Role of light modulated RNA-binding proteins in the coordination of organellar genomes to optimize canopy photosynthesis
Lead Research Organisation:
James Hutton Institute
Department Name: Cell & Molecular Sciences
Abstract
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.
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.
Technical Summary
The phytochrome photoreceptors (phys) play a central role in establishing photoautotrophic growth, promoting chloroplast development and photosynthetic homeostasis. While phys orchestrate vast transcriptional cascades from the nucleus to alter photosynthetic gene expression, we are characterizing a different role of these receptors in the regulation of RNA-binding proteins. This post-transcriptional mechanism has high potential to impact the interorganellar communication channels required for the coordinated expression of the chloroplast and the nuclear genome for photosynthesis.
We identified the nuclear encoded, chloroplast acting CPRNP RNA-binding proteins, general modulators of the plastome post-transcriptional control, as novel phy-signaling components, necessary for greening and PSII activity. Plastid gene expression, different from the nucleus, relies more on post-transcriptional RNA-processing, and CPRNPs participate in the stabilization, processing, splicing and editing of multiple chloroplastic RNAs to produce chloroplastic proteins.
Our studies show that CPRNPs respond to R-light in a phy dependent manner and that cprnp mutants show impairment in photosynthetic capacity. CPRNPs are in addition subject to phytochrome dependent Alternative Promoter Use (APU). Via APU phy modulates the production in-planta of CPRNPs' protein isoforms with dual subcellular localization (nuclear and chloroplastic). This correlates with an altered nuclear and plastome photosynthetic gene expression in cprnps. Our data points at a novel mechanism, centred in CPRNPs, with clear potential to coordinate the expression of two organellar genomes to build and acclimate photosynthetic complexes to different light environments, including canopy conditions. This novel inter-organellar communication pathway may be central to the nature of a plant cell and relevant for photosynthetic homeostasis.
We identified the nuclear encoded, chloroplast acting CPRNP RNA-binding proteins, general modulators of the plastome post-transcriptional control, as novel phy-signaling components, necessary for greening and PSII activity. Plastid gene expression, different from the nucleus, relies more on post-transcriptional RNA-processing, and CPRNPs participate in the stabilization, processing, splicing and editing of multiple chloroplastic RNAs to produce chloroplastic proteins.
Our studies show that CPRNPs respond to R-light in a phy dependent manner and that cprnp mutants show impairment in photosynthetic capacity. CPRNPs are in addition subject to phytochrome dependent Alternative Promoter Use (APU). Via APU phy modulates the production in-planta of CPRNPs' protein isoforms with dual subcellular localization (nuclear and chloroplastic). This correlates with an altered nuclear and plastome photosynthetic gene expression in cprnps. Our data points at a novel mechanism, centred in CPRNPs, with clear potential to coordinate the expression of two organellar genomes to build and acclimate photosynthetic complexes to different light environments, including canopy conditions. This novel inter-organellar communication pathway may be central to the nature of a plant cell and relevant for photosynthetic homeostasis.
