Integrative Transcriptomic and Phosphoproteomic Analysis Reveals Key Components of the SnRK1 Signaling Network in Rice

SnRK1 is an evolutionarily conserved protein kinase belonging to the SNF1/AMPK family of protein kinases that is central to adjusting growth in response to the energy status. Numerous studies have shown adaptive and developmental roles of SnRK1, but the understanding of the SnRK1 signaling network in monocots is limited. Using CRISPR/Cas9 mutagenesis to target the functional kinase subunits in rice, we carried out comprehensive phenotypic, transcriptomic, proteomic, and phosphoproteomic analyses of rice <i>snrk1</i> mutants displaying growth defects under normal and starvation conditions. These analyses revealed the role of SnRK1 signaling in controlling growth and stress-related processes in both energy-sufficient and energy-limited conditions and pointed to the subfunctionalization of SnRK1 kinase subunit genes. In addition to the classical protein targets of SnRK1, phosphoproteomics revealed novel targets including the key components of intracellular membrane trafficking, ethylene signaling, and ion transport. The upregulation of stress-related processes and suppression of growth-related processes in <i>snrk1</i> mutants correlated with their phenotypic defects. Overall, this study highlights a dual role of SnRK1 as a promoter of growth under favorable conditions and a critical regulator of adaptive response under stress conditions.