Porphyrin Binding to Gun4 Protein, Facilitated by a Flexible Loop, Controls Metabolite Flow through the Chlorophyll Biosynthetic Pathway

Kopečná, Jana; Adams, Nathan B. P.; Davison, Paul A.; Brindley, Amanda A.; Hunter, C. Neil; Guallar, Vı́ctor; Sobotka, Roman

doi:10.1074/jbc.m115.664987

Cited by 29 publications

(29 citation statements)

References 42 publications

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“…S9, A and B), and apparent dissociation constants (K d ) for Proto and MgP of all GUN4 variants tested were similar to published K d values of cyanobacterial and AtGUN4 homologs (Larkin et al, 2003;Davison et al, 2005;Verdecia et al, 2005;Adhikari et al, 2009). Furthermore, the binding of porphyrins takes place within a core domain, which is common to all GUN4 proteins and structurally independent from the C-terminal extension harboring the phosphorylation site (Verdecia et al, 2005;Chen et al, 2015b;Kope cná et al, 2015). Thus, it is unlikely that the substitution of Ser to Asp interferes with the structural integrity of GUN4 in vivo.…”

Section: Known Properties Of Gun4 Are Not Influenced By Phosphorylationsupporting

confidence: 71%

“…In summary, two of the main properties of GUN4 were not altered by the introduction of a negatively charged aa next to the C terminus: the Proto and MgP binding, which are discussed to have an important role in stimulating MgCh (Verdecia et al, 2005;Kope cná et al, 2015) and the subplastidic distribution of GUN4 in the stroma and at the thylakoid membrane (Adhikari et al, 2009). …”

Section: Known Properties Of Gun4 Are Not Influenced By Phosphorylationmentioning

confidence: 94%

“…It is essential for Chl accumulation during photoperiodic growth, but not for Chl synthesis per se (Larkin et al, 2003;Wilde et al, 2004;Sobotka et al, 2008;Peter and Grimm, 2009;Formighieri et al, 2012;Brzezowski et al, 2014). GUN4 has a stimulatory impact on MgCh via a proposed mechanism, which involves its interaction with CHLH and binding of both the enzyme's substrate Proto and product Mg Proto (MgP; Larkin et al, 2003;Davison et al, 2005;Verdecia et al, 2005;Adhikari et al, 2009Adhikari et al, , 2011Chen et al, 2015b;Kope cná et al, 2015). Low light-grown wildtype plants accumulate less GUN4 than plants under increasing light intensities, indicating that the GUN4 content likely correlates with the need of MgCh activity (Peter and Grimm, 2009).…”

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confidence: 99%

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Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

et al. 2016

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) is a positive regulator of light-dependent chlorophyll biosynthesis. GUN4 activates Mg chelatase (MgCh) that catalyzes the insertion of an Mg 2+ ion into protoporphyrin IX. We show that Arabidopsis (Arabidopsis thaliana) GUN4 is phosphorylated at Ser 264 (S264), the penultimate amino acid residue at the C terminus. While GUN4 is preferentially phosphorylated in darkness, phosphorylation is reduced upon accumulation of Mg porphyrins. Expression of a phosphomimicking GUN4(S264D) results in an incomplete complementation of the white gun4-2 null mutant and a chlorotic phenotype comparable to gun4 knockdown mutants. Phosphorylated GUN4 has a reduced stimulatory effect on MgCh in vitro and in vivo but retains its protein stability and tetrapyrrole binding capacity. Analysis of GUN4 found in oxygenic photosynthetic organisms reveals the evolution of a C-terminal extension, which harbors the phosphorylation site of GUN4 expressed in angiosperms. Homologs of GUN4 from Synechocystis and Chlamydomonas lack the conserved phosphorylation site found in a C-terminal extension of angiosperm GUN4. Biochemical studies proved the importance of the C-terminal extension for MgCh stimulation and inactivation of GUN4 by phosphorylation in angiosperms. An additional mechanism regulating MgCh activity is proposed. In conjunction with the dark repression of 5-aminolevulinic acid synthesis, GUN4 phosphorylation minimizes the flow of intermediates into the Mg branch of the tetrapyrrole metabolic pathway for chlorophyll biosynthesis.

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Section: Known Properties Of Gun4 Are Not Influenced By Phosphorylationsupporting

confidence: 71%

Section: Known Properties Of Gun4 Are Not Influenced By Phosphorylationmentioning

confidence: 94%

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confidence: 99%

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Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

et al. 2016

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“…Plant and cyanobacterial mutants in gun4 display reduced Chl content and impaired growth, and they accumulate the substrate for MgCH, whereas phototrophic bacteria lack orthologs of gun4 (34). Gun4 was found to stimulate cyanobacterial MgCH activity in vitro (35) and to be involved in increasing flux into the Chl biosynthesis pathway in vivo (36). Similarly, it is conceivable that Ycf54 may play a role in substrate channeling; pull-down experiments identified protein-protein interactions between Ycf54 and the cyanobacterial AcsF, CycI (21), and CycI with other Chl biosynthesis enzymes (22).…”

Section: Discussionmentioning

confidence: 99%

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Chen

Canniffe

Hunter

2017

Proc. Natl. Acad. Sci. U.S.A.

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The biosynthesis of (bacterio)chlorophyll pigments is among the most productive biological pathways on Earth. Photosynthesis relies on these modified tetrapyrroles for the capture of solar radiation and its conversion to chemical energy. (Bacterio)chlorophylls have an isocyclic fifth ring, the formation of which has remained enigmatic for more than 60 y. This reaction is catalyzed by two unrelated cyclase enzymes using different chemistries. The majority of anoxygenic phototrophic bacteria use BchE, an O 2 -sensitive [4Fe-4S] cluster protein, whereas plants, cyanobacteria, and some phototrophic bacteria possess an O 2 -dependent enzyme, the major catalytic component of which is a diiron protein, AcsF. Plant and cyanobacterial mutants in ycf54 display impaired function of the O 2 -dependent enzyme, accumulating the reaction substrate. Swapping cyclases between cyanobacteria and purple phototrophic bacteria reveals three classes of the O 2 -dependent enzyme. AcsF from the purple betaproteobacterium Rubrivivax (Rvi.) gelatinosus rescues the loss not only of its cyanobacterial ortholog, cycI, in Synechocystis sp. PCC 6803, but also of ycf54; conversely, coexpression of cyanobacterial cycI and ycf54 is required to complement the loss of acsF in Rvi. gelatinosus. These results indicate that Ycf54 is a cyclase subunit in oxygenic phototrophs, and that different classes of the enzyme exist based on their requirement for an additional subunit. AcsF is the cyclase in Rvi. gelatinosus, whereas alphaproteobacterial cyclases require a newly discovered protein that we term BciE, encoded by a gene conserved in these organisms. These data delineate three classes of O 2 -dependent cyclase in chlorophototrophic organisms from higher plants to bacteria, and their evolution is discussed herein.

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“…This reaction is catalyzed by Mg-chelatase consisting of the three subunits CHLD, CHIH, and CHLI in plants. GUN4, the regulatory protein of Mg-chelatase, assists this step by stabilizing the Mg-chelatase complex in membranes and mediating substrate and/or product channeling (Davison et al, 2005; Adhikari et al, 2011; Kopečná et al, 2015). Then a methyl group is added to Mg-Proto IX from S-adenosyl L -methionine by Mg-Proto IX methyltransferase, to result in Mg-Proto IX monomethyl ester (Mg-Proto ME).…”

Section: Introductionmentioning

confidence: 99%

Transcriptional Regulation of Tetrapyrrole Biosynthesis in Arabidopsis thaliana

Kobayashi

Masuda

2016

Front. Plant Sci.

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Biosynthesis of chlorophyll (Chl) involves many enzymatic reactions that share several first steps for biosynthesis of other tetrapyrroles such as heme, siroheme, and phycobilins. Chl allows photosynthetic organisms to capture light energy for photosynthesis but with simultaneous threat of photooxidative damage to cells. To prevent photodamage by Chl and its highly photoreactive intermediates, photosynthetic organisms have developed multiple levels of regulatory mechanisms to coordinate tetrapyrrole biosynthesis (TPB) with the formation of photosynthetic and photoprotective systems and to fine-tune the metabolic flow with the varying needs of Chl and other tetrapyrroles under various developmental and environmental conditions. Among a wide range of regulatory mechanisms of TPB, this review summarizes transcriptional regulation of TPB genes during plant development, with focusing on several transcription factors characterized in Arabidopsis thaliana. Key TPB genes are tightly coexpressed with other photosynthesis-associated nuclear genes and are induced by light, oscillate in a diurnal and circadian manner, are coordinated with developmental and nutritional status, and are strongly downregulated in response to arrested chloroplast biogenesis. LONG HYPOCOTYL 5 and PHYTOCHROME-INTERACTING FACTORs, which are positive and negative transcription factors with a wide range of light signaling, respectively, target many TPB genes for light and circadian regulation. GOLDEN2-LIKE transcription factors directly regulate key TPB genes to fine-tune the formation of the photosynthetic apparatus with chloroplast functionality. Some transcription factors such as FAR-RED ELONGATED HYPOCOTYL3, REVEILLE1, and scarecrow-like transcription factors may directly regulate some specific TPB genes, whereas other factors such as GATA transcription factors are likely to regulate TPB genes in an indirect manner. Comprehensive transcriptional analyses of TPB genes and detailed characterization of key transcriptional regulators help us obtain a whole picture of transcriptional control of TPB in response to environmental and endogenous cues.

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Porphyrin Binding to Gun4 Protein, Facilitated by a Flexible Loop, Controls Metabolite Flow through the Chlorophyll Biosynthetic Pathway

Cited by 29 publications

References 42 publications

Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Transcriptional Regulation of Tetrapyrrole Biosynthesis in Arabidopsis thaliana

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