Abstract
A full-length cDNA sequence putatively encoding an ATP-binding cassette (ABC) transporter (GintABC1) was isolated from the extraradical mycelia of the arbuscular mycorrhizal fungus Glomus intraradices. Bioinformatic analysis of the sequence indicated that GintABC1 encodes a 1513 amino acid polypeptide, containing two six-transmembrane clusters (TMD) intercalated with sequences characteristics of the nucleotide binding domains (NBD) and an extra N-terminus extension (TMD0). GintABC1 presents a predicted TMD0-(TMD-NBD)2 topology, typical of the multidrug resistance-associated protein subfamily of ABC transporters. Gene expression analyses revealed no difference in the expression levels of GintABC1 in the extra- vs the intraradical mycelia. GintABC1 was up-regulated by Cd and Cu, but not by Zn, suggesting that this transporter might be involved in Cu and Cd detoxification. Paraquat, an oxidative agent, also induced the transcription of GintABC1. These data suggest that redox changes may be involved in the transcriptional regulation of GintABC1 by Cd and Cu.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Argüello J, Eren E, González-Guerrero M (2007) The structure and function of heavy metal transport P1B-ATPases. Biometals 20:233–248
Bago B, Pfeffer PE, Douds DD, Brouillette J, Bécard G, Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121:263–271
Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillete J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 3:1496–1507
Benabdellah K, Merlos MA, Azcón-Aguilar C, Ferrol N (2009) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46:94–103
Bock KW, Lilienblum W, Fischer G, Schrimer G, Bock-Henning BS (1987) The role of conjugation reactions in detoxification. Arch Toxicol 60:22–29
Borst P, Evers R, Kool M, Wijnholds J (1999) The multidrug resistance protein family. Biochim Biophys Acta 1461:347–357
Bovet L, Eggmann T, Meylan-Bettex M, Polier J, Kammer P, Marin E, Feller U, Martinoia E (2003) Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ 26:371–381
Chabot S, Bécard G, Piché Y (1992) Life cycle of Glomus intraradix in root organ culture. Mycologia 84:315–321
Chen M, Abele R, Tampe R (2004) Functional non-equivalence of ATP-binding cassette signature motifs in the transporter associated with antigen processing (TAP). J Biol Chem 279:46073–46081
Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007a) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pol 147:374–380
Chen S, Sanchez-Fernandez R, Lyver ER, Dancis A, Rea PA (2007b) Functional characterization of AtATM1, AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated in iron homeostasis. J Biol Chem 282:21561–21571
Cherian GM, Chan HM (1993) Biological functions of metallothioneins—a review. In: Suzuki KT, Imura N, Kimura M (eds) Metallothionein III. Birkhauser, Basel, pp 87–109
Davidson AL, Chen J (2004) ATP-binding cassette transporters in bacteria. Ann Rev Biochem 73:241–268
Del Sorbo G, Schoonbeek H, De Waard MA (2000) Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30:1–15
Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1–3004.10
Eide D (2004) The ABC of solute carriers. The SLC39 family of metal ion transporters. Eur J Phys 447:796–800
Felstein J (1993) PHYLIP, version 3.5. Department of Genetics, University of Washington, USA
Footitt S, Dietrich D, Fait A, Fernie AR, Holdsworth MJ, Baker A, Theodoulou FL (2007) The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis. Plant Physiol 144:1467–1480
Fraústro da Silva JJR, Williams RJP (2001) The biological chemistry of the elements, 2nd edn. Oxford Univesity Press, New York
Gaillard S, Jacquet H, Vavasseur A, Leonhardt N, Forestier C (2008) AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol 8:22
Gerk PM, Li W, Megaraj V, Vore M (2007) Human multidrug resistance protein 2 transports the therapeutic bile salt tauroursodeoxycholate. J Pharmacol Exp Ther 320:893–899
Göhre V, Paszkowski V (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122
González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140
González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335
González-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcón-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54:103–110
González-Guerrero M, Benabdellah K, Azcón-Aguilar C, Ferrol N (2009) Heavy metal tolerance in arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas: functional processes and ecological impact. Springer, Heidelberg, pp 107–122
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146
Hofmann K, Stoffel W (1993) TMbase—a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 347:166
Jungwirth H, Kuchler K (2006) Yeast ABC transporters—a tale of sex, stress, drugs and aging. FEBS Lett 580:1131–1138
Ketchum CJ, Schmidt WK, Rajendrakumar GV, Michaelis S, Maloney PC (2001) The yeast a-factor transporter Ste6p, a member of the ABC superfamily, couples ATP hydrolysis to pheromone export. J Biol Chem 276:29007–29011
Klein M, Martinoia E, Hoffmann-Thoma G, Weissenbock G (2000) A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J 21:289–304
Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153
Li ZS, Szczypka M, Lu YP, Thiele DJ, Rea PA (1996) The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J Biol Chem 271:6509–6517
Li Z, Lu Y, Zhen R, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium. Proc Natl Acad Sci U S A 94:42–47
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Maher JM, Dieter MZ, Aleksunes LM, Slitt AL, Guo G, Tanaka Y, Scheffer GL, Chan JY, Manautou JE, Chen Y, Dalton TP, Yamamoto M, Klaasen CD (2007) Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 46:1597–1610
Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters—more than just detoxifiers. Planta 214:345–355
Mason DL, Michaelis S (2002) Requirement of the N-terminal extension for vacuolar trafficking and transport activity of yeast Ycf1p, an ATP-binding cassette transporter. Mol Biol Cell 13:4443–4455
Meharg AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253–1265
O’Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057–25060
Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728
Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pawlowska TE, Charvat I (2004) Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Rebbeor JF, Connolly GC, Ballatori N (2002) Inhibition of Mrp2- and Ycf1p-mediated transport by reducing agents: evidence for GSH transport on rat Mrp2. Biochim Biophys Acta 1559:171–178
St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332
Szczypka MS, Wemmie JA, Moyerowley WS, Thiele DJ (1994) A yeast metal resistance protein similar to human cystic-fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J Biol Chem 269:22853–22857
Theiss S, Kretschmar M, Nichterlein T, Hof H, Agabian N, Hacker J, Köhler GA (2002) Functional analysis of a vacuolar ABC transporter in wild-type Candida albicans reveals its involvement in virulence. Mol Microbiol 43:571–584
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tommasini R, Vogt E, Fromentau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773–780
van Endert PM, Saveanu L, Hewitt EW, Lehner PJ (2002) Powering the peptide pump: TAP crosstalk with energetic nucleotides. Trends Biochem Sci 27:454–461
Verrier PJ, Bird D, Buria B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159
Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951
Wang TL, Wu M (2006) An ATP-binding cassette transporter related to yeast vacuolar ScYCF1 is important for Cd sequestration in Chlamydomonas reinhardtii. Plant Cell Environ 29:1901–1912
Waschke A, Sieh D, Tamasloukht M, Fischer K, Mann P, Franken P (2006) Identification of heavy metal-induced genes encoding glutathione S-transferases in the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza 17:1–10
Wemmie JA, Szczypka MS, Thiele DJ, Moye-Rowley WS (1994) Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J Biol Chem 269:32592–32597
Yang R, Cui L, Hou YX, Riordan JR, Chang XB (2003) ATP binding to the first nucleotide binding domain of multidrug resistance-associated protein plays a regulatory role at low nucleotide concentration, whereas ATP hydrolysis at the second plays a dominant role in ATP-dependent leukotriene C4 transport. J Biol Chem 278:30764–30771
Zientara K, Wawrzynska A, Lukomska J, Lopez-Moya JR, Liszewska F, Assuncao AGL, Aarts MGM, Sirko A (2009) Activity of the AtMRP3 promoter in transgenic Arabidopsis thaliana and Nicotiana tabacum plants is increased by cadmium, nickel, arsenic, cobalt and lead but not by zinc and iron. J Biotechnol 139:258–263
Acknowledgements
This work was funded by the EU project Genomyca (QLK5-CT-2000-01319) and by a grant from the Consejería de Innovación, Ciencia y Empresa of the Junta de Andalucía, Spain (P06-CVI-02263). Karim Benabdellah was supported by an I3P contract from the Spanish Council for Scientific Research (CSIC).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
González-Guerrero, M., Benabdellah, K., Valderas, A. et al. GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd, and oxidative stress in Glomus intraradices. Mycorrhiza 20, 137–146 (2010). https://doi.org/10.1007/s00572-009-0273-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-009-0273-y