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High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana

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Abstract

The chloroplast Deg1 protein performs proteolytic cleavage of the photodamaged D1 protein of the photosystem II (PSII) reaction center, PSII extrinsic subunit PsbO and the soluble electron carrier plastocyanin. Using biochemical, immunological and mass spectrometry approaches we showed that the heterogeneously expressed Deg1 protease from Arabidopsis thaliana can be responsible for the degradation of the monomeric light-harvesting complex antenna subunits of PSII (LHCII), CP26 and CP29, as well as PSII-associated PsbS (CP22/NPQ4) protein. The results may indicate that cytochrome b 6 protein and two previously unknown thylakoid proteins, Ptac16 and an 18.3-kDa protein, may be the substrates for Deg1. The interaction of Deg1 with the PsbS protein and the minor LHCII subunits implies its involvement in the regulation of both excess energy dissipation and state transition adaptation processes.

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Abbreviations

BSA:

Bovine serum albumin

Chl:

Chlorophyll

EDTA:

Ethylene-diamine-tetraacetic acid

Fv/Fm:

Ratio of variable to maximum chlorophyll fluorescence

IPTG:

Isopropylthio-b-d-galactoside

LHCII:

Light harvesting complex II

OG:

n-Octyl-β-d-glucoside

PMSF:

Phenylmethylsulfonylfluoride

Pn:

Net photosynthesis rate

PPFD:

Photosynthetic photon flux density

PSII:

Photosystem II

References

  • Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76:343–370

    Article  PubMed  CAS  Google Scholar 

  • Ahn TK, Avenson JT, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

    Article  PubMed  CAS  Google Scholar 

  • Anastassiou R, Argyroudi-Akoyunoglou JH (1995) Thylakoid-bound proteolytic activity against LHC II apoprotein in bean. Photosynth Res 43:241–250

    Article  CAS  Google Scholar 

  • Andreasson E, Svensson P, Weibull C, Albertsson PA (1988) Separation and characterization of stroma and grana membranes—evidence for heterogeneity in antenna size of both photosystem I and photosystem II. BBA 936:339–350

    Article  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283:3550–3558

    Article  PubMed  CAS  Google Scholar 

  • Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283:8434–8445

    Article  PubMed  CAS  Google Scholar 

  • Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476

    Article  PubMed  CAS  Google Scholar 

  • Chassin Y, Kapri-Pardes E, Sinvany G, Arad T, Adam Z (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol 130:857–864

    Article  PubMed  CAS  Google Scholar 

  • Chen YE, Yuan S, Du JB, Xu MY, Zhang ZW, Lin HH (2009) Phosphorylation of photosynthetic antenna protein CP29 and photosystem II structure changes in monocotyledonous plants under environmental stresses. Biochemistry 48:9757–9763

    Article  PubMed  CAS  Google Scholar 

  • De Bianchi S, Dall’Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20:1012–1028

    Article  PubMed  Google Scholar 

  • Georgakopoulos JH, Sokolenko A, Arkas M, Sofou G, Herrmann RG, Argyroudi-Akoyunoglou JH (2002) Proteolytic activity against the light-harvesting complex and the D1/D2 core proteins of Photosystem II in close association to the light-harvesting complex II trimer. Biochim Biophys Acta 1556:1553–1564

    Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929–6932

    Article  PubMed  CAS  Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2009) Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Res Microbiol 160:726–732

    Article  PubMed  CAS  Google Scholar 

  • Itzhaki H, Naveh L, Lindahl M, Cook M, Adam Z (1998) Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. J Biol Chem 273:7094–7098

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Zhang Y, Chen Y, Wu Y, Zhou ZH, Chang ZY, Sui SF (2008) Activation of DegP chaperone-protease via formation of large cage-like oligomers upon binding to substrate proteins. Proc Natl Acad Sci USA 105:11939–11944

    Article  PubMed  CAS  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    Article  PubMed  CAS  Google Scholar 

  • Kargul J, Barber J (2008) Photosynthetic acclimation: structural reorganization of light harvesting antenna—role of redox-dependent phosphorylation of major and minor chlorophyll a/b binding proteins. FEBS J 275:1056–1068

    Article  PubMed  CAS  Google Scholar 

  • Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under state 2 transition. FEBS J 272:4797–4806

    Article  PubMed  CAS  Google Scholar 

  • Kieselbach T, Funk C (2003) The family of Deg/HtrA proteases: from Escherichia coli to Arabidopsis. Physiol Plant 119:337–346

    Article  CAS  Google Scholar 

  • Kley J, Schmidt B, Boyanov B, Stolt-Bergner PC, Kirk R, Ehrmann M, Knopf RR, Naveh L, Adam Z, Clausen T (2011) Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat Struct Mol Biol 18:728–731

    Article  PubMed  CAS  Google Scholar 

  • Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, Clausen T (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453:885–890

    Article  PubMed  CAS  Google Scholar 

  • Krojer T, Garrido-Franco M, Huber R, Ehrmann M, Clausen T (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416:455–459

    Article  PubMed  CAS  Google Scholar 

  • Li J, Sun XW, Zhang LX (2010) Deg1 is involved in the degradation of the PsbO oxygen-evolving protein of photosystem II in Arabidopsis. Chin Sci Bull 55:3145–3148

    Article  CAS  Google Scholar 

  • Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12:419–431

    Article  PubMed  CAS  Google Scholar 

  • Lipinska B, Zylicz M, Georgopoulos C (1990) The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an essential endopeptidase. J Bacteriol 172:1791–1797

    PubMed  CAS  Google Scholar 

  • Nelson N, Yocum CF (2006) The structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565

    Article  PubMed  CAS  Google Scholar 

  • Parys E, Romanowska E, Siedlecka M, Poskuta JW (1998) The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant 20:313–322

    Article  CAS  Google Scholar 

  • Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156

    Article  PubMed  CAS  Google Scholar 

  • Romanowska E, Albertsson PA (1994) Isolation and characterization of the cytochrome b/f complex from whole thylakoids, grana and stroma lamellae vesicles from spinach chloroplasts. Plant Cell Physiol 35:557–568

    CAS  Google Scholar 

  • Sakamoto W (2003) Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana. Genes Genet Syst 78:1–9

    Article  PubMed  CAS  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    Article  PubMed  CAS  Google Scholar 

  • Sinvany-Villalobo G, Davydov O, Ben-Ari G, Zaltsman A, Raskind A, Adam Z (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol 135:1336–1345

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Fu T, Chen N, Guo J, Ma J, Zou M, Lu C, Zhang L (2010a) The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol 152:1263–1273

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010b) The thylakoid protease Deg1 is involved in photosystem II assembly in Arabidopsis thaliana. Plant J 62:240–249

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Peng LW, Guo JK, Chi W, Ma JF, Lu CM, Zhang LX (2007a) Formation of Deg5 and Deg8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis thaliana. Plant Cell 19:1347–1361

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Wang LY, Zhang LX (2007b) Involvement of Deg5 and Deg8 proteases in the turnover of the photosystem II reaction center D1 protein under heat stress in Arabidopsis thaliana. Chin Sci Bull 52:1742–1745

    Article  CAS  Google Scholar 

  • Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482

    Article  PubMed  CAS  Google Scholar 

  • Tokutsu R, Iwai M, Minagawa J (2009) CP29, a monomeric light-harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J Biol Chem 284:7777–7782

    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 application. Proc Natl Acad Sci USA 76:4350–4354

    Article  PubMed  CAS  Google Scholar 

  • Tziveleka LA, Argyroudi-Akoyunoglou JH (1998) Implications of a developmental-stage-dependent thylakoid-bound protease in the stabilization of the light-harvesting pigment–protein complex serving photosystem II during thylakoid biogenesis in red kidney bean. Plant Physiol 117:961–970

    Article  PubMed  CAS  Google Scholar 

  • Wagner R, Aigner H, Pružinská A, Jänkänpää HJ, Jansson S, Funk C (2011) Fitness analyses of Arabidopsis thaliana mutants depleted of FtsH metalloproteases and characterization of three FtsH6 deletion mutants exposed to high light stress, senescence and chilling. New Phytol 191:449–458

    Article  PubMed  CAS  Google Scholar 

  • Wessel D, Fluegge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergent. Anal Biochem 138:141–143

    Article  PubMed  CAS  Google Scholar 

  • Yang DH, Paulsen H, Andersson B (2000) The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett 466:385–388

    Article  PubMed  CAS  Google Scholar 

  • Zelisko A, Garcıa-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102:13699–13704

    Article  PubMed  CAS  Google Scholar 

  • Zelisko A, Jackowski G (2004) Lhca polypeptides are maintained during dark-induced senescence of leaves. J Plant Physiol 161:1157–1170

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by the Grant N303605438 from the Polish Ministry of Science and Higher Education. We would like to thank Professor Zach Adam for providing the Deg1 antibody and a plasmid containing the A. thaliana Deg1 transgene. We are especially grateful to Dr. Joanna Kargul for helpful comments and correction of the manuscript.

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Correspondence to Maksymilian Zienkiewicz.

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Suppl. Table 1 (DOC 26 kb)

425_2011_1505_MOESM2_ESM.tif

Suppl. Fig. S1. Ni-NTA purification of recombinant Deg1 of A. thaliana. (a) SDS-PAGE analysis of Deg1 expression. Samples were resolved on SDS-PAGE and stained with Coomassie Blue. Lanes 1 and 2, crude bacterial extracts before and after induction of Deg1 overexpression, respectively; lane 3, purified Deg1 protein. (b) Mass spectrometric analysis of purified A. thaliana Deg1. A band containing the His-tagged Deg1 protein was excised from the gel and analyzed using mass spectrometry. Identified peptides that matched the Deg1 amino acid sequence are shown in bold. Matching peptides covered 43% of the Deg1 amino acid sequence. (TIFF 133 kb)

425_2011_1505_MOESM3_ESM.tif

Suppl. Fig. S2. Degradation of β-casein by purified Deg1 (wild type) and Deg1S280G (mutant). Fraction eluted from the Ni-NTA agarose column (3 'g) was incubated with β-casein (8 'g) for 1h at 30°C. At the end of the incubation, reaction mixtures were subjected to SDS-PAGE and stained with Coomassie Brilliant Blue. Similar results were obtained in three independent experiments. (TIFF 606 kb)

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Zienkiewicz, M., Ferenc, A., Wasilewska, W. et al. High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana . Planta 235, 279–288 (2012). https://doi.org/10.1007/s00425-011-1505-x

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