A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

. 2019 Sep ; 31 (9) : 2241-2258. [epub] 20190718

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31320483

Grantová podpora
BB/L003260/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/P00931X/1 Biotechnology and Biological Sciences Research Council - United Kingdom

Oxygenic photosynthesis relies on accessory factors to promote the assembly and maintenance of the photosynthetic apparatus in the thylakoid membranes. The highly conserved membrane-bound rubredoxin-like protein RubA has previously been implicated in the accumulation of both PSI and PSII, but its mode of action remains unclear. Here, we show that RubA in the cyanobacterium Synechocystis sp PCC 6803 is required for photoautotrophic growth in fluctuating light and acts early in PSII biogenesis by promoting the formation of the heterodimeric D1/D2 reaction center complex, the site of primary photochemistry. We find that RubA, like the accessory factor Ycf48, is a component of the initial D1 assembly module as well as larger PSII assembly intermediates and that the redox-responsive rubredoxin-like domain is located on the cytoplasmic surface of PSII complexes. Fusion of RubA to Ycf48 still permits normal PSII assembly, suggesting a spatiotemporal proximity of both proteins during their action. RubA is also important for the accumulation of PSI, but this is an indirect effect stemming from the downregulation of light-dependent chlorophyll biosynthesis induced by PSII deficiency. Overall, our data support the involvement of RubA in the redox control of PSII biogenesis.

Zobrazit více v PubMed

Adams N.B.P., Brindley A.A., Hunter C.N., Reid J.D. (2016). The catalytic power of magnesium chelatase: A benchmark for the AAA(+) ATPases. FEBS Lett. 590: 1687–1693. PubMed PMC

Anderson S.L., McIntosh L. (1991). Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. strain PCC 6803: A blue-light-requiring process. J. Bacteriol. 173: 2761–2767. PubMed PMC

Bečková M., Gardian Z., Yu J., Koník P., Nixon P.J., Komenda J. (2017). Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light. Mol. Plant 10: 62–72. PubMed

Boehm M., Romero E., Reisinger V., Yu J., Komenda J., Eichacker L.A., Dekker J.P., Nixon P.J. (2011). Investigating the early stages of photosystem II assembly in Synechocystis sp. PCC 6803: Isolation of CP47 and CP43 complexes. J. Biol. Chem. 286: 14812–14819. PubMed PMC

Boehm M., Yu J., Reisinger V., Bečkova M., Eichacker L.A., Schlodder E., Komenda J., Nixon P.J. (2012). Subunit composition of CP43-less photosystem II complexes of Synechocystis sp. PCC 6803: Implications for the assembly and repair of photosystem II. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367: 3444–3454. PubMed PMC

Bučinská L., Kiss É., Koník P., Knoppová J., Komenda J., Sobotka R. (2018). The ribosome-bound protein Pam68 promotes insertion of chlorophyll into the CP47 subunit of photosystem II. Plant Physiol. 176: 2931–2942. PubMed PMC

Calderon R.H., García-Cerdán J.G., Malnoë A., Cook R., Russell J.J., Gaw C., Dent R.M., de Vitry C., Niyogi K.K. (2013). A conserved rubredoxin is necessary for photosystem II accumulation in diverse oxygenic photoautotrophs. J. Biol. Chem. 288: 26688–26696. PubMed PMC

Chapman D.J., De Felice J., Davis K., Barber J. (1989). Effect of alkaline pH on photosynthetic water oxidation and the association of extrinsic proteins with Photosystem Two. Biochem. J. 258: 357–362. PubMed PMC

Czarnecki O., Grimm B. (2012). Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J. Exp. Bot. 63: 1675–1687. PubMed

Deák Z., Sass L., Kiss E., Vass I. (2014). Characterization of wave phenomena in the relaxation of flash-induced chlorophyll fluorescence yield in cyanobacteria. Biochim. Biophys. Acta 1837: 1522–1532. PubMed

Diner B.A., Rappaport F. (2002). Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant Biol. 53: 551–580. PubMed

Dobáková M., Sobotka R., Tichý M., Komenda J. (2009). Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 149: 1076–1086. PubMed PMC

Fang L., Ge H., Huang X., Liu Y., Lu M., Wang J., Chen W., Xu W., Wang Y. (2017). Trophic mode-dependent proteomic analysis reveals functional significance of light-independent chlorophyll synthesis in Synechocystis sp. PCC 6803. Mol. Plant 10: 73–85. PubMed

Flügge U.-I., Westhoff P., Leister D. (2016). Recent advances in understanding photosynthesis. F1000 Res. 5: 2890. PubMed PMC

Friso G., Giacomelli L., Ytterberg A.J., Peltier J.B., Rudella A., Sun Q., Wijk K.J. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: New proteins, new functions, and a plastid proteome database. Plant Cell 16: 478–499. PubMed PMC

Golbeck J.H., Shen G. (2006). Photosystem I: The light-driven plastocyanin:ferredoxin oxidoreductase. Adv. Photosynth. Respir. 24: 529–547.

Gomes C.M., Giuffrè A., Forte E., Vicente J.B., Saraiva L.M., Brunori M., Teixeira M. (2002). A novel type of nitric-oxide reductase: Escherichia coli flavorubredoxin. J. Biol. Chem. 277: 25273–25276. PubMed

Goto T., Aoki R., Minamizaki K., Fujita Y. (2010). Functional differentiation of two analogous coproporphyrinogen III oxidases for heme and chlorophyll biosynthesis pathways in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 51: 650–663. PubMed

Guo J., Nguyen A.Y., Dai Z., Su D., Gaffrey M.J., Moore R.J., Jacobs J.M., Monroe M.E., Smith R.D., Koppenaal D.W., Pakrasi H.B., Qian W.J. (2014). Proteome-wide light/dark modulation of thiol oxidation in cyanobacteria revealed by quantitative site-specific redox proteomics. Mol. Cell. Proteomics 13: 3270–3285. PubMed PMC

Hasunuma T., Matsuda M., Kato Y., Vavricka C.J., Kondo A. (2018). Temperature enhanced succinate production concurrent with increased central metabolism turnover in the cyanobacterium Synechocystis sp. PCC 6803. Metab. Eng. 48: 109–120. PubMed

Hedtke B., Alawady A., Chen S., Börnke F., Grimm B. (2007). HEMA RNAi silencing reveals a control mechanism of ALA biosynthesis on Mg chelatase and Fe chelatase. Plant Mol. Biol. 64: 733–742. PubMed

Hollingshead S., Kopecná J., Jackson P.J., Canniffe D.P., Davison P.A., Dickman M.J., Sobotka R., Hunter C.N. (2012). Conserved chloroplast open-reading frame ycf54 is required for activity of the magnesium protoporphyrin monomethylester oxidative cyclase in Synechocystis PCC 6803. J. Biol. Chem. 287: 27823–27833. PubMed PMC

Horáková E., Changmai P., Vancová M., Sobotka R., Van Den Abbeele J., Vanhollebeke B., Lukeš J. (2017). The Trypanosoma brucei TbHrg protein is a heme transporter involved in the regulation of stage-specific morphological transitions. J. Biol. Chem. 292: 6998–7010. PubMed PMC

Ishihara S., Takabayashi A., Ido K., Endo T., Ifuku K., Sato F. (2007). Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol. 145: 668–679. PubMed PMC

Iyer R.B., Silaghi-Dumitrescu R., Kurtz D.M. Jr., Lanzilotta W.N. (2005). High-resolution crystal structures of Desulfovibrio vulgaris (Hildenborough) nigerythrin: Facile, redox-dependent iron movement, domain interface variability, and peroxidase activity in the rubrerythrins. J. Biol. Inorg. Chem. 10: 407–416. PubMed

Jansson S., Andersson J., Kim S.J., Jackowski G. (2000). An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Mol. Biol. 42: 345–351. PubMed

Ke S.H., Madison E.L. (1997). Rapid and efficient site-directed mutagenesis by single-tube ‘megaprimer’ PCR method. Nucleic Acids Res. 25: 3371–3372. PubMed PMC

Klughammer C. (2008). Saturation pulse method for assessment of energy conversion in PS I. PAM Appl. Notes 1: 11–14.

Knoppová J., Sobotka R., Tichý M., Yu J., Koník P., Halada P., Nixon P.J., Komenda J. (2014). Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant Cell 26: 1200–1212. PubMed PMC

Knoppová J., Yu J., Koník P., Nixon P.J., Komenda J. (2016). CyanoP is involved in the early steps of photosystem II assembly in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 57: 1921–1931. PubMed

Komenda J. (2000). Role of two forms of the D1 protein in the recovery from photoinhibition of photosystem II in the cyanobacterium Synechococcus PCC 7942. Biochim. Biophys. Acta 1457: 243–252. PubMed

Komenda J. (2005). Autotrophic cells of the Synechocystis psbH deletion mutant are deficient in synthesis of CP47 and accumulate inactive PS II core complexes. Photosynth. Res. 85: 161–167. PubMed

Komenda J., Barber J. (1995). Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis. Biochemistry 34: 9625–9631. PubMed

Komenda J., Reisinger V., Müller B.C., Dobáková M., Granvogl B., Eichacker L.A. (2004). Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J. Biol. Chem. 279: 48620–48629. PubMed

Komenda J., Barker M., Kuviková S., de Vries R., Mullineaux C.W., Tichý M., Nixon P.J. (2006). The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp. PCC 6803. J. Biol. Chem. 281: 1145–1151. PubMed

Komenda J., Nickelsen J., Tichý M., Prásil O., Eichacker L.A., Nixon P.J. (2008). The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803. J. Biol. Chem. 283: 22390–22399. PubMed

Komenda J., Knoppová J., Krynická V., Nixon P.J., Tichý M. (2010). Role of FtsH2 in the repair of photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster. Biochim. Biophys. Acta 1797: 566–575. PubMed

Komenda J., Knoppová J., Kopečná J., Sobotka R., Halada P., Yu J., Nickelsen J., Boehm M., Nixon P.J. (2012a). The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 158: 476–486. PubMed PMC

Komenda J., Sobotka R., Nixon P.J. (2012b). Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr. Opin. Plant Biol. 15: 245–251. PubMed

Kopečná J., Komenda J., Bucinská L., Sobotka R. (2012). Long-term acclimation of the cyanobacterium Synechocystis sp. PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric photosystem I. Plant Physiol. 160: 2239–2250. PubMed PMC

Kopečná J., Sobotka R., Komenda J. (2013). Inhibition of chlorophyll biosynthesis at the protochlorophyllide reduction step results in the parallel depletion of photosystem I and photosystem II in the cyanobacterium Synechocystis PCC 6803. Planta 237: 497–508. PubMed

Kopečná J., Cabeza de Vaca I., Adams N.B., Davison P.A., Brindley A.A., Hunter C.N., Guallar V., Sobotka R. (2015a). Porphyrin binding to Gun4 protein, facilitated by a flexible loop, controls metabolite flow through the chlorophyll biosynthetic pathway. J. Biol. Chem. 290: 28477–28488. PubMed PMC

Kopečná J., Pilný J., Krynická V., Tomčala A., Kis M., Gombos Z., Komenda J., Sobotka R. (2015b). Lack of phosphatidylglycerol inhibits chlorophyll biosynthesis at multiple sites and limits chlorophyllide reutilization in Synechocystis sp. strain PCC 6803. Plant Physiol. 169: 1307–1317. PubMed PMC

Kopf M., Klähn S., Scholz I., Matthiessen J.K., Hess W.R., Voß B. (2014). Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Res. 21: 527–539. PubMed PMC

Li N., Zhao J.D., Warren P.V., Warden J.T., Bryant D.A., Golbeck J.H. (1991). PsaD is required for the stable binding of PsaC to the photosystem I core protein of Synechococcus sp. PCC 6301. Biochemistry 30: 7863–7872. PubMed

Li Y., Liu B., Zhang J., Kong F., Zhang L., Meng H., Li W., Rochaix J.-D., Li D., Peng L. (2019). OHP1, OHP2, and HCF244 form a transient functional complex with the photosystem II reaction center. Plant Physiol. 179: 195–208. PubMed PMC

Metz J.G., Pakrasi H.B., Seibert M., Arntzen C.J. (1986). Evidence for a dual function of the herbicide-binding D1 protein in photosystem II. FEBS Lett. 205: 269–274.

Meurer J., Plücken H., Kowallik K.V., Westhoff P. (1998). A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J. 17: 5286–5297. PubMed PMC

Pilný J., Kopečná J., Noda J., Sobotka R. (2015). Detection and quantification of heme and chlorophyll precursors using a high performance liquid chromatography (HPLC) system equipped with two fluorescence detectors. Bio Protoc. 5: e1390.

Prakash D., Walters K.A., Martinie R.J., McCarver A.C., Kumar A.K., Lessner D.J., Krebs C., Golbeck J.H., Ferry J.G. (2018). Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria. J. Biol. Chem. 293: 9198–9209. PubMed PMC

Prince C., Jia Z. (2015). An unexpected duo: Rubredoxin binds nine TPR motifs to form LapB, an essential regulator of lipopolysaccharide synthesis. Structure 23: 1500–1506. PubMed

Ritchie R.J. (2006). Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89: 27–41. PubMed

Rühle T., Leister D. (2016). Photosystem II assembly from scratch. Front. Plant Sci. 6: 1234. PubMed PMC

Sakuragi Y., Zybailov B., Shen G., Bryant D.A., Golbeck J.H., Diner B.A., Karygina I., Pushkar Y., Stehlik D. (2005). Recruitment of a foreign quinone into the A1 site of photosystem I: Characterization of a menB rubA double deletion mutant in Synechococcus sp. PCC 7002 devoid of FX, FA, and FB and containing plastoquinone or exchanged 9,10-anthraquinone. J. Biol. Chem. 280: 12371–12381. PubMed

Schägger H., von Jagow G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199: 223–231. PubMed

Scharfenberg M., Mittermayr L., von Roepenack-Lahaye E., Schlicke H., Grimm B., Leister D., Kleine T. (2015). Functional characterization of the two ferrochelatases in Arabidopsis thaliana. Plant Cell Environ. 38: 280–298. PubMed

Shen G., Vermaas W.F.J. (1994). Chlorophyll in a Synechocystis sp. PCC 6803 mutant without photosystem I and photosystem II core complexes: Evidence for peripheral antenna chlorophylls in cyanobacteria. J. Biol. Chem. 269: 13904–13910. PubMed

Shen G., Antonkine M.L., van der Est A., Vassiliev I.R., Brettel K., Bittl R., Zech S.G., Zhao J., Stehlik D., Bryant D.A., Golbeck J.H. (2002a). Assembly of photosystem I. II. Rubredoxin is required for the in vivo assembly of FX in Synechococcus sp. PCC 7002 as shown by optical and EPR spectroscopy. J. Biol. Chem. 277: 20355–20366. PubMed

Shen G., Zhao J., Reimer S.K., Antonkine M.L., Cai Q., Weiland S.M., Golbeck J.H., Bryant D.A. (2002b). Assembly of photosystem I. I. Inactivation of the rubA gene encoding a membrane-associated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of photosystem I activity. J. Biol. Chem. 277: 20343–20354. PubMed

Shinopoulos K.E., Yu J., Nixon P.J., Brudvig G.W. (2014). Using site-directed mutagenesis to probe the role of the D2 carotenoid in the secondary electron-transfer pathway of photosystem II. Photosynth. Res. 120: 141–152. PubMed PMC

Sieker L.C., Stenkamp R.E., LeGall J. (1994). Inorganic microbial sulfur metabolism. Methods Enzymol. 243: 203–216. PubMed

Sobotka R., Komenda J., Bumba L., Tichý M. (2005). Photosystem II assembly in CP47 mutant of Synechocystis sp. PCC 6803 is dependent on the level of chlorophyll precursors regulated by ferrochelatase. J. Biol. Chem. 280: 31595–31602. PubMed

Sobotka R., McLean S., Žuberová M., Hunter C.N., Tichý M. (2008). The C-terminal extension of ferrochelatase is critical for enzyme activity and for functioning of the tetrapyrrole pathway in Synechocystis strain PCC 6803. J. Bacteriol. 190: 2086–2095. PubMed PMC

Staleva H., Komenda J., Shukla M.K., Šlouf V., Kaňa R., Polívka T., Sobotka R. (2015). Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat. Chem. Biol. 11: 287–291. PubMed

Steccanella V., Hansson M., Jensen P.E. (2015). Linking chlorophyll biosynthesis to a dynamic plastoquinone pool. Plant Physiol. Biochem. 97: 207–216. PubMed

Strašková A., Knoppová J., Komenda J. (2018). Isolation of the cyanobacterial YFP-tagged photosystem I using GFP-Trap®. Photosynthetica 56: 300–305.

Tichý M., Bečková M., Kopečná J., Noda J., Sobotka R., Komenda J. (2016). Strain of Synechocystis PCC 6803 with aberrant assembly of photosystem II contains tandem duplication of a large chromosomal region. Front. Plant Sci. 7: 648. PubMed PMC

Umena Y., Kawakami K., Shen J.R., Kamiya N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473: 55–60. PubMed

Vass I., Kirilovsky D., Etienne A.-L. (1999). UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 38: 12786–12794. PubMed

Wastl J., Duin E.C., Iuzzolino L., Dörner W., Link T., Hoffmann S., Sticht H., Dau H., Lingelbach K., Maier U.G. (2000). Eukaryotically encoded and chloroplast-located rubredoxin is associated with photosystem II. J. Biol. Chem. 275: 30058–30063. PubMed

Willows R.D. (2006). Chlorophyll synthesis. In The Structure and Function of Plastids, Wise R.R. and Hoober J.K., eds (Amsterodam, The Netherlands: Springer; ), pp. 295–313.

Wittig I., Karas M., Schägger H. (2007). High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell. Proteomics 6: 1215–1225. PubMed

Wittwer M., Luo Q., Kaila V.R., Dames S.A. (2016). Oxidative unfolding of the rubredoxin domain and the natively disordered N-terminal region regulate the catalytic activity of Mycobacterium tuberculosis protein kinase G. J. Biol. Chem. 291: 27062–27072. PubMed PMC

Woodson J.D., Perez-Ruiz J.M., Chory J. (2011). Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr. Biol. 21: 897–903. PubMed PMC

Yamazaki S., Nomata J., Fujita Y. (2006). Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. Plant Physiol. 142: 911–922. PubMed PMC

Yu J., Knoppová J., Michoux F., Bialek W., Cota E., Shukla M.K., Strašková A., Pascual G.A., Sobotka R., Komenda J., Murray J.W., Nixon P.J. (2018). Ycf48 involved in the biogenesis of the oxygen-evolving photosystem II complex is a seven-bladed beta-propeller protein. Proc. Natl. Acad. Sci. USA 115: E7824–E7833. PubMed PMC

Zhao W., Ye Z., Zhao J. (2007). RbrA, a cyanobacterial rubrerythrin, functions as a FNR-dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC 7120. Mol. Microbiol. 66: 1219–1230. PubMed

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

The biogenesis and maintenance of PSII: Recent advances and current challenges

. 2024 Oct 03 ; 36 (10) : 3997-4013.

Chlorophyll biosynthesis under the control of arginine metabolism

. 2023 Nov 28 ; 42 (11) : 113265. [epub] 20231020

The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis

. 2023 Aug 04 ; 14 (1) : 4681. [epub] 20230804

Assembly of D1/D2 complexes of photosystem II: Binding of pigments and a network of auxiliary proteins

. 2022 Jun 01 ; 189 (2) : 790-804.

Psb34 protein modulates binding of high-light-inducible proteins to CP47-containing photosystem II assembly intermediates in the cyanobacterium Synechocystis sp. PCC 6803

. 2022 Jun ; 152 (3) : 333-346. [epub] 20220313

Photosystem II antenna modules CP43 and CP47 do not form a stable 'no reaction centre complex' in the cyanobacterium Synechocystis sp. PCC 6803

. 2022 Jun ; 152 (3) : 363-371. [epub] 20220111

Tandem gene amplification restores photosystem II accumulation in cytochrome b559 mutants of cyanobacteria

. 2022 Jan ; 233 (2) : 766-780. [epub] 20211030

The Photosystem II Assembly Factor Ycf48 from the Cyanobacterium Synechocystis sp. PCC 6803 Is Lipidated Using an Atypical Lipobox Sequence

. 2021 Apr 02 ; 22 (7) : . [epub] 20210402

Purification of Protein-complexes from the Cyanobacterium Synechocystis sp. PCC 6803 Using FLAG-affinity Chromatography

. 2020 May 20 ; 10 (10) : e3616. [epub] 20200520

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...