Amino Acid Export in Developing Arabidopsis Seeds Depends on UmamiT Facilitators

Abstract

Essential amino acids cannot be synthesized by humans and animals. They often are limiting in plant-derived foods and determine the nutritional value of a given diet. Seeds and fruits often represent the harvestable portion of plants. In order to improve the amino acid composition of these tissues, it is indispensable to understand how these substrates are transported within the plant. Amino acids result from nitrogen assimilation, which often occurs in leaves, the source tissue. They are transported via the vasculature, the xylem, and the phloem into the seeds, the so-called sink tissue, where they are stored or consumed. In seeds, several tissues are symplasmically isolated, i.e., not connected by plasmodesmata, channels in the cell walls that enable a cytoplasmic continuum in plants. Consequently, amino acids must be exported from cells into the apoplast and re-imported many times to support seed development. Several amino acid importers are known, but exporters remained elusive. Here, we characterize four members of the plant-specific UmamiT transporter family from Arabidopsis, related to the amino acid facilitator SIAR1 and the vacuolar auxin transporter WAT1. We show that the proteins transport amino acids along their (electro)chemical potential across the plasma membrane. In seeds, they are found in tissues from which amino acids are exported. Loss-of-function mutants accumulate high levels of free amino acids in fruits and produce smaller seeds. Our results strongly suggest a crucial role for the UmamiTs in amino acid export and possibly a means to improve yield quality.

UMAMIT14 is an amino acid exporter involved in phloem unloading in Arabidopsis roots

“…Increased Gln secretion from cells expressing UMAMIT14 suggested that the protein was endowed with an amino acid exporter activity. This result is in good agreement with Müller et al (2015), who reported an increased export of [ 14 C]Gln from Xenopus oocytes expressing UMAMIT14. We sought to develop a system using 22Δ10α cells that allows facile detection of amino acid export activities.…”

“…UMAMIT14-GFP was almost exclusively localized at the plasma membrane, with some additional fluorescence in intracellular structures (Fig. 3E–H), in good agreement with Müller et al (2015).…”

“…Walls Are Thin1 (WAT1/UMAMIT05) has been shown to be a tonoplastic transporter for auxin, a molecule with a chemical structure similar to Trp (Ranocha et al , 2013). UMAMIT14 has recently been shown to mediate both import and export of amino acids, and to be involved in amino acid loading in seeds (Müller et al , 2015). Here, we report the functional characterization of UMAMIT14 as an amino acid exporter in yeast and its involvement in unloading amino acids from the phloem in roots.…”

PHO1 Exports Phosphate from the Chalazal Seed Coat to the Embryo in Developing Arabidopsis Seeds

“…The expression pattern of PHO1 in the CZSC is similar to the amino acid facilitator UmamiT11 and 14, involved in amino acid export from the seed coat, while UmamiT28 was expressed in the endothelium and cellularized endosperm, and UmamiT29 in the seed coat inner and outer integuments. Interestingly, single mutants in any of these four UmamiT genes resulted in an increase in amino acid content in seeds, indicating that efflux of amino acids in all of these tissues contribute to the seed nitrogen content [6].…”

“…Recently, proteins belonging to the SWEET and UmamiT family of transporters have been implicated in the export of sucrose and amino acids, respectively, out of the seed coat for nutrient transfer to the embryo [5,6]. Similarly, members of the HMA family of heavy metal transporting ATPase have been shown to mediate zinc export out of the seed coat [7].…”