Evolutionary Significance of NHX Family and NHX1 in Salinity Stress Adaptation in the Genus Oryza

Abstract

Rice (<i>Oryza sativa</i>), a staple crop for a substantial part of the world's population, is highly sensitive to soil salinity; however, some wild <i>Oryza</i> relatives can survive in highly saline environments. Sodium/hydrogen antiporter (NHX) family members contribute to Na⁺ homeostasis in plants and play a major role in conferring salinity tolerance. In this study, we analyzed the evolution of NHX family members using phylogeny, conserved domains, tertiary structures, expression patterns, and physiology of cultivated and wild <i>Oryza</i> species to decipher the role of NHXs in salt tolerance in <i>Oryza</i>. Phylogenetic analysis showed that the NHX family can be classified into three subfamilies directly related to their subcellular localization: endomembrane, plasma membrane, and tonoplast (vacuolar subfamily, <i>vNHX1</i>). Phylogenetic and structural analysis showed that <i>vNHX1s</i> have evolved from streptophyte algae (e.g., <i>Klebsormidium nitens</i>) and are abundant and highly conserved in all major land plant lineages, including <i>Oryza</i>. Moreover, we showed that tissue tolerance is a crucial trait conferring tolerance to salinity in wild rice species. Higher Na⁺ accumulation and reduced Na⁺ effluxes in leaf mesophyll were observed in the salt-tolerant wild rice species <i>O. alta</i>, <i>O. latifolia</i>, and <i>O. coarctata</i>. Among the key genes affecting tissue tolerance, expression of <i>NHX1</i> and <i>SOS1/NHX7</i> exhibited significant correlation with salt tolerance among the rice species and cultivars. This study provides insights into the evolutionary origin of plant NHXs and their role in tissue tolerance of <i>Oryza</i> species and facilitates the inclusion of this trait during the development of salinity-tolerant rice cultivars.