ZxAKT1 is essential for K+ uptake and K+/Na+ homeostasis in the succulent xerophyte Zygophyllum xanthoxylum

The inward-rectifying K+ channel AKT1 constitutes an important pathway for K+ acquisition in plant roots. In glycophytes, excessive accumulation of Na+ is accompanied by K+ deficiency under salt stress. However, in the succulent xerophyte Zygophyllum xanthoxylum, which exhibits excellent adaptability to adverse environments, K+ concentration remains at a relatively constant level despite increased levels of Na+ under salinity and drought conditions. In this study, the contribution of ZxAKT1 to maintaining K+ and Na+ homeostasis in Z.xanthoxylum was investigated. Expression of ZxAKT1 rescued the K+-uptake-defective phenotype of yeast strain CY162, suppressed the salt-sensitive phenotype of yeast strain G19, and complemented the low-K+-sensitive phenotype of Arabidopsis akt1 mutant, indicating that ZxAKT1 functions as an inward-rectifying K+ channel. ZxAKT1 was predominantly expressed in roots, and was induced under high concentrations of either KCl or NaCl. By using RNA interference technique, we found that ZxAKT1-silenced plants exhibited stunted growth compared to wild-type Z.xanthoxylum. Further experiments showed that ZxAKT1-silenced plants exhibited a significant decline in net uptake of K+ and Na+, resulting in decreased concentrations of K+ and Na+, as compared to wild-type Z.xanthoxylum grown under 50mm NaCl. Compared with wild-type, the expression levels of genes encoding several transporters/channels related to K+/Na+ homeostasis, including ZxSKOR, ZxNHX, ZxSOS1 and ZxHKT1;1, were reduced in various tissues of a ZxAKT1-silenced line. These findings suggest that ZxAKT1 not only plays a crucial role in K+ uptake but also functions in modulating Na+ uptake and transport systems in Z.xanthoxylum, thereby affecting its normal growth. Significance Statement Succulent plants can better adapt to drought and salinity. Here we show that an inward-rectifying potassium channel (ZxAKT1) contributes to this adaptation in Z.xanthoxylum, as unlike in glycophytes, where excessive accumulation of Na+ is accompanied by K+ deficiency under salt stress, in succulents K+ was maintained at a relatively constant level, despite increased Na+. Thus ZxAKT1 not only plays a crucial role in K+ uptake but also functions in modulating Na+ uptake and transport systems.