Nutrient-driven TOR signalling controls a chromatin-associated complex for orchestrating plant growth and stress tolerance

Abstract

The conserved target of rapamycin (TOR) kinase acts as a master regulator of growth by integrating nutrient and environmental signals in eukaryotes. However, how TOR influences chromatin remains poorly understood. Here we identified a multi-subunit complex in Arabidopsis thaliana, termed the chromatin-associated complex for growth (CACG). Our findings indicate that under nutrient-rich conditions, active TOR kinase enhances CACG mRNA translation, which is facilitated by pyrimidine-rich motifs in their 5′ untranslated regions. CACG components co-occupy stress-responsive genes marked by histone acetylation, repressing their transcription to promote growth. Conversely, under nutrient-deficient conditions, inactive TOR reduces CACG mRNA translation, relieving transcriptional repression of stress-responsive genes and leading to increased stress tolerance but impaired growth. These results indicate that the CACG complex acts as a critical nutrient-responsive transcriptional regulator that is required for coordinating plant growth and stress tolerance in a TOR-dependent manner. The molecular mechanism revealed here could aid in developing high-yield crops capable of thriving in adverse environments. A chromatin-associated complex, which is dynamically regulated by TOR kinase at the translational level, functions to suppress the transcription of stress-responsive genes marked by histone acetylation, thereby coordinating plant growth and stress tolerance.