Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum

Masahiko Morita, Nobukazu Shitan, Keisuke Sawada, Marc C.E. Van Montagu, Dirk Inzé, Heiko Rischer, Alain Goossens, Kirsi Marja Oksman-Caldentey, Yoshinori Moriyama, Kazufumi Yazaki

Research output: Contribution to journalArticle

145 Citations (Scopus)

Abstract

Alkaloids play a key role in plant defense mechanisms against pathogens and herbivores, but the plants themselves need to cope with their toxicity as well. The major alkaloid of the Nicotiana species, nicotine, is translocated via xylem transport from the root tissues where it is biosynthesized to the accumulation sites, the vacuoles of leaves. To unravel the molecular mechanisms behind this membrane transport, we characterized one transporter, the tobacco (Nicotiana tabacum) jasmonate-inducible alkaloid transporter 1 (Nt-JAT1), whose expression was coregulated with that of nicotine biosynthetic genes in methyl jasmonate-treated tobacco cells. Nt-JAT1, belonging to the family of multidrug and toxic compound extrusion transporters, was expressed in roots, stems, and leaves, and localized in the tonoplast of leaf cells. When produced in yeast cells, Nt-JAT1 occurred mainly in the plasma membrane and showed nicotine efflux activity. Biochemical analysis with proteoliposomes reconstituted with purified Nt-JAT1 and bacterial F0F1-ATPase revealed that Nt-JAT1 functioned as a proton antiporter and recognized endogenous tobacco alkaloids, such as nicotine and anabasine, and other alkaloids, such as hyoscyamine and berberine, but not flavonoids. These findings strongly suggest that Nt-JAT1 plays an important role in the nicotine translocation by acting as a secondary transporter responsible for unloading of alkaloids in the aerial parts and deposition in the vacuoles.

Original languageEnglish
Pages (from-to)2447-2452
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number7
DOIs
Publication statusPublished - Feb 17 2009
Externally publishedYes

Keywords

  • Nicotine
  • Vacuole

ASJC Scopus subject areas

  • General

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    Morita, M., Shitan, N., Sawada, K., Van Montagu, M. C. E., Inzé, D., Rischer, H., Goossens, A., Oksman-Caldentey, K. M., Moriyama, Y., & Yazaki, K. (2009). Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proceedings of the National Academy of Sciences of the United States of America, 106(7), 2447-2452. https://doi.org/10.1073/pnas.0812512106