Abstract
Extracellular ATP (eATP) has been implicated in mediating plant growth and antioxidant defense; however, it is largely unknown whether eATP might mediate salinity tolerance. We used confocal microscopy, a non-invasive vibrating ion-selective microelectrode, and quantitative real time PCR analysis to evaluate the physiological significance of eATP in the salt resistance of cell cultures derived from a salt-tolerant woody species, Populus euphratica. Application of NaCl (200 mM) shock induced a transient elevation in [eATP]. We investigated the effects of eATP by blocking P2 receptors with suramin and PPADS and applying an ATP trap system of hexokinase-glucose. We found that eATP regulated a wide range of cellular processes required for salt adaptation, including vacuolar Na+ compartmentation, Na+/H+ exchange across the plasma membrane (PM), K+ homeostasis, reactive oxygen species regulation, and salt-responsive expression of genes related to K+/Na+ homeostasis and PM repair. Furthermore, we found that the eATP signaling was mediated by H2O2 and cytosolic Ca2+ released in response to high salt in P. euphratica cells. We concluded that salt-induced eATP was sensed by purinoceptors in the PM, and this led to the induction of downstream signals, like H2O2 and cytosolic Ca2+, which are required for the up-regulation of genes linked to K+/Na+ homeostasis and PM repair. Consequently, the viability of P. euphratica cells was maintained during a prolonged period of salt stress.
Highlights
Plant tolerance to salinity is mediated by a multi-trait, regulatory network
We investigated the effects of NaCl on ATP release in the extracellular matrix (ECM), and we aimed to clarify the roles of salt-induced Extracellular ATP (eATP) in ion homeostasis and antioxidant defense
In addition to the gene expression elicited by high salt exposure, we examined the effects of suramin, PPADS, H-G, ATP (100 and 200 mM), and ATPlS (200 mM) on the expression of salt-responsive genes in control cells that were not exposed to high salt conditions (Fig. S4)
Summary
Plant tolerance to salinity is mediated by a multi-trait, regulatory network. Plant regulation of ion homeostasis has received much attention. Ca2+ and H2O2 have been widely considered as second messengers involved in salt stress signaling [1,2,3,4,5]. Salt treatment generates transient calcium signals to activate salt overly sensitive (SOS) Ca2+ sensors that participate in the SOS3-SOS2-SOS1 signaling cascades in Arabidopsis, rice, and poplar [6,7,8]. In the SOS pathway, plasma membrane (PM) Na+/H+ antiporters (SOS1) play a crucial role in active Na+ extrusion under saline conditions [9,10,11,12,13]. Ca2+ signaling was shown to be essential for cytosolic Na+ detoxification; i.e., the Ca2+
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