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Review
. 2009 Aug;4(8):718-26.
doi: 10.4161/psb.4.8.9236. Epub 2009 Aug 9.

Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange

Paulo Silva  1 , Hernâni Gerós
Affiliations
Review

Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange

Paulo Silva et al. Plant Signal Behav. 2009 Aug.

Abstract

Over the last decades several efforts have been carried out to determine the mechanisms of salt homeostasis in plants and, more recently, to identify genes implicated in salt tolerance, with some plants being successfully genetically engineered to improve resistance to salt. It is well established that the efficient exclusion of Na(+) excess from the cytoplasm and vacuolar Na(+) accumulation are the most important steps towards the maintenance of ion homeostasis inside the cell. Therefore, the vacuole of plant cells plays a pivotal role in the storage of salt. After the identification of the vacuolar Na(+)/H(+) antiporter Nhx1 in Saccharomyces cerevisiae, the first plant Na(+)/H(+) antiporter, AtNHX1, was isolated from Arabidopsis and its overexpression resulted in plants exhibiting increased salt tolerance. Also, the identification of the plasma membrane Na(+)/H(+) exchanger SOS1 and how it is regulated by a protein kinase SOS2 and a calcium binding protein SOS3 were great achievements in the understanding of plant salt resistance. Both tonoplast and plasma membrane antiporters exclude Na+ from the cytosol driven by the proton-motive force generated by the plasma membrane H(+)-ATPase and by the vacuolar membrane H(+)-ATPase and H(+)-pyrophosphatase and it has been shown that the activity of these proteins responds to salinity. In this review we focus on the transcriptional and post-transcriptional regulation by salt of tonoplast proton pumps and Na(+)/H(+) exchangers and on the signalling pathways involved in salt sensing.

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Figures

Figure 1
Figure 1
Phylogenetic tree of Na+/H+ antiporters. Sequence analysis was performed online using Mobyle (http://mobyle.pasteur.fr/). A multiple sequence alignment of several antiporter protein sequences was generated using ClustalW and the neighbour-joining method was used to calculate evolutionary distances. The unrooted phylogenetic tree was constructed using the FigTree software package (FigTree 1.2.2, http://tree.bio.ed.ac.uk/software/figtree/). Antiporter sequences from the following species were used in the construction of the tree: Atriplex dimorphostegia (AdNHX1, AY211397), Atriplex gmelini (AgNHX1, AB038492), Arabidopsis thaliana (AtNHX1, NM_122597; AtNHX2, NM_111375; AtNHX3, NM_124929; AtNHX4, NM_111512; AtNHX5, NM_104315; AtNHX6, NM_106609), Brassica napus (BnNHX1, AY189676), Chenopodium glaucum (CgNHX1, AY371319), Citrus reticulata (CrNHX1, AY607026), Gossypium hirsutum (GhNHX1, AF515632), Glycine max (GmNHX1, AY972078), Hordeum vulgare (HvNHX1, AB089197), Kalidium foliatum (KfNHX1, AY825250), Limonium gmelinii (LgNHX1, EU780457), Mesembryanthemum crystallinum (McNHX1, AM746985; McNHX2, AM748092), Medicago sativa (MsNHX1, AY456096), Oryza sativa (OsNHX1, AB021878), Populus euphratica (PeNHX2, EU382999), Petunia hybrida (PhNHX1, AB051817), Plantago maritima (PmNHX1, EU233808), Populus tomentosa (PtNHX1, AY660749), Rosa hybrida (RhNHX1, AB199912), Salicornia brachiata (SbNHX1, EU448383), Salicornia europaea (SeNHX1, AY131235), Suaeda japonica (SjNHX1, AB198178), Solanum lycopersicum (SlNHX1, AJ306630; SlNHX2, AJ306631), Suaeda salsa (SsNHX1, AY261806), Tetragonia tetragonioides (TtNHX1, AF527625), Thellungiella halophila (ThNHX1, FJ713100), Triticum aestivum (TaNHX1, AY461512), Vitis vinifera (VvNHX1, AY634283), Zea mays (ZmNHX1, NM_001111751). The shaded area represents halophytic species.
Figure 2
Figure 2
Topological model of the Arabidopsis Na+/H+ exchanger AtNHX1, showing 12 transmembrane domains, and with a hydrophobic, luminal N-terminal and a hydrophilic, cytosolic C-terminal. The model was constructed and adapted according to the work of Sato and co-workers. The darker transmembrane domains represent the predicted active site.
Figure 3
Figure 3
Dissipation of a PPi-dependent H+ gradient upon addition of 200 mM and 400 mM NaCl (final concentrations) to tonoplast vesicles isolated from P. euphratica suspension-cultured cells grown in the absence of salt (A) and in the presence of 150 mM NaCl (B). Inserts: Confocal imaging of Na+ accumulation in P. euphratica suspension cells stained with Sodium Green (Adapted from Silva et al. with kind permission from Springer).
Figure 4
Figure 4
Signalling pathways responsible for sodium extrusion in Arabidopsis under salt stress. Excess Na+ and high osmolarity are separately perceived by yet unidentified sensors at the plasma membrane level, which then induce an increase in cytosolic Ca2+ concentration. This increase is then sensed by SOS3 which activates SOS2. The activated SOS3-SOS2 protein complex phosphorylates SOS1, the plasma membrane Na+/H+ antiporter, resulting in the efflux of Na+ ions. SOS2 has also been shown to regulate NHX1 antiport activity and V-H+-ATPase activity in a SOS3-independent manner, possibly by SOS3-like Ca2+-binding proteins (SCaBP) that target it to the tonoplast. Salt stress can also induce the accumulation of ABA, which, by means of ABI1 and ABI2, can negatively regulate SOS2 or SOS1 and NHX1.
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