Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance

Abstract

Intracellular potassium homeostasis is a prerequisite for the optimal operation of plant metabolic machinery and plant's overall performance. It is controlled by K(+) uptake, efflux and intracellular and long-distance relocation, mediated by a large number of K(+) -selective and non-selective channels and transporters located at both plasma and vacuolar membranes. All abiotic and biotic stresses result in a significant disturbance to intracellular potassium homeostasis. In this work, we discuss molecular mechanisms and messengers mediating potassium transport and homeostasis focusing on four major environmental stresses: salinity, drought, flooding and biotic factors. We argue that cytosolic K(+) content may be considered as one of the 'master switches' enabling plant transition from the normal metabolism to 'hibernated state' during first hours after the stress exposure and then to a recovery phase. We show that all these stresses trigger substantial disturbance to K(+) homeostasis and provoke a feedback control on K(+) channels and transporters expression and post-translational regulation of their activity, optimizing K(+) absorption and usage, and, at the extreme end, assisting the programmed cell death. We discuss specific modes of regulation of the activity of K(+) channels and transporters by membrane voltage, intracellular Ca(2+) , reactive oxygen species, polyamines, phytohormones and gasotransmitters, and link this regulation with plant-adaptive responses to hostile environments.

Cell-Type-Specific H+-ATPase Activity in Root Tissues Enables K+ Retention and Mediates Acclimation of Barley (Hordeum vulgare) to Salinity Stress

“…Consistent with previous observations, the OH $ -induced current was biphasic, composed of the instantaneous and the time-dependent depolarization-activated components (Fig. 6A), which could be tentatively assigned to ROS-activated NSCC and GORK, respectively (Demidchik et al, 2014;Shabala and Pottosin, 2014). Due to a strong outward rectification, a reversal potential of the time-dependent current could not be defined unequivocally; instantaneous currents reversed around 230 mV (i.e.…”

“…By interacting with transition metals such as either copper or iron, increased accumulation of hydrogen peroxide (H 2 O 2 ) may result in the formation of highly reactive hydroxyl radicals (OH $ ) in both the apoplast (Demidchik, 2015) and cytosol (Rodrigo-Moreno et al, 2013). Both H 2 O 2 and OH $ may cause a major perturbation in intracellular ionic homeostasis by activating a range of cation-permeable ion channels (Demidchik and Maathuis, 2007;Demidchik et al, 2010;Shabala and Pottosin, 2014). Thus, tissuespecific salinity stress sensitivity between the root apex and mature zones may be causally related to the patterns of OH $ production and/or sensitivity of membrane transporters to OH $ .…”

“…Physiologically, plant adaptive responses to salinity can be grouped into four major categories: (1) dealing with the osmotic component of salt stress; (2) handling toxic Na + and Cl 2 ions; (3) detoxifying reactive oxygen species (ROS) produced in plant tissues under saline conditions; and (4) mediating cytosolic K + homeostasis (Tester and Davenport, 2003;Ji et al, 2013;Shabala, 2013;Shabala and Pottosin, 2014;Flowers et al, 2015;Julkowska and Testerink, 2015;Kurusu et al, 2015). All these responses rely heavily on the regulation of transport activity across cellular membranes and, specifically, those for Na + and K + ions.…”

“…High cytosolic Na + concentrations are considered to be toxic for cell metabolism and, thus, are reduced by various means (Tester and Davenport, 2003;Ji et al, 2013;Flowers et al, 2015). At the same time, superior K + retention and a cell's ability to maintain cytosolic K + homeostasis correlate with salinity tolerance in a broad range of plant species (Anschütz et al, 2014;Shabala and Pottosin, 2014) and are essential for preventing salinityinduced programmed cell death (Shabala, 2009;Demidchik et al, 2010). High cytosolic K + levels also are essential to maintain high vacuolar H + -PPase activity, thus enabling the operation of tonoplast NHX proteins that mediate vacuolar Na + sequestration (Shabala, 2013).…”

“…In addition, ROS detoxification activity in plant cells is critically dependent on K + availability (Sun et al, 2015). This explains why the cytosolic sodium-potassium ratio is widely regarded a major determinant of plant salinity stress tolerance (Anschütz et al, 2014;Shabala and Pottosin, 2014) and why understanding the tissue specificity of its regulation may be the key to improving salinity tolerance in plants.…”