Alternative splicing substantially diversifies the transcriptome during early photomorphogenesis and correlates with the energy availability in Arabidopsis

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.

植物以光作为能量与信息来源，以此感知昼夜节律与季节变化。感知光照条件的动态变化，对于调控植物代谢、启动发育转变至关重要。本研究针对暴露于蓝光、红光或白光后进入光形态建成的黄化幼苗，开展了全转录组水平的基因表达与可变剪接（alternative splicing, AS）差异分析。分析结果显示，全转录组发生大规模重编程：约20%的基因呈现差异表达，数百个可变剪接事件出现变化。在所有受调控的可变剪接事件中，超60%的事件里，光会促进生成疑似编码蛋白质的剪接变体，同时减少携带无义介导的mRNA降解（nonsense-mediated decay, NMD）触发特征的mRNA的产量。据此，此前被鉴定为红光信号转导组分的推定剪接因子CRY1CRY2背景下红光响应减弱1（REDUCED RED-LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1, RRC1）的可变剪接，在光照条件下转向产生功能性剪接变体。对候选可变剪接事件的下游分析表明，光受体信号转导仅在单色光处理中发挥作用，而在白光处理中无此功能。此外，本研究证实，光照处理与外源糖供给均可引发相似的可变剪接变化，且该过程依赖激酶信号转导的关键调控作用。本研究提出，可变剪接是植物中感知并传递能量可用性信息的信号通路的整合节点。