Light regulates alternative splicing outcomes via the TOR kinase pathway.

Stefan Riegler,Andrea Barta,Christian Meyer,Peter Venhuizen,Maria Kalyna,Micaela A Godoy Herz,María G Kubaczka,Ezequiel Petrillo,Jacob O Brunkard,Lucas Servi,M Regina Scarpin

doi:10.1016/j.celrep.2021.109676

Abstract

SUMMARYFor plants, light is the source of energy and the most relevant regulator of growth and adaptations to the environment by inducing changes in gene expression at various levels, including alternative splicing. Light-triggered chloroplast retrograde signals control alternative splicing in Arabidopsis thaliana. Here, we provide evidence that light regulates the expression of a core set of splicing-related factors in roots. Alternative splicing responses in roots are not directly caused by light but are instead most likely triggered by photo-synthesized sugars. The target of rapamycin (TOR) kinase plays a key role in this shoot-to-root signaling pathway. Knocking down TOR expression or pharmacologically inhibiting TOR activity disrupts the alternative splicing responses to light and exogenous sugars in roots. Consistently, splicing decisions are modulated by mitochondrial activity in roots. In conclusion, by activating the TOR pathway, sugars act as mobile signals to coordinate alternative splicing responses to light throughout the whole plant.

Highlights

Light is essential for plants: it is their source of energy and makes carbon fixation possible, allowing life on Earth as we know it
We reported that nuclear alternative splicing is modulated by light through a chloroplast retrograde signaling pathway (Petrillo et al, 2014) and that this process is related to an increase in transcription elongation (Godoy Herz et al, 2019)
We show that by activating the target of rapamycin (TOR) pathway in roots, sugars act as mobile signals to coordinate alternative splicing responses to light throughout the whole plant

Summary

Introduction

Light is essential for plants: it is their source of energy and makes carbon fixation possible, allowing life on Earth as we know it. Light is the main source of information about the everchanging environment for plants. Since their success depends on this environmental cue, it is not surprising that plants have evolved a rich variety of mechanisms to sense light wavelength, direction, and quantity (Gyula et al, 2003; Perrella and Kaiserli, 2016). We reported that nuclear alternative splicing is modulated by light through a chloroplast retrograde signaling pathway (Petrillo et al, 2014) and that this process is related to an increase in transcription elongation (Godoy Herz et al, 2019). We showed that photosynthesis modulates alternative splicing responses in roots, suggesting the existence of intercellular mobile retrograde signals (Petrillo et al, 2014). The central question that arises is how light sensed by shoot chloroplasts coordinates nuclear splicing throughout the whole plant

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