TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings

Significance

Light enhances the translation efficiency of thousands of mRNAs during photomorphogenic development in Arabidopsis, but the underlying molecular mechanism remains elusive. Here we show that light activates the auxin-target of rapamycin (TOR)-ribosome protein S6 (RPS6) pathway to enhance translation in deetiolating Arabidopsis. We discovered that CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) represses TOR activity in dark-grown seedlings. The perception of far-red and blue light by photoreceptors inactivates COP1, which leads to the derepression of the auxin-TOR-RPS6 pathway and enhanced de novo protein synthesis. Our study revealed a light-triggered signaling pathway for translational regulation. This sophisticated regulation also functions to ensure that young seedlings have strict skotomorphogenic development in the dark and a timely switch to photomorphogenic development.

Abstract

Deetiolation is an essential developmental process transforming young plant seedlings into the vegetative phase with photosynthetic activities. Light signals initiate this important developmental process by triggering massive reprogramming of the transcriptome and translatome. Compared with the wealth of knowledge of transcriptional regulation, the molecular mechanism underlying this light-triggered translational enhancement remains unclear. Here we show that light-enhanced translation is orchestrated by a light perception and signaling pathway composed of photoreceptors, CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1), the phytohormone auxin, target of rapamycin (TOR), and ribosomal protein S6 (RPS6). In deetiolating Arabidopsis seedlings, photoreceptors, including phytochrome A and cryptochromes, perceive far-red and blue light to inactivate the negative regulator COP1, which leads to activation of the auxin pathway for TOR-dependent phosphorylation of RPS6. Arabidopsis mutants defective in TOR, RPS6A, or RPS6B exhibited delayed cotyledon opening, a characteristic of the deetiolating process to ensure timely vegetative development of a young seedling. This study provides a mechanistic view of light-triggered translational enhancement in deetiolating Arabidopsis.