Ion channels in plants Hedrich, Rainer
Physiological reviews
92, Številka:
4
Journal Article
Recenzirano
Since the first recordings of single potassium channel activities in the plasma membrane of guard cells more than 25 years ago, patch-clamp studies discovered a variety of ion channels in all cell ...types and plant species under inspection. Their properties differed in a cell type- and cell membrane-dependent manner. Guard cells, for which the existence of plant potassium channels was initially documented, advanced to a versatile model system for studying plant ion channel structure, function, and physiology. Interestingly, one of the first identified potassium-channel genes encoding the Shaker-type channel KAT1 was shown to be highly expressed in guard cells. KAT1-type channels from Arabidopsis thaliana and its homologs from other species were found to encode the K(+)-selective inward rectifiers that had already been recorded in early patch-clamp studies with guard cells. Within the genome era, additional Arabidopsis Shaker-type channels appeared. All nine members of the Arabidopsis Shaker family are localized at the plasma membrane, where they either operate as inward rectifiers, outward rectifiers, weak voltage-dependent channels, or electrically silent, but modulatory subunits. The vacuole membrane, in contrast, harbors a set of two-pore K(+) channels. Just very recently, two plant anion channel families of the SLAC/SLAH and ALMT/QUAC type were identified. SLAC1/SLAH3 and QUAC1 are expressed in guard cells and mediate Slow- and Rapid-type anion currents, respectively, that are involved in volume and turgor regulation. Anion channels in guard cells and other plant cells are key targets within often complex signaling networks. Here, the present knowledge is reviewed for the plant ion channel biology. Special emphasis is drawn to the molecular mechanisms of channel regulation, in the context of model systems and in the light of evolution.
Stomatal guard cells control leaf CO2 intake and concomitant water loss to the atmosphere. When photosynthetic CO2 assimilation is limited and the ratio of CO2 intake to transpiration becomes ...suboptimal, guard cells, sensing the rise inCO2 concentration in the substomatal cavity, deflate and the stomata close. Screens for mutants that do not close in response to experimentally imposed high CO2 atmospheres identified the guard cell-expressed Slowly activating anion channel, SLAC1, as the key player in the regulation of stomatal closure. SLAC1 evolved, though, before the emergence of guard cells. In Arabidopsis, SLAC1 is the founder member of a family of anion channels, which comprises four homologues. SLAC1 and SLAH3 mediate chloride and nitrate transport in guard cells, while SLAH1, SLAH2 and SLAH3 are engaged in root nitrate and chloride acquisition, and anion translocation to the shoot. The signal transduction pathways involved in CO2, water stress and nutrient-sensing activate SLAC/SLAH via distinct protein kinase/phosphatase pairs. In this review, we discuss the role that SLAC/SLAH channels play in guard cell closure, on the one hand, and in the root–shoot continuum on the other, along with the molecular basis of the channels’ anion selectivity and gating.
Today, the base code of DNA is mostly determined through sequencing by synthesis as provided by the Illumina sequencers. Although highly accurate, resulting reads are short, making their analyses ...challenging. Recently, a new technology, single molecule real-time (SMRT) sequencing, was developed that could address these challenges, as it generates reads of several thousand bases. But, their broad application has been hampered by a high error rate. Therefore, hybrid approaches that use high-quality short reads to correct erroneous SMRT long reads have been developed. Still, current implementations have great demands on hardware, work only in well-defined computing infrastructures and reject a substantial amount of reads. This limits their usability considerably, especially in the case of large sequencing projects.
Here we present proovread, a hybrid correction pipeline for SMRT reads, which can be flexibly adapted on existing hardware and infrastructure from a laptop to a high-performance computing cluster. On genomic and transcriptomic test cases covering Escherichia coli, Arabidopsis thaliana and human, proovread achieved accuracies up to 99.9% and outperformed the existing hybrid correction programs. Furthermore, proovread-corrected sequences were longer and the throughput was higher. Thus, proovread combines the most accurate correction results with an excellent adaptability to the available hardware. It will therefore increase the applicability and value of SMRT sequencing.
proovread is available at the following URL: http://proovread.bioapps.biozentrum.uni-wuerzburg.de.
The non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be an ancient messenger for cellular communication conserved across biological kingdoms. GABA has well-defined signalling ...roles in animals; however, whilst GABA accumulates in plants under stress it has not been determined if, how, where and when GABA acts as an endogenous plant signalling molecule. Here, we establish endogenous GABA as a bona fide plant signal, acting via a mechanism not found in animals. Using Arabidopsis thaliana, we show guard cell GABA production is necessary and sufficient to reduce stomatal opening and transpirational water loss, which improves water use efficiency and drought tolerance, via negative regulation of a stomatal guard cell tonoplast-localised anion transporter. We find GABA modulation of stomata occurs in multiple plants, including dicot and monocot crops. This study highlights a role for GABA metabolism in fine tuning physiology and opens alternative avenues for improving plant stress resilience.
Temporally and spatially defined changes in Ca2+ concentration in distinct compartments of cells represent a universal information code in plants. Recently, it has become evident that Ca2+ signals ...not only govern intracellular regulation but also appear to contribute to long distance or even organismic signal propagation and physiological response regulation. Ca2+ signals are shaped by an intimate interplay of channels and transporters, and during past years important contributing individual components have been identified and characterized. Ca2+ signals are translated by an elaborate toolkit of Ca2+-binding proteins, many of which function as Ca2+ sensors, into defined downstream responses. Intriguing progress has been achieved in identifying specific modules that interconnect Ca2+ decoding proteins and protein kinases with downstream target effectors, and in characterizing molecular details of these processes. In this review, we reflect on recent major advances in our understanding of Ca2+ signaling and cover emerging concepts and existing open questions that should be informative also for scientists that are currently entering this field of ever-increasing breath and impact.
Electrical signalling over long distances is an efficient way of achieving cell-to-cell communication in living organisms. In plants, the phloem can be considered as a ‘green cable’ that allows the ...transmission of action potentials (APs) induced by stimuli such as wounding and cold. Measuring phloem potential changes and separating them from secondary responses of surrounding tissues can be achieved using living aphids as bioelectrodes. Two glutamate receptor-like genes (GLR3.3 and 3.6) were identified as being involved in the propagation of electrical activity from the damaged to undamaged leaves. However, phloem APs are initiated and propagated independently of these glutamate receptors. Here, we propose new screening approaches to obtain further information on the components required for electrical signalling in phloem cables.
The phloem of higher plants serves as a cable for long-distance electrical signalling.
Aphids can be used as bioelectrodes to study plant electrical communication.
Leaf wounding and cold stimuli induce phloem-travelling APs.
APs do not require the GLR 3.3/3.6 glutamate receptor pair.
•The plant vacuole is the major site for sugar storage.•The activities of vacuolar sugar porters determine plant yield and stress tolerance.•The vacuole is energized by two proton pumps, the V-ATPase ...and the tonoplast pyrophosphatase. However, in some species a plasma membrane P3A/B type ATPase contributes in addition to the proton-motive force.•Vacuolar sugar transporters helped to identify target mechanisms allowing to direct membrane proteins to the tonoplast.
The ability of higher plants to store sugars is of crucial importance for plant development, adaption to endogenous or environmental cues and for the economic value of crop species. Sugar storage and accumulation, and its homeostasis in plant cells are managed by the vacuole. Although transport of sugars across the vacuolar membrane has been monitored for about four decades, the molecular entities of the transporters involved have been identified in the last 10 years only. Thus, it is just recently that our pictures of the transporters that channel the sugar load across the tonoplast have gained real shape. Here we describe the molecular nature and regulation of an important group of tonoplast sugar transporter (TST) allowing accumulation of sugars against large concentration gradients. In addition, we report on proton-driven tonoplast sugar exporters and on facilitators, which are also involved in balancing cytosolic and vacuolar sugar levels.
The most prominent ion channel localized in plant vacuoles is the slow activating SV type. Slow vacuolar （SV） channels were discovered by patch clamp studies as early as 1986. In the following two ...decades, numerous studies revealed that these calcium- and voltage-activated, nonselective cation channels are expressed in the vacuoles of all plants and every plant tissue. The voltage-dependent properties of the SV channel are susceptible to modulation by calcium, pH, redox state, as well as regulatory proteins. In Arabidopsis, the SV channel is encoded by the AtTPC1 gene, and even though its gene product represents the by far largest conductance of the vacuolar membrane, tpcl-loss-of-function mutants appeared not to be impaired in major physiological functions such as growth, development, and reproduction. In contrast, the fou2 gain-of-function point mutation D454N within TPC1 leads to a pronounced growth phenotype and increased synthesis of the stress hormone jasmonate. Since the TPC1 gene is present in all land plants, it likely encodes a very general function. In this review, we will discuss major SV channel properties and their impact on plant cell physiology.
During drought, abscisic acid (ABA) induces closure of stomata via a signaling pathway that involves the calcium (Ca2+)-independent protein kinase OST1, as well as Ca2+-dependent protein kinases. ...However, the interconnection between OST1 and Ca2+ signaling in ABA-induced stomatal closure has not been fully resolved.
ABA-induced Ca2+ signals were monitored in intact Arabidopsis leaves, which express the ratiometric Ca2+ reporter R-GECO1-mTurquoise and the Ca2+-dependent activation of S-type anion channels was recorded with intracellular double-barreled microelectrodes.
ABA triggered Ca2+ signals that occurred during the initiation period, as well as in the acceleration phase of stomatal closure. However, a subset of stomata closed in the absence of Ca2+ signals. On average, stomata closed faster if Ca2+ signals were elicited during the ABA response. Loss of OST1 prevented ABA-induced stomatal closure and repressed Ca2+ signals, whereas elevation of the cytosolic Ca2+ concentration caused a rapid activation of SLAC1 and SLAH3 anion channels.
Our data show that the majority of Ca2+ signals are evoked during the acceleration phase of stomatal closure, which is initiated by OST1. These Ca2+ signals are likely to activate Ca2+-dependent protein kinases, which enhance the activity of S-type anion channels and boost stomatal closure.
Upon stimulation, plants elicit electrical signals that can travel within a cellular network analogous to the animal nervous system. It is well-known that in the human brain, voltage changes in ...certain regions result from concerted electrical activity which, in the form of action potentials (APs), travels within nerve-cell arrays. Electro- and magnetophysiological techniques like electroencephalography, magnetoencephalography, and magnetic resonance imaging are used to record this activity and to diagnose disorders. Here we demonstrate that APs in a multicellular plant system produce measurable magnetic fields. Using atomic optically pumped magnetometers, biomagnetism associated with electrical activity in the carnivorous Venus flytrap, Dionaea muscipula, was recorded. Action potentials were induced by heat stimulation and detected both electrically and magnetically. Furthermore, the thermal properties of ion channels underlying the AP were studied. Beyond proof of principle, our findings pave the way to understanding the molecular basis of biomagnetism in living plants. In the future, magnetometry may be used to study long-distance electrical signaling in a variety of plant species, and to develop noninvasive diagnostics of plant stress and disease.
PDF
