Calcium transport across plant membranes Demidchik, Vadim; Shabala, Sergey; Isayenkov, Stanislav ...
The New phytologist,
October 2018, Letnik:
220, Številka:
1
Journal Article
Recenzirano
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Calcium is an essential structural, metabolic and signalling element. The physiological functions of Ca2+ are enabled by its orchestrated transport across cell membranes, mediated by Ca2+-permeable ...ion channels,Ca2+-ATPases andCa2+/H+ exchangers. Bioinformatics analysis has not determined any Ca2+-selective filters in plant ion channels, but electrophysiological tests do reveal Ca2+ conductances in plant membranes. The biophysical characteristics of plant Ca2+ conductances have been studied in detail and were recently complemented by molecular genetic approaches. Plant Ca2+ conductances are mediated by several families of ion channels, including cyclic nucleotide-gated channels (CNGCs), ionotropic glutamate receptors, two-pore channel 1 (TPC1), annexins and several types of mechanosensitive channels. Key Ca2+-mediated reactions (e.g. sensing of temperature, gravity, touch and hormones, and cell elongation and guard cell closure) have now been associated with the activities of specific subunits from these families. Structural studies have demonstrated a unique selectivity filter in TPC1, which is passable for hydrated divalent cations. The hypothesis of a ROS-Ca2+ hub is discussed, linking Ca2+ transport to ROS generation. CNGC inactivation by cytosolic Ca2+, leading to the termination of Ca2+ signals, is now mechanistically explained. The structure–function relationships of Ca2+-ATPases and Ca2+/H+ exchangers, and their regulation and physiological roles are analysed.
Potassium transport and plant salt tolerance Shabala, Sergey; Cuin, Tracey A
Physiologia Plantarum (København. 1948),
August 2008, Letnik:
133, Številka:
4
Journal Article, Conference Proceeding
Recenzirano
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Salinity is a major abiotic stress affecting approximately 7% of the world's total land area resulting in billion dollar losses in crop production around the globe. Recent progress in molecular ...genetics and plant electrophysiology suggests that the ability of a plant to maintain a high cytosolic K⁺/Na⁺ ratio appears to be critical to plant salt tolerance. So far, the major efforts of plant breeders have been aimed at improving this ratio by minimizing Na⁺ uptake and transport to shoot. In this paper, we discuss an alternative approach, reviewing the molecular and ionic mechanisms contributing to potassium homeostasis in salinized plant tissues and discussing prospects for breeding for salt tolerance by targeting this trait. Major K⁺ transporters and their functional expression under saline conditions are reviewed and the multiple modes of their control are evaluated, including ameliorative effects of compatible solutes, polyamines and supplemental calcium. Subsequently, the genetic aspects of inheritance of K⁺ transport 'markers' are discussed in the general context of salt tolerance as a polygenic trait. The molecular identity of 'salt tolerance' genes is analysed, and prospects for future research and breeding are examined.
Salinity stress tolerance in durum wheat is strongly associated with a plant’s ability to control Na⁺ delivery to the shoot. Two loci, termed Nax1 and Nax2, were recently identified as being critical ...for this process and the sodium transporters HKT1;4 and HKT1;5 were identified as the respective candidate genes. These transporters retrieve Na⁺ from the xylem, thus limiting the rates of Na⁺ transport from the root to the shoot. In this work, we show that the Nax loci also affect activity and expression levels of the SOS1-like Na⁺/H⁺ exchanger in both root cortical and stelar tissues. Net Na+ efflux measured in isolated steles from salt-treated plants, using the non-invasive ion flux measuring MIFE technique, decreased in the sequence: Tamaroi (parental line)>Nax1=Nax2>Nax1:Nax2 lines. This efflux was sensitive to amiloride (a known inhibitor of the Na⁺/H⁺ exchanger) and was mirrored by net H⁺ flux changes. TdSOS1 relative transcript levels were 6–10-fold lower in Nax lines compared with Tamaroi. Thus, it appears that Nax loci confer two highly complementary mechanisms, both of which contribute towards reducing the xylem Na⁺ content. One enhances the retrieval of Na⁺ back into the root stele via HKT1;4 or HKT1;5, whilst the other reduces the rate of Na⁺ loading into the xylem via SOS1. It is suggested that such duality plays an important adaptive role with greater versatility for responding to a changing environment and controlling Na⁺ delivery to the shoot.
Reactive oxygen species (ROS) are central to plant stress response, signalling, development and a multitude of other processes. In this study, the plasma-membrane hydroxyl radical (HR)-activated K⁺ ...channel responsible for K⁺ efflux from root cells during stress accompanied by ROS generation is characterised. The channel showed 16-pS unitary conductance and was sensitive to Ca²⁺, tetraethylammonium, Ba²⁺, Cs⁺ and free-radical scavengers. The channel was not found in the gork1-1 mutant, which lacks a major plasma-membrane outwardly rectifying K⁺ channel. In intact Arabidopsis roots, both HRs and stress induced a dramatic K⁺ efflux that was much smaller in gork1-1 plants. Tests with electron paramagnetic resonance spectroscopy showed that NaCl can stimulate HR generation in roots and this might lead to K⁺-channel activation. In animals, activation of K⁺-efflux channels by HRs can trigger programmed cell death (PCD). PCD symptoms in Arabidopsis roots developed much more slowly in gork1-1 and wild-type plants treated with K⁺-channel blockers or HR scavengers. Therefore, similar to animal counterparts, plant HR-activated K⁺ channels are also involved in PCD. Overall, this study provides new insight into the regulation of plant cation transport by ROS and demonstrates possible physiological properties of plant HR-activated K⁺ channels.
ABSTRACT
This work investigates the role of cytosolic Na+ exclusion in roots as a means of salinity tolerance in wheat, and offers in planta methods for the functional assessment of major ...transporters contributing to this trait. An electrophysiological protocol was developed to quantify the activity of plasma membrane Na+ efflux systems in roots, using the microelectrode ion flux estimation (MIFE) technique. We show that active efflux of Na+ from wheat root epidermal cells is mediated by a SOS1‐like homolog, energized by the plasma membrane H+‐ATPase. SOS1‐like efflux activity was highest in Kharchia 65, a salt‐tolerant bread wheat cultivar. Kharchia 65 also had an enhanced ability to sequester large quantities of Na+ into the vacuoles of root cells, as revealed by confocal microscopy using Sodium Green. These findings were consistent with the highest level of expression of both SOS1 and NHX1 transcripts in plant roots in this variety. In the sensitive wheat varieties, a greater proportion of Na+ was located in the root cell cytosol. Overall, our findings suggest a critical role of cytosolic Na+ exclusion for salinity tolerance in wheat and offer convenient protocols to quantify the contribution of the major transporters conferring this trait, to screen plants for salinity tolerance.
Plant salinity tolerance is a polygenic trait with contributions from genetic, developmental, and physiological interactions, in addition to interactions between the plant and its environment. In ...this study, we show that in salt-tolerant genotypes of barley (Hordeum vulgare), multiple mechanisms are well combined to withstand saline conditions. These mechanisms include: (1) better control of membrane voltage so retaining a more negative membrane potential; (2) intrinsically higher H⁺ pump activity; (3) better ability of root cells to pump Na⁺ from the cytosol to the external medium; and (4) higher sensitivity to supplemental Ca²⁺. At the same time, no significant difference was found between contrasting cultivars in their unidirectional ²²Na⁺ influx or in the density and voltage dependence of depolarization-activated outward-rectifying K⁺ channels. Overall, our results are consistent with the idea of the cytosolic K⁺-to-Na⁺ ratio being a key determinant of plant salinity tolerance, and suggest multiple pathways of controlling that important feature in salt-tolerant plants.
Despite numerous reports implicating polyamines in plant salinity responses, the specific ionic mechanisms of polyamine-mediated adaptation to salt-stress remain elusive. In this work, we show that
...micromolar concentrations of polyamines are efficient in preventing NaCl-induced K
+ efflux from the leaf mesophyll, and that this effect can be attributed to the inhibition of non-selective cation channels in mesophyll. The inhibition by externally applied polyamines developed slowly over time, suggesting a cytosolic mode of action. Overall, we suggest that elevated levels of cellular polyamine may modulate the activity of plasma membrane ion channels, improving ionic relations and assisting in a plant’s adaptation to salinity.
Acidification of the cell wall space outside the plasma membrane is required for plant growth and is the result of proton extrusion by the plasma membrane‐localized H⁺‐ATPases. Here we show that the ...major plasma membrane proton pumps in Arabidopsis, AHA1 and AHA2, interact directly in vitro and in planta with PSY1R, a receptor kinase of the plasma membrane that serves as a receptor for the peptide growth hormone PSY1. The intracellular protein kinase domain of PSY1R phosphorylates AHA2/AHA1 at Thr‐881, situated in the autoinhibitory region I of the C‐terminal domain. When expressed in a yeast heterologous expression system, the introduction of a negative charge at this position caused pump activation. Application of PSY1 to plant seedlings induced rapid in planta phosphorylation at Thr‐881, concomitant with an instantaneous increase in proton efflux from roots. The direct interaction between AHA2 and PSY1R observed might provide a general paradigm for regulation of plasma membrane proton transport by receptor kinases.
Control of ion loading into the xylem has been repeatedly named as a crucial factor determining plant salt tolerance. In this study we further investigate this issue by applying a range of ...biophysical the microelectrode ion flux measurement (MIFE) technique for non-invasive ion flux measurements, the patch clamp technique, membrane potential measurements and physiological (xylem sap and tissue nutrient analysis, photosynthetic characteristics, stomatal conductance) techniques to barley varieties contrasting in their salt tolerance. We report that restricting Na⁺ loading into the xylem is not essential for conferring salinity tolerance in barley, with tolerant varieties showing xylem Na⁺ concentrations at least as high as those of sensitive ones. At the same time, tolerant genotypes are capable of maintaining higher xylem K⁺/Na⁺ ratios and efficiently sequester the accumulated Na⁺ in leaves. The former is achieved by more efficient loading of K⁺ into the xylem. We argue that the observed increases in xylem K⁺ and Na⁺ concentrations in tolerant genotypes are required for efficient osmotic adjustment, needed to support leaf expansion growth. We also provide evidence that K⁺-permeable voltage-sensitive channels are involved in xylem loading and operate in a feedback manner to maintain a constant K⁺/Na⁺ ratio in the xylem sap.
Plant cell growth and stress signaling require Ca²⁺ influx through plasma membrane transport proteins that are regulated by reactive oxygen species. In root cell growth, adaptation to salinity ...stress, and stomatal closure, such proteins operate downstream of the plasma membrane NADPH oxidases that produce extracellular Superoxide anion, a reactive oxygen species that is readily converted to extracellular hydrogen peroxide and hydroxyl radicals, OH˙ In root cells, extracellular OH˙ activates a plasma membrane Ca²⁺ -permeable conductance that permits Ca²⁺ influx. In Arabidopsis thaliana, distribution of this conductance resembles that of annexin1 (ANN1). Annexins are membrane binding proteins that can form Ca²⁺ -permeable conductances in vitro. Here, the Arabidopsis loss-of-function mutant for annexin1 (Atann1) was found to lack the root hair and epidermal OH˙-activated Ca²⁺ -and K⁺ -permeable conductance. This manifests in both impaired root cell growth and ability to elevate root cell cytosolic free Ca²⁺ in response to OH˙. An OH˙-activated Ca²⁺ conductance is reconstituted by recombinant ANN1 in planar lipid bilayers. ANN1 therefore presents as a novel Ca²⁺-permeable transporter providing a molecular link between reactive oxygen species and cytosolic Ca²⁺ in plants.
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