Abstract
The vacuolar H(+)-translocating ATPase (H(+)-ATPase), originally reported to consist of three major subunits, has been further purified from oat roots (Avena sativa var Lang) to determine the complete subunit composition. Triton-solubilized ATPase activity was purified by gel filtration on Sephacryl S400 and ion-exchange chromatography (Q-Sepharose). ATP hydrolysis activity of purified preparations was inhibited by 100 nanomolar bafilomycin A(1), a specific vacuolar-type ATPase inhibitor. The purified oat H(+)-ATPase (relative molecular weight = 650,000) was composed of polypeptides of 70, 60, 44, 42, 36, 32, 29, 16, 13, and 12 kilodaltons. To analyze the organization of the H(+)-ATPase subunits, native vacuolar membranes were treated with KI and MgATP to dissociate peripheral proteins. Release of 70, 60, 44, 42, 36, and 29 kilodalton polypeptides from the membrane was accompanied by a loss of ATP hydrolysis and ATP-dependent H(+)-pumping activities. Five of the peripheral subunits were released from the membrane as a large complex of 540 kilodaltons. Vesicles that had lost the peripheral sector of the ATPase could hold a pH gradient generated by the proton-translocating pyrophosphatase, suggesting that the integral sector of the ATPase did not form a H(+)-conducting pathway. Negative staining of native vesicles revealed knob-like structures of 10 to 12 nanometers in dense patches on the surface of vacuolar membranes. These structures were removed by MgATP and KI, which suggested that they were the peripheral sectors of the H(+)-ATPase. These results demonstrate that the vacuolar H(+)-ATPase from oat roots has 10 different subunits. The oat vacuolar ATPase is organized as a large peripheral sector and an integral sector with a subunit composition similar, although not identical to, other eukaryotic vacuolar ATPases. Variations in subunit composition observed among several ATPases support the idea that distinct types of vacuolar H(+)-ATPases exist in plants.
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ward J M
Department of Botany, University of Maryland, College Park, Maryland 20742.
Sze H
References (25)
25 references, click to expand
-
Subunit composition of vacuolar membrane H(+)-ATPase from mung bean.
Eur J Biochem. 1990 Feb 14;187(3):745-51
PMID: 2137412
-
Properties of the partially purified tonoplast H+-pumping ATPase from oat roots.
J Biol Chem. 1986 Jan 25;261(3):1364-71
PMID: 2867999
-
Topography and subunit stoichiometry of the coated vesicle proton pump.
J Biol Chem. 1988 Jun 25;263(18):8796-802
PMID: 2897963
-
Isolation of genes encoding the Neurospora vacuolar ATPase. Analysis of vma-1 encoding the 67-kDa subunit reveals homology to other ATPases.
J Biol Chem. 1988 Oct 5;263(28):13994-4001
PMID: 2971651
-
Dissociation and Reassembly of the Vacuolar H-ATPase Complex from Oat Roots.
Plant Physiol. 1992 May;99(1):161-9
PMID: 16668845
-
Proteolysis and orientation on reconstitution of the coated vesicle proton pump.
J Biol Chem. 1990 Jan 15;265(2):960-6
PMID: 1967251
-
Peripheral and integral subunits of the tonoplast H+-ATPase from oat roots.
J Biol Chem. 1988 Nov 15;263(32):16731-7
PMID: 2903155
-
H+-translocating ATPase in Golgi apparatus. Characterization as vacuolar H+-ATPase and its subunit structures.
J Biol Chem. 1989 Nov 5;264(31):18445-50
PMID: 2530222
-
N,N'-dicyclohexylcarbodiimide-binding proteolipid of the vacuolar H+-ATPase from oat roots.
J Biol Chem. 1988 Jan 25;263(3):1282-7
PMID: 2891708
-
Functional reassembly of the coated vesicle proton pump.
J Biol Chem. 1990 Sep 5;265(25):14836-41
PMID: 1975587
-
Interaction of anions and ATP with the coated vesicle proton pump.
Biochemistry. 1989 Apr 4;28(7):3075-82
PMID: 2568125
-
Probing the catalytic subunit of the tonoplast H+-ATPase from oat roots. Binding of 7-chloro-4-nitrobenzo-2-oxa-1,3,-diazole to the 72-kilodalton polypeptide.
J Biol Chem. 1987 May 25;262(15):7135-41
PMID: 2884218
-
Structure and function of vacuolar class of ATP-driven proton pumps.
Physiol Rev. 1989 Jul;69(3):765-96
PMID: 2526342
-
The cDNA sequence of the 69-kDa subunit of the carrot vacuolar H+-ATPase. Homology to the beta-chain of F0F1-ATPases.
J Biol Chem. 1988 Jul 5;263(19):9102-12
PMID: 2897965
-
High purity preparations of higher plant vacuolar H+-ATPase reveal additional subunits. Revised subunit composition.
J Biol Chem. 1989 Nov 25;264(33):20025-32
PMID: 2531142
-
Partial purification of a tonoplast ATPase from corn coleoptiles.
Plant Physiol. 1985 Jun;78(2):327-33
PMID: 16664239
-
Dissociation, cross-linking, and glycosylation of the coated vesicle proton pump.
J Biol Chem. 1990 Jan 15;265(2):967-73
PMID: 1967252
-
Inhibition of the coated vesicle proton pump and labeling of a 17,000-dalton polypeptide by N,N'-dicyclohexylcarbodiimide.
J Biol Chem. 1987 Aug 15;262(23):11006-11
PMID: 2440881
-
Cold inactivation of vacuolar proton-ATPases.
J Biol Chem. 1989 Feb 25;264(6):3577-82
PMID: 2521638
-
Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells.
Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972-6
PMID: 2973058
-
Molecular cloning and sequencing of cDNAs encoding the proteolipid subunit of the vacuolar H(+)-ATPase from a higher plant.
J Biol Chem. 1991 Aug 25;266(24):16078-84
PMID: 1831453
-
The vacuolar ATPase of Neurospora crassa contains an F1-like structure.
J Biol Chem. 1989 Sep 15;264(26):15606-12
PMID: 2527854
-
Structural studies of the vacuolar membrane ATPase from Neurospora crassa and comparison with the tonoplast membrane ATPase from Zea mays.
Proc Natl Acad Sci U S A. 1986 Jan;83(1):48-52
PMID: 3079903
-
Identification of 3-O-(4-benzoyl)benzoyladenosine 5'-triphosphate- and N,N'-dicyclohexylcarbodiimide-binding subunits of a higher plant H+-translocating tonoplast ATPase.
J Biol Chem. 1985 Oct 5;260(22):12273-9
PMID: 2864339
-
cDNA sequence and homologies of the "57-kDa" nucleotide-binding subunit of the vacuolar ATPase from Arabidopsis.
J Biol Chem. 1988 Dec 5;263(34):17987-94
PMID: 2903860