Cryptochrome photoreceptors in green algae: Unexpected versatility of mechanisms and functions

Kottke, Tilman; Oldemeyer, Sabine; Wenzel, Sandra; Zou, Yangjun; Mittag, Maria

doi:10.1016/j.jplph.2017.05.021

Cited by 61 publications

(68 citation statements)

References 118 publications

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“…Among the five genes encoding cryptochrome (CRY) photoreceptors (for a recent review on algal CRYs, see Duanmu et al, 2017;Kottke et al, 2017), expression levels for the gene encoding plant CRY (pCRY) are highest, peak in the dark, and are rapidly repressed upon the onset of light. This is similar to diurnal conditions where transcripts of pCRY were found to be highest during the night and rapidly declined during the day (Zones et al, 2015).…”

Section: Hmox1 Is Dispensable For Light-dependent Transcript Accumulamentioning

confidence: 99%

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

et al. 2017

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In land plants, linear tetrapyrrole (bilin)-based phytochrome photosensors optimize photosynthetic light capture by mediating massive reprogramming of gene expression. But, surprisingly, many green algal genomes lack phytochrome genes. Studies of the heme oxygenase mutant (hmox1) of the green alga Chlamydomonas reinhardtii suggest that bilin biosynthesis in plastids is essential for proper regulation of a nuclear gene network implicated in oxygen detoxification during dark-to-light transitions. hmox1 cannot grow photoautotrophically and photoacclimates poorly to increased illumination. We show that these phenotypes are due to reduced accumulation of photosystem I (PSI) reaction centers, the PSI electron acceptors 59-monohydroxyphylloquinone and phylloquinone, and the loss of PSI and photosystem II antennae complexes during photoacclimation. The hmox1 mutant resembles chlorophyll biosynthesis mutants phenotypically, but can be rescued by exogenous biliverdin IXa, the bilin produced by HMOX1. This rescue is independent of photosynthesis and is strongly dependent on blue light. RNA-seq comparisons of hmox1, genetically complemented hmox1, and chemically rescued hmox1 reveal that tetrapyrrole biosynthesis and known photoreceptor and photosynthesis-related genes are not impacted in the hmox1 mutant at the transcript level. We propose that a bilin-based, bluelight-sensing system within plastids evolved together with a bilin-based retrograde signaling pathway to ensure that a robust photosynthetic apparatus is sustained in light-grown Chlamydomonas.

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Section: Hmox1 Is Dispensable For Light-dependent Transcript Accumulamentioning

confidence: 99%

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

et al. 2017

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“…In contrast to other cryptochromes, CraCRY appears to be capable of inducing a genetic response not only to blue, but also to red light. [20][21][22] This feature is probably related to another unique property of CraCRY, the very efficient formation and stabilization of its semireduced (red light-absorbing) flavin cofactor (FADH • ) that can be easily accumulated under blue light illumination and lives for seconds to minutes (depending on pH). 20,23 This process relies on the oxidation of the phenolic moiety of the tyrosine residue Y 373 as its mutation to phenylalanine abolishes this effect.…”

Section: Introductionmentioning

confidence: 99%

Ultrafast Oxidation of a Tyrosine by Proton-Coupled Electron Transfer Promotes Light Activation of an Animal-like Cryptochrome

et al. 2019

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The animal-like cryptochrome of Chlamydomonas reinhardtii (CraCRY) is a recently discovered photoreceptor that controls the transcriptional profile and sexual life cycle of this alga by both blue and red light. CraCRY has the uncommon feature of efficient formation and longevity of the semi-reduced neutral form of its FAD cofactor upon blue light illumination. Tyrosine Y 373 plays hereby a crucial role by elongating as fourth member the electron transfer (ET) chain that comprises the tryptophan triad otherwise found in most other cryptochromes and DNA photolyases. Here, we report the full mechanism of light-induced FADH • formation in CraCRY using transient absorption spectroscopy from hundreds of femtoseconds to seconds. Electron transfer starts from ultrafast reduction of excited FAD to FAD •by the proximal tryptophan (0.4 ps) and is followed by delocalized migration of the produced WH •+ radical along the tryptophan triad (3.7 and 55 ps). Oxidation of Y 373 by coupled ET to WH •+ and deprotonation then proceeds in ~800 ps, without any significant kinetic isotope effect, nor a pH effect between pH 6.5 and 9.0. The FAD •-/Y 373 • pair is formed with high quantum yield (~60%); its intrinsic decay by recombination is slow (~50 ms), favoring reduction of Y 373 • by extrinsic agents and protonation of FAD •to form the long-lived, red-light absorbing FADH • species. Possible mechanisms of tyrosine oxidation by ultrafast proton-coupled ET in CraCRY, a process about 40 times faster than the archetypal tyrosine-Z oxidation in photosystem II, are discussed in detail.

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“…CRYs are furthermore separated into the animal types I and II, plant CRYs and CRY-DASH photoreceptors (DASH: Drosophila, Arabidopsis, Synechocystis, Homo ). During the last decade, several animal-like CRYs (aCRY) have been discovered and characterized outside the animal kingdom, especially in photosynthetic algae (2,3), where they may act not only in signaling, but also as (6-4) photolyases.…”

Section: Introductionmentioning

confidence: 99%

Structure of the bifunctional cryptochrome aCRY from Chlamydomonas reinhardtii

Franz

Ignatz

Wenzel

et al. 2018

Nucleic Acids Research

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102

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Photolyases and cryptochromes form an almost ubiquitous family of blue light photoreceptors involved in the repair and maintenance of DNA integrity or regulatory control. We found that one cryptochrome from the green alga Chlamydomonas reinhardtii (CraCRY) is capable of both, control of transcript levels and the sexual cycle of the alga in a positive (germination) and negative manner (mating ability), as well as catalyzing the repair of UV-DNA lesions. Its 1.6 Å crystal structure shows besides the FAD chromophore an aromatic tetrad that is indispensable in animal-like type I cryptochromes for light-driven change of their signaling-active redox state and formation of a stable radical pair. Given CraCRY’s catalytic activity as (6-4) photolyase in vivo and in vitro, we present the first co-crystal structure of a cryptochrome with duplex DNA comprising a (6-4) pyrimidine–pyrimidone lesion. This 2.9 Å structure reveals a distinct conformation for the catalytic histidine His1, H357, that challenges previous models of a single-photon driven (6-4) photolyase mechanism.

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Cryptochrome photoreceptors in green algae: Unexpected versatility of mechanisms and functions

Cited by 61 publications

References 118 publications

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

Ultrafast Oxidation of a Tyrosine by Proton-Coupled Electron Transfer Promotes Light Activation of an Animal-like Cryptochrome

Structure of the bifunctional cryptochrome aCRY from Chlamydomonas reinhardtii

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