Advances in Sensing, Response and Regulation Mechanism of Salt Tolerance in Rice

Abstract

Soil salinity is a serious menace in rice production threatening global food security. Rice responses to salt stress involve a series of biological processes, including antioxidation, osmoregulation or osmoprotection, and ion homeostasis, which are regulated by different genes. Understanding these adaptive mechanisms and the key genes involved are crucial in developing highly salt-tolerant cultivars. In this review, we discuss the molecular mechanisms of salt tolerance in rice-from sensing to transcriptional regulation of key genes-based on the current knowledge. Furthermore, we highlight the functionally validated salt-responsive genes in rice.

Keywords: antioxidation; ion homeostasis; osmoregulation; rice; salinity; sensing; signaling; transcription factors.

Figure 1

Salt sensing and signaling involved in rice responses to salt stress. Under high salinity, salt-induced osmotic stress begins, which is sensed by putative osmosensor OsHK3b, activated by OsHpt2. SIT1 also acts as a sensor via elevated kinase activity and induces reactive oxygen species (ROS) production and mitogen-activated protein kinase (MAPK) signaling. The activity of SIT1 is deactivated by the B’κ-PP2A subunit. Later, ionic stress occurs and is sensed by an unknown Na⁺ sensor. The Na⁺ enters the mature epidermal cell through nonselective cation channel (NSCC), causing membrane depolarization, and is polarized by P-type ATPases. Excess salt triggers a spike in the concentration of cytosolic secondary messengers, including Ca²⁺, reactive oxygen species (ROS), and phosphatidic acid (PA). ROS triggers Ca²⁺ influx through the cyclic nucleotide-gated ion channel (CNGC), activated by an unknown molecule. Ca²⁺ not only decreases K⁺ efflux but also induces further ROS accumulation; thus, a positive feedback loop exists between Ca²⁺ and ROS. The cytosolic Ca²⁺ also induces vacuolar Ca²⁺ release and activates Ca²⁺-binding proteins, such as OsCIPK24-OsCBL4 complex. This complex, together with MAPK, activated by phosphatidic acid, upregulates the OsSOS1 to remove cytosolic Na⁺. The vacuolar OsNHX1 gene is activated by OsCPK21, whereas the V-type ATPase is activated by OsCIPK24, establishing a proton gradient and driving the activity of OsNHX1.

Figure 2

Transcriptional regulation involved in activating salt stress-responsive genes in rice. The transcriptional regulation occurs via abscisic acid (ABA)-dependent and -independent pathway, whereby transcription factors (TFs) bind with their corresponding cis-regulatory element. The APETALA2/ethylene responsive factor (AP2/ERF) and NAC (NAM, ATAF, and CUC) TFs operate in an ABA-independent pathway. NAC TFs regulate other TFs, such as dehydration responsive element-binding (DREB), myeloblastosis (MYB), and basic leucine-zipper (bZIP). The MYB, bZIP, zinc finger (ZF), basic-helix-loop-helix (bHLH), DREB, and other TFs are involved in the ABA-dependent pathway.

Figure 3

Rice salt tolerance adaptive mechanisms. In the leaf, (a) stomatal closure mediated either by DST or SNAC1 is the initial response of rice to salinity. Salt stress downregulates DST which interacts with DCA1 and activates OsPrx24 and LP2. Conversely, SNAC1 is upregulated, activating the OsSRO1c. These downstream genes mediate stomatal closure via H₂O₂ inhibition. (b,c) Na⁺ content in the leaf cytoplasm is controlled by vacuolar sequestration, xylem unloading, and phloem loading. Excess Na⁺ is sequestered into the vacuole via OsNHX1 coupled with H⁺-pump and OsVP1, a vacuolar-type H⁺-pyrophosphatase encoding gene. Na⁺ unloading at the xylem and Na⁺ loading at the phloem are mediated by OsHKT1;4 and OsHKT1;1, respectively. In the root, (d) Na⁺ is loaded at the xylem through nonselective cation channel (NSCC) and OsSOS1 coupled with H⁺-pump. Conversely, OsHKT1;5 unloads the Na⁺ ions from the xylem and shuttles them back to the parenchyma cells. Apart from Na⁺, K⁺ influx occurs mediated by OsHAK21, thereby increasing the K⁺/Na⁺ ratio. (e) Enhanced suberin deposition in the root exodermis and endodermis also inhibits Na⁺ influx to the stele. Similarly, it blocks water transport out of the stele. (f) The plasma membrane-bound OsPIP2;2 gene increases hydraulic conductivity in the root endodermis, allowing water uptake. (g) Na⁺ enters the root epidermis via NSCC and is shuttled back to the external medium via the OsSOS1 coupled with H⁺-pump.