Chlorophyll f synthesis by a super-rogue photosystem II complex

. 2020 Mar ; 6 (3) : 238-244. [epub] 20200309

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32170286

Grantová podpora
BB/P00931X/1 RCUK | Biotechnology and Biological Sciences Research Council (BBSRC) - International

Odkazy

PubMed 32170286
DOI 10.1038/s41477-020-0616-4
PII: 10.1038/s41477-020-0616-4
Knihovny.cz E-zdroje

Certain cyanobacteria synthesize chlorophyll molecules (Chl d and Chl f) that absorb in the far-red region of the solar spectrum, thereby extending the spectral range of photosynthetically active radiation1,2. The synthesis and introduction of these far-red chlorophylls into the photosynthetic apparatus of plants might improve the efficiency of oxygenic photosynthesis, especially in far-red enriched environments, such as in the lower regions of the canopy3. Production of Chl f requires the ChlF subunit, also known as PsbA4 (ref. 4) or super-rogue D1 (ref. 5), a paralogue of the D1 subunit of photosystem II (PSII) which, together with D2, bind cofactors involved in the light-driven oxidation of water. Current ideas suggest that ChlF oxidizes Chl a to Chl f in a homodimeric ChlF reaction centre (RC) complex and represents a missing link in the evolution of the heterodimeric D1/D2 RC of PSII (refs. 4,6). However, unambiguous biochemical support for this proposal is lacking. Here, we show that ChlF can substitute for D1 to form modified PSII complexes capable of producing Chl f. Remarkably, mutation of just two residues in D1 converts oxygen-evolving PSII into a Chl f synthase. Overall, we have identified a new class of PSII complex, which we term 'super-rogue' PSII, with an unexpected role in pigment biosynthesis rather than water oxidation.

Erratum v

PubMed

Zobrazit více v PubMed

Miyashita, H. et al. Chlorophyll d as a major pigment. Nature 383, 402–402 (1996).

Chen, M., Li, Y., Birch, D. & Willows, R. D. A cyanobacterium that contains chlorophyll f —a red-absorbing photopigment. FEBS Lett. 586, 3249–3254 (2012). PubMed

Blankenship, R. E. & Chen, M. Spectral expansion and antenna reduction can enhance photosynthesis for energy production. Curr. Opin. Chem. Biol. 17, 457–461 (2013). PubMed

Ho, M.-Y., Shen, G., Canniffe, D. P., Zhao, C. & Bryant, D. A. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353, aaf9178 (2016). PubMed

Murray, J. W. Sequence variation at the oxygen-evolving centre of photosystem II: a new class of ‘rogue’ cyanobacterial D1 proteins. Photosynth. Res. 110, 177–184 (2012). PubMed

Shen, G. et al. Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002. Photosynth. Res. 140, 77–92 (2019). PubMed

Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011). PubMed PMC

Cardona, T., Shao, S. & Nixon, P. J. Enhancing photosynthesis in plants: the light reactions. Essays Biochem. 62, 85–94 (2018). PubMed PMC

Long, S. P., Marshall-Colon, A. & Zhu, X.-G. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161, 56–66 (2015). PubMed

Nowaczyk, M. M. et al. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of Photosystem II. Plant Cell 18, 3121–3131 (2006). PubMed PMC

Barber, J. Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere. Q. Rev. Biophys. 49, e14 (2016). PubMed

Shen, G., Boussiba, S. & Vermaas, W. F. J. Synechocystis sp. PCC 6803 strains lacking Photosystem I and phycobilisome function. Plant Cell 5, 1853–1863 (2007).

Bečková, M. et al. 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 (2017). PubMed

Komenda, J. et al. 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. 47, 48620–48629 (2004).

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

Garg, H., Loughlin, P. C., Willows, R. D. & Chen, M. The C2 PubMed PMC

Vass, I. Molecular mechanisms of photodamage in the Photosystem II complex. Biochim. Biophys. Acta 1817, 209–217 (2012). PubMed

Masuda, T. et al. Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ. Microbiol. 20, 546–560 (2018). PubMed

Wegener, K. M., Nagarajan, A. & Pakrasi, H. B. An atypical psbA gene encodes a sentinel D1 protein to form a physiologically relevant inactive photosystem II complex in cyanobacteria. J. Biol. Chem. 290, 3764–3774 (2015). PubMed

Gan, F. et al. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312–1317 (2014). PubMed

Nürnberg, D. J. et al. Photochemistry beyond the red-limit in chlorophyll f-containing systems. Science 360, 1210–1213 (2018). PubMed

Tichý, M. et al. Strain of Synechocystis PCC 6803 with aberrant assembly of photosystem II contains tandem duplication of a large chromosomal region. Front. Plant Sci. 7, 648 (2016). PubMed PMC

Forsman, J. A., Winter, R. T. & Eaton-Rye, J. J. An improved system for the targeted mutagenesis of the psbA2 gene in Synechocystis sp. PCC 6803: mutation of D1-Glu244 to His impairs electron transfer between Q

Debus, R. J. et al. Does histidine 332 of the D1 polypeptide ligate the manganese cluster in photosystem II? An electron spin echo envelope modulation study. Biochemistry 40, 3690–3699 (2001). PubMed

Debus, R. J., Barry, B. A., Sithole, I., Babcock, G. T. & Mcintosh, L. Directed mutagenesis indicates that the donor to P680 PubMed

Ried, J. L. & Collmer, A. An nptI-sacB-sacR cartridge for constructing directed, unmarked mutations in Gram-negative bacteria by marker exchange–eviction mutagenesis. Gene 57, 239–246 (1987). PubMed

Williams, J. G. K. Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 167, 766–778 (1988).

Hollingshead, S. et al. 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 (2012). PubMed PMC

Zhu, B., Cai, G., Hall, E. O. & Freeman, G. J. In-Fusion PubMed

Komenda, J. & Barber, J. Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the Q PubMed

Suzuki, H. et al. Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by Fourier transform infrared analysis. Biochemistry 52, 4748–4757 (2013). PubMed

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

Dobáková, M., Sobotka, R., Tichý, M. & Komenda, J. 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 (2009). PubMed PMC

Komenda, J., Tichý, M. & Eichacker, L. A. The PsbH protein is associated with the inner antenna CP47 and facilitates D1 processing and incorporation into PSII in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol. 46, 1477–1483 (2005). PubMed

Rögner, M., Nixon, P. J. & Diner, B. A. Purification and characterization of photosystem I and photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 265, 6189–6196 (1990). PubMed

Komenda, J. et al. 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 (2008). PubMed

Bumba, L., Prasil, O. & Vacha, F. Antenna ring around trimeric Photosystem I in chlorophyll b containing cyanobacterium Prochlorothrix hollandica. Biochim. Biophys. Acta Bioenerg. 1708, 1–5 (2005).

Li, N. et al. PsaD is required for the stable binding of PsaC to the photosystem I core protein of Synechococcus sp. PCC 6301. Biochemistry 30, 7863–7872 (1991). PubMed

Dobáková, M., Tichý, M. & Komenda, J. Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 145, 1681–1691 (2007). PubMed PMC

Yu, J. et al. 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 (2018). PubMed PMC

Komenda, J. et al. The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 158, 476–486 (2012). PubMed

Bučinská, L. et al. The ribosome-bound protein Pam68 promotes insertion of chlorophyll into the CP47 subunit of photosystem II. Plant Physiol. 176, 2931–2942 (2018). PubMed PMC

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

Li, Y., Scales, N., Blankenship, R. E., Willows, R. D. & Chen, M. Extinction coefficient for red-shifted chlorophylls: chlorophyll d and chlorophyll f. Biochim. Biophys. Acta Bioenerg. 1817, 1292–1298 (2012).

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...