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Plant signaling networks involving Ca2+ and Rboh/Nox-mediated ROS production under salinity stress

Takamitsu Kurusu, Kazuyuki Kuchitsu, Yuichi Tada

Frontiers in Plant Science · 2015 · Review

doi:10.3389/fpls.2015.00427

Abstract

Salinity stress, which induces both ionic and osmotic damage, impairs plant growth and causes severe reductions in crop yield. Plants are equipped with defense responses against salinity stress such as regulation of ion transport including Na(+) and K(+), accumulation of compatible solutes and stress-related gene expression. The initial Ca(2+) influx mediated by plasma membrane ion channels has been suggested to be crucial for the adaptive signaling. NADPH oxidase (Nox)-mediated production of reactive oxygen species (ROS) has also been suggested to play crucial roles in regulating adaptation to salinity stress in several plant species including halophytes. Respiratory burst oxidase homolog (Rboh) proteins show the ROS-producing Nox activity, which are synergistically activated by the binding of Ca(2+) to EF-hand motifs as well as Ca(2+)-dependent phosphorylation. We herein review molecular identity, structural features and roles of the Ca(2+)-permeable channels involved in early salinity and osmotic signaling, and comparatively discuss the interrelationships among spatiotemporal dynamic changes in cytosolic concentrations of free Ca(2+), Rboh-mediated ROS production, and downstream signaling events during salinity adaptation in planta.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 25, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Soil salinity impairs plant growth and development and is an important factor limiting crop productivity and yield worldwide. Salinity stress reduces water potential, thereby preventing water uptake by roots and provoking a set of responses similar to those of a water deficit. Thus, by causing osmotic stress, salinity provokes the stomatal limitation of photosynthesis, loss of turgor, enhanced photorespiration, and excess production of ROS. The ionic component of salinity stress is attributed to the direct toxic effects of Na+ and imbalances in the homeostasis of other ions such as K+ and Ca2+.

To mount an effective response to cope with salinity stress, land plants have developed the ability to sense both osmotic stress and Na+. Plants exhibit a rapid increase in the cytosolic Ca2+ concentration within seconds of being exposed to NaCl or mannitol. The Ca2+ rise originated within the roots is propagated systemically, and occurs in several cell types.

Reactive oxygen species such as O2⋅− (superoxide anion radical), H2O2 (hydrogen peroxide), and OH⋅ (hydroxyl radical) are highly toxic substances produced through aerobic respiration and photosynthesis that oxidize various biomolecules such as DNA, proteins and lipids, and disrupt the cell redox state. Therefore, plants have developed various systems to scavenge ROS. Direct exposure of plant tissues to H2O2 activates antioxidant enzymes as well as the expression of the corresponding genes. ROS are also enzymatically produced and act as signaling molecules in plant responses to abiotic and/or biotic stresses.

Respiratory burst oxidase homologs has been identified as ROS-producing Noxs that generate O2⋅− by oxidizing NADPH and transferring an electron to oxygen. Noxs are rapidly activated in response to various stimuli to induce ROS production and are involved in the regulation of a wide range of physiological functions in plants. Rbohs play central roles in the Ca2+-ROS signaling network triggered by their phosphorylation during stress adaptation.

We here review molecular mechanisms and roles of PM Ca2+-permeable channels as putative osmosensors and enzymatic ROS production involved in early salinity and osmotic responses, and discuss the interrelationships among dynamic changes in [Ca2+]cyt, ROS production, downstream signaling events during salinity sensing and adaptation in plants including halophytes.

Candidates for Plant Ca2+-Permeable MS Channels as Osmosensors

Mechanical stimuli, such as touch, bending, and barriers for growth as well as osmotic potential changes, all elicit rapid and transient increases in [Ca2+]cyt. Expression of cellular Ca2+-binding regulatory proteins including CaM and CML are induced by mechanical stimuli. Early responses to salinity stress reflect turgor changes and involve Ca2+-mediated signaling. PM Ca2+-permeable MS channels are suggested to sense salinity stress-triggered osmotic potential change. The following protein families are suggested as putative plant PM Ca2+-permeable MS channels as osmosensors.

OSCA1

OSCA1 was recently identified as a novel putative PM hyper-osmolality-gated Ca2+-permeable channel in guard cells and roots of Arabidopsis. OSCA1 comprises nine transmembrane α-helices, but shows no significant similarity to known ion channels. Electrophysiological analyses of OSCA1 expressed in HEK293 cells showed its hyper-osmolality-gated Ca2+-permeable channel activity. In osca1, early osmotic signaling events in guard cells were impaired and downstream adaptation responses against osmotic stress were attenuated.

MCA Family

The yeast Mid1 protein shows MS channel activity when expressed in mammalian cells. MCAs were identified in Arabidopsis based on their ability to complement the yeast mutant mid1. MCAs comprise at least one transmembrane domain and contain an EF hand, but show no significant similarity to known ion channels. All MCAs are localized to the PM and mediate Ca2+ uptake, with the N-terminal and EF hand regions being necessary structures for transport. MCAs are present in all land plants, including ferns and mosses, but not in algae, animals, protists, or fungi, suggesting that the function of MCAs is fundamental to land plants.

Ca2+ current induced by trinitrophenol, a potent compound to generate membrane distortion to activate MS channels, is enhanced in the MCA1-overexpressing cells, and MCA1 and MCA2 expressed in Xenopus oocytes showed MS cation channel activity. Touch response in the primary root is impaired in mca1, while mca2 showed lower root Ca2+ uptake, suggesting that MCA1 and MCA2 play different physiological roles. Hypo-osmotic shock-induced PM Ca2+ influx and ROS production are partially impaired in OsMCA1-suppressed rice cultured cells. Tobacco MCA homologs are localized at the Hechtian strand that connects PM and cell wall. These findings suggest that MCAs are involved in hypo-osmotic stress-induced PM Ca2+ influx. MCA1 and MCA2 form a tetramer, suggesting that MCA proteins may function as a tetramer to form a Ca2+-permeable pore.

MSL Family and Others

Genome-wide screening to search for plant MS channels homologous to eukaryotic and prokaryotic MS channels identified the MSL protein family. MSLs are present in land plants, and electrophysiological studies suggest that MSL9 and MSL10 permeate Cl- rather than Ca2+. It remains unknown whether any of MSLs are involved in the mechanical stimuli-induced Ca2+ influx as Ca2+-permeable channels.

Piezo proteins in mouse and Drosophila are also pore-forming subunits of MS channels and respond to mechanical stimuli. Many eukaryotic species including plants but not yeast and bacteria have a single Piezo protein. Functional roles of plant Piezo protein have not yet been reported.

An Arabidopsis histidine kinase HK1 may share a similar function with yeast SLN1 as an osmosensor. It is of interest to determine whether any of these putative MS channels or osmosensors interacts with each other physically or functionally to monitor mechanical stimuli under salinity stress.

Physiological Roles of Rboh/Nox in Early Salinity Responses in Arabidopsis

Reactive oxygen species are highly toxic substances that oxidize various biomolecules. Generation of OH⋅ has significant implications to cell metabolism and causes lipid peroxidation. K+ deficiency causes an increase in O2⋅− production by Rboh/Nox in root cells, and enhanced activation of antioxidant enzymes under salinity stress involves cytosolic K+ retention, suggesting that optimizing the K+ nutritional status may reduce the toxic effect of ROS by regulating Nox activity, and is essential for plant performance against salinity.

Exposure to salinity activates the SOS pathway, leading to Ca2+-dependent activation of SOS1, a PM Na+/H+ exchanger that enables adaptation through Na+ efflux. Expression of SOS1 is induced under salinity stress, which requires activation of the Ca2+ sensor SOS3/CBL4 (calcineurin B-like 4). Nox-mediated ROS production stabilizes SOS1 transcripts. Growth of better-adapted secondary roots is impaired in sos1 and involves O2⋅− production, possibly by Rboh/Nox.

Arabidopsis contains 10 Nox genes, RbohA-J, which exhibit different patterns of expression and in response to environmental factors. Expression of RbohD and RbohF are highly induced under salinity stress. An RbohF mutant showed strong Na+ hypersensitivity in its shoots and lacked ROS accumulation in its vasculature, suggesting that RbohF plays a role in the regulation of xylem loading of Na+ to protect leaves from salinity stress in Arabidopsis. ROS production by Rboh/Nox is also suggested to be coordinated by signaling pathways involving phospholipid and actin in salinity stress responses, and is required for heme oxygenase-mediated salt acclimation signaling.

The Interrelationships between Ca2+ Influx and Rboh/Nox-Mediated ROS Production in Early Salinity Responses

Plant Rbohs have two N-terminal EF-hand motifs. A heterologous expression system based on HEK293T cells is effective to quantitatively evaluate and reconstitute the ROS-producing activity of Rbohs. Rbohs are basically synergistically activated by the Ca2+-binding to the EF-hand motifs and phosphorylation. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Rbohs. Arabidopsis CIPK26, binds to RbohF in planta and in the presence of PM-localized Ca2+ sensor proteins CBL1/CBL9, CIPK26 enhances the activity of RbohF. Rbohs are phosphorylated and activated by two families of Ca2+-dependent protein kinases (CBL-CIPK complexes and CDPKs;;; ), and two families of Ca2+-independent protein kinases (RLCKs and SnRK2s;; ).

Reactive oxygen species-activated Ca2+-permeable channels and Rbohs have been suggested to constitute a positive feedback mechanism that enhances Ca2+ and ROS signals in root cells. RbohC/RHD2 affects mechanical stress-induced ROS generation, and regulates Arabidopsis root hair elongation in a Ca2+-dependent manner. Hyperpolarization- and depolarization-activated PM Ca2+-permeable channels may play roles in salinity-induced [Ca2+]cyt increase.

Salinity-induced elevation of [Ca2+]cyt corresponds to PM Ca2+ influx as well as Ca2+ release from intracellular Ca2+ stores, and plays important roles in ROS signaling and salt tolerance. Salinity-induced Ca2+ influx currents were markedly suppressed in the rbohD/F double mutant in Arabidopsis, implicating the roles of RbohD and RbohF in salt-stimulated [Ca2+]cyt rise.

Plant annexins have been reported to form Ca2+-permeable channels in planar lipid bilayers. Arabidopsis AtANN1 is localized at the PM and responsible for root epidermal PM Ca2+-permeable conductance, which is activated by extracellular OH⋅. High concentration of NaCl promotes extracellular formation of OH⋅ and accumulation of AtANN1 in membranes, and promotes secondary root formation. AtANN1-mediated Ca2+ influx through the PM depends on extracellular Ca2+ and ROS, and the atann1 mutant shows reduced secondary root formation and reduced activation of NaCl-induced transcription under salinity stress conditions, suggesting a role of AtANN1 in root cell adaptation to salinity in Arabidopsis.

Salinity-induced Na+ accumulation in the cytosol triggers [Ca2+]cyt elevation, leading to activation of Rboh/Nox and apoplastic H2O2 accumulation. By interacting with transition metals such as Fe in the cell wall, H2O2 forms OH⋅. OH⋅ directly activates both outward-rectifying depolarization-activating K+ channels (GORKs) and K+-permeable NSCCs, resulting in K+ leakage from roots. The absolute concentration of K+ is essential to confer salinity stress tolerance, and the loss of K+ is suggested to play a primary role in the activation of caspase-like proteases and PCD.

Salinity also induces accumulation of polyamines. Polyamines could generate ROS as a substrate of amine oxidases in the apoplast. Both OH⋅ and polyamines may provoke a substantial remodeling of PM conductance of cations and anions and affect Ca2+ signaling in plants including halophytes. Crosstalk between ROS and polyamines in the regulation of PM ion transport may reveal a novel function of ROS production as signaling molecules during salinity adaptation.

A Ca2+-ROS Signaling Network in Osmotic Responses in Roots under Salinity Stress

Osmotic-shock induces Ca2+ influx followed by ROS production in many cell types in plants. The Ca2+ influx and Nox-mediated ROS production triggered by osmotic shock both require extracellular Ca2+, suggesting that PM Ca2+ influx is a prerequisite for ROS production.

mid1-complementing activities (MCAs), putative PM Ca2+-permeable MS channel components are suggested to play a role in the regulation of mechanical responses via signal transduction pathways dependent on Ca2+ and ROS. The overexpression of OsMCA1 enhances Rboh/Nox-mediated ROS production in rice cultured cells. MCA1 and ROS produced by RbohD and/or RbohF may play roles in the modulation of osmosensitive metabolic changes. Overexpression of MCAs enhances the expression of touch-inducible gene TCH3/CML12 encoding a CML in Arabidopsis.

Apoplastic ROS production plays a key role in regulating cell wall metabolism, e.g., cross-linking of polysaccharides and glycoproteins to control cell wall rigidity. H2O2 is also transported to the cytosol by PM aquaporins to modify the cysteine residues of target proteins, thereby promoting redox signaling.

These findings suggest the following initial PM signaling mechanism in response to osmo-stimulation under salinity stress (Figure 1): Salinity stress causes osmotic shock to trigger the activation of PM MS Ca2+-permeable channels and Ca2+ influx. Elevated cytosolic Ca2+ leads to the activation of various Ca2+ sensor proteins including CaMs, CMLs, CBLs, and CDPKs. Rbohs are synergistically activated by Ca2+-binding to the EF-hand motifs and phosphorylation to produce ROS. Elevated cytosolic Ca2+ and apoplastic ROS may also activate not only ROS-activated PM Ca2+-permeable channels including annexins but also as-yet-unidentified Ca2+-permeable channels/transporters localized at the endomembranes to sustain further Ca2+ mobilization. The signaling network dependent on Ca2+ and ROS may play a crucial role in regulating downstream events such as the Ca2+-dependent activation of Na+/H+ exchangers, SOS1 and NHX1, Na+ efflux from the cytosol, regulation of xylem loading of Na+, Na+ exclusion from leaves, induction of osmolytes and osmo-protective proteins, and the retention of cytosolic ion balance. Once this signaling is over, elevated [Ca2+]cyt would be reverted by the orchestrated action of Ca2+ exchangers and Ca2+-ATPases at the PM and tonoplast (reviewed in ).

Calcium-dependent protein kinases and CBL-CIPK complexes are suggested to transduce the osmotic signal to regulate downstream posttranslational modification and gene transcription. Furthermore, transcription factors such as calmodulin-binding transcription activators (CAMTAs; ) are suggested to be directly activated by Ca2+/CaM. Interestingly, a recent comparative expression study in glycophytes and halophytes revealed that the induction of Ca2+/CaM-like proteins such as CDPKs are clearly enhanced in halophytes against salinity stress. Such Ca2+-binding proteins may play roles as important ‘amplifier’ of initial PM Ca2+ influx and Rboh-mediated ROS production in salinity stress signaling.

Ca2+ signaling also plays a critical role in salinity stress-triggered systemic signaling. A cation channel TPC1 is reported to be involved in the propagation of salinity stress-triggered systemic Ca2+ wave in roots, and may also be contributing to whole-plant resistance to salinity stress in Arabidopsis. Ca2+-ROS waves involving TPC1 may elicit systemic molecular responses in target organs and contribute to whole-plant stress tolerance.

Hydrogen peroxide transported from the apoplast to the cytosol by PM aquaporins may also interact with O2⋅− generated in the mitochondria under salinity stress to generate OH⋅ in the cytosol by Fenton reaction, which could activate NSCCs from the cytosolic site. As NSCCs are permeable to Na+, Ca2+, and K+, this activation may enhance Na+ uptake and K+ loss, further causing the cytosolic K+/Na+ imbalance. The resultant K+ loss from the cell may induce activation of caspase-like proteases and leading to PCD. Moreover, OH⋅-induced activation of NSCCs may further boost Ca2+ uptake, providing an additional positive feedback loop.

Possible Function of Initial ROS Production and Downstream Signaling Events during Stress Adaptation in Halophytes

The salt tolerance of halophytes is typically examined after long-term exposure to different NaCl concentrations. However, plant responses to salinity may be determined by rapid perception of salt shock that occurs within hours.

Recent comparative studies of three Brassicaceae species, namely two halophytes, Cakile maritime and Thellungiella salsuginea, and a glycophyte, Arabidopsis thaliana, demonstrated that both osmotic potential changes and enhanced transient ROS production occurred in the halophyte roots within hours of exposure to NaCl, and subsequently enhanced the activation of antioxidant defenses as well as expression of transcription factors in the leaves and roots under long-term salinity stress. In contrast, the ROS accumulation continued in the glycophyte, Arabidopsis, during the entire observation period, indicating that osmotic shock triggered by salinity stress may activate the initial production of ROS, and this phase is the basis of all functional changes leading to a second phase to activate defense mechanisms. The early production of H2O2 by RbohD and RbohF is suggested to be required for salinity-induced antioxidant defense responses in Arabidopsis under short-term stress treatments. Interestingly, the Nox activity decreased under salinity stress in a glycophyte (B. juncea), while it was unaffected in a halophyte (S. portulacastrum). These findings suggest that early production of low levels of H2O2 acts as an acclimation signal to trigger a preconditioning response by inducing antioxidant enzyme activities in order to efficiently cope with the subsequent production of ROS and lipid peroxidation, thereby preventing or minimizing salinity stress-derived injuries in several halophytes. Regulatory mechanisms of Nox-mediated ROS production in the salinity stress response have not yet been examined genetically in halophytes. Future studies on Rbohs/Noxs in various plant species including halophytes may reveal a novel function of ROS production as signaling molecules during salinity adaptation.

Halophytes do not always need to possess high antioxidant activity because of their higher capacity to prevent ROS generation. Salt-tolerant species equipped with efficient mechanisms for Na+ exclusion from the cytosol may not require a high level of antioxidant activity. Such exclusion is most probably achieved by the orchestrated action of several complementary mechanisms including SOS1-mediated Na+ exclusion from the cell, vacuolar Na+ sequestration by tonoplast NHXs and efficient control of tonoplast fast (FV) and slow (SV) channels to prevent Na+ back-leak into the cytosol.

Although a rapid [Ca2+]cyt increase mediated by PM Ca2+-permeable MS channels and their interacting molecules is a hallmark response to osmotic stress, Ca2+-independent osmotic sensory mechanisms may also play a role. Effectors of ROS and signaling cascades downstream of Rbohs need to be elucidated to better understand their roles. The crosstalk of Rboh/Nox-mediated Ca2+-dependent ROS production with other signaling pathways involving ABA, MAPK, and NO as well as jasmonic acid may be important in transcriptional regulation.

In addition, mild salinity stress in the seedling stage induces osmotic priming in Arabidopsis. Since salinity stress has been shown to affect DNA methylation status of many promoters in soybean, the promoter regions of Rboh in halophytes may have characteristic consensus sequences involved in chromatin modification, and may, thus, enhance plant salinity tolerance.

Conflict of Interest Statement

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

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    Kurusu T. Kuchitsu K. Nakano M. Nakayama Y. Iida H. (2013 ). Plant mechanosensing and Ca2+ transport. Trends Plant Sci. 18 227–233.

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    Kurusu T. Nishikawa D. Yamazaki Y. Gotoh M. Nakano M. Hamada H. (2012a ). Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol. 12:11

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    Kurusu T. Yamanaka T. Nakano M. Takiguchi A. Ogasawara Y. Hayashi T. (2012b ). Involvement of the putative Ca2+-permeable mechanosensitive channels, NtMCA1 and NtMCA 2, in Ca2+ uptake, Ca2+-dependent cell proliferation and mechanical stress-induced gene expression in tobacco (Nicotiana tabacum) BY-2 cells. J. Plant Res. 125 555–568.

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    Laohavisit A. Davies J. M. (2011 ). Annexins. New Phytol. 189 40–53.

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    Laohavisit A. Shang Z. Rubio L. Cuin T. A. Véry A. A. Wang A. (2012 ). Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+-permeable conductance in root cells. Plant Cell 24 1522–1533.

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    Monshausen G. B. Gilroy S. (2009 ). Feeling green: mechanosensing in plants. Trends Cell Biol. 19 228–235.

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    Munns R. Tester M. (2008 ). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59 651–681.

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    Mylona P. V. Polidoros A. N. Scandalios J. G. (2007 ). Antioxidant gene responses to ROS-generating xenobiotics in developing and germinated scutella of maize. J. Exp. Bot. 58 1301–1312.

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    Nakagawa Y. Katagiri T. Shinozaki K. Qi Z. Tatsumi H. Furuichi T. (2007 ). Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc. Natl. Acad. Sci. U.S.A. 104 3639–3644.

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    Nakano M. Iida K. Nyunoya H. Iida H. (2011 ). Determination of structural regions important for Ca2+ uptake activity in Arabidopsis MCA1 and MCA2 expressed in yeast. Plant Cell Physiol. 52 1915–1930.

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    O’Brien J. A. Daudi A. Butt V. S. Bolwell G. P. (2012 ). Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236 765–779.

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    Ogasawara Y. Kaya H. Hiraoka G. Yumoto F. Kimura S. Kadota Y. (2008 ). Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J. Biol. Chem. 283 8885–8892.

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  59. 59.
    CAMTA 1 regulates drought responses in Arabidopsis thaliana · 2013
    No notice
  60. 60.

    Pottosin I. Velarde-Buendía A. M. Bose J. Zepeda-Jazo I. Shabala S. Dobrovinskaya O. (2014 ). Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J. Exp. Bot. 65 1271–1283.

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    Reguera M. Bassil E. Blumwald E. (2014 ). Intracellular NHX-type cation/H+ antiporters in plants. Mol. Plant 7 261–263.

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    Rengasamy P. (2006 ). World salinization with emphasis on Australia. J. Exp. Bot. 57 1017–1023.

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    Rodrigo-Moreno A. Andrés-Colás N. Poschenrieder C. Gunsé B. Peñarrubia L. Shabala S. (2013 ). Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant Cell Environ. 36 844–855.

    Not in our library10.1111/pce.12020

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    Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome · 2013
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    Shabala S. (2009 ). Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J. Exp. Bot. 60 709–712.

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    Shabala S. Newman I. (2000 ). Salinity effects on the activity of plasma membrane H+ and Ca2+ transporters in bean leaf mesophyll: masking role of the cell wall. Ann. Bot. 85 681–686.

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    Shabala S. Pottosin I. (2014 ). Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol. Plant. 151 257–279.

    Not in our library10.1111/ppl.12165

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    The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter · 2000
    Not checked
  70. 70.
    Structural characterization of the mechanosensitive channel candidate MCA2 from Arabidopsis thaliana. · 2014
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    Sirichandra C. Gu D. Hu H. C. Davanture M. Lee S. Djaoui M. (2009 ). Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583 2982–2986.

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    Not checked
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    Spoel S. H. Loake G. J. (2011 ). Redox-based protein modifications: the missing link in plant immune signalling. Curr. Opin. Plant Biol. 14 358–364.

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    Srivastava A. K. Srivastava S. Lokhande V. H. D’souza S. F. Suprasanna P. (2015 ). Salt stress reveales differential antioxidant and energetics responses in glycophyte (Brassica juncea L.) and halophyte (Sesuvium portulacastrum L.). Front. Environ. Sci. 3:19

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    Sumimoto H. (2008 ). Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275 3249–3277.

    Not in our library10.1111/j.1742-4658.2008.06488.x

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    Sunarpi Horie T. Motoda J. Kubo M. Yang H. Yoda K. (2005 ). Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J. 44 928–938.

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    Tada Y. Komatsubara S. Kurusu T. (2014 ). Growth and physiological adaptation of whole plants and cultured cells from a halophyte turf grass under salt stress. AoB Plants 6:plu041

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    Takeda S. Gapper C. Kaya H. Bell E. Kuchitsu K. Dolan L. (2008 ). Local positive feedback regulation determines cell shape in root hair cells. Science 319 1241–1244.

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    Tracy F. E. Gilliham M. Dodd A. N. Webb A. A. Tester M. (2008 ). NaCl-induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ. 31 1063–1073.

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    Urao T. Yakubov B. Satoh R. Yamaguchi-Shinozaki K. Seki M. Hirayama T. (1999 ). A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11 1743–1754.

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    Wang Q. Wu C. Xie B. Liu Y. Cui J. Chen G. (2012 ). Model analysing the antioxidant responses of leaves and roots of switchgrass to NaCl-salinity stress. Plant Physiol. Biochem. 58 288–296.

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    Weinl S. Kudla J. (2009 ). The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol. 184 517–528.

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    Wohlbach D. J. Quirino B. F. Sussman M. R. (2008 ). Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20 1101–1117.

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    Wormit A. Butt S. M. Chairam I. McKenna J. F. Nunes-Nesi A. Kjaer L. (2012 ). Osmosensitive changes of carbohydrate metabolism in response to cellulose biosynthesis inhibition. Plant Physiol. 159 105–117.

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    Xie Y. J. Xu S. Han B. Wu M. Z. Yuan X. X. Han Y. (2011 ). Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J. 66 280–292.

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    Xu P. Liu Z. Fan X. Gao J. Zhang X. Zhang X. (2013 ). De novo transcriptome sequencing and comparative analysis of differentially expressed genes in Gossypium aridum under salt stress. Gene 525 26–34.

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    Yuan F. Yang H. Xue Y. Kong D. Ye R. Li C. (2014 ). OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514 367–371.

    Not in our library10.1038/nature13593

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