High-Affinity Potassium Transport in Barley Roots. Ammonium-Sensitive and -Insensitive Pathways

Santa-Marı́a, Guillermo E.; Danna, Cristian H.; Czibener, Cecilia

doi:10.1104/pp.123.1.297

Cited by 103 publications

(94 citation statements)

References 46 publications

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“…The absence of evidence that subfamily 2 HKT transporters contribute to K + fluxes in planta, while these systems are clearly permeable to K + , highly expressed in plant cells, and functional in the cell membrane (as shown by their strong contribution to Na + transport) might be due to redundancy in K + transport systems from different families. For instance, in root periphery tissues, when plants are grown in classical environmental conditions and/or when experiments are performed in classical bath solutions, K + transport activity of HKT transporters might be masked by that of K + channels from the Shaker family (Sentenac et al, 1992;Hirsch et al, 1998;Santa-María et al, 2000;Pilot et al, 2003;Véry and Sentenac, 2003) and/or H + -K + symporters from the KUP/HAK family (Santa-María et al, 2000;Bañ uelos et al, 2002;Gierth and Mäser, 2007). The question of the existence of Na + -K + symport activity in plants, owing to its importance, clearly deserves to be readdressed.…”

Section: Expression Patterns and Roles In The Plantmentioning

confidence: 99%

Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family

et al. 2009

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Plant growth under low K + availability or salt stress requires tight control of K + and Na + uptake, long-distance transport, and accumulation. The family of membrane transporters named HKT (for High-Affinity K + Transporters), permeable either to K + and Na + or to Na + only, is thought to play major roles in these functions. Whereas Arabidopsis (Arabidopsis thaliana) possesses a single HKT transporter, involved in Na + transport in vascular tissues, a larger number of HKT transporters are present in rice (Oryza sativa) as well as in other monocots. Here, we report on the expression patterns and functional properties of three rice HKT transporters, OsHKT1;1, OsHKT1;3, and OsHKT2;1. In situ hybridization experiments revealed overlapping but distinctive and complex expression patterns, wider than expected for such a transporter type, including vascular tissues and root periphery but also new locations, such as osmocontractile leaf bulliform cells (involved in leaf folding). Functional analyses in Xenopus laevis oocytes revealed striking diversity. OsHKT1;1 and OsHKT1;3, shown to be permeable to Na + only, are strongly different in terms of affinity for this cation and direction of transport (inward only or reversible). OsHKT2;1 displays diverse permeation modes, Na + -K + symport, Na + uniport, or inhibited states, depending on external Na + and K + concentrations within the physiological concentration range. The whole set of data indicates that HKT transporters fulfill distinctive roles at the whole plant level in rice, each system playing diverse roles in different cell types. Such a large diversity within the HKT transporter family might be central to the regulation of K + and Na + accumulation in monocots.Although it is not clear what levels of Na + are toxic in the plant cell cytosol and actually unacceptable in vivo, the hypothesis that this cation must be excluded from the cytoplasm is widely accepted. The most abundant inorganic cation in the cytosol is K + , in plant as in animal cells. This cation has probably been selected during evolution because it is less chaotropic than Na + (i.e. more compatible with protein structure even at high concentrations; Clarkson and Hanson, 1980). Its selection might also be due to the fact that in primitive cells, which originated in environmental conditions (seawater) where Na + was more abundant than K + , a straightforward process to energize the cell membrane was to accumulate the less abundant cation and to exclude the most abundant one.In the cell, K + plays a role in basic functions, such as regulation of cell membrane polarization, electrical neutralization of anionic groups, and osmoregulation. Concerning the latter function, K + uptake or release is the usual way through which plant cells control their water potential and turgor. Although toxic at high concentrations, Na + can be used as osmoticum and substituted for K and tissue levels have actually been shown to be essential in plant adaptation to salt stress (Greenway and Munns, 1980;Flowers, 1985;Hasegawa...

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Section: Expression Patterns and Roles In The Plantmentioning

confidence: 99%

Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family

et al. 2009

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“…During the last decades several molecular components of potassium transport systems have been identified and functionally characterized in plants (3,4). Mutant analyses, heterologous expression, as well as radiotracer uptake experiments characterized the K ϩ channels AKT1⅐AtKC1 and members of the HAK⅐KT⅐KUP family as major components of the Arabidopsis thaliana root-localized potassium transport system (5)(6)(7)(8)(9). In this study we focused on AKT1 and AtKC1, members of the Arabidopsis Shaker-like K ϩ channel family.…”

mentioning

confidence: 99%

Heteromeric AtKC1·AKT1 Channels in Arabidopsis Roots Facilitate Growth under K+-limiting Conditions

Geiger

Becker

Vosloh

et al. 2009

Journal of Biological Chemistry

156

171

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Fundamental plant functions such as control of the membrane potential, osmo-regulation, and turgor-driven growth and movements are based on the availability to gain high cellular potassium concentrations (1). The absorption of this inorganic osmolyte from the soil by the root therefore represents a pivotal process for plant life. Classical experiments by Epstein et al. in 1963 (2) described K ϩ root uptake as a biphasic process mediated by two uptake mechanisms: high affinity potassium transport with apparent affinities of ϳ20 M and a low affinity transport system with K m values in the millimolar range. During the last decades several molecular components of potassium transport systems have been identified and functionally characterized in plants (3, 4). Mutant analyses, heterologous expression, as well as radiotracer uptake experiments characterized the K ϩ channels AKT1⅐AtKC1 and members of the HAK⅐KT⅐KUP family as major components of the Arabidopsis thaliana root-localized potassium transport system (5-9). In this study we focused on AKT1 and AtKC1, members of the Arabidopsis Shaker-like K ϩ channel family. AKT1 is a voltagedependent inward-rectifying K ϩ channel mediating potassium uptake over a wide range of external potassium concentrations (10 -15). Root cells of the akt1-1 loss-of-function mutant completely lack inward rectifying K ϩ currents (12). As a consequence the growth of akt1-1 seedlings is strongly impaired on low potassium medium (100 M and less) (11,12,15). Rescue of yeast growth on 20 M K ϩ and patch clamp experiments (16, 17) directly demonstrated that plant inward rectifying K ϩ channels are capable of serving as high affinity potassium uptake transporters. AtKC1 shares its expression pattern with . AtKC1 ␣-subunits, however, neither form functional channels in akt1-1 knock-out plants nor in heterologous expression systems. In contrast to root cells of akt1-1 loss of function mutants, root protoplasts of AtKC1 null mutants (atkc1-f) still exhibit inward rectifying potassium currents most likely derived from homomeric AKT1 tetramers (20). Inward K ϩ currents in this atkc1-f mutant were characterized by a more positive activation voltage. These data suggested that the AtKC1 ␣-subunits do not form K ϩ channels per se but modulate the properties of the AKT1⅐AtKC1 heterocomplex (20 -22

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“…However, the main qualitative difference found is the absence of NH 4 ϩ in the new medium, whereas the concentration of NH 4 ϩ in the Murashige and Skoog medium is 20 mm. The inhibitory effects of NH 4 ϩ on K ϩ uptake have been reported previously (Scherer et al, 1984;Vale et al, 1987;Spalding et al, 1999;Santa-María et al, 2000). Supplementing the medium with 5 mm NH 4 ϩ restored the tss1 hypersensitivity to NaCl (Fig.…”

Section: Hypersensitivity Of Tss1 Seedlings To Namentioning

confidence: 76%

“…Evidence for an inhibitory effect of NH 4 ϩ on K ϩ transport has been reported in other plant species on the basis of short-term radiometric studies (Scherer et al, 1984;Vale et al, 1987Vale et al, , 1988Wang et al, 1996;Spalding et al, 1999;Santa-María et al, 2000). In medium containing NH 4 ϩ , increasing K ϩ concentrations also evoked rapid membrane depolarizations in both wild-type and tss1 seedlings (Fig.…”

Section: Effect Of Camentioning

confidence: 89%

Regulation of K+ Transport in Tomato Roots by the TSS1 Locus. Implications in Salt Tolerance

Rubio

Rosado²,

Linares-Rueda³

et al. 2004

Plant Physiology

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The tss1 tomato (Lycopersicon esculentum) mutant exhibited reduced growth in low K+ and hypersensitivity to Na+ and Li+. Increased Ca2+ in the culture medium suppressed the Na+ hypersensitivity and the growth defect on low K+ medium of tss1 seedlings. Interestingly, removing NH4 + from the growth medium suppressed all growth defects of tss1, suggesting a defective NH4 +-insensitive component of K+ transport. We performed electrophysiological studies to understand the contribution of the NH4 +-sensitive and -insensitive components of K+ transport in wild-type and tss1 roots. Although at 1 mm Ca2+ we found no differences in affinity for K+ uptake between wild type and tss1 in the absence of NH4 +, the maximum depolarization value was about one-half in tss1, suggesting that a set of K+ transporters is inactive in the mutant. However, these transporters became active by raising the external Ca2+ concentration. In the presence of NH4 +, a reduced affinity for K+ was observed in both types of seedlings, but tss1 at 1 mm Ca2+ exhibited a 2-fold higher K m than wild type did. This defect was again corrected by raising the external concentration of Ca2+. Therefore, membrane potential measurements in root cells indicated that tss1 is affected in both NH4 +-sensitive and -insensitive components of K+ transport at low Ca2+ concentrations and that this defective transport is rescued by increasing the concentration of Ca2+. Our results suggest that the TSS1 gene product is part of a crucial pathway mediating the beneficial effects of Ca2+ involved in K+ nutrition and salt tolerance.

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High-Affinity Potassium Transport in Barley Roots. Ammonium-Sensitive and -Insensitive Pathways

Cited by 103 publications

References 46 publications

Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family

Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family

Heteromeric AtKC1·AKT1 Channels in Arabidopsis Roots Facilitate Growth under K+-limiting Conditions

Regulation of K+ Transport in Tomato Roots by the TSS1 Locus. Implications in Salt Tolerance

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