TY - JOUR
AU - González,, Wendy
AB - Potassium, potassium channel, potassium redistribution, voltage gate Potassium is an essential nutrient for plants. The uptake of K+from the soil and its redistribution throughout the plant is accomplished by an ensemble of K+transporters and channels. Detailed investigations on the model plant Arabidopsis thaliana have found a clear picture of the basic principles of these transport processes. The knowledge gained from research on Arabidopsis, however, cannot explain all facets of K+transport in the plant world, as Arabidopsis does not have large seeds and berries like grapes, for instance.Villette et al. (2019)now report for the Vitis K+channel VvK5.1 an expression pattern not previously described in Arabidopsis. Potassium plays an essential role in the life of a plant. Together with organic solutes, it is the most important osmolyte used to establish cell turgor and to drive pressure-dependent processes like stomatal movement, cell elongation and long-distance phloem transport. However, while plants produce sugars in photosynthesis, they are K+ auxotrophic and require sophisticated transport logistics to extract and accumulate potassium from the soil and distribute it throughout the plant. This process involves the shuttling of K+ across several cell membranes mediated by a set of K+ transporters and channels. A cell energizes the uptake of K+ by H+-ATPases that establish an electrical and a proton gradient. Proton-coupled K+ transporters use these gradients for the accumulation of K+. Alternatively, K+ ions can harvest the electrical gradient to enter the cell via potassium channels. Potassium channels can also mediate the release of K+ from a cell when acting in concert with anion channels, for instance during xylem loading. The flux direction of K+ through potassium channels can be rectified by a voltage-gating mechanism. Voltage-gated K+ channels in plants Voltage-gated plant K+ channels are historically called “plant Shaker channels” although they are only distantly related with the Shaker K+ channel from Drosophila melanogaster. Instead, they belong to the cyclic nucleotide-binding domain (CNBD) superfamily that includes cyclic nucleotide-gated channels, metazoan Ether-a-go-go and HCN channels (Riedelsberger et al., 2015; Jegla et al., 2018). Previous studies on the evolutionary origin of plant K+ channels indicate that algae have a large structural variability of (putatively) voltage-gated potassium channels, while higher plants do not, although they comprise an astonishing functional assortment of channels. The diversity of voltage-gated K+ channels observable in Chlorophyta collapsed contemporaneously with the transition of green plants from an aqueous to a dry environment (Gomez-Porras et al., 2012; Riedelsberger et al., 2015; Box 1). The subsequent functional diversification into the various subfamilies observed today in higher plants apparently took place on the basis of a single remaining channel class (red clade in Box 1). In early land plants, e.g. the liverwort Marchantia polymorpha, two clearly distinct K+ channel subfamilies originating from a common ancestor can be found. They might be associated with the basic tasks of K+ uptake and release. Vascular plants, however, likely need more control over their K+ fluxes. Gymnosperms display four or five functionally different K+ channel subfamilies on the basis of the same ancestral structure (Box 2): (i) outward-rectifying Kout channels mediate the efflux of K+ from cells; (ii & iii) inward-rectifying Kin channels (Kin-AKT1 & Kin-KAT1) allow the influx of K+. In their basic functions channels of subfamilies II and III are not different from each other; structurally, however, they show characteristic differences: AKT1-like channels have a longer cytosolic C-terminus, which contains more protein-protein interaction sites than KAT1-like channels; (iv) Kweak channels can switch between uptake-mediating inward-rectification and a non-rectifying status allowing both K+ uptake and release; (v) subunits of the Ksilent type do not form functional channels alone but associate with subunits of other types and modify the features of the heteromeric K+ channels. The potential for hetero-oligomerization adds another level of complexity and plasticity to the family of voltage-gated plant K+ channels (Lebaudy et al., 2008). A functional K+ channel is a tetramer built of four subunits. Hetero-tetramerization is observed within Kout channel subunits and within Kin/Kweak/Ksilent subunits but not in between these two larger groups (Dreyer et al., 1997; Dreyer et al., 2004). Thus, even though higher plants have only a modest number of genes coding for voltage-gated K+ channel subunits (A. thaliana and Vitis vinifera both have 9, for instance), the combinatorial power between them adds substantially to the achievable complexity. The effects that K+ channels can have on a tissue and on cells also depend on their spatial and temporal expression and on their targeting dynamics. Channel subunits with similar functional properties realize individual physiological roles by unique promoter-regulatory elements and by special interaction sites linking them with the cellular targeting machinery (Karnik et al. 2017). Thus, unique features of K+ channels are realized by spatial, temporal and molecular specificity. Box 1. Evolution of voltage-gated plant K+ channels The structural diversity of voltage-gated K+ channels observable in Chlorophyta collapsed contemporaneously with the transition of green plants from an aqueous to a dry environment. The functional diversification of the K+ channels in higher plants then started from one remaining channel class (Gomez-Porras et al., 2012). Early land plants like Marchantia polymorpha have already prototypes of inward-rectifying and outward-rectifying K+ channels. Gymnosperms like Picea abies already display the different subgroups Kout, Kin, Kweak, and Ksilent. Along with the separation of Kin into Kin-a (AKT1) and Kin-b (KAT1), only the number of the different channel types changed during angiosperm evolution. Vitis vinifera has four different genes coding for Kout channel subunits, while Arabidopsis thaliana has only two. The phylogenetic trees were generated with sequence data from Gomez-Porras et al. (2012) for the algal channels, from Sussmilch et al. (2019) for the M. polymorpha, P. abies, and A. thaliana channels and from Nieves-Cordones et al. (2019) for K+ channels from V. vinifera. In this issue Villette et al. (2019) present their findings on the K+ channel gene VvK5.1. Box 2. Same structure – different function Despite a very similar structure, at the functional level voltage-gated plant K+ channels segregate into fundamentally distinct types: Outward-rectifying K+ (Kout) channels open at depolarizing voltages at which the electrochemical driving force for K+ is directed out of the cell. They thus mediate the release of K+ from the cytosol to the apoplastic space (yellow). Inward-rectifying K+ (Kin) channels open at hyperpolarizing voltages at which the electrochemical driving force for K+ is directed into the cell. They thus mediate the uptake of K+ from the apoplastic space (green). The dashed lines indicate the behavior of K+ channels without voltage-gating. Weak-rectifying K+ (Kweak) channels are specialized Kin channels. They are switched by post-translational modifications into a non-rectifying K+ selective channel that allows both the uptake and the release of K+ depending on the electrochemical gradient. Ksilent subunits have not been reported to form functional channels on their own. Instead, they heteromerize with Kin subunits and modify specific channel properties. From a structural point of view, a functional voltage-gated plant K+ channel is built of four identical or different subunits. Hetero-tetramerization is observed within Kout channel subunits and within Kin/Kweak/Ksilent subunits but not in between these two larger groups. For better illustration the structure of a homotetrameric VvK5.1 channel has been generated by homology modeling (left: side view; right: top view) using the structure of the human Ether-a-go-go Related Gene channel (hERG; Kv11.1; PDB ID: 5VA1) as template. The sequence identity between VvK5.1 and hERG was 22.6% in the modeled region. Shown is the best model from 2,000 conformations obtained with Modeller. Each subunit (blue, red, green, yellow) is built of six membrane-spanning regions (1–6) where regions 1–4 form the voltage-sensing module and regions 5 and 6 shield the central permeation pathway. In algae a large diversity of voltage-sensing modules is reported (different clades for algal K+ channels in Box 1), while all voltage-gated K+ channels in higher plants share a highly similar structure originating from a common ancestor. The limitations of K+ channel research in Arabidopsis From diverse studies on the model plant A. thaliana, we have a clear and detailed picture of the structure and function of voltage-gated K+ channels and their physiological roles in that particular plant (Sharma et al., 2013). One might therefore think that this topic has been addressed exhaustively and that studies on other plants should not bring any exciting news. At first glance, this may appear correct since several findings simply reconfirm results obtained on Arabidopsis. Closer inspection, however, disproves this assumption as too short-sighted (Véry et al., 2014). Arabidopsis for instance does not have large seeds, fruits and extended vascular tissues like grapevine. How can results from Arabidopsis then explain the role of potassium channels/transporters in K+ distribution during fruit ripening in grapevine? Furthermore, A. thaliana has two genes coding for Kout channel subunits, while V. vinifera has four. Why? Answers to these questions can only be provided when investigating the K+ transporters and channels of the respective species. Vitis, the new Arabidopsis in K+ channel research Meanwhile voltage-gated K+ channels were characterized at the molecular level from maize, rice, potato, tomato, tobacco, Chinese cabbage, Ammopiptanthus, strawberry, and carrot, among others. The most systematic approach, however, has been initiated by researchers from INRA-Montpellier, France, for the common grapevine (V. vinifera L.). Just as for Arabidopsis before, one channel gene after another is characterized according to the current state of the art. From the nine K+ channel genes in Vitis, all three Kin genes (VvK1.1: Cuéllar et al., 2010; VvK1.2: Cuéllar et al., 2013; VvK2.1: Pratelli et al., 2002) and the only Kweak gene VvK3.1 (Nieves‐Cordones et al., 2019) have been characterized already, leaving the Ksilent gene VvK4.1 and four Kout genes (VvK5.1 - 5.4). This endeavor is complemented by work of other groups on proton-coupled K+ transporters from V. vinifera (Davies et al., 2006). V. vinifera is not only a model plant for studying the physiology of fleshy fruits. The work on this species is inspired by practical agricultural issues. Grapevine is one of the most important fruit crops and plays a significant role in the agriculture of countries like France (the country of the authors of the commented study) and Chile (the country of the authors of this insight article). Interestingly, potassium is one of the key players determining grape quality. On the one hand, K+is essential for the initiation and the control of the massive sugar and nutrient fluxes needed for berry loading. On the other hand, a large accumulation of K+during grape ripening leads to a neutralization of organic acids, which is unfavorable for wine quality. Grape berries harvested with lower acidity yield wines with poorer aroma properties and lower aging potential. Thus, systematic elucidation of the molecular determinants that control K+accumulation and acidity during berry maturation is a pre-requisite for future improvements aiming at breeding new varieties that guarantee a stable high wine quality under varying environmental conditions. Investigating Kout channels in grapevine In the latest approach, Villette et al. (2019) have now chosen the Kout gene VvK5.1 for an in-depth analysis. As expected, the functional characterization of the gene product confirmed our knowledge obtained from the Arabidopsis Kout channels SKOR and GORK. The expression of VvK5.1 (structural model in Box 2) in isolation in Xenopus oocytes resulted in Kout channels with properties similar to those observed already for the Arabidopsis counterparts. However, VvK5.1 has apparently acquired many new physiological roles as indicated by its broader expression pattern. Using in situ hybridization, Villette et al. (2019) demonstrate the expression of VvK5.1 in flowers, grape berry phloem, and roots; a spectrum not observed for any Arabidopsis Kout gene. Thus, the promoter of VvK5.1 has apparently acquired unique features allowing VvK5.1 to take on functions not recognized for Kout channels before. The peculiar activity of the VvK5.1-promoter in transgenic Arabidopsis corroborates its individual flair. These analyses suggest a role of VvK5.1 in lateral root formation, for instance. Admittedly, it is not fully certain that the VvK5.1-promoter activity determined in Arabidopsis mirrors one by one its activity in Vitis. However, such promoter-activity experiments are hardly feasible in grapevine due to the long generation cycle. Therefore, the eudicot Arabidopsis might still serve well as a feasible alternative for other eudicots to get at least some information. Perspective With the completion of the work of Villette et al. (2019) there remain four more voltage-gated K+ channel genes of V. vinifera waiting for their characterization: VvK4.1 (Ksilent), VvK5.2, VvK5.3, and VvK5.4 (all Kout). All four encoded voltage-gated K+ channel subunits might assemble with other subunits into heteromeric channels: VvK4.1 potentially with subunits of the Kin-derived pool (VvK1.1, VvK1.2, VvK2.1, VvK3.1), and all Kout subunits might be able to form heteromeric channels among them. The heteromerization potential is testable after co-expression in Xenopus oocytes using a dominant-negative strategy (Baizabal-Aguirre et al., 1999). Most important, however, will certainly be the investigation of the expression pattern of the remaining four genes to identify whether there are unique or overlapping expression profiles of the different K+ channel subunits. A further challenge will be to locate putative binding-sites for regulatory proteins as kinases or phosphatases in particular in the long cytosolic C-terminus (see structural model in Box 2). Differences in regulation might help to address the different roles that the diverse K+ channel subunits play in K+ nutrition of grapevine. These open gaps indicate that the article of Villette et al. (2019) will not be the last one of its kind. There is a need for more research on the function and regulation of potassium channels in species other than Arabidopsis if we want to understand potassium uptake and homeostasis in, for example, important crop plants or extremophiles. References Baizabal-Aguirre VM , Clemens S , Uozumi N , Schroeder JI . 1999 . Suppression of inward-rectifying K+ channels KAT1 and AKT2 by dominant negative point mutations in KAT1 . Journal of Membrane Biology 167 , 119 – 125 . Google Scholar Crossref Search ADS PubMed WorldCat Cuéllar T , Pascaud F , Verdeil JL , Torregrosa L , Adam-Blondon AF , Thibaud JB , Sentenac H , Gaillard I . 2010 . A grapevine Shaker inward K+ channel activated by the calcineurin B-like calcium sensor 1-protein kinase CIPK23 network is expressed in grape berries under drought stress conditions . The Plant Journal 61 , 58 – 69 . Google Scholar Crossref Search ADS PubMed WorldCat Cuéllar T , Azeem F , Andrianteranagna M , Pascaud F , Verdeil JL , Sentenac H , Zimmermann S , Gaillard I . 2013 . Potassium transport in developing fleshy fruits: the grapevine inward K+ channel VvK1.2 is activated by CIPK-CBL complexes and induced in ripening berry flesh cells . The Plant Journal 73 , 1006 – 1018 . Google Scholar Crossref Search ADS PubMed WorldCat Davies C , Shin R , Liu W , Thomas MR , Schachtman DP . 2006 . Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation . Journal of Experimental Botany 57 , 3209 – 3216 . Google Scholar Crossref Search ADS PubMed WorldCat Dreyer I , Porée F , Schneider A , Mittelstädt J , Bertl A , Sentenac H , Thibaud JB , Mueller-Roeber B 2004 . Assembly of plant Shaker-like Kout channels requires two distinct sites of the channel alpha-subunit . Biophysical Journal 87 , 858 – 872 . Google Scholar Crossref Search ADS PubMed WorldCat Dreyer I , Antunes S , Hoshi T , Müller-Röber B , Palme K , Pongs O , Reintanz B , Hedrich R 1997 . Plant K+ channel α-subunits assemble indiscriminately . Biophysical Journal 72 , 2143 – 2150 . Google Scholar Crossref Search ADS PubMed WorldCat Gomez-Porras JL , Riaño-Pachón DM , Benito B , Haro R , Sklodowski K , Rodríguez-Navarro A , Dreyer I . 2012 . Phylogenetic analysis of K+ transporters in bryophytes, lycophytes, and flowering plants indicates a specialization of vascular plants . Frontiers in Plant Science 3 , 167 . Google Scholar Crossref Search ADS PubMed WorldCat Jegla T , Busey GW , Assmann SM . 2018 . Evolution and structural characteristics of plant voltage-gated K+ channels . The Plant Cell 30 , 2898 – 2909 . Google Scholar Crossref Search ADS PubMed WorldCat Karnik R , Waghmare S , Zhang B , Larson E , Lefoulon C , Gonzalez W , Blatt MR . 2017 . Commandeering channel voltage sensors for secretion, cell turgor, and volume control . Trends in Plant Science 22 , 81 – 95 . Google Scholar Crossref Search ADS PubMed WorldCat Lebaudy A , Hosy E , Simonneau T , Sentenac H , Thibaud JB , Dreyer I . 2008 . Heteromeric K+ channels in plants . The Plant Journal 54 , 1076 – 1082 . Google Scholar Crossref Search ADS PubMed WorldCat Nieves‐Cordones M , Andrianteranagna M , Cuéllar T , Chérel I , Gibrat R , Boeglin M , Moreau B , Paris N , Verdeil JL , Zimmermann SD , Gaillard I . 2019 . Characterization of the grapevine Shaker K+ channel VvK3.1 supports its function in massive potassium fluxes necessary for berry potassium loading and pulvinus‐actuated leaf movements . New Phytologist 222 , 286 – 300 . Google Scholar Crossref Search ADS PubMed WorldCat Pratelli R , Lacombe B , Torregrosa L , Gaymard F , Romieu C , Thibaud JB , Sentenac H . 2002 . A grapevine gene encoding a guard cell K+ channel displays developmental regulation in the grapevine berry . Plant Physiology 128 , 564 – 577 . Google Scholar Crossref Search ADS PubMed WorldCat Riedelsberger J , Dreyer I , Gonzalez W . 2015 . Outward rectification of voltage-gated K+ channels evolved at least twice in life history . PLoS One 10 , e0137600 . Google Scholar Crossref Search ADS PubMed WorldCat Sharma T , Dreyer I , Riedelsberger J . 2013 . The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana . Frontiers in Plant Science 4 , 224 . Google Scholar PubMed WorldCat Sussmilch FC , Roelfsema MRG , Hedrich R . 2019 . On the origins of osmotically driven stomatal movements . New Phytologist 222 , 84 – 90 . Google Scholar Crossref Search ADS PubMed WorldCat Véry AA , Nieves-Cordones M , Daly M , Khan I , Fizames C , Sentenac H . 2014 . Molecular biology of K+ transport across the plant cell membrane: what do we learn from comparison between plant species? Journal of Plant Physiology 171 , 748 – 769 . Google Scholar Crossref Search ADS PubMed WorldCat Villette J , Cuéllar T , Zimmermann SD , Verdeil JL , Gaillard I . 2019 . Unique features of the grapevine VvK5.1 channel support novel functions for outward K+ channels in plants . Journal of Experimental Botany 70 , 6181 – 6194 . Google Scholar Crossref Search ADS PubMed WorldCat © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Exploring the fundamental role of potassium channels in novel model plants
JF - Journal of Experimental Botany
DO - 10.1093/jxb/erz413
DA - 2019-11-18
UR - https://www.deepdyve.com/lp/oxford-university-press/exploring-the-fundamental-role-of-potassium-channels-in-novel-model-cXZeGSpiZG
SP - 5985
VL - 70
IS - 21
DP - DeepDyve
ER -