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Vacuolar Transport of Nicotine Is Mediated by a Multidrug and Toxic Compound Extrusion (MATE) Transporter in Nicotiana Tabacum

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Vacuolar Transport of Nicotine Is Mediated by a Multidrug and Toxic Compound Extrusion (MATE) Transporter in Nicotiana Tabacum Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum Masahiko Moritaa,1, Nobukazu Shitana,1, Keisuke Sawadab, Marc C. E. Van Montaguc,2, Dirk Inze´ c, Heiko Rischerd, Alain Goossensc, Kirsi-Marja Oksman-Caldenteyd, Yoshinori Moriyamab, and Kazufumi Yazakia,2, aLaboratory of Plant Gene Expression, Research Institute for Sustainable Humanosphere, Kyoto University, Gokasho, Uji 611-0011, Japan; bLaboratory of Membrane Biochemistry, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama 700-8530, Japan; cDepartment of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium; and dVTT Technical Research Centre of Finland, Tietotie 2, FIN-02044 VTT, Espoo, Finland Contributed by Marc C. E. Van Montagu, December 12, 2008 (sent for review July 16, 2008) Alkaloids play a key role in plant defense mechanisms against root cells is exported to the apoplast by a plasma membrane- pathogens and herbivores, but the plants themselves need to cope localized transporter, mainly to the xylem. Second, after the with their toxicity as well. The major alkaloid of the Nicotiana movement to the aerial tissues, nicotine is taken up at the plasma species, nicotine, is translocated via xylem transport from the root membrane of leaf cells, and finally transported to the vacuolar tissues where it is biosynthesized to the accumulation sites, the lumen by a tonoplast-localized transporter. However, none of vacuoles of leaves. To unravel the molecular mechanisms behind these transporters has been identified yet. To discover the this membrane transport, we characterized one transporter, the transporter(s) and proteins involved in nicotine accumulation in tobacco (Nicotiana tabacum) jasmonate-inducible alkaloid trans- Nicotiana species, a cDNA-amplified fragment length polymor- porter 1 (Nt-JAT1), whose expression was coregulated with that of phism-based transcript profiling (cDNA-AFLP) had been car- nicotine biosynthetic genes in methyl jasmonate-treated tobacco ried out previously with Bright Yellow-2 (BY-2) cells elicited cells. Nt-JAT1, belonging to the family of multidrug and toxic with methyl jasmonate (MeJA). In such elicited BY-2 cells, the compound extrusion transporters, was expressed in roots, stems, production of nicotine biosynthetic enzymes is induced and a PLANT BIOLOGY and leaves, and localized in the tonoplast of leaf cells. When multidrug and toxic compound extrusion (MATE)-type trans- produced in yeast cells, Nt-JAT1 occurred mainly in the plasma porter gene has been identified that was highly up-regulated in membrane and showed nicotine efflux activity. Biochemical anal- a coordinate manner with these biosynthetic genes (5). ysis with proteoliposomes reconstituted with purified Nt-JAT1 and Here, we characterized this MATE transporter, designated as bacterial F0F1-ATPase revealed that Nt-JAT1 functioned as a proton Nicotiana tabacum jasmonate-inducible alkaloid transporter 1 antiporter and recognized endogenous tobacco alkaloids, such as (Nt-JAT1), as a nicotine transporter. Membrane separation and nicotine and anabasine, and other alkaloids, such as hyoscyamine protein gel blot analysis indicated that Nt-JAT1 localized to the and berberine, but not flavonoids. These findings strongly suggest tonoplast in tobacco leaf cells. In Nt-JAT1-expressing yeast that Nt-JAT1 plays an important role in the nicotine translocation (Saccharomyces cerevisae) cells, the nicotine transport activity by acting as a secondary transporter responsible for unloading of increased. Analysis of the driving force in proteoliposomes alkaloids in the aerial parts and deposition in the vacuoles. revealed a proton antiport activity and specificity restricted to organic cations, such as the tobacco alkaloids. These data nicotine ͉ vacuole suggest that Nt-JAT1 is involved in the vacuolar accumulation of nicotine in tobacco plants, at least in the aerial parts. ne of the largest groups of plant secondary metabolites Results Ocomprises the alkaloids of which many exhibit strong biological activities. In most cases, after their biosynthesis, Cloning and Sequence Analysis of Nt-JAT1. In intact plants and also alkaloids are deposited in the central vacuoles of alkaloid- in cultivated BY-2 cells, treatment with MeJA strongly induces producing plants, sometimes after translocation from the organ the biosynthesis of nicotine. Previously, a transcriptome analysis where they are produced to another organ where they prefer- with cDNA-AFLP of MeJA-elicited tobacco BY-2 cells identi- entially accumulate. However, only few transporters responsible fied a number of nicotine biosynthetic genes, such as arginine for alkaloids or other secondary metabolites have been reported decarboxylase, ornithine decarboxylase, aspartate oxidase, and so far (1, 2), and no protein involved in vacuolar alkaloid quinolinate phosphoribosyltransferase (5). Simultaneously, sev- accumulation has been identified yet. eral MeJA-inducible genes encoding putative transporter pro- Nicotine, a pyridine alkaloid predominantly found in Nicoti- teins were found, among which a MATE transporter (clone No. ana species, functions as a defensive toxin by acting on the T401) that nicely coregulated with these nicotine biosynthetic nervous system of herbivores and is produced in root tissues, where its biosynthesis increases specifically in response to attacks Author contributions: M.C.E.V.M., D.I., A.G., K.-M.O.-C., Y.M., and K.Y. designed research; by pathogens, herbivores, or wounding, usually incurring jas- M.M., N.S., K.S., and A.G. performed research; M.M., N.S., H.R., A.G., and K.Y. analyzed monate signaling. The produced nicotine is then translocated to data; and N.S., A.G., and K.Y. wrote the paper. the aerial parts of the plant and finally accumulates in the central The authors declare no conflict of interest. vacuoles of the leaves (3). Accordingly, putrescine N- Data deposition: The sequences reported in this paper have been deposited in the GenBank methyltransferase (PMT), the enzyme catalyzing the first com- database [accession nos. AM991692 (Nt-JAT1) and AM991691 (ST30)]. mitted step in nicotine biosynthesis, is specifically produced in 1M.M. and N.S. contributed equally to this work. the root pericycle, and not in the aerial parts (3). After nicotine 2To whom correspondence may be addressed. E-mail: [email protected] or is loaded into the xylem tissue, it is delivered at the leaf [email protected]. mesophyll cells and finally is deposited in the vacuoles (4). This This article contains supporting information online at www.pnas.org/cgi/content/full/ translocation process implies the transport of nicotine across at 0812512106/DCSupplemental. least 3 different membranes. First, the nicotine produced in the © 2009 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0812512106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 25, 2021 A A 3 MeJA DMSO NAA Cont IAA BA ABA GA BL MeJA SA SC Cold Dark Dry 0 1 2 4 6 8 12 24 0 4 8 12 24 C330=AP2-domain transcription factor NtJAP1 2 kb C308=Ornithine decarboxylase Nt-JAT1 MAP3=AP2-domain transcription factor NTORC1 C228=Arginine decarboxylase C309=S-adenosyl-L-methionine synthetase C215=Putative MATE transporter rRNA T449=Putative MATE transporter T142=L-aspartate oxidase-like protein C47=Quinolinate phosphoribosyltransferase T401=Putative MATE transporter (Nt-JAT1) B B 500 PMT Leaf Stem Root 400 Nt-JAT1 2 kb 300 200 rRNA 100 0 Fig. 2. Expression of Nt-JAT1 in tobacco plants. (A) Nt-JAT1 expression in Relative expression (PMT/RNA-helicase) Cont0 Cont24 MeJA24 response to various treatments. Fourteen-day-old seedlings were treated for 24 h with 10 ␮M 1-naphthaleneacetic acid (NAA), 10 ␮M IAA, 10 ␮M 6-ben- zyladenine (BA), 10 ␮M abscisic acid (ABA), 10 ␮M gibberellic acid (GA3), 5 ␮M 20 brassinolide (BL), 100 ␮M MeJA, 100 ␮M salicylic acid (SA), 100 ␮M sclareol (SC), Nt-JAT1 at 4 °C (cold)/low light, dark (dark), and drought (dry). Cont., untreated 16 control. Total RNA (7.5 ␮g) prepared from aerial parts of seedlings was probed with a 32P-labeled Nt-JAT1 fragment (top). Loading controls are shown by 12 EtBr-stained 18S rRNA (bottom). (B) Organ-specific expression of Nt-JAT1 in tobacco. Total RNA (7.5 ␮g) prepared from tobacco organs was probed with 8 32P-labeled Nt-JAT1 fragment (0.5 kb) (top). The amount of total RNA applied to each lane is shown by EtBr-stained 18S rRNA (bottom). 4 0 We isolated the full-length cDNA of Nt-JAT1 from tobacco Relative expression (JAT1/RNA-helicase) Cont0 Cont24 MeJA24 BY-2 cells by RT-PCR and 5Ј- and 3Ј-RACE. Nt-JAT1 was approximately 1.8 kb long and encoded a putative polypeptide C 0 2 6 12 24 48 72 (h) consisting of 470 amino acids. The TMpred prediction program for transmembrane regions (http://www.ch.embnet.org/software/ 2 kb TMPRED࿝form.html) suggested that the structure of Nt-JAT1 Nt-JAT1 was very similar to that of the human MATE1 with 12 trans- membrane helices. Regarding the phylogenetic relationships to other plant MATE transporters, Nt-JAT1 showed a relatively rRNA high similarity (50% at amino acid level) to DTX1 of Arabidopsis thaliana, that is located in the plasma membrane and has been proposed to mediate the efflux of xenobiotics mostly by a Fig. 1. Isolation of Nt-JAT1 as a MeJA-inducible transporter gene. (A) proton-motive force (supporting information (SI) Fig. S1) (6). Average linkage hierarchical clustering of MeJA-modulated gene tags iden- tified by cDNA-AFLP (5). The time points (h) are indicated at the top. Red boxes Expression Analysis of Nt-JAT1. The response of Nt-JAT1 to various reflect transcriptional activation relative to the average expression level in plant hormones, signaling molecules, and abiotic stresses was control (DMSO) cells. Gray boxes correspond to missing time points. (B) studied in 14-day-old seedlings by using RNA gel blot analysis qRT-PCR of PMT (top) and Nt-JAT1 (bottom) in BY-2 cells treated with MeJA.
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