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Photosynthesis sustains life on earth, underpinning global agriculture and food security. Photosynthetic energy production is a process heavily environmentally regulated, that needs to adapt to constantly fluctuating conditions. Our rising population, have made strategies to boosting agricultural productivity a top research priority. These include improvements in photosynthesis under conditions that limit photosynthetic capacity, such as dense vegetation environments common in modern intensive agriculture. Among the environmental factors that modulate photosynthesis and tune it with plant growth, light plays an essential role. Light acts not only as energy to drive photosynthesis, but as an important informational cue to ensure proper adaptive responses. The plant photoreceptors in charge of Red (R) and Far-Red (FR) light sensing, called phytochromes, convert the information from external light cues into biological signals for the synchronization of plant development and photosynthesis. In part they do so by transcriptionally modulating gene expression form the nucleus, including multiple nuclear-encoded genes that have a functional role in the chloroplasts and in photosynthesis. Yet, photosynthesis is a tale of two genomes, being built on complexes of mixed genetic origin, encoded in the nuclear genome and in the chloroplastic genome (the plastome). The accurate sensing and interpretation of environmental signals is essential to assemble and adjust the photosynthetic multiprotein complexes to the environment. At present we have limited understanding of how the light signals participate in the cross talk between these two genomes for photosynthesis. What we know is that these two genomes have differential modulatory preferences. The nuclear genome is heavily modulated, including by the phytochromes, at the level of transcription. We recently revealed that these photoreceptors are also essential for the global expression of the plastome, a genome that has a strong regulation at the post-transcriptional level. The post-transcriptional control of the plastome encoded mRNAs, is likely linked to the origin of the organelle and is conducted by nuclear encoded, but chloroplast acting RNA-binding proteins. One of such classes of RNA-binding proteins are the chloroplastic RNA-binding proteins (CPRNPs), that are core components of the chloroplast RNA processing machinery with fundamental roles in multiple RNA-processing steps (stabilization, processing, editing, splicing). We have established that CPRNPs are phytochrome signaling components, essential for greening and important for the proper gene expression and of plastid genes including those involved in PSII activity. In addition, we discovered that CPRNPs are target of a novel mechanism of phytochrome-action, the light-selection of alternative promoter use (APU). This mechanism generates "CPRNPs isoforms" with dual, nuclear and chloroplastic localization. These results integrate with our gene expression studies that show that defects in CPRNPs, impact the plastid and the nuclear gene expression. Our current data suggest a novel and potentially central post transcriptional signalling pathway capable of coordinating environmental adjustments for the expression of genes necessary for photosynthesis and encoded in two different organelles. The characterization of this novel pathway in canopy environments may have significant implications in advancing our understanding of how plant cells achieve photosynthetic homeostasis. We envision impact of the research beyond plants, in particular in the areas of inter-organellar communication and coordinated reprogramming of organellar gene expression, with the opening of new research avenues in environmental sensing, genome coordination and the homeostasis of cellular energy production.
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