Chloride-dependent plasma membrane hyperpolarization confers superior salinity tissue tolerance in wild rice Oryza coarctata

Salinity tissue tolerance is a key trait that confers adaptive potential in halophytic species. The aim of this study was to understand the mechanistic basis of salinity tissue tolerance in the Oryza coarctata, a halophytic wild relative of cultivated rice Oryza sativa, to be then used as novel targets for improving salinity stress tolerance of O. sativa. Salinity led to ∼80% decline in mesophyll cell viability in cultivated rice, whereas only 15% reduction was observed in the wild rice. In response to NaCl treatments, mesophyll cells of O. coarctata showed less Na⁺ uptake and better K⁺ retention than cultivated rice. Pharmacological experiments suggested that salinity-induced Na⁺ uptake and K⁺ loss in O. coarctata were mediated by non-selective cation channels (NSCCs) while K⁺ loss in cultivated rice was mediated predominantly by GORK (guard cell outward-rectifying K⁺) channels. Salt treatment resulted in a depolarization of the plasma membrane (PM) in O. sativa. In contrast, O. coarctata had NaCl dose-dependent hyperpolarization in the mesophyll cells, due to its higher preference for Cl⁻ uptake. This difference in plant ionic relations was partially attributable to differences in transcriptional expression levels of Potassium transporter 1 (AKT1), Salt overly sensitive 1 (SOS1), Sodium transporter OsHKT1;4, and Chloride channel (OsCLC1). It is concluded that O. coarctata possesses a strong ability to discriminate between Cl⁻ and Na⁺ uptake (a trait lacking in cultivated rice) and use it to maintain negative membrane potential (MP) values without activating H⁺-ATPase, thus enabling more efficient K⁺ retention in mesophyll with low energy costs. The above traits should be considered as potential targets in the rice breeding program for salt tolerance enhancement.