Regulation of Vacuolar Na+/H+ Exchange in Arabidopsis thaliana by the Salt-Overly-Sensitive (SOS) Pathway

Qiu, Quan Sheng; Guo, Yan; Quintero, Francisco J.; Pardo, José M.; Schumaker, Karen S.; Zhu, Jian Kang

doi:10.1074/jbc.m307982200

Cited by 340 publications

(258 citation statements)

References 40 publications

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“…An increase in the transcript level of SYP61 was observed in both wild-type and tno1 mutant plants in all stress conditions. SOS1, DREB2A, and RD29 increased as expected (Yamaguchi-Shinozaki and Shinozaki, 1993b;Liu et al, 1998;Qiu et al, 2004), and no difference between wild-type and tno1 mutant plants was observed (Supplemental Fig. S4).…”

Section: Identification Of the Tno1 Knockout Mutantmentioning

confidence: 86%

TNO1 Is Involved in Salt Tolerance and Vacuolar Trafficking in Arabidopsis

Kim

Bassham

2011

Plant Physiology

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The Arabidopsis (Arabidopsis thaliana) soluble N-ethylmaleimide-sensitive factor attachment protein receptor SYP41 is involved in vesicle fusion at the trans-Golgi network (TGN) and interacts with AtVPS45, SYP61, and VTI12. These proteins are involved in diverse cellular processes, including vacuole biogenesis and stress tolerance. A previously uncharacterized protein, named TNO1 (for TGN-localized SYP41-interacting protein), was identified by coimmunoprecipitation as a SYP41-interacting protein.TNO1 was found to localize to the TGN by immunofluorescence microscopy. A tno1 mutant showed increased sensitivity to high concentrations of NaCl, KCl, and LiCl and also to mannitol-induced osmotic stress. Localization of SYP61, which is involved in the salt stress response, was disrupted in the tno1 mutant. Vacuolar proteins were partially secreted to the apoplast in the tno1 mutant, suggesting that TNO1 is required for efficient protein trafficking to the vacuole. The tno1 mutant had delayed formation of the brefeldin A (BFA) compartment in cotyledons upon application of BFA, suggesting less efficient membrane fusion processes in the mutant. Unlike most TGN proteins, TNO1 does not relocate to the BFA compartment upon BFA treatment. These data demonstrate that TNO1 is involved in vacuolar trafficking and salt tolerance, potentially via roles in vesicle fusion and in maintaining TGN structure or identity.

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Section: Identification Of the Tno1 Knockout Mutantmentioning

confidence: 86%

TNO1 Is Involved in Salt Tolerance and Vacuolar Trafficking in Arabidopsis

Kim

Bassham

2011

Plant Physiology

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“…In Arabidopsis, SOS2 mutants show a 60% reduction in Na + /H + exchange and a 30% reduction in V-ATPase H + transport activity. However, only Na + /H + exchange activity was returned to wild-type levels in the sos2 mutant by incubation with a constitutively activated SOS2 protein (Qiu et al, 2004). Neither transporter appeared to be directly phosphorylated by SOS2, and, in the case of the V-ATPase, regulation appears to be via direct interaction of the SOS2 protein with VHA-B (Batelli et al, 2007), although how this regulation is achieved was not addressed.…”

Section: Introductionmentioning

confidence: 98%

“…In both salt-tolerant halophytes and salt-sensitive glycophytes, sodium regulates the expression at the transcript and protein levels for the tonoplast NHXs (Shi and Zhu, 2002;Yokoi et al, 2002) and different subunits of the V-ATPase Tsiantis et al, 1996;Dietz et al, 2001;Vera-Estrella et al, 2005). In addition, their transport activity has been shown to increase under salt stress (Reuveni et al, 1990;Barkla et al, 1995;Qiu et al, 2004;Vera-Estrella et al, 2004). In Arabidopsis thaliana, mutants of NHX family members displayed enhanced salt sensitivity (Shi et al, 2000;Apse et al, 2003), as do mutants in subunits of the V-ATPase.…”

Section: Introductionmentioning

confidence: 99%

“…Accumulating evidence implicates components of the salt overly sensitive (SOS) pathway, and, specifically, the calcineurin B-like interacting protein kinase-interacting protein kinase, SOS2/CIPK24, has recently been revealed to regulate both the activity of the tonoplast Na + /H + exchanger, NHX1 (Qiu et al, 2004), and that of the V-ATPase (Batelli et al, 2007), through a possible calcineurin B-like protein-calcineurin B-like interacting protein kinase network. In Arabidopsis, SOS2 mutants show a 60% reduction in Na + /H + exchange and a 30% reduction in V-ATPase H + transport activity.…”

Section: Introductionmentioning

confidence: 99%

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Quantitative Proteomics of the Tonoplast Reveals a Role for Glycolytic Enzymes in Salt Tolerance

et al. 2009

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To examine the role of the tonoplast in plant salt tolerance and identify proteins involved in the regulation of transporters for vacuolar Na + sequestration, we exploited a targeted quantitative proteomics approach. Two-dimensional differential in-gel electrophoresis analysis of free flow zonal electrophoresis separated tonoplast fractions from control, and salt-treated Mesembryanthemum crystallinum plants revealed the membrane association of glycolytic enzymes aldolase and enolase, along with subunits of the vacuolar H + -ATPase V-ATPase. Protein blot analysis confirmed coordinated salt regulation of these proteins, and chaotrope treatment indicated a strong tonoplast association. Reciprocal coimmunoprecipitation studies revealed that the glycolytic enzymes interacted with the V-ATPase subunit B VHA-B, and aldolase was shown to stimulate V-ATPase activity in vitro by increasing the affinity for ATP. To investigate a physiological role for this association, the Arabidopsis thaliana cytoplasmic enolase mutant, los2, was characterized. These plants were salt sensitive, and there was a specific reduction in enolase abundance in the tonoplast from salt-treated plants. Moreover, tonoplast isolated from mutant plants showed an impaired ability for aldolase stimulation of V-ATPase hydrolytic activity. The association of glycolytic proteins with the tonoplast may not only channel ATP to the V-ATPase, but also directly upregulate H + -pump activity.

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“…(6,28). Accordingly, the reduced electrochemical proton gradient should render the vha-a2 vha-a3 mutant more salt sensitive.…”

mentioning

confidence: 99%

Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation

Krebs

Beyhl

Görlich

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

281

335

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The productivity of higher plants as a major source of food and energy is linked to their ability to buffer changes in the concentrations of essential and toxic ions. Transport across the tonoplast is energized by two proton pumps, the vacuolar H + -ATPase (VATPase) and the vacuolar H + -pyrophosphatase (V-PPase); however, their functional relation and relative contributions to ion storage and detoxification are unclear. We have identified an Arabidopsis mutant in which energization of vacuolar transport solely relies on the activity of the V-PPase. The vha-a2 vha-a3 double mutant, which lacks the two tonoplast-localized isoforms of the membrane-integral V-ATPase subunit VHA-a, is viable but shows day-length-dependent growth retardation. Nitrate content is reduced whereas nitrate assimilation is increased in the vha-a2 vha-a3 mutant, indicating that vacuolar nitrate storage represents a major growth-limiting factor. Zinc is an essential micronutrient that is toxic at excess concentrations and is detoxified via a vacuolar Zn 2+ /H + -antiport system. Accordingly, the double mutant shows reduced zinc tolerance. In the same way the vacuolar Na + /H + -antiport system is assumed to be an important component of the system that removes sodium from the cytosol. Unexpectedly, salt tolerance and accumulation are not affected in the vhaa2 vha-a3 double mutant. In contrast, reduction of V-ATPase activity in the trans-Golgi network/early endosome (TGN/EE) leads to increased salt sensitivity. Taken together, our results show that during gametophyte and embryo development V-PPase activity at the tonoplast is sufficient whereas tonoplast V-ATPase activity is limiting for nutrient storage but not for sodium tolerance during vegetative and reproductive growth.proton-pump | pH-homeostasis | vacuole | nitrate | salt tolerance T he productivity of higher plants as a major source of food and renewable energy is linked to their ability to cope with fluctuations in essential as well as toxic ion and metabolite concentrations. In plants the large central vacuoles function as reservoirs for ions and metabolites that allow buffering of changes in nutrients as well as challenges by toxic components that plants, as sessile, photoautotrophic organisms, frequently encounter. Furthermore, vacuoles are essential for plant growth and development. Expansion of plant cells is achieved by osmotically driven water influx into the vacuole that, in combination with the cell wall, generates turgor, the driving force for hydraulic stiffness and plant growth.All vacuolar functions require massive fluxes of ions and metabolites that are channeled by a battery of vacuolar transport proteins, many of which have been well characterized physiologically, but the nature of several transporters remains to be identified (1). Among those characterized on the molecular level are, e.g., those transporting NO 3 − , Na + , and protons. Nitrate, a major plant nutrient, is accumulated and stored in the vacuole from where it can be retrieved according to metabolic deman...

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Regulation of Vacuolar Na+/H+ Exchange in Arabidopsis thaliana by the Salt-Overly-Sensitive (SOS) Pathway

Cited by 340 publications

References 40 publications

TNO1 Is Involved in Salt Tolerance and Vacuolar Trafficking in Arabidopsis

TNO1 Is Involved in Salt Tolerance and Vacuolar Trafficking in Arabidopsis

Quantitative Proteomics of the Tonoplast Reveals a Role for Glycolytic Enzymes in Salt Tolerance

Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation

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