Abstract
Sodium at high millimolar levels in the cytoplasm is toxic to plant and yeast cells. Sequestration of Na(+) ions into the vacuole is one mechanism to confer Na(+)-tolerance on these organisms. In the present study we provide direct evidence that the Arabidopsis thaliana At-NHX1 gene and the yeast NHX1 gene encode low-affinity electroneutral Na(+)/H(+) exchangers. We took advantage of the ability of heterologously expressed At-NHX1 to functionally complement the yeast nhx1-null mutant. Experiments on vacuolar vesicles isolated from yeast expressing At-NHX1 or NHX1 provided direct evidence for pH-gradient-energized Na(+) accumulation into the vacuole. A major difference between NHX1 and At-NHX1 is the presence of a cleavable N-terminal signal peptide (SP) in the former gene. Fusion of the SP to At-NHX1 resulted in an increase in the magnitude of Na(+)/H(+) exchange, indicating a role for the SP in protein targeting or regulation. Another distinguishing feature between the plant and yeast antiporters is their sensitivity to the diuretic compound amiloride. Whereas At-NHX1 was completely inhibited by amiloride, NHX1 activity was reduced by only 20-40%. These results show that yeast as a heterologous expression system provides a convenient model to analyse structural and regulatory features of plant Na(+)/H(+) antiporters.
MeSH Terms
Amiloride/metabolism,pharmacology
Arabidopsis/genetics,metabolism
Arabidopsis Proteins
Carrier Proteins/chemistry,genetics,metabolism
Cation Transport Proteins
Cinnamates
Cloning, Molecular
Conserved Sequence
Diuretics/metabolism,pharmacology
Fungal Proteins/chemistry,genetics,metabolism
Gene Deletion
Genetic Complementation Test
Hydrogen/metabolism
Hydrogen-Ion Concentration
Hygromycin B/analogs & derivatives,pharmacology
Inhibitory Concentration 50
Intracellular Membranes/drug effects,metabolism
Ion Transport/drug effects
Phenotype
Plant Proteins/chemistry,genetics,metabolism
Protein Binding
Protein Sorting Signals/physiology
Protein Structure, Tertiary
Saccharomyces cerevisiae/cytology,genetics,metabolism
Saccharomyces cerevisiae Proteins
Salts/pharmacology
Sodium/metabolism,pharmacology
Sodium-Hydrogen Exchangers/chemistry,genetics,metabolism
Vacuoles/drug effects,metabolism
Chemicals
Arabidopsis Proteins
Carrier Proteins
Cation Transport Proteins
Cinnamates
Diuretics
Fungal Proteins
NHX1 protein, Arabidopsis
NHX1 protein, S cerevisiae
Plant Proteins
Protein Sorting Signals
Saccharomyces cerevisiae Proteins
Salts
Sodium-Hydrogen Exchangers
Hygromycin B
hygromycin A
Amiloride
Hydrogen
Sodium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Darley C P
Department of Developmental Genetics, Vrije Universiteit, BioCentrum Amsterdam, De Boelelaan 1087, Amsterdam, 1081 HV, The Netherlands.
van Wuytswinkel O C
van der Woude K
Mager W H
de Boer A H
References (32)
32 references, click to expand
-
Methods for studying the yeast vacuole.
Methods Enzymol. 1991;194:644-61
PMID: 1706462
-
The yeast endosomal Na+/H+ exchanger, Nhx1, confers osmotolerance following acute hypertonic shock.
Microbiology. 1999 Nov;145 ( Pt 11):3221-8
PMID: 10589731
-
Ion Homeostasis in NaCl Stress Environments.
Plant Physiol. 1995 Nov;109(3):735-742
PMID: 12228628
-
Salt stress induces an increased expression of V-type H(+)-ATPase in mature sugar beet leaves.
Plant Mol Biol. 1996 Nov;32(3):543-7
PMID: 8980504
-
Pleiotropic plasma membrane ATPase mutations of Saccharomyces cerevisiae.
Mol Cell Biol. 1987 Nov;7(11):4082-8
PMID: 2963211
-
Structure function of the growth factor-activatable Na+/H+ exchanger (NHE1).
Rev Physiol Biochem Pharmacol. 1992;119:157-86
PMID: 1318573
-
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
Genetics. 1989 May;122(1):19-27
PMID: 2659436
-
Tonoplast Na+/H+ Antiport Activity and Its Energization by the Vacuolar H+-ATPase in the Halophytic Plant Mesembryanthemum crystallinum L.
Plant Physiol. 1995 Oct;109(2):549-556
PMID: 12228611
-
Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential.
J Biol Chem. 1998 Jun 12;273(24):14838-44
PMID: 9614085
-
Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. Implications for vacuole biogenesis.
J Biol Chem. 1998 Aug 14;273(33):21054-60
PMID: 9694857
-
Active proton uptake in lipid vesicles reconstituted with the purified yeast plasma membrane ATPase. Fluorescence quenching of 9-amino-6-chloro-2-methoxyacridine.
J Biol Chem. 1982 Aug 25;257(16):9365-71
PMID: 6213606
-
Salt tolerance in plants and microorganisms: toxicity targets and defense responses.
Int Rev Cytol. 1996;165:1-52
PMID: 8900956
-
The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast.
Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1480-5
PMID: 9990049
-
Amiloride and its analogs as tools in the study of ion transport.
J Membr Biol. 1988 Oct;105(1):1-21
PMID: 2852254
-
Na/H Antiport in Isolated Tonoplast Vesicles from Storage Tissue of Beta vulgaris.
Plant Physiol. 1985 May;78(1):163-7
PMID: 16664191
-
NaCl Induces a Na/H Antiport in Tonoplast Vesicles from Barley Roots.
Plant Physiol. 1988 Jan;86(1):231-6
PMID: 16665872
-
A general method for polyethylene-glycol-induced genetic transformation of bacteria and yeast.
Gene. 1983 Nov;25(2-3):333-41
PMID: 6363214
-
Properties of enhanced tonoplast zinc transport in naturally selected zinc-tolerant silene vulgaris
Plant Physiol. 1999 Jul;120(3):779-86
PMID: 10398713
-
The capacity to transport potassium influences sodium tolerance in Saccharomyces cerevisiae.
FEMS Microbiol Lett. 1996 Jan 15;135(2-3):157-60
PMID: 8595852
-
Evidence for a selective and electroneutral K+/H(+)-exchange in Saccharomyces cerevisiae using plasma membrane vesicles.
Yeast. 1996 Oct;12(13):1301-13
PMID: 8923735
-
Rapid induction of na/h exchange activity in barley root tonoplast.
Plant Physiol. 1989 Jan;89(1):1-4
PMID: 16666496
-
Properties and physiologic roles of the plasma membrane sodium-hydrogen exchanger.
J Clin Invest. 1986 Oct;78(4):859-64
PMID: 3020091
-
Characterization of the NHA1 gene encoding a Na+/H+-antiporter of the yeast Saccharomyces cerevisiae.
FEBS Lett. 1996 May 27;387(1):89-93
PMID: 8654575
-
A point mutation of the Na+/H+ exchanger gene (NHE1) and amplification of the mutated allele confer amiloride resistance upon chronic acidosis.
Proc Natl Acad Sci U S A. 1993 May 15;90(10):4508-12
PMID: 8389452
-
A knowledge base for predicting protein localization sites in eukaryotic cells.
Genomics. 1992 Dec;14(4):897-911
PMID: 1478671
-
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.
Science. 1999 Aug 20;285(5431):1256-8
PMID: 10455050
-
Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase. Insights into mechanisms of sodium tolerance.
J Biol Chem. 1997 Oct 17;272(42):26145-52
PMID: 9334180
-
The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux.
Microbiology. 1998 Oct;144 ( Pt 10):2749-58
PMID: 9802016
-
Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa.
Biochim Biophys Acta. 1999 Jul 7;1446(1-2):149-55
PMID: 10395929
-
Multiple transduction pathways regulate the sodium-extrusion gene PMR2/ENA1 during salt stress in yeast.
FEBS Lett. 1996 Mar 11;382(1-2):89-92
PMID: 8612770
-
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):427-41
PMID: 8431946
-
Na(+)-ATPases and Na+/H+ antiporters in fungi.
Biochim Biophys Acta. 1994 Aug 30;1187(2):203-5
PMID: 8075113