Transcriptional regulation of photoprotection in dark-to-light transition—More than just a matter of excess light energy

Abstract

In nature, photosynthetic organisms are exposed to different light spectra and intensities depending on the time of day and atmospheric and environmental conditions. When photosynthetic cells absorb excess light, they induce nonphotochemical quenching to avoid photodamage and trigger expression of “photoprotective” genes. In this work, we used the green alga Chlamydomonas reinhardtii to assess the impact of light intensity, light quality, photosynthetic electron transport, and carbon dioxide on induction of the photoprotective genes ( LHCSR1 , LHCSR3 , and PSBS ) during dark-to-light transitions. Induction (mRNA accumulation) occurred at very low light intensity and was independently modulated by blue and ultraviolet B radiation through specific photoreceptors; only LHCSR3 was strongly controlled by carbon dioxide levels through a putative enhancer function of CIA5, a transcription factor that controls genes of the carbon concentrating mechanism. We propose a model that integrates inputs of independent signaling pathways and how they may help the cells anticipate diel conditions and survive in a dynamic light environment.

Light-independent regulation of algal photoprotection by CO2 availability

“…1) a marked increase (5 to 600-fold) in CCM transcript levels was observed in WT cells (Supplementary Fig. 3), in accordance with recent studies 28,32 ; this increase was strongly suppressed by CO2 and to a lesser extent by acetate, which did not affect CCM gene expression in the icl mutant (Supplementary Fig. 3).…”

“…CO2 and CIA5 appear to be of paramount importance in signal integration and transduction, regulating expression of both photoprotection and CCM genes. For instance, CO2 represses the UV-B elicited, UVR8-mediated expression of LHCSR3, and CIA5 is absolutely required for this expression 28 . Moreover, our results have shown that high CO2 levels or the absence of CIA5 have a severe impact on LHCSR3 gene expression and, although HL can still induce LHCSR3 transcription, no protein is detected (Fig.…”

“…5a), and that was rescued to WT-levels in the cia5-C complemented line. This CIA5-independent regulation of mRNA in the presence of light could account for the contribution of light signaling in LHCSR3 gene expression, possibly via phototropin 10 or via the generation of reactive oxygen species 28 .…”

“…CIA5 has been shown to regulate accumulation of transcripts from both the CCM genes 26,27 and LHCSR3 28 . To obtain a comprehensive view of the photoprotection capacity of the cia5 mutant, air sparged WT and cia5 cells grown in LL were shifted to HL, and the transcript and protein levels from the qE effector genes were monitored.…”

“…Despite the evident connection between light and CO2 levels, the physiological responses to different light and CO2 availabilities have been traditionally studied separately. However, several lines of evidence indicate that both acetate and Ci abundance impact not only qE but also the establishment of the CCM in Chlamydomonas [23][24][25][26] , while LHCSR3 transcripts accumulation have been reported to be CIA5-dependent [26][27][28] . Yet, the mechanism(s) associated with carbon-dependent regulation of qE and CCM induction and the intimate link between the two processes have still not been clearly defined.…”