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Understanding Non-Photochemical Quenching Regulation in a Dynamic Environment.

Periodic Reporting for period 1 - UNREDE (Understanding Non-Photochemical Quenching Regulation in a Dynamic Environment.)

Reporting period: 2018-01-15 to 2020-01-14

Photosynthesis supports most life on Earth through the conversion of light energy, H2O and CO2 to chemical energy. Photosynthetic organisms have evolved to maximize the capability to capture light energy, allowing organisms to grow even in very low light environments. However, light intensity and quality oscillate throughout the day and the annual seasons and, therefore, photosynthetic organisms may need to acclimate from very low to extremely high light intensities on a time scale that ranges from seconds to months (e.g. cloudy days, winter-summer periods, etc.). During high light conditions or nutrient deprivation, when light absorption exceeds the capacity for carbon dioxide fixation, the excess absorbed energy can elicit the generation of reactive oxygen species that cause severe oxidative damage. Coping with a dynamic environment requires critical adaptations of the photosynthetic apparatus to optimize photosynthetic efficiency while at the same time minimizing phototoxic effects. In this project, we study the mechanism called non-photochemical quenching (NPQ) that alleviate this photo-oxidative stress in the timescale of seconds to minutes. This NPQ is critical to protect the integrity of the photosynthetic apparatus, allowing the organisms to survive in conditions of excess light energy.
The study of NPQ regulation is essential to predict how photosynthetic organisms will behave under changes in light, atmospheric CO2 levels, temperature and nutrient availability, and, therefore, it will also impact strategies for improving photosynthetic efficiency and tolerance to harsh conditions. A better understanding of these processes at the molecular level has already allowed improving crop productivity by 15% in tobacco. In addition, beyond the ecological implications, this project might have a significant impact on the use of photosynthetic organisms for biotechnological purposes. Microalgae, widely used in industry, waste a large part of the absorbed solar radiation as heat (NPQ). The study of NPQ regulation and the capacity to control it can improve both the production of biomass and the synthesis and accumulation of high-value products.
NPQ mechanisms vary between plants and photosynthetic microbes. In plants, the PSBS protein works in collaboration with the light-harvesting complexes (LHCs) to mediate this process in chloroplasts, but in photosynthetic microorganisms, there exist other proteins involved in the fast NPQ (LHCSRs and LHCXs in algae and diatoms respectively, or OCP in cyanobacteria). Chlamydomonas reinhardtii, the model green alga used in this project, is one of the few organisms having genes encoding PSBSs and LHCSRs proteins on its genome. However, we know very little about the regulation and role of these proteins in NPQ. Our goals are to understand the regulation of LHCSRs and PSBS expression in a wide variety of physiological conditions (different light intensity and quality, CO2 concentrations and nutrient deprivation), to characterize their role and to identify molecular signals that control the induction and functionality of NPQ. 
During these two years, we have focused on the role of carbon, nitrogen, and sulfur availability as well as light intensity and quality on the regulation of NPQ. We have measured the expression and protein accumulation of LHCSRs and PSBSs in Chlamydomonas reinhardtii. We also studied how this regulation is affected in mutants lacking blue and UV light photoreceptors. Moreover, we have characterized a mutant affected in LHCSR1 accumulation, we identified new signal molecules involved in NPQ regulation, and we generated a strain, expressing a reporter gene, that can be potentially used to perform mutagenesis and identify and isolate new mutants impaired in the transcriptional regulation of NPQ.
So far, our results have unraveled a fine-tuned and very complex network of regulation that integrates different pathways in order to control a progressive induction of NPQ. This gradual induction allows cells to anticipate excess light and to be ready for photoprotection. We have studied different pathways that can impact the transcriptional regulation of NPQ in an independent or additive way. Moreover, we have improved our knowledge about how cells integrate the information present in sunlight (intensity and quality) in order to acclimate to a dynamic environment.
Our results are changing some of the current assumptions in the field. We already know that the NPQ-related genes can be induced at very low light, and that induction depends on the blue and UV light that impact transcriptional and posttranslational regulation through different pathways. Moreover, results from this project have allowed us to understand that these genes can be induced even in the dark because of their connection with cellular metabolism.
Altogether these data will help us understand NPQ regulation and will provide us with the tools to engineer these pathways involved in NPQ to improve photosynthesis and to obtain higher benefits from photosynthetic organisms in agriculture and the biotechnological industry.