Cell-type specific H+-ATPase activity enables root K+ retention and mediates acclimation to salinity

While the importance of cell-type specificity in plant adaptive responses is widely accepted, only a limited number of studies have addressed this issue at the functional level. We have combined electrophysiological, imaging, and biochemical techniques to reveal physiological mechanisms conferring higher sensitivity of apical root cells to salinity in barley. We show that salinity application to the root apex arrests root growth in a highly tissue- and treatment-specific manner. Although salinity-induced transient net Na+ uptake was about 4-fold higher in the root apex compared with the mature zone, mature root cells accumulated more cytosolic and vacuolar Na+ suggesting that higher sensitivity of apical cells to salt is not related to either enhanced Na+ exclusion or sequestration inside the root. Rather, the above differential sensitivity between the two zones originates from a 10-fold difference in K+ efflux between the mature zone and the apical region (much poorer in the root apex) of the root. Major factors contributing to this poor K+ retention ability are: (1) an intrinsically lower H+-ATPase activity in the root apex; (2) greater salt-induced membrane depolarization and (3) a higher ROS production under NaCl and a larger density of ROS-activated cation currents in the apex. Salinity treatment increased (2 to 5 fold) the content of 10 (out of 25 detected) amino acids in the root apex but not in the mature zone and changed the organic acid and sugar contents. The causal link between observed changes in the root metabolic profile and regulation of transporters activity is discussed

Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses

First published online: January 24, 2014Many stresses are associated with increased accumulation of reactive oxygen species (ROS) and polyamines (PAs). PAs act as ROS scavengers, but export of putrescine and/or PAs to the apoplast and their catabolization by amine oxidases gives rise to H2O2 and other ROS, including hydroxyl radicals (•OH). PA catabolization-based signalling in apoplast is implemented in plant development and programmed cell death and in plant responses to a variety of biotic and abiotic stresses. Central to ROS signalling is the induction of Ca2+ influx across the plasma membrane. Different ion conductances may be activated, depending on ROS, plant species, and tissue. Both H2O2 and •OH can activate hyperpolarization-activated Ca2+-permeable channels. •OH is also able to activate both outward K+ current and weakly voltage-dependent conductance (ROSIC), with a variable cation-to-anion selectivity and sensitive to a variety of cation and anion channel blockers. Unexpectedly, PAs potentiated •OH-induced K+ efflux in vivo, as well as ROSIC in isolated protoplasts. This synergistic effect is restricted to the mature root zone and is more pronounced in salt-sensitive cultivars compared with salt-tolerant ones. ROS and PAs suppress the activity of some constitutively expressed K+ and non-selective cation channels. In addition, both •OH and PAs activate plasma membrane Ca2+-ATPase and affect H+ pumping. Overall, •OH and PAs may provoke a substantial remodelling of cation and anion conductance at the plasma membrane and affect Ca2+ signalling.Igor Pottosin, Ana María Velarde-Buendía, Jayakumar Bose, Isaac Zepeda-Jazo, Sergey Shabala and Oxana Dobrovinskay

Cell-type-specific H(+)-ATPase activity in root tissues enables K(+) retention and mediates acclimation of barley (Hordeum vulgare) to salinity stress

Published October 21, 2016.While the importance of cell type specificity in plant adaptive responses is widely accepted, only a limited number of studies have addressed this issue at the functional level. We have combined electrophysiological, imaging, and biochemical techniques to reveal the physiological mechanisms conferring higher sensitivity of apical root cells to salinity in barley (Hordeum vulgare). We show that salinity application to the root apex arrests root growth in a highly tissue- and treatment-specific manner. Although salinity-induced transient net Na+ uptake was about 4-fold higher in the root apex compared with the mature zone, mature root cells accumulated more cytosolic and vacuolar Na+, suggesting that the higher sensitivity of apical cells to salt is not related to either enhanced Na+ exclusion or sequestration inside the root. Rather, the above differential sensitivity between the two zones originates from a 10-fold difference in K+ efflux between the mature zone and the apical region (much poorer in the root apex) of the root. Major factors contributing to this poor K+ retention ability are (1) an intrinsically lower H+-ATPase activity in the root apex, (2) greater salt-induced membrane depolarization, and (3) a higher reactive oxygen species production under NaCl and a larger density of reactive oxygen species-activated cation currents in the apex. Salinity treatment increased (2- to 5-fold) the content of 10 (out of 25 detected) amino acids in the root apex but not in the mature zone and changed the organic acid and sugar contents. The causal link between the observed changes in the root metabolic profile and the regulation of transporter activity is discussed.Lana Shabala, Jingyi Zhang, Igor Pottosin, Jayakumar Bose, Min Zhu, Anja Thoe Fuglsang, Ana Velarde-Buendia, Amandine Massart, Camilla Beate Hill, Ute Roessner, Antony Bacic, Honghong Wu, Elisa Azzarello, Camilla Pandolfi, Meixue Zhou, Charlotte Poschenrieder, Stefano Mancuso, and Sergey Shabal

ROS homeostasis in halophytes in the context of salinity stress tolerance

Halophytes are defined as plants that are adapted to live in soils containing high concentrations of salt and benefiting from it, and thus represent an ideal model to understand complex physiological and genetic mechanisms of salinity stress tolerance. It is also known that oxidative stress signalling and reactive oxygen species (ROS) detoxification are both essential components of salinity stress tolerance mechanisms. This paper comprehensively reviews the differences in ROS homeostasis between halophytes and glycophytes in an attempt to answer the questions of whether stress-induced ROS production is similar between halophytes and glycophytes; is the superior salinity tolerance in halophytes attributed to higher antioxidant activity; and is there something special about the specific 'pool' of enzymatic and non-enzymatic antioxidants in halophytes. We argue that truly salt-tolerant species possessing efficient mechanisms for Na(+) exclusion from the cytosol may not require a high level of antioxidant activity, as they simply do not allow excessive ROS production in the first instance. We also suggest that H2O2 'signatures' may operate in plant signalling networks, in addition to well-known cytosolic calcium 'signatures'. According to the suggested concept, the intrinsically higher superoxide dismutase (SOD) levels in halophytes are required for rapid induction of the H2O2 'signature', and to trigger a cascade of adaptive responses (both genetic and physiological), while the role of other enzymatic antioxidants may be in decreasing the basal levels of H2O2, once the signalling has been processed. Finally, we emphasize the importance of non-enzymatic antioxidants as the only effective means to prevent detrimental effects of hydroxyl radicals on cellular structures.Jayakumar Bose, Ana Rodrigo-Moreno, Sergey Shabal