Sulfate-TOR signaling controls transcriptional reprogramming for shoot apex activation

Plants play a primary role for the global sulfur cycle in the earth ecosystems by reduction of inorganic sulfate from the soil to organic sulfur-containing compounds. How plants sense and transduce the sulfate availability to mediate their growth remains largely unclear. The target of rapamycin (TOR) kinase is an evolutionarily conserved master regulator of nutrient sensing and metabolic signaling to control cell proliferation and growth in all eukaryotes. By tissue-specific Western blotting and RNA-sequencing analysis, we investigated sulfate-TOR signal pathway in regulating shoot apex development. Here, we report that inorganic sulfate exhibits high potency activating TOR and cell proliferation to promote true leaf development in Arabidopsis in a glucose-energy parallel pathway. Genetic and metabolite analyses suggest that this sulfate activation of TOR is independent from the sulfate-assimilation process and glucose-energy signaling. Significantly, tissue specific transcriptome analyses uncover previously unknown sulfate-orchestrating genes involved in DNA replication, cell proliferation and various secondary metabolism pathways, which largely depends on TOR signaling. Systematic comparison between the sulfate- and glucose-TOR controlled transcriptome further reveals that TOR kinase, as the central growth integrator, responds to different nutrient signals to control both shared and unique transcriptome networks, therefore, precisely modulates plant proliferation, growth and stress responses.

Automated summary

Plants play a crucial role in the global sulfur cycle and their growth is regulated by the sulfate-TOR signal pathway. Activation of TOR by inorganic sulfate promotes true leaf development in Arabidopsis independently of sulfate-assimilation and glucose-energy signaling. The TOR signaling pathway controls DNA replication, cell proliferation, and secondary metabolism pathways, and responds to different nutrient signals to precisely modulate plant growth and stress responses.