DASH cryptochrome 1, a UV‐A receptor, balances the photosynthetic machinery of Chlamydomonas reinhardtii

Abstract

 DASH cryptochromes belong to the cryptochrome/photolyase family and can act as DNA repair enzymes. In bacteria and fungi, they can also play regulatory roles, but in plants their biological functions remain elusive. Here, we characterize CRY-DASH1 from the green alga Chlamydomonas reinhardtii. We perform biochemical and in vitro photochemical analysis. For functional characterization, a knock-out mutant of cry-dash1 is used. CRY-DASH1 protein is localized in the chloroplast and accumulates at midday. Albeit the photoautotrophic growth of the mutant is significantly reduced compared to wild type, the mutant has increased levels of photosynthetic pigments and a higher maximum photochemical efficiency of photosystem II. Hyper-stacking of thylakoid membranes occurs in parallel and an increase in proteins of the photosystem II reaction center, D1 and its antenna CP43, but not of their transcripts. CRY-DASH1 binds fully reduced flavin adenine dinucleotide and the antenna 5,10-methenyltetrahydrofolate leading to an absorption peak in the UV-A range.Supplementation of white light with UV-A increases photoautotrophic growth of wild type but not of the cry-dash1 mutant. These results suggest a balancing function of CRY-DASH1 in the photosynthetic machinery and point to its role as a photoreceptor for the UV-A range separated from the absorption of photosynthetic pigments.

The World of Algae Reveals a Broad Variety of Cryptochrome Properties and Functions

“…The third CRY from Cr, Cr CRY-DASH1 reaches its maximal protein abundance at midday and is lowest at the beginning of the night (change in amplitude about 4-fold; Rredhi et al, 2021). Taken together, the acrophases of peak expression vary with all three investigated Cr CRYs, ranging from early day until late night.…”

“…They perceive light via pigments or specialized photoreceptors. Light regulates their photosynthesis and balances their photosynthetic apparatus, controls their behavior (photoorientation), entrains their circadian clocks, and influences their cell and sexual cycles as well as developmental processes (reviewed in Hegemann, 2008;Kianianmomeni and Hallmann, 2014;Kottke et al, 2017;Rredhi et al, 2021). Cyanobacteria, also known as prokaryotic blue-green algae, and eukaryotic algae have an amazing repertoire of different photoreceptors compared to land plants or animals.…”

“…The land plant At CRY3 was found in the chloroplast and in mitochondria ( Kleine et al, 2003 ), while the algal Cr CRY-DASH1 protein was only found in the chloroplast ( Rredhi et al, 2021 ; Figure 2 ). Recently, algal CRY-DASHs were shown to be involved in further biological functions beside DNA repair, supporting their additional or alternative role as photoreceptors ( Yang et al, 2020 ; Rredhi et al, 2021 ). CRY-DASH proteins were found in all selected algal systems ( Figure 3 ), including an Antarctic Chlamydomonas sp.…”

“… Cryptochrome categories in algae ( Juhas et al, 2014 ; Kottke et al, 2017 ; Makita et al, 2021 ; Rredhi et al, 2021 ). A representative member of each of the five known categories is shown, starting with the classical plant cryptochrome of the green flagellate alga Chlamydomonas reinhardtii (Cr pCRY) and its long C-terminal extension.…”

“…ǀ The sexual cycle of Chlamydomonas : vegetative cells turn into pregametes in the dark without a nitrogen source and then become gametes in the light in the absence of a nitrogen source; gametes fuse and a resilient zygote is formed that needs a nitrogen source and light to undergo meiosis. ǀ Light is needed for photosynthesis and influences the chloroplast architecture; thylakoid membranes are shown exemplarily ( Rredhi et al, 2021 ) ǀ Light influences developmental processes in the multicellular algae Saccharina and Volvox ( Kianianmomeni and Hallmann, 2015 ; Yang et al, 2020 ). ǀ The cell cycle is symbolized; algal cells are synchronized by light–dark cycles; M, mitosis; G1, gap1; S, synthesis; G2, gap2 ( Coesel et al, 2009 ; Cross and Umen, 2015 ).…”