regulate the distribution of amino acids and, thus the partitioning of amino nitrogen. Understanding the distribution of amino acids in plants requires understanding the organ and tissue-specific distribution of amino acid transporters with their substrate affinity, substrate specificity, and transport mechanism. With advancements in plant biology research, we understand the amino acid distribution route in theory, although many of the necessary amino acid transporters in this route are obscure. This chapter focused on the amino nitrogen translocation and distribution in Arabidopsis thaliana with a specific focus on amino acid translocation to seeds and specifies the amino acid transporters in this route that are functionally characterized to date.

Amino acids have diverse functions in plants beyond their role in protein synthesis, such as signaling molecules, osmolytes, antioxidants, precursors for secondary metabolites, and regulators of gene expression. This chapter will discuss translocation, storage, and distribution of amino acids in seeds regardless of the specific functions these amino acids may conduct. The number and classification of amino acid transporters in plants continue to evolve as genome sequencing and annotation technologies advance, and as new research is conducted in this area. The scope of this chapter is limited to the functionally characterized or annotated amino acid transporters to date.

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2. Source and sink tissues for amino acids in Arabidopsis thaliana

2.1 Amino acid sources and sinks in the whole plant

It is hard to distinguish organs or tissues as the sole source or sink of amino acids. Most tissues participate in both import and export of amino acids throughout their developmental stages. We call the tissues or organs that play as net exporters of amino acids “source tissues” and the tissues or organs that play as net importers of amino acids “sink tissues.” In general, photosynthetically active green tissues are sources of amino acids. Amino acids are produced primarily in photosynthetically active leaves and, to a lesser extent, in other green tissues such as stems and flowers, and in roots. Senescing leaves do not produce amino acids, but as they die and decay, they recycle the cellular components and become a source of amino acids. Once amino acids are synthesized or recycled in the source tissues, they are transported to various parts of the plant where they are needed. Sink tissues in plants include actively growing tissues such as shoot and root apex, developing seeds, and fruits. These tissues have a high demand for amino acids for protein synthesis and other metabolic processes, seeds being the final sink that stores amino acids as a storage protein.

2.2 Amino acid sources for seeds

At the postfertilization stage in Arabidopsis, green carpel cells in the fruit develop distinctive features with well-defined stomata in the epidermal cells for gas exchange and three layers of mesophyll tissue with photosynthetic capacity [9]. Due to the profusion of open stomata in green fruits, the transpiration pull of xylem sap can deliver amino acids from roots, green leaves, or senescing leaves to the green carpel cells. Fruit carpel cells, therefore, may play an important role in seed nutrition. However, as the stream of the xylem sap is stronger toward the leaves due to the higher rate of transpiration in the leaves, amino acids loaded in the xylem from the root are translocated predominantly to the leaves, where they are temporarily stored or metabolized before being transported to the seeds [10]. Green leaves and roots serve as sources of amino acids for seeds during the early reproductive stages. However, most species, including Arabidopsis, accumulates seed storage compounds concomitantly with the acquisition of dormancy and desiccation tolerance [11]. During this stage, recycled amino acids in leaves derived from photorespiration and leaf senescence feed the reproductive sink tissues [12]. During seed maturation, up to 80 per cent of seed amino acids may come from leaves, especially from the senescing leaves [13, 14].

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3. Amino acid transporters in Arabidopsis siliques and seeds

The most recent report suggests that there are more than 100 annotated amino acid transporters in Arabidopsis thaliana (Table 1), although the number varies in other published reports [3]. Based on expression analysis, 22 of these amino acid transporters are expressed in siliques and seeds (Table 2). These transporters mostly belong to the cationic amino acid transporter (CAT) family, and usually multiple amino acids move in and out transporter (UMAMIT) family, followed by the amino acid permease (AAP) family. Acquisition of amino acids in seeds can be influenced by any amino acid transporter expressed in the source and sink tissues or along the vascular transport path. However, the CAT, UMAMIT, and AAP families, with notable members expressed in seeds and siliques, appear to have significant importance in amino acid transport to seeds. There was a gap in understanding the amino acid export process in plants until the recent identification of the UMAMIT family. Members of this family are capable of both importing and exporting amino acids and are localized in both plasma and organelle membranes [22, 23, 24].

Name(s)Gene ID/LocusTransporter familyTissue expressionSubcellular localizationPossible transport type
AAP1/NAT2AT1G58360AAPSiliquesPMIm
AAP2AT5G09220AAPSiliques–Im
AAP5AT1G44100AAPSiliques–Im
AAP8AT1G10010AAPSilique and seedPMIm
BAT1/GABPAT2G01170ACTSiliqueMMEx/Im
CAT1AT4G21120CATSiliquePMIm
CAT2AT1G58030CATSiliqueTM–
CAT3AT5G36940CATSiliqueERIm
CAT4AT3G03720CATSiliqueTM–
CAT5AT2G34960CATSiliquePMIm
CAT6AT5G04770CATSilique and seedPMIm
CAT8AT1G17120CATSiliqueTM and PMIm
LAT4/PUT2/PAR1AT1G31830PHS/LATSilique and seedGAEx/Im
LAT5AT3G19553PHS/LATSiliqueEREx/Im
LHT1AT5G40780LHTSiliquePMIm
UMAMIT11At2g40900UMAMITSiliquePMEx/Im
UMAMIT14At2g39510UMAMITSiliquePMEx/Im
UMAMIT18/SIAR1At1g44800UMAMITSiliquePMEx/Im
UMAMIT24At1g25270UMAMITSeed (coat)TMEx/Im
UMAMIT25At1g09380UMAMITSeed (endosperm)PMEx/Im
UMAMIT28At1g01070UMAMITSilique (mature)PMEx/Im
UMAMIT29At4g01430UMAMITSilique (young)PMEx/Im

Table 2.

Annotated amino acid transporters expressed in Arabidopsis siliques and seeds. The transporters listed in this table may also express in other organs and tissues.

AAP, amino acid permease; LHT, lysine histidine transporter; CAT, cationic amino acid transporter; ACT, amino acid choline transporter; PHS, polyamine H + —symporters; LAT, L-type amino acid transporter; UMAMIT, usually multiple amino acids move in and out transporter; PM, plasma membrane; ER, endoplasmic reticulum; GA, Golgi apparatus; MM, mitochondrion membrane; TM, tonoplast membrane; –, unknown; Ex, export; Im, import.

Source: [3, 15, 16, 17, 18, 19, 20, 21] and references therein.

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4. Amino acid mobilization to seeds

Mobilization of amino acids from source tissues to sink tissues involves two steps: intracellular movement through organelle membranes and cell-to-cell or long-distance movement through plasma membrane.

4.1 Intracellular movement of amino acids through organelle membrane

4.1.1 Chloroplast

Primary assimilation of inorganic nitrogen and reassimilation of recycled nitrogen into amino acids occur through a series of chemical reactions taking place in both cytosol and plastid or chloroplast [25, 26]. During primary assimilation, NO3− taken up by plants is transported to plastids or chloroplast where it is reduced to NH4+ and subsequently assimilated into glutamine via glutamate. Reassimilation of recycled NH4+, derived from photorespiration or protein hydrolysis, also occurs in the chloroplast [25, 26]. During photorespiration in C3 plants, such as Arabidopsis, the 2-carbon compound produced through the oxygenase activity of Rubisco needs to be converted to a 3-carbon compound so that the photosynthetically fixed carbon can be rescued and fed back into the Calvin cycle (Figure 1). This occurs through a complex series of biochemical reactions taking place in the chloroplast, peroxisome, and mitochondria. The 2-carbon compound (2-phosphoglycolate) finally leads to the formation of glycine and a 3-carbon compound (3-phosphoglycerate) [27, 28]. During this process, both nitrogen and carbon are released in the forms of NH3 and CO2 in the mitochondria. This photorespiratory NH3 is recaptured by the GS2/Fdx-GOGAT pathway in the chloroplast. Thus, chloroplasts/plastids are vital organelles for nitrogen assimilation and remobilization [29, 30]. Nitrogen, stored in the forms of storage proteins, peptides, or amino acids, is mobilized primarily in the form of amino acids. Most amino acids required for protein synthesis are produced in the chloroplast/plastid. Plants follow a basipetal growth pattern, where developing tissues depend on mature tissues for the supply of amino acids for protein synthesis. Amino acids, synthesized in the chloroplast/plastid in mature cells, are subject to both intracellular and long-distance transport. Amino acids biosynthesized in the chloroplast/plastid cannot cross the inner and outer membrane without a membrane transporter or a channel protein. Plants thus need both amino acid export- and import systems in the inner and outer membranes of chloroplast. In the outer membrane of the chloroplast, Outer Envelope Protein 16 and 24 (OEP16 & 24) facilitate amino acid transport. In Arabidopsis, several OEP16- and OEP24-family genes have been identified that may mediate amino acid transport through the outer membrane of the chloroplast/plastid [30, 31, 32]. Microarray analysis and in silico subcellular localization analysis have identified putative amino acid transporters that may be localized in the inner chloroplast membrane [33, 34]. A Glutamate/Malate antiporter (DiT2 coupled with DiT1) in the inner chloroplast membrane mediates glutamate export from the stroma in exchange for malate (Figure 1) [35, 36, 37]. Not many amino acid transporters, with a net export capacity, in the inner chloroplast membrane are known to date.

Figure 1.

A simplified model of intracellular amino acid transport shows the movement of amino acids in- and out of membrane-bound organelles in a plant cell. Based on the available information to date, amino acid transporters yet to be identified have been indicated with a ‘?’ mark within a circle. Nitrogen metabolism in chloroplast and plastid has been shown together in the same organelle. AA, amino acid; GS, glutamine synthetase; GOGAT, glutamate synthase; IM, inner membrane; OM, outer membrane; PM, plasma membrane. Primary assimilation of nitrate (NO3-) takes place in the chloroplast or plastid. Amino acids derived from the primary assimilation of nitrogen that occurs through cytosolic GS/GOGAT are imported into the chloroplast or plastid for the biosynthesis of other amino acids. All amino acids synthesized in the chloroplast or plastid are exported into the cytosol for cellular use or translocation. Channel proteins OEP16 & 24 in the outer envelope mediate amino acid transport. In the inner membrane, glutamate/malate antiporter (DiT2) mediates glutamate export. No other amino acid transporters are known to mediate amino acid import or export through the inner membrane. Amino acids derived from protein hydrolysis are catabolized in the mitochondria. Reserve nitrogen enters uni-directionally into the mitochondria to be catabolized during seed germination. During photorespiration, glycine produced in the peroxisome enters mitochondria where it is converted to serine and exported back to peroxisome. In the outer envelope, porins mediate amino acid transport. In the inner membrane arginine/ornithine antiporter (BAC1, 2) and a bi-directional transporter (GABP) are known so far. In the tonoplast, temporary storage of amino acids and subsequent release requires amino acid transporters with both export and import capacity. Arabidopsis CAT2, 4, & 8, LHT4, AVT3, UMAMIT15 & 24 are localized in the tonoplast membrane and may function as vacuolar amino acid transporters. Three peptide transporters (PTR2, 4, 6) are also localized in the tonoplast membrane with unknown transport direction.

4.1.2 Mitochondria

Plant mitochondria are also important in intracellular nitrogen metabolism, including the synthesis and catabolism of amino acids [38, 39]. Mitochondria, together with chloroplasts and peroxisomes, manage both photorespiration and photosynthesis along with many other metabolic pathways [40]. Mitochondria also play an important role in the remobilization of storage nitrogen during seed germination [41]. Characterization of transporter proteins involved in the transport of nitrogen compounds in the inner and outer mitochondrial membrane will contribute to a better understanding of the role of mitochondria in nitrogen metabolism and distribution. More than 50 genes in Arabidopsis have been annotated to encode mitochondrial carrier proteins, and several proteins have been speculated to encode amino acid transporters and localized in the inner and outer envelope of mitochondria [41, 42, 43]. In the inner mitochondrial membrane, two basic amino acid carriers, BAC1 and BAC2, have been experimentally shown to be involved in amino acid transport [44, 45]. These carrier proteins mediate arginine/ornithine (or Citrulline) antiport in the inner mitochondrial membrane (Figure 1). To exchange glycine and serine with the peroxisome during photorespiration, there might be an exchanger or a glycine/serine antiporter in the inner mitochondrial membrane that is yet to be identified. A report has shown that the GABP (also known as BAT1) in Arabidopsis is localized in the mitochondrial membrane [46]. The transporter mediates both the import and export of amino acids, suggesting that it might be a bi-directional facilitator [21]. The outer membrane of mitochondria is permeable to solutes up to a size of 4–5 kDa through porins [47]. The average size of an amino acid is much smaller than 5 kDa. The mitochondrial porins in the outer membrane, also called VDAC (Voltage Dependent Anion Channels), that were characterized as relatively nonspecific general diffusion pores may mediate amino acid transport through the outer envelope [48]. Movement of amino acids through porins in the outer envelope of mitochondria has yet to be studied in plants.

4.1.3 Tonoplast

Amino acids are temporarily stored in the vacuole and subsequently released into the cytoplasm. This process requires amino acid transporters in the tonoplast membrane with export and import capacity. The Arabidopsis CAT2, 4, & 8, LHT4, AVT3, UMAMIT15 & 24 are localized to the tonoplast membrane and may function as vacuolar amino acid transporters (reviewed in [3, 15]). Arabidopsis PTR2, 4, & 6, members of the PTR/NRT1 family, were shown to be localized in the tonoplast membrane and are candidates to mediate peptide transport in and out of the tonoplast [49].

4.2 Amino acid translocation from source tissues to seeds

4.2.1 Loading amino acids from leaf mesophyll cells into the phloem minor vein

Regardless of the source, amino acids travel to seeds via both xylem and phloem but are delivered into seed sink tissues via phloem minor veins [50, 51]. Loading amino acids from leaf mesophyll cells into the phloem minor vein may occur both symplastically and apoplastically. While symplastic loading via the plasmodesmata can be rate-limiting [52], it is improbable in some species since the solute concentration in sieve elements and companion cells in the phloem can be much greater than those in the surrounding source cells. High solute concentration enables the hydrostatic pressure in the phloem that drives long-distance transport of solutes [52, 53, 54, 55]. Thus, in many species including Arabidopsis, loading assimilates into the phloem occurs apoplastically [52, 56]. In the apoplastic loading, amino acids are exported from mesophyll cells into the apoplasm, followed by active uptake into the sieve element-companion cell complex of the phloem [52, 57, 58, 59, 60]. While amino acid exporters in leaf mesophyll cell plasma membrane are obscure, published reports suggest that Arabidopsis AAP2, 5, & 8, CAT6 & 9, ProT1, and LAT5 are either expressed in the phloem or demonstrated to have a role in phloem loading [16, 19, 51, 61, 62, 63, 64, 65, 66]. The LAT4 is expressed in green carpel cells in the silique with a possible role in mobilizing amino acids from these tissues toward seeds [20]. The recently identified UMAMIT facilitators (UMAMIT 14, 18, 28, &29) that are expressed in phloem may also have a role in phloem loading and unloading [15, 22]. Figure 2 shows the possible role of the amino acid transporters characterized to date.

Figure 2.

A simplified model of amino acid transport from source to sink tissues in Arabidopsis thaliana. The dark circles show the positions of one or more amino acid transporters involved in the route with import, export, or bi-directional facilitator capacity. This figure represents the plasma membrane crossing between symplasm and apoplasm for amino acid translocation from source tissues to the seed embryo. The orange arrows indicate directions of amino acid transport. Transporters for other forms of nitrogen are not shown in this figure.

4.2.2 Phloem-xylem-phloem exchange

Amino acids, loaded into the phloem from source tissues in the leaf, may undergo transfer from phloem to xylem for upward translocation. The importance of this phloem-xylem exchange for amino acid distribution within plants has been demonstrated in several physiological studies [67, 68, 69]. However, at the end of the long-distance transport through the xylem, amino acids are loaded back to the phloem because in Arabidopsis, amino acids are delivered to seeds via the phloem [52]. Exchanges of amino acids from phloem to xylem or xylem to phloem are an exchange between symplasm and apoplasm, and thus require amino acid transporters in the plasma membrane of phloem companion cells with a net export or import capacity. In Arabidopsis, CAT1, 6, & 9, AAP2, 3, 5, 6, & 8, ProT1, UMAMIT14, 18, 28, 29 are either expressed in the vascular tissues or demonstrated to have a role in phloem-xylem-phloem exchange of amino acids. For example, the expression of the AAP2 [51, 70] along the vascular transport strand in the stem indicated its involvement in active exchange of amino acids between the xylem and phloem. The AAP2 is expressed in the phloem in the stem, and in funiculi in the silique [70]. It is an import transporter and, therefore, plays a potential role in xylem-to-phloem loading and delivering amino acids to the seed [51]. The AAP6 is expressed in the xylem parenchyma, mediating amino acid import in heterologous system [17]. An in-planta study showed that knocking out the AAP6 reduces total amino acid concentration in the phloem suggesting an indirect role in loading amino acids into the phloem [71].

4.2.3 Loading into the seeds

In Arabidopsis siliques, phloem terminates at the funiculus, and the seed outer integument cells work as a symplastic extension of the funicular phloem [72]. However, transferring amino acids from the outer integument to the inner integument, from the inner integument to the embryo, and from the embryo to the endosperm, may be apoplastic. The seed embryo is separated from the mother plant phloem by three apoplastic borders that require amino acid transporters with export and import capacity at each border to transfer amino acids from the funicular phloem into the embryo [72]. The recently identified UMAMIT 11, 14, 28, & 29 are expressed in siliques in tissues adjacent to phloem from which amino acids are usually exported. Knocking out these genes results in accumulating free amino acids in fruits and producing smaller seeds. These plasma membrane-localized facilitators are a good candidate to facilitate amino acid export and import in seeds [3, 15, 22]. The UMAMIT24 is expressed in the chalazal seed coat but is localized in the tonoplast membrane [23]. Its direct role is likely in the intracellular movement of amino acids. The UMAMIT25 is a plasma membrane-localized transporter expressed in the seed endosperm suggesting a possible role in amino acid transfer between embryo and endosperm [23]. The AAP8 plays a role in importing amino acids into the endosperm and supplying the developing embryo with amino acids during early embryogenesis [73]. The Arabidopsis AAP1 is expressed in the developing embryo during embryo morphogenesis and early maturation in the filial tissues and plays a role in importing amino acids into the embryo [70, 74, 75, 76]. Knocking out the AAP1 gene caused amino acids to accumulate in the seed coat/endosperm [76]. The CAT6 is expressed in the seed with a possible role in amino acid distribution within the seed [64]. The LAT5 is expressed in phloem and in siliques, and it possibly has a bi-directional amino acid transport capacity. However, knocking out this transporter caused increased nitrogen content in seeds [19]. It probably plays a role in amino acid homeostasis rather than importing amino acids into seeds. In Arabidopsis, the endosperm degenerates during early seed maturation, and the embryo becomes the final sink of storage protein, while in other species, the endosperm serves as the source of nutrients during seed germination [77]. Regardless, the transfer of amino acids from the endosperm into the embryo is important in terms of seed protein content and yield achievement. Identification of amino acid transporter with net export capacity in the inner and outer integument cells will allow a clearer understanding of amino acid distribution mechanism during seed maturity.

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5. Conclusion

Crop improvement research strives to understand the amino nitrogen (i.e., amino acids) distribution process in plants primarily to improve crops’ nitrogen use efficiency and grain nutritional quality by improving the protein content in seeds. With advancements in plant science research, we understand the amino acid distribution route in theory but many of the necessary amino acid transporters that enable this route are still unknown. Identification and characterization of amino acid transporters in plants have advanced significantly in the recent decade, although many more are still unknown. In Arabidopsis, there are at least 100 annotated amino acid transporters, with more than 20 expressed in the seeds and siliques alone. This suggests a robust and complex process regulating plant amino acid distribution and protein storage in seeds. The process is further nuanced at various developmental stages or as plants respond to biotic and abiotic factors. We need to understand the organ and tissue-specific distribution of all amino acid transporters, their substrate affinity, and transport mechanism to understand the source-sink distribution of amino acids in plants fully.

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Acknowledgments

We are thankful to the reviewers, the editors, and the editorial office for their technical and scientific support in compiling this chapter.

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Written By

Rowshon A. Begam and Michael Deyholos

Submitted: 11 June 2023 Reviewed: 08 July 2023 Published: 09 August 2023

© The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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