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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (1 March 2018) | Viewed by 79914

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Special Issue Editors

Prof. Dr. Sergey Shabala

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Tasmanian Institute of Agriculture, College of Science and Engineering, University of Tasmania, Hobart 7001, Australia
Interests: stress physiology; membrane transport; extreme temperature; salinity stress; drought stress; oxidative stress
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Vadim V. Demidchik

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Department of Plant Cell Biology and Bioengineering, Biological Faculty, Belarusian State University, 220030, 4 Independence Square, Minsk, Belarus
Interests: ion channels; signaling; receptors and electrophysiology; programmed cell death; mineral nutrition; reactive oxygen and nitrogen species; plant micropropagation and vegetative cloning; brassinosteroids; charophyte algae; phenomics

Prof. Dr. Igor Pottosin

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Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Colima, México
Interests: plant electrophysiology; abiotic stress responses; vacuole; polyamines; ROS signaling; calcium signaling

Special Issue Information

Dear Colleagues,

Biologic membranes are indispensable components of living eukaryotic cells, which separate cytoplasm from the external medium and organelles from the cytoplasm, thus, underlying the unique environment in each of these subcellular compartments. They not only prevent the free movement of molecules, but also underlie a multitude of other essential functions, including nutrient acquisition, signal perception and processing, electrical phenomena, water balance, and ionic homeostasis. Membranes are also central in the perception of external stimuli from a constantly-changing environment and co-ordination of respective plant responses. Both mineral uptake and signaling are mediated by so-called transport proteins that “occupy” at least 5% of plant genome. These transport proteins are differentially expressed in various membranes and tissues. Numerous electrophysiological and molecular studies have been undertaken to understand how the membrane transport network and its individual components operate. This volume summarizes and reviews some of this work and provides a timely update in the field revealing the role, functional expression patterns, and regulatory modes of some plasma- and organelle-membrane-based cation and anion transporters that enables plant core functions, such as growth, development, and adaptive responses.

Prof. Sergey Shabala
Prof. Vadim V. Demidchik
Prof. Igor Pottosin
Guest Editors

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Keywords

membrane
organelle
plant
ion channels
ionic homeostasis
water balance
signal perception
signal processing
nutrient acquisition
electrical phenomena

Published Papers (12 papers)

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Research

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13 pages, 1498 KiB

Open AccessArticle

Na⁺-Dependent High-Affinity Nitrate, Phosphate and Amino Acids Transport in Leaf Cells of the Seagrass Posidonia oceanica (L.) Delile

by Lourdes Rubio, Delia García-Pérez, María Jesús García-Sánchez and José A. Fernández

Int. J. Mol. Sci. 2018, 19(6), 1570; https://doi.org/10.3390/ijms19061570 - 24 May 2018

Cited by 12 | Viewed by 3349

Abstract

Posidonia oceanica (L.) Delile is a seagrass, the only group of vascular plants to colonize the marine environment. Seawater is an extreme yet stable environment characterized by high salinity, alkaline pH and low availability of essential nutrients, such as nitrate and phosphate. Classical depletion experiments, membrane potential and cytosolic sodium measurements were used to characterize the high-affinity NO₃⁻, Pi and amino acids uptake mechanisms in this species. Net uptake rates of both NO₃⁻ and Pi were reduced by more than 70% in the absence of Na⁺. Micromolar concentrations of NO₃⁻ depolarized mesophyll leaf cells plasma membrane. Depolarizations showed saturation kinetics (Km = 8.7 ± 1 μM NO₃⁻), which were not observed in the absence of Na⁺. NO₃⁻ induced depolarizations at increasing Na⁺ also showed saturation kinetics (Km = 7.2 ± 2 mM Na⁺). Cytosolic Na⁺ measured in P. oceanica leaf cells (17 ± 2 mM Na⁺) increased by 0.4 ± 0.2 mM Na⁺ upon the addition of 100 μM NO₃⁻. Na⁺-dependence was also observed for high-affinity l-ala and l-cys uptake and high-affinity Pi transport. All together, these results strongly suggest that NO₃⁻, amino acids and Pi uptake in P. oceanica leaf cells are mediated by high-affinity Na⁺-dependent transport systems. This mechanism seems to be a key step in the process of adaptation of seagrasses to the marine environment. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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21 pages, 1852 KiB

Open AccessArticle

Functional Analysis of the Arabidopsis thaliana CDPK-Related Kinase Family: AtCRK1 Regulates Responses to Continuous Light

by Abu Imran Baba, Gábor Rigó, Ferhan Ayaydin, Ateeq Ur Rehman, Norbert Andrási, Laura Zsigmond, Ildikó Valkai, János Urbancsok, Imre Vass, Taras Pasternak, Klaus Palme, László Szabados and Ágnes Cséplő

Int. J. Mol. Sci. 2018, 19(5), 1282; https://doi.org/10.3390/ijms19051282 - 25 Apr 2018

Cited by 26 | Viewed by 7658

Abstract

The Calcium-Dependent Protein Kinase (CDPK)-Related Kinase family (CRKs) consists of eight members in Arabidopsis. Recently, AtCRK5 was shown to play a direct role in the regulation of root gravitropic response involving polar auxin transport (PAT). However, limited information is available about the function of the other AtCRK genes. Here, we report a comparative analysis of the Arabidopsis CRK genes, including transcription regulation, intracellular localization, and biological function. AtCRK transcripts were detectable in all organs tested and a considerable variation in transcript levels was detected among them. Most AtCRK proteins localized at the plasma membrane as revealed by microscopic analysis of 35S::cCRK-GFP (Green Fluorescence Protein) expressing plants or protoplasts. Interestingly, 35S::cCRK1-GFP and 35S::cCRK7-GFP had a dual localization pattern which was associated with plasma membrane and endomembrane structures, as well. Analysis of T-DNA insertion mutants revealed that AtCRK genes are important for root growth and control of gravitropic responses in roots and hypocotyls. While Atcrk mutants were indistinguishable from wild type plants in short days, Atcrk1-1 mutant had serious growth defects under continuous illumination. Semi-dwarf phenotype of Atcrk1-1 was accompanied with chlorophyll depletion, disturbed photosynthesis, accumulation of singlet oxygen, and enhanced cell death in photosynthetic tissues. AtCRK1 is therefore important to maintain cellular homeostasis during continuous illumination. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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17 pages, 1824 KiB

Open AccessArticle

The Role of Potassium Channels in Arabidopsis thaliana Long Distance Electrical Signalling: AKT2 Modulates Tissue Excitability While GORK Shapes Action Potentials

by Tracey Ann Cuin, Ingo Dreyer and Erwan Michard

Int. J. Mol. Sci. 2018, 19(4), 926; https://doi.org/10.3390/ijms19040926 - 21 Mar 2018

Cited by 63 | Viewed by 6409

Abstract

Fast responses to an external threat depend on the rapid transmission of signals through a plant. Action potentials (APs) are proposed as such signals. Plant APs share similarities with their animal counterparts; they are proposed to depend on the activity of voltage-gated ion channels. Nonetheless, despite their demonstrated role in (a)biotic stress responses, the identities of the associated voltage-gated channels and transporters remain undefined in higher plants. By demonstrating the role of two potassium-selective channels in Arabidopsis thaliana in AP generation and shaping, we show that the plant AP does depend on similar Kv-like transport systems to those of the animal signal. We demonstrate that the outward-rectifying potassium-selective channel GORK limits the AP amplitude and duration, while the weakly-rectifying channel AKT2 affects membrane excitability. By computational modelling of plant APs, we reveal that the GORK activity not only determines the length of an AP but also the steepness of its rise and the maximal amplitude. Thus, outward-rectifying potassium channels contribute to both the repolarisation phase and the initial depolarisation phase of the signal. Additionally, from modelling considerations we provide indications that plant APs might be accompanied by potassium waves, which prime the excitability of the green cable. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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10 pages, 1496 KiB

Open AccessArticle

An Anion Conductance, the Essential Component of the Hydroxyl-Radical-Induced Ion Current in Plant Roots

by Igor Pottosin, Isaac Zepeda-Jazo, Jayakumar Bose and Sergey Shabala

Int. J. Mol. Sci. 2018, 19(3), 897; https://doi.org/10.3390/ijms19030897 - 18 Mar 2018

Cited by 11 | Viewed by 4152

Abstract

Oxidative stress signaling is essential for plant adaptation to hostile environments. Previous studies revealed the essentiality of hydroxyl radicals (HO•)-induced activation of massive K⁺ efflux and a smaller Ca²⁺ influx as an important component of plant adaptation to a broad range of abiotic stresses. Such activation would modify membrane potential making it more negative. Contrary to these expectations, here, we provide experimental evidence that HO• induces a strong depolarization, from −130 to −70 mV, which could only be explained by a substantial HO•-induced efflux of intracellular anions. Application of Gd³⁺ and NPPB, non-specific blockers of cation and anion conductance, respectively, reduced HO•-induced ion fluxes instantaneously, implying a direct block of the dual conductance. The selectivity of an early instantaneous HO•-induced whole cell current fluctuated from more anionic to more cationic and vice versa, developing a higher cation selectivity at later times. The parallel electroneutral efflux of K⁺ and anions should underlie a substantial leak of the cellular electrolyte, which may affect the cell’s turgor and metabolic status. The physiological implications of these findings are discussed in the context of cell fate determination, and ROS and cytosolic K⁺ signaling. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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18 pages, 3912 KiB

Open AccessArticle

Hydrogen Peroxide-Induced Root Ca²⁺ and K⁺ Fluxes Correlate with Salt Tolerance in Cereals: Towards the Cell-Based Phenotyping

by Haiyang Wang, Lana Shabala, Meixue Zhou and Sergey Shabala

Int. J. Mol. Sci. 2018, 19(3), 702; https://doi.org/10.3390/ijms19030702 - 01 Mar 2018

Cited by 51 | Viewed by 5035

Abstract

Salinity stress-induced production of reactive oxygen species (ROS) and associated oxidative damage is one of the major factors limiting crop production in saline soils. However, the causal link between ROS production and stress tolerance is not as straightforward as one may expect, as ROS may also play an important signaling role in plant adaptive responses. In this study, the causal relationship between salinity and oxidative stress tolerance in two cereal crops—barley (Hordeum vulgare) and wheat (Triticum aestivum)—was investigated by measuring the magnitude of ROS-induced net K⁺ and Ca²⁺ fluxes from various root tissues and correlating them with overall whole-plant responses to salinity. We have found that the association between flux responses to oxidative stress and salinity stress tolerance was highly tissue specific, and was also dependent on the type of ROS applied. No correlation was found between root responses to hydroxyl radicals and the salinity tolerance. However, when oxidative stress was administered via H₂O₂ treatment, a significant positive correlation was found for the magnitude of ROS-induced K⁺ efflux and Ca²⁺ uptake in barley and the overall salinity stress tolerance, but only for mature zone and not the root apex. The same trends were found for wheat. These results indicate high tissue specificity of root ion fluxes response to ROS and suggest that measuring the magnitude of H₂O₂-induced net K⁺ and Ca²⁺ fluxes from mature root zone may be used as a tool for cell-based phenotyping in breeding programs aimed to improve salinity stress tolerance in cereals. Full article

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10 pages, 5806 KiB

Open AccessArticle

A Novel Sugar Transporter from Dianthus spiculifolius, DsSWEET12, Affects Sugar Metabolism and Confers Osmotic and Oxidative Stress Tolerance in Arabidopsis

by Aimin Zhou, Hongping Ma, Shuang Feng, Shufang Gong and Jingang Wang

Int. J. Mol. Sci. 2018, 19(2), 497; https://doi.org/10.3390/ijms19020497 - 07 Feb 2018

Cited by 33 | Viewed by 5417

Abstract

Plant SWEETs (sugars will eventually be exported transporters) play a role in plant growth and plant response to biotic and abiotic stresses. In the present study, DsSWEET12 from Dianthus spiculifolius was identified and characterized. Real-time quantitative PCR analysis revealed that DsSWEET12 expression was induced by sucrose starvation, mannitol, and hydrogen peroxide. Colocalization experiment showed that the DsSWEET12-GFP fusion protein was localized to the plasma membrane, which was labeled with FM4-64 dye, in Arabidopsis and suspension cells of D. spiculifolius. Compared to wild type plants, transgenic Arabidopsis seedlings overexpressing DsSWEET12 have longer roots and have a greater fresh weight, which depends on sucrose content. Furthermore, a relative root length analysis showed that transgenic Arabidopsis showed higher tolerance to osmotic and oxidative stresses. Finally, a sugar content analysis showed that the sucrose content in transgenic Arabidopsis was less than that in the wild type, while fructose and glucose contents were higher than those in the wild type. Taken together, our results suggest that DsSWEET12 plays an important role in seedling growth and plant response to osmotic and oxidative stress in Arabidopsis by influencing sugar metabolism. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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14 pages, 10602 KiB

Open AccessArticle

T-DNA Tagging-Based Gain-of-Function of OsHKT1;4 Reinforces Na Exclusion from Leaves and Stems but Triggers Na Toxicity in Roots of Rice Under Salt Stress

by Yuuka Oda, Natsuko I. Kobayashi, Keitaro Tanoi, Jian Feng Ma, Yukiko Itou, Maki Katsuhara, Takashi Itou and Tomoaki Horie

Int. J. Mol. Sci. 2018, 19(1), 235; https://doi.org/10.3390/ijms19010235 - 12 Jan 2018

Cited by 23 | Viewed by 5009

Abstract

The high affinity K⁺ transporter 1;4 (HKT1;4) in rice (Oryza sativa), which shows Na⁺ selective transport with little K⁺ transport activity, has been suggested to be involved in reducing Na in leaves and stems under salt stress. However, detailed physiological roles of OsHKT1;4 remain unknown. Here, we have characterized a transfer DNA (T-DNA) insertion mutant line of rice, which overexpresses OsHKT1;4, owing to enhancer elements in the T-DNA, to gain an insight into the impact of OsHKT1;4 on salt tolerance of rice. The homozygous mutant (the O/E line) accumulated significantly lower concentrations of Na in young leaves, stems, and seeds than the sibling WT line under salt stress. Interestingly, however, the mutation rendered the O/E plants more salt sensitive than WT plants. Together with the evaluation of biomass of rice lines, rhizosphere acidification assays using a pH indicator bromocresol purple and ²²NaCl tracer experiments have led to an assumption that roots of O/E plants suffered heavier damages from Na which excessively accumulated in the root due to increased activity of Na⁺ uptake and Na⁺ exclusion in the vasculature. Implications toward the application of the HKT1-mediated Na⁺ exclusion system to the breeding of salt tolerant crop cultivars will be discussed. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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Review

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25 pages, 1410 KiB

Open AccessReview

Transport and Use of Bicarbonate in Plants: Current Knowledge and Challenges Ahead

by Charlotte Poschenrieder, José Antonio Fernández, Lourdes Rubio, Laura Pérez, Joana Terés and Juan Barceló

Int. J. Mol. Sci. 2018, 19(5), 1352; https://doi.org/10.3390/ijms19051352 - 03 May 2018

Cited by 65 | Viewed by 7951

Abstract

Bicarbonate plays a fundamental role in the cell pH status in all organisms. In autotrophs, HCO₃⁻ may further contribute to carbon concentration mechanisms (CCM). This is especially relevant in the CO₂-poor habitats of cyanobacteria, aquatic microalgae, and macrophytes. Photosynthesis of terrestrial plants can also benefit from CCM as evidenced by the evolution of C₄ and Crassulacean Acid Metabolism (CAM). The presence of HCO₃⁻ in all organisms leads to more questions regarding the mechanisms of uptake and membrane transport in these different biological systems. This review aims to provide an overview of the transport and metabolic processes related to HCO₃⁻ in microalgae, macroalgae, seagrasses, and terrestrial plants. HCO₃⁻ transport in cyanobacteria and human cells is much better documented and is included for comparison. We further comment on the metabolic roles of HCO₃⁻ in plants by focusing on the diversity and functions of carbonic anhydrases and PEP carboxylases as well as on the signaling role of CO₂/HCO₃⁻ in stomatal guard cells. Plant responses to excess soil HCO₃⁻ is briefly addressed. In conclusion, there are still considerable gaps in our knowledge of HCO₃⁻ uptake and transport in plants that hamper the development of breeding strategies for both more efficient CCM and better HCO₃⁻ tolerance in crop plants. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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18 pages, 797 KiB

Open AccessReview

ROS-Activated Ion Channels in Plants: Biophysical Characteristics, Physiological Functions and Molecular Nature

by Vadim Demidchik

Int. J. Mol. Sci. 2018, 19(4), 1263; https://doi.org/10.3390/ijms19041263 - 23 Apr 2018

Cited by 100 | Viewed by 8094

Abstract

Ion channels activated by reactive oxygen species (ROS) have been found in the plasma membrane of charophyte Nitella flixilis, dicotyledon Arabidopsis thaliana, Pyrus pyrifolia and Pisum sativum, and the monocotyledon Lilium longiflorum. Their activities have been reported in charophyte giant internodes, root trichoblasts and atrichoblasts, pollen tubes, and guard cells. Hydrogen peroxide and hydroxyl radicals are major activating species for these channels. Plant ROS-activated ion channels include inwardly-rectifying, outwardly-rectifying, and voltage-independent groups. The inwardly-rectifying ROS-activated ion channels mediate Ca²⁺-influx for growth and development in roots and pollen tubes. The outwardly-rectifying group facilitates K⁺ efflux for the regulation of osmotic pressure in guard cells, induction of programmed cell death, and autophagy in roots. The voltage-independent group mediates both Ca²⁺ influx and K⁺ efflux. Most studies suggest that ROS-activated channels are non-selective cation channels. Single-channel studies revealed activation of 14.5-pS Ca²⁺ influx and 16-pS K⁺ efflux unitary conductances in response to ROS. The molecular nature of ROS-activated Ca²⁺ influx channels remains poorly understood, although annexins and cyclic nucleotide-gated channels have been proposed for this role. The ROS-activated K⁺ channels have recently been identified as products of Stellar K⁺ Outward Rectifier (SKOR) and Guard cell Outwardly Rectifying K⁺ channel (GORK) genes. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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23 pages, 12939 KiB

Open AccessReview

Roles of Chloroplast Retrograde Signals and Ion Transport in Plant Drought Tolerance

by Chenchen Zhao, Anthony M. Haigh, Paul Holford and Zhong-Hua Chen

Int. J. Mol. Sci. 2018, 19(4), 963; https://doi.org/10.3390/ijms19040963 - 23 Mar 2018

Cited by 21 | Viewed by 7700

Abstract

Worldwide, drought affects crop yields; therefore, understanding plants’ strategies to adapt to drought is critical. Chloroplasts are key regulators of plant responses, and signals from chloroplasts also regulate nuclear gene expression during drought. However, the interactions between chloroplast-initiated retrograde signals and ion channels under stress are still not clear. In this review, we summarise the retrograde signals that participate in regulating plant stress tolerance. We compare chloroplastic transporters that modulate retrograde signalling through retrograde biosynthesis or as critical components in retrograde signalling. We also discuss the roles of important plasma membrane and tonoplast ion transporters that are involved in regulating stomatal movement. We propose how retrograde signals interact with ion transporters under stress. Full article

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22 pages, 2549 KiB

Open AccessReview

Mechanisms of Sodium Transport in Plants—Progresses and Challenges

by Monika Keisham, Soumya Mukherjee and Satish C. Bhatla

Int. J. Mol. Sci. 2018, 19(3), 647; https://doi.org/10.3390/ijms19030647 - 25 Feb 2018

Cited by 144 | Viewed by 12934

Abstract

Understanding the mechanisms of sodium (Na⁺) influx, effective compartmentalization, and efflux in higher plants is crucial to manipulate Na⁺ accumulation and assure the maintenance of low Na⁺ concentration in the cytosol and, hence, plant tolerance to salt stress. Na⁺ influx across the plasma membrane in the roots occur mainly via nonselective cation channels (NSCCs). Na⁺ is compartmentalized into vacuoles by Na⁺/H⁺ exchangers (NHXs). Na⁺ efflux from the plant roots is mediated by the activity of Na⁺/H⁺ antiporters catalyzed by the salt overly sensitive 1 (SOS1) protein. In animals, ouabain (OU)-sensitive Na⁺, K⁺-ATPase (a P-type ATPase) mediates sodium efflux. The evolution of P-type ATPases in higher plants does not exclude the possibility of sodium efflux mechanisms similar to the Na⁺, K⁺-ATPase-dependent mechanisms characteristic of animal cells. Using novel fluorescence imaging and spectrofluorometric methodologies, an OU-sensitive sodium efflux system has recently been reported to be physiologically active in roots. This review summarizes and analyzes the current knowledge on Na⁺ influx, compartmentalization, and efflux in higher plants in response to salt stress. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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12 pages, 4251 KiB

Open AccessReview

Plant Cation-Chloride Cotransporters (CCC): Evolutionary Origins and Functional Insights

by Sam W. Henderson, Stefanie Wege and Matthew Gilliham

Int. J. Mol. Sci. 2018, 19(2), 492; https://doi.org/10.3390/ijms19020492 - 06 Feb 2018

Cited by 19 | Viewed by 4825

Abstract

Genomes of unicellular and multicellular green algae, mosses, grasses and dicots harbor genes encoding cation-chloride cotransporters (CCC). CCC proteins from the plant kingdom have been comparatively less well investigated than their animal counterparts, but proteins from both plants and animals have been shown to mediate ion fluxes, and are involved in regulation of osmotic processes. In this review, we show that CCC proteins from plants form two distinct phylogenetic clades (CCC1 and CCC2). Some lycophytes and bryophytes possess members from each clade, most land plants only have members of the CCC1 clade, and green algae possess only the CCC2 clade. It is currently unknown whether CCC1 and CCC2 proteins have similar or distinct functions, however they are both more closely related to animal KCC proteins compared to NKCCs. Existing heterologous expression systems that have been used to functionally characterize plant CCC proteins, namely yeast and Xenopus laevis oocytes, have limitations that are discussed. Studies from plants exposed to chemical inhibitors of animal CCC protein function are reviewed for their potential to discern CCC function in planta. Thus far, mutations in plant CCC genes have been evaluated only in two species of angiosperms, and such mutations cause a diverse array of phenotypes—seemingly more than could simply be explained by localized disruption of ion transport alone. We evaluate the putative roles of plant CCC proteins and suggest areas for future investigation. Full article

(This article belongs to the Special Issue Plasma-Membrane Transport)

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