Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes

Significance

The modulation of growth and development is central to sessile plants. Shoot and root meristems share almost identical molecular machineries but are responsible for different types of aboveground and underground organogenesis. How two such highly similar biological systems respond to different environmental cues and regulate distinct developmental programs remains largely unknown. We report that, in harmony with nature, the shoot, but not the root, demands light for the activation of cell proliferation during organogenesis. We decipher the underlying mechanism that light is necessary for continuous auxin biosynthesis only in the shoot, but not the root, to activate target of rapamycin (TOR) kinase signaling. We further elucidate an auxin-Rho-related protein 2 (ROP2)-TOR-transcription factors E2Fa,b signaling cascade that integrates different environmental signals to orchestrate plant growth and development.

Abstract

The developmental plasticity of plants relies on the remarkable ability of the meristems to integrate nutrient and energy availability with environmental signals. Meristems in root and shoot apexes share highly similar molecular players but are spatially separated by soil. Whether and how these two meristematic tissues have differential activation requirements for local nutrient, hormone, and environmental cues (e.g., light) remain enigmatic in photosynthetic plants. Here, we report that the activation of root and shoot apexes relies on distinct glucose and light signals. Glucose energy signaling is sufficient to activate target of rapamycin (TOR) kinase in root apexes. In contrast, both the glucose and light signals are required for TOR activation in shoot apexes. Strikingly, exogenously applied auxin is able to replace light to activate TOR in shoot apexes and promote true leaf development. A relatively low concentration of auxin in the shoot and high concentration of auxin in the root might be responsible for this distinctive light requirement in root and shoot apexes, because light is required to promote auxin biosynthesis in the shoot. Furthermore, we reveal that the small GTPase Rho-related protein 2 (ROP2) transduces light-auxin signal to activate TOR by direct interaction, which, in turn, promotes transcription factors E2Fa,b for activating cell cycle genes in shoot apexes. Consistently, constitutively activated ROP2 plants stimulate TOR in the shoot apex and cause true leaf development even without light. Together, our findings establish a pivotal hub role of TOR signaling in integrating different environmental signals to regulate distinct developmental transition and growth in the shoot and root.