• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of plntcellLink to Publisher's site
Plant Cell. Feb 1998; 10(2): 267–282.
PMCID: PMC143980

AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with Atmrp1.

Abstract

Three ATP binding cassette (ABC) transporter-like activities directed toward large amphipathic organic anions have recently been identified on the vacuolar membrane of plant cells. These are the Mg-ATP-energized, vanadate-inhibitable vacuolar accumulation of glutathione S-conjugates (GS conjugates), chlorophyll catabolites, and bile acids, respectively. Although each of these activities previously had been assigned to distinct pumps in native plant membranes, we describe here the molecular cloning, physical mapping, and heterologous expression of a gene, AtMRP2, from Arabidopsis thaliana that encodes a multispecific ABC transporter competent in the transport of both GS conjugates and chlorophyll catabolites. Unlike its isoform, AtMRP1, which transports the model Brassica napus chlorophyll catabolite transporter substrate Bn-NCC-1 at low efficiency, heterologously expressed AtMRP2 has the facility for simultaneous high-efficiency parallel transport of GS conjugates and Bn-NCC-1. The properties of AtMRP2 therefore establish a basis for the manipulation of two previously identified plant ABC transporter activities and provide an explanation for how the comparable transporter in native plant membranes would be systematically mistaken for two distinct transporters. These findings are discussed with respect to the functional organization of AtMRP2, the inability of AtMRP2 and AtMRP1 to transport the model bile acid transporter substrate taurocholate (despite the pronounced sensitivity of both to direct inhibition by this agent), the differential patterns of expression of their genes in the intact plant, and the high capacity of AtMRP2 for the transport of glutathionated herbicides and anthocyanins.

Full Text

The Full Text of this article is available as a PDF (288K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science. 1992 Dec 4;258(5088):1650–1654. [PubMed]
  • Creusot F, Fouilloux E, Dron M, Lafleuriel J, Picard G, Billault A, Le Paslier D, Cohen D, Chabouté ME, Durr A, et al. The CIC library: a large insert YAC library for genome mapping in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):763–770. [PubMed]
  • Davies TG, Theodoulou FL, Hallahan DL, Forde BG. Cloning and characterisation of a novel P-glycoprotein homologue from barley. Gene. 1997 Oct 15;199(1-2):195–202. [PubMed]
  • Dudler R, Hertig C. Structure of an mdr-like gene from Arabidopsis thaliana. Evolutionary implications. J Biol Chem. 1992 Mar 25;267(9):5882–5888. [PubMed]
  • Gietz RD, Schiestl RH. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast. 1991 Apr;7(3):253–263. [PubMed]
  • Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. [PubMed]
  • Hinder B, Schellenberg M, Rodoni S, Ginsburg S, Vogt E, Martinoia E, Matile P, Hörtensteiner S. How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem. 1996 Nov 1;271(44):27233–27236. [PubMed]
  • Höfte H, Desprez T, Amselem J, Chiapello H, Rouzé P, Caboche M, Moisan A, Jourjon MF, Charpenteau JL, Berthomieu P, et al. An inventory of 1152 expressed sequence tags obtained by partial sequencing of cDNAs from Arabidopsis thaliana. Plant J. 1993 Dec;4(6):1051–1061. [PubMed]
  • Hörtensteiner S, Vogt E, Hagenbuch B, Meier PJ, Amrhein N, Martinoia E. Direct energization of bile acid transport into plant vacuoles. J Biol Chem. 1993 Sep 5;268(25):18446–18449. [PubMed]
  • Huber M, Guhlmann A, Jansen PL, Keppler D. Hereditary defect of hepatobiliary cysteinyl leukotriene elimination in mutant rats with defective hepatic anion excretion. Hepatology. 1987 Mar-Apr;7(2):224–228. [PubMed]
  • Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DR, Hubbard RE, Higgins CF. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature. 1990 Jul 26;346(6282):362–365. [PubMed]
  • Ishikawa T, Müller M, Klünemann C, Schaub T, Keppler D. ATP-dependent primary active transport of cysteinyl leukotrienes across liver canalicular membrane. Role of the ATP-dependent transport system for glutathione S-conjugates. J Biol Chem. 1990 Nov 5;265(31):19279–19286. [PubMed]
  • Ishikawa T, Li ZS, Lu YP, Rea PA. The GS-X pump in plant, yeast, and animal cells: structure, function, and gene expression. Biosci Rep. 1997 Apr;17(2):189–207. [PubMed]
  • Jedlitschky G, Leier I, Buchholz U, Barnouin K, Kurz G, Keppler D. Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res. 1996 Mar 1;56(5):988–994. [PubMed]
  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 Feb 12;72(3):427–441. [PubMed]
  • Kim EJ, Zhen RG, Rea PA. Site-directed mutagenesis of vacuolar H(+)-pyrophosphatase. Necessity of Cys634 for inhibition by maleimides but not catalysis. J Biol Chem. 1995 Feb 10;270(6):2630–2635. [PubMed]
  • Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [PubMed]
  • Leier I, Jedlitschky G, Buchholz U, Cole SP, Deeley RG, Keppler D. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem. 1994 Nov 11;269(45):27807–27810. [PubMed]
  • Li ZS, Szczypka M, Lu YP, Thiele DJ, Rea PA. The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J Biol Chem. 1996 Mar 15;271(11):6509–6517. [PubMed]
  • Li ZS, Alfenito M, Rea PA, Walbot V, Dixon RA. Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry. 1997 Jun;45(4):689–693. [PubMed]
  • Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):42–47. [PMC free article] [PubMed]
  • Lu YP, Li ZS, Rea PA. AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8243–8248. [PMC free article] [PubMed]
  • Müller M, Meijer C, Zaman GJ, Borst P, Scheper RJ, Mulder NH, de Vries EG, Jansen PL. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):13033–13037. [PMC free article] [PubMed]
  • Newman T, de Bruijn FJ, Green P, Keegstra K, Kende H, McIntosh L, Ohlrogge J, Raikhel N, Somerville S, Thomashow M, et al. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 1994 Dec;106(4):1241–1255. [PMC free article] [PubMed]
  • Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, Oude Elferink RP. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science. 1996 Feb 23;271(5252):1126–1128. [PubMed]
  • Peterson GL. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem. 1977 Dec;83(2):346–356. [PubMed]
  • Sathirakul K, Suzuki H, Yamada T, Hanano M, Sugiyama Y. Multiple transport systems for organic anions across the bile canalicular membrane. J Pharmacol Exp Ther. 1994 Jan;268(1):65–73. [PubMed]
  • Szczypka MS, Wemmie JA, Moye-Rowley WS, Thiele DJ. A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J Biol Chem. 1994 Sep 9;269(36):22853–22857. [PubMed]
  • Tommasini R, Evers R, Vogt E, Mornet C, Zaman GJ, Schinkel AH, Borst P, Martinoia E. The human multidrug resistance-associated protein functionally complements the yeast cadmium resistance factor 1. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6743–6748. [PMC free article] [PubMed]
  • Tommasini R, Vogt E, Schmid J, Fromentau M, Amrhein N, Martinoia E. Differential expression of genes coding for ABC transporters after treatment of Arabidopsis thaliana with xenobiotics. FEBS Lett. 1997 Jul 14;411(2-3):206–210. [PubMed]
  • Wang W, Takezawa D, Poovaiah BW. A potato cDNA encoding a homologue of mammalian multidrug resistant P-glycoprotein. Plant Mol Biol. 1996 Jun;31(3):683–687. [PubMed]
  • Zhen RG, Kim EJ, Rea PA. Acidic residues necessary for pyrophosphate-energized pumping and inhibition of the vacuolar H+-pyrophosphatase by N,N'-dicyclohexylcarbodiimide. J Biol Chem. 1997 Aug 29;272(35):22340–22348. [PubMed]

Articles from The Plant Cell are provided here courtesy of American Society of Plant Biologists

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Compound
    Compound
    PubChem Compound links
  • Gene
    Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • HomoloGene
    HomoloGene
    HomoloGene links
  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links
  • Taxonomy
    Taxonomy
    Related taxonomy entry
  • Taxonomy Tree
    Taxonomy Tree

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...