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A dual role for the OsK5.2 ion channel in stomatal movements and K + loading into xylem sap

Nguyen T.H., Huang S., Meynard D., Chaine C., Michel R., Roelfsema M.R.G., Guiderdoni E., Sentenac H., Very A.A.. 2017. Plant Physiology, 174 (4) : p. 2409-2418.

The roles of potassium channels from the Shaker family in stomatal movements have been investigated by reverse genetics analyses in Arabidopsis (Arabidopsis thaliana), but corresponding information is lacking outside this model species. Rice (Oryza sativa) and other cereals possess stomata that are more complex than those of Arabidopsis. We examined the role of the outward Shaker K+ channel gene OsK5.2. Expression of the OsK5.2 gene (GUS reporter strategy) was observed in the whole stomatal complex (guard cells and subsidiary cells), root vasculature, and root cortex. In stomata, loss of OsK5.2 functional expression resulted in lack of time-dependent outward potassium currents in guard cells, higher rates of water loss through transpiration, and severe slowdown of stomatal closure. In line with the expression of OsK5.2 in the plant vasculature, mutant plants displayed a reduced K+ translocation from the root system toward the leaves via the xylem. The comparison between rice and Arabidopsis show that despite the strong conservation of Shaker family in plants, substantial differences can exist between the physiological roles of seemingly orthologous genes, as xylem loading depends on SKOR and stomatal closure on GORK in Arabidopsis, whereas both functions are executed by the single OsK5.2 Shaker in rice. Since a waxy cuticle covers outer leaf tissues, water vapor diffusion into the atmosphere occurs mainly through the stomatal pores at the leaf surface. The size of the stomatal aperture is tightly regulated to optimize gas exchanges between the leaf inner tissues and the atmosphere, including CO2 intake for photosynthesis and water loss by transpiration (Lawson and Blatt, 2014). This is achieved by fine tuning of the turgor pressure of the two guard cells that surround the stomatal pore and involves a complex coordinated activity of transport systems at the guard cell plasma membrane and vacuolar membrane (Hedrich, 2012; Chen et al., 2012; Hills et al., 2012; Kollist et al., 2014). This control also affects long-distance transport of mineral nutrients from the roots, which take up these nutrients, to the aerial parts, to support plant growth (Marschner et al., 1996). Potassium ion (K+), as a major inorganic constituent of the plant cells and the most abundant cation in the cytosol, is an essential macronutrient for growth and development. It is involved in various functions, including electrical neutralization of negative charges, control of cell membrane polarization, and osmoregulation (Clarkson and Hanson, 1980; Leigh and Wyn Jones, 1984). K+ is thus the main cation absorbed by the roots and circulating within the plant at the cellular or long-distance levels. In guard cells, it is well known as a major contributor, with Cl-, NO3? and malate, to the osmolarity (Raschke and Schnabl, 1978; Willmer and Fricker, 1996). Stomatal opening is initiated by activation of plasma membrane proton pumps in guard cells, which promotes K+ influx through voltage-gated inward K+ channels, as well as anion uptake through H+-anion symporters (Blatt, 1987a; Schroeder et al., 1987; Roelfsema and Prins, 1997; Talbott and Zeiger, 1998; Guo et al., 2003; Jezek and Blatt, 2017). Conversely, stomatal closure requires inhibition of proton pumping at the guard cell membrane and activation of both anion channels and voltage-gated outward K+ channels. The molecular mechanisms responsible for inward and outward K+ fluxes across the plasma membrane have been extensively investigated in Arabidopsis (Arabidopsis thaliana). Shaker channel subunits, present as a nine-member family in Arabidopsis, have been shown to form the major pathways for these fluxes throughout the plant (Véry and Sentenac, 2003). In the Arabidopsis model species, four genes encoding Shaker channel subunits have been identified as playing a major role in root to shoot K+ translocation and in stomatal movements. The SKOR subunit, which is expressed in root pericycle and xylem parenchyma, fo

Mots-clés : arabidopsis thaliana; oryza sativa

Thématique : Physiologie et biochimie végétales; Génétique et amélioration des plantes

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