The Arabidopsis ATP-binding Cassette Protein AtMRP5/AtABCC5 Is a High Affinity Inositol Hexakisphosphate Transporter Involved in Guard Cell Signaling and Phytate Storage

• Published in: The Journal of biological chemistry 2009-11, Vol.284 (48), p.33614-33622
• Main Authors: Nagy, Réka, Grob, Hanne, Weder, Barbara, Green, Porntip, Klein, Markus, Frelet-Barrand, Annie, Schjoerring, Jan K., Brearley, Charles, Martinoia, Enrico
• Format: Article
• Language: English
• Subjects: Adenylyl Imidodiphosphate - pharmacology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biological Transport - drug effects; Genetic Complementation Test; Green Fluorescent Proteins - genetics; Green Fluorescent Proteins - metabolism; Inositol Phosphates - metabolism; Membrane Transport, Structure, Function, and Biogenesis; Microscopy, Confocal; Microsomes - drug effects; Microsomes - metabolism; Multidrug Resistance-Associated Proteins - genetics; Multidrug Resistance-Associated Proteins - metabolism; Mutation; Phosphorus - metabolism; Phytic Acid - metabolism; Plant Epidermis - cytology; Plant Epidermis - drug effects; Plant Epidermis - metabolism; Plant Stomata - physiology; Plants, Genetically Modified; Seeds - genetics; Seeds - metabolism; Signal Transduction - physiology; Yeasts - genetics; Yeasts - metabolism
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1074/jbc.M109.030247

Arabidopsis possesses a superfamily of ATP-binding cassette (ABC) transporters. Among these, the multidrug resistance-associated protein AtMRP5/AtABCC5 regulates stomatal aperture and controls plasma membrane anion channels of guard cells. Remarkably, despite the prominent role of AtMRP5 in conferring partial drought insensitivity upon Arabidopsis, we know little of the biochemical function of AtMRP5. Our phylogenetic analysis showed that AtMRP5 is closely related to maize MRP4, mutation of which confers a low inositol hexakisphosphate kernel phenotype. We now show that insertion mutants of AtMRP5 display a low inositol hexakisphosphate phenotype in seed tissue and that this phenotype is associated with alterations of mineral cation and phosphate status. By heterologous expression in yeast, we demonstrate that AtMRP5 encodes a specific and high affinity ATP-dependent inositol hexakisphosphate transporter that is sensitive to inhibitors of ABC transporters. Moreover, complementation of the mrp5-1 insertion mutants of Arabidopsis with the AtMRP5 cDNA driven from a guard cell-specific promoter restores the sensitivity of the mutant to abscisic acid-mediated inhibition of stomatal opening. Additionally, we show that mutation of residues of the Walker B motif prevents restoring the multiple phenotypes associated with mrp5-1. Our findings highlight a novel function of plant ABC transporters that may be relevant to other kingdoms. They also extend the signaling repertoire of this ubiquitous inositol polyphosphate signaling molecule.