Initial Steps in the Assembly of the Vacuole-type H+-ATPase

Overview

Journal Plant Physiol

Specialty Physiology

Date 1998 Sep 11

PMID 9733533

Citations 2

Authors

FREY

Randall

Affiliations

Soon will be listed here.

Abstract

The plant vacuole is acidified by a complex multimeric enzyme, the vacuole-type H+-ATPase (V-ATPase). The initial association of ATPase subunits on membranes was studied using an in vitro assembly assay. The V-ATPase assembled onto microsomes when V-ATPase subunits were supplied. However, when the A or B subunit or the proteolipid were supplied individually, only the proteolipid associated with membranes. By using poly(A+) RNA depleted in the B subunit and proteolipid subunit mRNA, we demonstrated A subunit association with membranes at substoichiometric amounts of the B subunit or the 16-kD proteolipid. These data suggest that poly(A+) RNA-encoded proteins are required to catalyze the A subunit membrane assembly. Initial events were further studied by in vivo protein labeling. Consistent with a temporal ordering of V-ATPase assembly, membranes contained only the A subunit at early times; at later times both the A and B subunits were found on the membranes. A large-mass ATPase complex was not efficiently formed in the absence of membranes. Together, these data support a model whereby the A subunit is first assembled onto the membrane, followed by the B subunit.

Citing Articles

The Plant V-ATPase.

Seidel T Front Plant Sci. 2022; 13:931777.

PMID: 35845650 PMC: 9280200. DOI: 10.3389/fpls.2022.931777.

New insight into the structure and regulation of the plant vacuolar H+-ATPase.

Kluge C, Lahr J, Hanitzsch M, Bolte S, Golldack D, Dietz K J Bioenerg Biomembr. 2003; 35(4):377-88.

PMID: 14635783 DOI: 10.1023/a:1025737117382.

References

Randall S, Sze H . Properties of the partially purified tonoplast H+-pumping ATPase from oat roots. J Biol Chem. 1986; 261(3):1364-71. View

Matsuoka K, Bassham D, Raikhel N, Nakamura K . Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J Cell Biol. 1995; 130(6):1307-18. PMC: 2120585. DOI: 10.1083/jcb.130.6.1307. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Ward J, Sze H . Subunit Composition and Organization of the Vacuolar H-ATPase from Oat Roots. Plant Physiol. 1992; 99(1):170-9. PMC: 1080422. DOI: 10.1104/pp.99.1.170. View

Graham L, Hill K, Stevens T . VMA7 encodes a novel 14-kDa subunit of the Saccharomyces cerevisiae vacuolar H(+)-ATPase complex. J Biol Chem. 1994; 269(42):25974-7. View

Arai H, TERRES G, Pink S, Forgac M . Topography and subunit stoichiometry of the coated vesicle proton pump. J Biol Chem. 1988; 263(18):8796-802. View

Ho M, Hill K, Lindorfer M, Stevens T . Isolation of vacuolar membrane H(+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H(+)-ATPase. J Biol Chem. 1993; 268(1):221-7. View

Hirata R, Umemoto N, Ho M, Ohya Y, Stevens T, Anraku Y . VMA12 is essential for assembly of the vacuolar H(+)-ATPase subunits onto the vacuolar membrane in Saccharomyces cerevisiae. J Biol Chem. 1993; 268(2):961-7. View

Randall S, Sze H . Biosynthesis of the Tonoplast H-ATPase from Oats. Plant Physiol. 1989; 89(4):1292-8. PMC: 1056011. DOI: 10.1104/pp.89.4.1292. View

10.

Hoh B, Hinz G, Jeong B, Robinson D . Protein storage vacuoles form de novo during pea cotyledon development. J Cell Sci. 1995; 108 ( Pt 1):299-310. DOI: 10.1242/jcs.108.1.299. View

11.

Herman E, Li X, Su R, Larsen P, Hsu H, Sze H . Vacuolar-Type H+ -ATPases Are Associated with the Endoplasmic Reticulum and Provacuoles of Root Tip Cells. Plant Physiol. 1994; 106(4):1313-1324. PMC: 159669. DOI: 10.1104/pp.106.4.1313. View

12.

Lai S, Randall S, Sze H . Peripheral and integral subunits of the tonoplast H+-ATPase from oat roots. J Biol Chem. 1988; 263(32):16731-7. View

13.

Lai S, Watson J, Hansen J, Sze H . Molecular cloning and sequencing of cDNAs encoding the proteolipid subunit of the vacuolar H(+)-ATPase from a higher plant. J Biol Chem. 1991; 266(24):16078-84. View

14.

Rea P, Griffith C, Sanders D . Purification of the N,N'-dicyclohexylcarbodiimide-binding proteolipid of a higher plant tonoplast H+-ATPase. J Biol Chem. 1987; 262(30):14745-52. View

15.

Bremberger C, Luttge U . Dynamics of tonoplast proton pumps and other tonoplast proteins of Mesembryanthemum crystallinum L. during the induction of Crassulacean acid metabolism. Planta. 2013; 188(4):575-80. DOI: 10.1007/BF00197051. View

16.

Kane P, Kuehn M, Stevens T . Assembly and targeting of peripheral and integral membrane subunits of the yeast vacuolar H(+)-ATPase. J Biol Chem. 1992; 267(1):447-54. View

17.

Ali M, Akazawa T . Association of H-Translocating ATPase in the Golgi Membrane System from Suspension-Cultured Cells of Sycamore (Acer pseudoplatanus L.). Plant Physiol. 1986; 81(1):222-7. PMC: 1075310. DOI: 10.1104/pp.81.1.222. View

18.

Kaestner K, Randall S, Sze H . N,N'-dicyclohexylcarbodiimide-binding proteolipid of the vacuolar H+-ATPase from oat roots. J Biol Chem. 1988; 263(3):1282-7. View

19.

Dupont F, Morrissey P . Subunit composition and Ca(2+)-ATPase activity of the vacuolar ATPase from barley roots. Arch Biochem Biophys. 1992; 294(2):341-6. DOI: 10.1016/0003-9861(92)90693-q. View

20.

Hill K, Stevens T . Vma22p is a novel endoplasmic reticulum-associated protein required for assembly of the yeast vacuolar H(+)-ATPase complex. J Biol Chem. 1995; 270(38):22329-36. DOI: 10.1074/jbc.270.38.22329. View