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Review
. 2022 Jun 30:13:931777.
doi: 10.3389/fpls.2022.931777. eCollection 2022.

The Plant V-ATPase

Thorsten Seidel  1
Affiliations
Review

The Plant V-ATPase

Thorsten Seidel. Front Plant Sci. .

Abstract

V-ATPase is the dominant proton pump in plant cells. It contributes to cytosolic pH homeostasis and energizes transport processes across endomembranes of the secretory pathway. Its localization in the trans Golgi network/early endosomes is essential for vesicle transport, for instance for the delivery of cell wall components. Furthermore, it is crucial for response to abiotic and biotic stresses. The V-ATPase's rather complex structure and multiple subunit isoforms enable high structural flexibility with respect to requirements for different organs, developmental stages, and organelles. This complexity further demands a sophisticated assembly machinery and transport routes in cells, a process that is still not fully understood. Regulation of V-ATPase is a target of phosphorylation and redox-modifications but also involves interactions with regulatory proteins like 14-3-3 proteins and the lipid environment. Regulation by reversible assembly, as reported for yeast and the mammalian enzyme, has not be proven in plants but seems to be absent in autotrophic cells. Addressing the regulation of V-ATPase is a promising approach to adjust its activity for improved stress resistance or higher crop yield.

Keywords: Arabidopsis; V-ATPase; glucose; pH-homeostasis; proton pump.

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Conflict of interest statement

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Localization of proton pumps. V-ATPase is present in all endomembranes of the secretory pathway, including ER membranes. V-PPases are localized in the vacuole and rarely in the Golgi, while PM-ATPases are present in the plasma membrane and, in some tissues, even in tonoplasts. Two transport routes exist for V-ATPases. Proton pumps destined for TGN/EE bear VHA-a1 and travel along the secretory pathway, while VHA-a3-bearing pumps are destined for the vacuole and take a direct route from the ER to the vacuole. The structure of V-PPase relies on pdb file 6afs and that of the plasma membrane on file 5 ksd (Croll and Andersen, 2016; Tsai et al., 2019). The structure of V-ATPase is based on pdb 3j9t (Zhao et al., 2015).
FIGURE 2
FIGURE 2
V-ATPase complex. V-ATPase comprises of the membrane integral subsector V0 and the membrane-associated subsector V1. V0 is responsible for proton transport and dominated by a ring composed of ten molecules of proteolipid VHA-c. A single proteolipid is highlighted in blue (VHA-c”). ATP hydrolysis takes place in V1, in particular in VHA-A, and drives the rotation of the central stalk by VHA-D and VHA-F. The peripheral subunits serve as a scaffold and anchor the complex to the membrane via VHA-a. The structure is based on pdb7tmr (Vasanthakumar et al., 2022).
FIGURE 3
FIGURE 3
Structure of proteolipids VHA-c and VHA-c” and subunit VHA-a. (A) VHA-a has a bipartite structure of the cytosolic N-terminal domain and the C-terminal membrane integral domain. The N-terminal domain serves as part of stator and bears the TGN localization domain in the case of VHA-a1 (position is indicated by dark green color). Helices of the C-terminal domain form semi-channels for proton loading and unloading of VHA-c (light green helices), and the barrier charge surrounds a conserved arginine residue on helix seven (red colored). (B–D) The proteolipids consist of four transmembrane helices [refer to the view from the cytosolic side: (C,E)], and the protein binding site is a conserved glutamate residue (red color) located in the fourth helix [VHA-c; (B)] or the second helix [VHA-c”, (D)]. A cytosolic loop of VHA-c (green color) serves as a binding site for VHA-d. Structures were obtained with Phyre2 (Kelley et al., 2015), and a complete set of pdb files for A. thaliana VHA subunits is available as Supplementary Data.
FIGURE 4
FIGURE 4
Structure-function relationship of the subunit arrangement. (A) Subunits that are directly involved in catalysis of proton pumping are given, starting with ATP-hydrolysis at the catalytic head, transformation of conformational changes into rotation of the central shaft by VHA-D and VHA-F, and VHA-d-mediated transduction of the rotation to the proteolipid ring, are given. VHA-a contributes the semi-channels for loading and unloading of proton binding sites. (B) The peripheral stalk subunits form a structure that resembles a rigid cage. It anchors the catalytic head to the membrane and prevents its co-rotation. Subunits of the peripheral stalk have a direct impact on coupling ratio. (C) Top view of the V1 sector reveals the arrangement of VHA-A subunits with VHA-D located in the center. The structures are based on pdb 3j9t (Zhao et al., 2015).
FIGURE 5
FIGURE 5
Conserved cysteine of VHA-A. VHA-A bears three conserved cysteines. Their distances of 11–29 Å exceed the maximum distance for disulfide formation. Cys256 is located in the catalytic ATP-binding P-loop, and its redox modulation efficiently inhibits V-ATPase activity. The structure is based on pdb 3j9t (Zhao et al., 2015).
FIGURE 6
FIGURE 6
Reversible assembly of yeast V-ATPases. In the absence of glucose, the glycolytic aldolase dissociates from the complex, followed by VHA-C and the entire V1-sector; VHA-C and the residual V1 sector bind to actin to prevent free diffusion. Supply with glucose results in re-assembly of V-ATPase, mediated by the RAVE complex. The structure of V-ATPase relies on pdb-file 3j9t, the aldolase on 7ka2, and Skp1 on 5xyl (Zhao et al., 2015; Shukla et al., 2018; Cash et al., 2020).
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