Mycorrhizal symbiosis reprograms ion fluxes and fatty acid metabolism in wild jujube during salt stress

Chinese jujube (Ziziphus jujuba) is an important fruit tree in China, and soil salinity is the main constraint affecting jujube production. It is unclear how arbuscular mycorrhizal (AM) symbiosis supports jujube adaptation to salt stress. Herein, we performed comparative physiological, ion flux, fatty acid (FA) metabolomic, and transcriptomic analyses to examine the mechanism of AM jujube responding to salt stress. AM seedlings showed better performance during salt stress. AM symbiosis altered phytohormonal levels: indole-3-acetic acid and abscisic acid contents were significantly increased in AM roots and reduced by salt stress. Mycorrhizal colonization enhanced root H+ efflux and K+ influx, while inducing expression of plasma membrane-type ATPase 7 (ZjAHA7) and high-affinity K+ transporter 2 (ZjHAK2) in roots. High K+/Na+ homeostasis was maintained throughout salt exposure. FA content was elevated in AM leaves as well as roots, especially for palmitic acid, oleic acid, trans oleic acid, and linoleic acid, and similar effects were also observed in AM poplar (Populus. alba x Populus. glandulosa cv. 84K) and Medicago truncatula, indicating AM symbiosis elevating FA levels could be a conserved physiological effect. Gene co-expression network analyses uncovered a core gene set including 267 genes in roots associated with AM symbiosis and conserved transcriptional responses, for example, FA metabolism, phytohormone signal transduction, SNARE interaction in vesicular transport, and biotin metabolism. In contrast to widely up-regulated genes related to FA metabolism in AM roots, limited genes were affected in leaves. We propose a model of AM symbiosis-linked reprogramming of FA metabolism and provide a comprehensive insight into AM symbiosis with a woody species adaptation to salt stress. Arbuscular mycorrhizal symbiosis improves salt tolerance of jujube plants by maintaining K+/Na+ homeostasis and reprogramming plant fatty acid metabolism.

Automated summary

This study investigated the mechanism of how arbuscular mycorrhizal (AM) symbiosis supports the adaptation of Chinese jujube trees to salt stress. The results showed that AM symbiosis improves salt tolerance by maintaining K+/Na+ homeostasis and reprogramming plant fatty acid metabolism. Gene co-expression network analysis revealed key genes associated with AM symbiosis and conserved transcriptional responses in roots, including those involved in fatty acid metabolism and phytohormone signal transduction.