Cotransport of water and solutes in plant membranes: The molecular basis, and physiological functions

Wegner, Lars H.

doi:10.3934/biophy.2017.2.192

Cited by 25 publications

(34 citation statements)

References 45 publications

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“…This implies that the seemingly futile cycling of Na + and K + has a physiological function rather than being just a waste of energy. Evidence in support of this hypothesis has been provided previously (Wegner, 2017). It should be noted that the osmotic and nonosmotic water uptake mechanisms proposed by Wegner (2017) are mutually exclusive, at least at the cellular level, because water fluxes across the plasma membrane are facilitated by a high activity of aquaporins, which would short-circuit nonosmotic water uptake, rendering it unfeasible from an energetic point of view (Wegner, 2015(Wegner, , 2017Fricke, 2017).…”

Section: Reviewmentioning

confidence: 82%

“…This would require a close coupling of water and solute transport, allowing a transfer of free energy between the fluxes, which can be tested experimentally. Nonosmotic water transport may play a role in the generation of root pressure, repair of embolized xylem vessels and control of cell elongation (Fricke, 2015;Wegner, 2015Wegner, , 2017. This mechanism implies large circular fluxes of the solute(s) driving the water transport, because solutes permeating together with a fixed number of water molecules need to be re-translocated back immediately at the expense of metabolic energy to maintain the (electro)chemical gradient.…”

Section: Reviewmentioning

confidence: 99%

“…Bertram et al, 2006) could be adapted to quantitatively model ATP production in plant mitochondria. Modelling also can be used to investigate currently unproven hypotheses, such as the possibility of water co-transport with ions such as Na + (Wegner, 2017). Although existing models of ion and water transport in plants assume that water transport is passive, they could be adapted to explore the possibility of active water transport.…”

Section: Where To From Here?mentioning

confidence: 99%

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Energy costs of salt tolerance in crop plants

et al. 2019

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Agricultureisexpandingintoregionsthatareaffectedbysalinity.Thisreviewconsiderstheenergetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion uptake are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H +-ATPase also is a critical component. One proposed leak, that of Na + influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na + and Cl À concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will informexperimentationandallowaquantitativeassessmentoftheenergycostsofNaCltoleranceto guide breeding and engineering of molecular components.

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Section: Reviewmentioning

confidence: 82%

Section: Reviewmentioning

confidence: 99%

Section: Where To From Here?mentioning

confidence: 99%

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Energy costs of salt tolerance in crop plants

et al. 2019

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“…AtHKT1;1 consists of a single polypeptide with four repeated domains (reviewed by Hamamoto et al, 2015;Shabala, White et al, 2016), and its major role is assigned to Na + retrieval from the xylem (Byrt et al, 2007;Davenport et al, 2007;Horie et al, 2009;Ren et al, 2005;Sunarpi et al, 2005). Far less is known about the role of Class 2 exhibits characteristics typical of NSCCs (reviewed by Wegner, 2017), it was suggested as one of these (Byrt et al, 2017).…”

Section: Hktmentioning

confidence: 99%

Xylem Ion Loading and Its Implications for Plant Abiotic Stress Tolerance

Ishikawa

Cuin

Bazihizina

et al. 2018

Advances in Botanical Research

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Plant adaptive potential is critically dependent on efficient communication and coordination of resource allocation and signalling between above and below-ground plant parts. Control of xylem ion loading plays an important role in this process. This review focuses on the molecular identity, tissue-specific expression patterns, and transcriptional and posttranslational regulation of transporters mediating xylem loading of Na + , K + , and Clin plants grown under abiotic stress conditions such as drought, salinity, and soil flooding. The data is discussed in the context of breeding crops for stress resilience, which remains one of the highest priorities for dealing with the global food security challenge. This resilience was present in wild ancestors, but has been then lost during domestication of crop species and exacerbated by the selection for higher yielding cultivars over the last 100 years. Thus, the progress in the field requires a major rethink of current paradigms in crop breeding and the targeting of previously unexplored genes and traits. We argue that control of xylem ion loading is one of these traits and represents an unexplored opportunity for genetic improvement of plant germplasms. HKT transporters. From a biophysical point of view, these transporters are highly suited for active xylem Na + loading under conditions that favour passive outward K + movement across the parenchyma cell plasma membrane (e.g. the depolarised membrane potential that occurs under saline conditions; Wegner et al., 2011). Supporting this notion, strong OsHKT2;1 expression was reported in the stellar root tissues of rice (Jabnoune et al., 2009). NSCC. Xylem Na + loading could also be mediated by a passive mechanism that involves non-selective cation channels (NSCC). NSCC show diverse characteristics in terms of regulation and functional expression (Demidchik & Maathuis, 2007). NSCC do not strongly differentiate between cations, particularly between K + and Na + ; K + /Na + permeability ratios range between 0.3 and 3 (see Pottosin & Dobrovinskaya, 2014 for review). The two major known families of NSCC are the cyclic nucleotide gated channels (CNGC; 20 genes in Arabidopsis) and the ionotropic glutamate receptors (GLR; 20 genes in Arabidopsis), some of which show high expression in root tissues (Demidchik, Davenport, & Tester, 2002; Gobert et al., 2006; Lam et al., 1998). The potential importance of CNGC and GLR in generating cytosolic Ca 2+ signals in response to stress conditions has been proposed (Swarbreck, Colaço, & Davies, 2013) and their engagement in Na + transport at the xylem/symplast boundary is also highly plausible. CNGC. CNGC are considered likely candidates for the voltage-independent NSCC (Demidchik, Davenport, & Tester, 2002; Kaplan, Sherman, & Fromm, 2007). Heterologously expressed CNGCs act as cation transporters (Gobert et al., 2006; Li et al., 2005) and electrophysiological studies have shown that both AtCNGC1 and AtCNGC4 can transport K + and Na + (Balague et al., 2003; Leng et al., 2002). Furthermore, CNGC...

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“… The Na + influx through molecularly unidentified nonselective cation channels (NSCCs) may be coupled to the uphill transport of another ion or water, thus conserving some of the Na + leak energy. The latter possibility was discussed in view of recent hypotheses on ion–water coupling (Fricke, ; Wegner, ) and the observation that PIP2;1 and PIP2;2 aquaporins could be candidates for the NSCCs (Byrt et al ., ). The vacuolar H + ‐PPase contributes to significant acidification of the vacuole, meaning that plants are using less ATP to set up conditions for proton antiporters to compartmentalize ions (Schilling et al ., ); its possible role as an alternative pump at the PM needs to be examined (Davies et al ., ). Also, PPases working as a synthase to generate PPi may result in enhanced sucrose hydrolysis and ATP production (Gaxiola et al ., ). How are the major metabolic processes contained within the mitochondria and chloroplasts affected by salinity, and what is the impact of the availability of ATP on cellular and tissue salinity responses (Bose et al ., ; Che‐Othman et al ., )? There are major uncertainties with respect to the production of ATP from oxidative phosphorylation due to species and tissue variations in the supply of respiratory substrates and the activity of the alternative oxidase and other respiratory bypasses (Millar et al ., , ).…”

Section: Energy Demandsmentioning

confidence: 99%