A brassinosteroid signaling protein acts as an integrative regulator of K+ and Na+ transport in rice response to salt stress

Abstract

Maintaining the cytosolic K+/Na+ homeostasis is crucial for plants’ salt tolerance. Therefore, elucidating the regulatory mechanism governing K+/Na+ transport is pivotal to engineering salt-tolerant crops. Although many regulators have been shown specifically to modulate either Na+ or K+ transporters, little is known about integrative regulators that orchestrate the transport of both cations. In this study, we reveal that a rice basic helix-loop-helix (bHLH) transcription factor, BES1-INTERACTING MYC-LIKE1 (OsBIM1), negatively regulates K+/Na+ homeostasis under salt stress. Loss of OsBIM1 function conferred salt tolerance and K+/Na+ homeostasis in rice, whereas its overexpression produced the opposite effect. The K+ transporter OsHAK5 and transcription factor OsWRKY53 were identified as the targets of OsBIM1. By binding to E-box elements in their promoter regions, OsBIM1 not only repressed OsHAK5 expression and the root K+ uptake, but also trans-activated OsWRKY53 to suppress transcription of the Na+ transporter gene OsHKT1;5 and the Na+ unloading from xylem. OsBIM1 expression was attenuated by salt stress, and the loss of OsBIM1 function leads to synergistic upregulation of OsHAK5 and OsHKT1;5, thereby enhancing salt tolerance. As a positive regulator of Brassinosteroid (BR) signaling, OsBIM1 was also found to be indispensable for BR-induced attenuation of salt tolerance and involved in BR-mediated regulation of OsHAK5 and OsWRKY53 expression. This study reveals an integrative regulator of K+/Na+ transport and a negative regulatory mechanism by which BR affects salt tolerance, providing a promising strategy for breeding salt-tolerant rice.