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Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II

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Abstract

The cyanobacterial small CAB-like proteins (SCPs) are one-helix proteins with compelling similarity to the first and third transmembrane helix of proteins belonging to the CAB family of light-harvesting complex proteins in plants. The SCP proteins are transiently expressed at high light intensity and other stress conditions but their exact function remains largely unknown. Recently we showed association of ScpD with light-stressed, monomeric Photosystem II in Synechocystis sp. PCC 6803 (Yao et al. J Biol Chem 282:267–276, 2007). Here we show that ScpB associates with Photosystem II at normal growth conditions. Moreover, upon introduction of a construct into Synechocystis so that ScpB is expressed continuously under normal growth conditions, ScpE was detected under non-stressed conditions as well, and was copurified with tagged ScpB and Photosystem II. We also report on a one-helix protein, Slr1544, that is somewhat similar to the SCPs and whose gene is cotranscribed with that of ScpD; Slr1544 is another member of the extended light-harvesting-like (Lil) protein family, and we propose to name it LilA.

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Abbreviations

CAB:

Chlorophyll a/b binding

ELIP:

Early-light induced protein

HLIP:

High-light induced protein

LHC:

Light-harvesting complex

Lil:

Light-harvesting like

PAGE:

Polyacrylamide gel electrophoresis

PS:

Photosystem

SCP:

Small CAB-like protein

LC-MS/MS:

Liquid chromatography combined with tandem mass spectrometry

β-dM:

β-d-maltoside

References

  • Adamska I (1997) ELIPs: light induced stress proteins. Physiol Plant 100:798–805

    Article  Google Scholar 

  • Adamska I (2001) The Elip family of stress proteins in the thylakoid membrane of pro- and eukaryota. In: Aro E-M, Andersson B (eds) Advances in photosynthesis and respiration: regulation of photosynthesis, vol 11. Kluwer Academic Publishers, Dordrecht, pp 487–505

    Google Scholar 

  • Anderson JM, Waldron JC, Thorne SW (1978) Chlorophyll-protein complexes of spinach and barley thylakoids: spectral characterization of six complexes resolved by an improved electrophoretic procedure. FEBS Lett 92:227–233

    Article  CAS  Google Scholar 

  • Bhaya D, Dufresne A, Vaulot D, Grossman A (2002) Analysis of the hli gene family in marine and freshwater cyanobacteria. FEMS Microbiol Lett 215:209–219

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E, Green BR (1999) A phylogenetic assessment of the eurkaryotic light-harvesting antenna proteins with implications for plastid evolution. J Mol Evol 48:59–68

    Article  PubMed  CAS  Google Scholar 

  • Eaton-Rye JJ, Vermaas WFJ (1991) Oligonucleotide-directed mutagenesis of psbB, the gene encoding CP47, employing a deletion mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 17:1165–1177

    Article  PubMed  CAS  Google Scholar 

  • Funk C (2000) Functional analysis of the PsbX protein by deletion of the corresponding gene in Synechocystis sp. PCC 6803. Plant Mol Biol 44:815–827

    Article  PubMed  CAS  Google Scholar 

  • Funk C (2001) The PsbS protein: a Cab-protein with a function of its own. In: Aro E-M, Andersson B (eds) Advances in photosynthesis and respiration: regulation of photosynthesis, vol 11. Kluwer Academic Publishers, Dordrecht, pp 453–467

    Google Scholar 

  • Funk C, Vermaas W (1999) A cyanobacterial gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants. Biochemistry 38:9397–9404

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Guedeney G, He Q, Grossman AR (2003) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim Biophys Acta 1557:21–33

    Article  PubMed  CAS  Google Scholar 

  • He Q, Schlich T, Paulsen H, Vermaas W (1999) Expression of a higher plant light-harvesting chlorophyll a/b-binding protein in Synechocystis sp. PCC 6803. Eur J Biochem 263:561–570

    Article  PubMed  CAS  Google Scholar 

  • He Q, Dolganov N, Bjorkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314

    Article  PubMed  CAS  Google Scholar 

  • Heddad M, Adamska I (2000) Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. Proc Natl Acad Sci USA 97:3741–3746

    Article  PubMed  CAS  Google Scholar 

  • Heddad M, Adamska I (2002) The evolution of light stress proteins in photosynthetic organisms. Comp Funct Genom 3:504–510

    Article  CAS  Google Scholar 

  • Hihara Y, Sonoike K, Kanehisa M, Ikeuchi M (2003) DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:1719–1725

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Krol M, Sveshnikov D, Selstam E, Sandstrom S, Koochek M, Park YI, Vasil’ev S, Bruce D, Oquist G, Huner NP (2006) Iron deficiency in cyanobacteria causes monomerization of photosystem I trimers and reduces the capacity for state transitions and the effective absorption cross section of photosystem I in vivo. Plant Physiol 141:1436–1445

    Article  PubMed  CAS  Google Scholar 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240

    Article  PubMed  Google Scholar 

  • Jansson S (2005) A protein family saga: from photoprotection to light-harvesting (and back?) In: Demming-Adams B (ed) Photoprotection, photoinhibition, gene regulation and environment. Springer, The Netherlands, pp 145–153

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Joset F (1988) Transformation in Synechocystis PCC 6714 and PCC 6803:preparation of chromosomal DNA. Methods Enzymol 167:712–714

    Article  PubMed  CAS  Google Scholar 

  • Klimmek F, Sjödin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140:793–804

    Article  PubMed  CAS  Google Scholar 

  • Kufryk G (1997) Changes in pigment-protein composition of maize subchloroplast fragments under phosphorylation. Ukr Biochem J 69:66–71

    Google Scholar 

  • Kuhlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367:614–621

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428:287–292

    Article  PubMed  CAS  Google Scholar 

  • Maniatis T, Frisch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C (2000) Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 479:72–77

    Article  PubMed  CAS  Google Scholar 

  • Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100:9061–9066

    Article  PubMed  CAS  Google Scholar 

  • Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Microbiol 46:905–915

    Article  PubMed  CAS  Google Scholar 

  • Mohamed A, Eriksson J, Osiewacz HD, Jansson C (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238:161–168

    PubMed  CAS  Google Scholar 

  • Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363

    Article  PubMed  CAS  Google Scholar 

  • Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77

    Article  PubMed  CAS  Google Scholar 

  • Pandey A, Andersen JS, Mann M (2000) Use of mass spectrometry to study signaling pathways. Sci STKE 2000(37):pl1

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:385–394

    Google Scholar 

  • Promnares K, Komenda J, Bumba L, Nebesarova J, Vacha F, Tichy M (2006) Cyanobacterial small chlorophyll binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits. J Biol Chem 281:32705–32713

    Article  PubMed  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RT (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Rögner M, Nixon PJ, Diner BA (1990) 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

    PubMed  Google Scholar 

  • Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379

    Article  PubMed  CAS  Google Scholar 

  • Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68:850–858

    Article  PubMed  CAS  Google Scholar 

  • Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24:919–928

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244

    Article  PubMed  CAS  Google Scholar 

  • Teramoto H, Itoh T, Ono TA (2004) High-intensity-light-dependent and transient expression of new genes encoding distant relatives of light-harvesting chlorophyll a/b proteins in Chlamydomonas reinhardtii. Plant Cell Physiol 45:1221–1232

    Article  PubMed  CAS  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Article  PubMed  CAS  Google Scholar 

  • Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall’Osto L, Carriere F, Bassi R, Grimm B, Nussaume L, Havaux M (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50:795–809

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Vavilin D, Funk C, Vermaas W (2002) Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 49:149–160

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Vavilin D, Funk C, Vermaas W (2004) Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803:consequences for pigment biosynthesis and accumulation. J Biol Chem 279:27971–27979

    Article  PubMed  CAS  Google Scholar 

  • Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MA, Tichy M, Vermaas W, Funk C (2007) Localization of the small CAB-like proteins in photosystem II. J Biol Chem 282:267–276

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank the Swedish Foundation for International Cooperation in Research and Higher Education (STINT) for supporting the collaboration between the two research groups. C.F. is very grateful to the Royal Swedish Academy of Sciences (KVA) for granting her research position and to the Swedish Research Council (VR) for financial support. W.V. acknowledges research grant support from the US Department of Energy (DE-FG02-04ER15543).

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Correspondence to Christiane Funk.

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Galyna Kufryk and Miguel Hernandez-Prieto have contributed equally to this work.

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Kufryk, G., Hernandez-Prieto, M.A., Kieselbach, T. et al. Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II. Photosynth Res 95, 135–145 (2008). https://doi.org/10.1007/s11120-007-9244-3

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