A Chloroplast Retrograde Signal Regulates Nuclear Alternative Splicing

PETRILLO, EZEQUIEL; GODOY HERZ, MICAELA A; FUCHS, ARMIN; REIFER, DOMINIK; BARTA, ANDREA; KALYNA, MARIA; KORNBLIHTT, ALBERTO

Conferencia; 11th EMBL Conference: Transcription and Chromatin 2014; 2014

In plants light is not only the main source of energy but also a signal used to optimize plant growth and development in response to environmental changing conditions. The relevance of light signaling in plants is such that, according to recent estimates, regulates approximately 20% of the transcriptome in Arabidopsis thaliana and rice. Among the different levels of mRNA processing, alternative splicing has been shown to be important in the modulation of gene expression during plant development and in response to environmental cues. Our studies reveal that light signals affect alternative splicing of a subset of Arabidopsis genes, preferentially of those encoding proteins involved in RNA processing. As a model for our analysis we used the responses of At-RS31 (a plant-specific SR protein) transcriptional unit. This gene gives rise to three alternative splicing isoforms, among which, only the shorter one (called mRNA1) is the isoform encoding for a protein. In seedlings, light exposure increases the abundance of mRNA1 while dark incubation increase the relative amounts of the non-protein coding isoforms. We discard mRNA stability as the mechanism underlying the light/dark transition effects on the alternative splicing of At-RS31 by using transcription inhibitors and mRNA degradation defective mutant lines. Different wavelengths, mutants and photosynthetic electron transfer inhibitors allowed us to rule out the participation of cryptochrome and phytochrome photoreceptors and revealed the need for functional chloroplasts to control alternative splicing. Surprisingly, this effect is not only observed in green tissues but also in roots when the communication with the photosynthetic tissues is not interrupted, suggesting that a signaling molecule travels through the plant. Furthermore, by using electron transfer inhibitors and photosynthesis related mutants we demonstrate that the reduced pool of plastoquinones initiates a chloroplast retrograde signaling that regulates nuclear alternative splicing in Arabidopsis. Alternative splicing is an alien process for the chloroplasts due to their prokaryotic origin. The regulation of alternative splicing by this organelle constitutes an unexpected extra layer of gene control that might allow plants to respond and adapt in a more specific way to environmental and developmental challenges.