Comparative transcriptome analysis reveals unique genetic adaptations conferring salt tolerance in a xerohalophyte

Abstract

Most studies on salt tolerance in plants have been conducted using glycophytes like Arabidopsis thaliana (L.) Heynh., with limited resistance to salinity. The xerohalophyte Zygophyllum xanthoxylum (Bunge) Engl. is a salt-accumulating desert plant that efficiently transports Na+ into vacuoles to manage salt and exhibits increased growth under salinity conditions, suggesting a unique transcriptional response compared with glycophytes. We used transcriptome profiling by RNA-seq to compare gene expression in roots of Z. xanthoxylum and A. thaliana under 50 mM NaCl treatments. Gene Ontology (GO) functional annotation and Kyoto Encyclopedia of Genes and Genomes (KEGG) metabolic pathway analysis suggested that 50 mM NaCl was perceived as a stimulus for Z. xanthoxylum whereas a stress for A. thaliana. Exposure to 50 mM NaCl caused metabolic shifts towards gluconeogenesis to stimulate growth of Z. xanthoxylum, but triggered defensive systems in A. thaliana. Compared with A. thaliana, a vast array of ion transporter genes was induced in Z. xanthoxylum, revealing an active strategy to uptake Na+ and nutrients from the environment. An ascorbate-glutathione scavenging system for reactive oxygen species was also crucial in Z. xanthoxylum, based on high expression of key enzyme genes. Finally, key regulatory genes for the biosynthesis pathways of abscisic acid and gibberellin showed distinct expression patterns between the two species and auxin response genes were more active in Z. xanthoxylum compared with A. thaliana. Our results provide an important framework for understanding unique patterns of gene expression conferring salt resistance in Z. xanthoxylum.