The rice SnRK family: biological roles and cell signaling modules

Abstract

Stimulus-activated signaling pathways orchestrate cellular responses to control plant growth and development and mitigate the effects of adverse environmental conditions. During this process, signaling components are modulated by central regulators of various signal transduction pathways. Protein phosphorylation by kinases is one of the most important events transmitting signals downstream, via the posttranslational modification of signaling components. The plant serine and threonine kinase SNF1-related protein kinase (SnRK) family, which is classified into three subgroups, is highly conserved in plants. SnRKs participate in a wide range of signaling pathways and control cellular processes including plant growth and development and responses to abiotic and biotic stress. Recent notable discoveries have increased our understanding of how SnRKs control these various processes in rice (Oryza sativa). In this review, we summarize current knowledge of the roles of OsSnRK signaling pathways in plant growth, development, and stress responses and discuss recent insights. This review lays the foundation for further studies on SnRK signal transduction and for developing strategies to enhance stress tolerance in plants.

Keywords: SNF1-related protein kinase; abiotic stress; biotic stress; cell signaling; phosphorylation; plant growth and development; rice.

Figure 1

Structural domains and major functions of the three SnRK subfamilies. Top, SNF1-related protein kinase 1 (SnRK1) members contain a highly conserved N-terminal α-subunit kinase catalytic domain (KD) and a C-terminal regulatory domain including the ubiquitin-associated (UBA) and kinase-associated 1 (KA1) domains. Two amino acids in the KD are required for its kinase activity: the conserved lysine 43 (K43) conferring ATP binding (ATP-B) and the phosphorylated threonine 170 (T170) in the activation loop (T-loop) of OsSnRK1A are both required for its activation. The UBA domain interacts with the ubiquitination protein (Ub-P) and enhances its catalytic activity. The KA1 domain interacts with proteins including protein phosphatases (PPs). SnRK1s function as master regulators of energy-stress signaling. Middle, SnRK2/Stress-activated protein kinase (SAPK) members contain a KD and a divergent C-terminal domain and are central regulators of abiotic stress and ABA signaling. Bottom, SnRK3/Calcineurin B-like protein (CBL)-interacting protein kinase (CIPK) members contain a KD and a C-terminal regulatory domain containing a NAF or FISL motif (comprising 21 amino acids including the highly conserved [N, A, and F] or [F, I, S and L] residues) and a protein phosphatase interaction (PPI) domain. The autoinhibitory NAF or FISL motif interacts with CBL, resulting in CIPK activation via CBL-CIPK complex formation. The PPI domain interacts with the type 2C protein phosphatase (PP2C). Therefore, SnRK3s play important roles in the Ca²⁺ signaling pathway.

Figure 2

OsSnRK1A-Tre6P signaling loop functions in rice growth and development. The energy-stress master regulator SNF1-related protein kinase 1 (SnRK1) and Trehalose 6-phosphate (Tre6P) play central roles in plant energy homeostasis, growth, and development. Tre6P levels are very low in the basal state but respond dramatically to changes in sugar contents. Tre6P is produced from UDP-glucose (UDPG) and glucose-6-phosphate (Glc6P) by trehalose-6-phosphate synthase (TPS). Subsequently, Tre6P is converted to trehalose by trehalose-6-phosphate phosphatase (TPP) and is hydrolyzed into two glucose molecules by trehalase (TRE). Two groups recently revealed the roles of SnRK1-Tre6P signaling in regulating plant growth and development (Li et al., 2022; Wang et al., 2023). High sugar content increases the activity of the NAC (NAM, ATAF, and CUC) transcription factor OsNAC23 in repressing OsSnRK1A and Trehalose 6-phosphate phosphatase 1 (OsTPP1) activity (Li et al., 2022). Since TPPs convert Tre6P to trehalose, OsNAC23-mediated repression of OsTPP1 leads to Tre6P accumulation under high sugar levels. To maintain sugar homeostasis, the OsNAC23-induced Tre6P signal enhances the movement of sugar from source to sink, resulting in improved grain yield. Under energy-stress condition, OsSnRK1A and Starvation-associated growth inhibitor 1 (OsSGI1)/Basic helix–loop–helix 111 (OsbHLH111) are activated (Wang et al., 2023). OsSGI1 (when phosphorylated by OsSnRK1A) represses the expression of OsTPP7 and increases Tre6P levels under sugar-deficiency condition. Hence, high Tre6P levels induced by the OsSnRK1A-OsSGI1-OsTPP7 module result in inhibited plant growth under sugar-starvation condition.

Figure 3

ABA signaling cascade and signaling components associated with OsSnRK2. SNF1-related protein kinase 2 (SnRK2)/Stress-activated protein kinase (SAPK) is a core regulator of ABA signaling and abiotic stress responses in plants. For the ABA response, the ABA receptor PYL/RCAR (Pyrabactin-resistance like/Regulatory component of ABA receptors) inactivates the type 2C protein phosphatase (PP2C), which is a negative regulator of SnRK2. Activated SnRK2 phosphorylates effectors including transcription factors to transfer the signal downstream. In rice, all OsSAPKs are activated by hyperosmotic stress, but only OsSAPK8–10 (belonging to subgroup III) are activated by ABA (Kobayashi et al., 2004). Many studies have identified various regulators of OsSAPK-mediated ABA signaling. This figure shows the signaling components known to be associated with the different OsSnRK2 subgroups.

Figure 4

OsSnRK3 signaling cascades conferring abiotic stress tolerance. SNF1-related protein kinase 3 (SnRK3)/CBL-interacting protein kinase (CIPK) is key regulator of the Ca²⁺ signaling pathway in response to various abiotic stresses. Under salt-stress conditions, Salt overly sensitive 2 (OsSOS2)/OsCIPK24 forms complex with OsSOS3/OsCBL4 to recognize Ca²⁺. The complex then activates OsSOS1/NA⁺ and H⁺ antiporter 7 (OsNHX7) to maintain Na⁺ homeostasis (Martinez-Atienza et al., 2007). Flooding-induced sucrose starvation activates OsCIPK15 to regulate OsSnRK1A-MYBS1 module-induced starch mobilization via α-Amylase 3 (αAmy3), as well as ethanol fermentation via Alcohol dehydrogenase 1 (ADH1), resulting in energy production and anaerobic germination tolerance (Lee et al., 2009; Kudahettige et al., 2011). The OsCBL8-OsCIPK17 complex contributes to heat and drought tolerance by interacting with stress-associated proteins including OsNAC77, a transcription factor that induces the expression of genes related to heat and/or drought tolerance (Gao et al., 2022a). Under chilling conditions, Calreticulin 3 (OsCRT3) and OsCIPK7 undergo conformation changes in the endoplasmic reticulum (ER), resulting in high cytosolic Ca²⁺ levels and the formation of the OsCBL7-OsCIPK7 and OsCBL8-OsCIPK7 complexes, which activate Ca²⁺ signaling at the plasma membrane (PM) to enhance cold tolerance (Guo et al., 2023).