Plants use light as source of energy and information to detect diurnal rhythms and seasonal changes. Sensing changing light conditions is critical to adjust plant metabolism and to initiate developmental transitions. Here we analyzed transcriptome-wide alterations in gene expression and alternative splicing (AS) of etiolated seedlings undergoing photomorphogenesis upon exposure to blue, red, or white light. Our analysis revealed massive transcriptome reprograming as reflected by differential expression of ~20% of all genes and changes in several hundred AS events. For more than 60% of all regulated AS events, light promoted the production of a presumably protein-coding variant at the expense of an mRNA with nonsense-mediated decay-triggering features. Accordingly, AS of the putative splicing factor REDUCED RED-LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1 (RRC1), previously identified as a red light signaling component, was shifted to the functional variant under light. Downstream analyses of candidate AS events pointed at a role of photoreceptor signaling only in monochromatic but not in white light. Furthermore, we demonstrated similar AS changes upon light exposure and exogenous sugar supply, with a critical involvement of kinase signaling. We propose that AS is an integration point of signaling pathways that sense and transmit information regarding the energy availability in plants.

Supplemental Dataset 1Computational Analysis of Transcriptome-Wide AS.Supplemental_Data_set_1_AS_analysis.xlsxSupplemental Data Set 2Computational Analysis of Transcriptome-Wide Differential Gene Expression.Supplemental_Data_Set_2_Diff_Expression.xlsxSupplemental Data Set 3Splicing Index Analysis.Supplemental_Data_set_3_SI.xlsxSupplemental Data Set 4Analysis of NMD Target Features and Overlap between NMD- and Light-Regulated AS.Supplemental_Data_Set_4_NMD_Features_Overlap_NMD_set.xlsxSupplemental Data Set 5Categorization of Light-Regulated and Reference Gene Sets into Functional Subgroups.Supplemental_Data_Set_5_GO.xlsxSupplemental Data Set 6Expressed Intergenic Regions.Supplemental_Data_Set_6_Intergenic_regions.xlsxSupplemental Data Set 7Computational Analysis of Transcriptome-Wide AS Changes in Response to Red Light Based on the Data from Shikata et al. (2014).Supplemental_Data_set_7_Shikata.xlsx