ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport

BACKGROUND AND AIMS: In order to cope with arid environments, the xerohalophyte Zygophyllum xanthoxylum efficiently compartmentalizes Na(+) into vacuoles, mediated by ZxNHX, and maintains stability of K(+) in its leaves. However, the function of ZxNHX in controlling Na(+) and K(+) homeostasis at the whole-plant level remains unclear. In this study, the role of ZxNHX in regulating the expression of genes involved in Na(+) and K(+) transport and spatial distribution was investigated. METHODS: The role of ZxNHX in maintaining Na(+) and K(+) homeostasis in Z. xanthoxylum was studied using post-transcriptional gene silencing via Agrobacterium-mediated transformation. Transformed plants were grown with or without 50 mm NaCl, and expression levels and physiological parameters were measured. KEY RESULTS: It was found that 50 mm NaCl induced a 620 % increase in transcripts of ZxSOS1 but only an 80 % increase in transcripts of ZxHKT1;1 in roots of wild-type (WT) plants. Consequently, the ability of ZxSOS1 to transport Na(+) exceeded that of ZxHKT1;1, and Na(+) was loaded into the xylem by ZxSOS1 and delivered to the shoots. However, in a ZxNHX-silenced line (L7), the capacity to sequester Na(+) into vacuoles of leaves was weakened, which in turn regulated long-distance Na(+) transport from roots to shoots. In roots of L7, NaCl (50 mm) increased transcripts of ZxSOS1 by only 10 %, whereas transcripts of ZxHKT1;1 increased by 53 %. Thus, in L7, the transport ability of ZxHKT1;1 for Na(+) outweighed that of ZxSOS1. Na(+) was unloaded from the xylem stream, consequently reducing Na(+) accumulation and relative distribution in leaves, but increasing the relative distribution of Na(+) in roots and the net selective transport capacity for K(+) over Na(+) from roots to shoots compared with the WT. Silencing of ZxNHX also triggered a downregulation of ZxAKT1 and ZxSKOR in roots, resulting in a significant decrease in K(+) accumulation in all the tissues in plants grown in 50 mm NaCl. These changes led to a significant reduction in osmotic adjustment, and thus an inhibition of growth in ZxNHX-silenced lines. CONCLUSIONS: The results suggest that ZxNHX is essential for controlling Na(+), K(+) uptake, long-distance transport and their homeostasis at whole-plant level via feedback regulation of the expression of genes involved in Na(+), K(+) transport. The net result is the maintenance of the characteristic salt accumulation observed in Z. xanthoxylum and the regulation of its normal growth. A model is proposed for the role of ZxNHX in regulating the Na(+) transport system in Z. xanthoxylum under saline conditions.