In the photosynthetic process solar energy is con- verted to chemical energy. The energy-rich products of photosynthesis are utilised directly or indirectly by all vertebrates on this planet; the by-product of the light reaction, oxygen, is a vital constituent of the atmosphere and has enabled the diversity of life as we know it today. The world’s growing population consumes ever-increasing amounts of food and energy. Therefore, there are two key objectives in plant research: increasing biomass production and generating new sustainable energy sources. The foundation to address these important objectives is a detailed understanding of the process of photo- synthesis. Despite their fundamental importance, our knowledge of the molecular mechanisms involved
in the biogenesis and turnover of the photosynthetic complexes is still limited. I focus on the photosyn- thetic light reaction with the aim to optimize plant growth for enhanced food and biomass production.
Wolfgang Schroder 1150 766The chloroplast, an organelle with a complex architecture, consists of several distinct compartments that contain both nu- clear- and plastid-encoded proteins. Photosynthetic electron transport occurs in the thylakoid membrane, while CO2  xa- tion takes place in the stroma. In 1997 we started to develop a method for the isolation of a highly puri ed thylakoid lumen using spinach chloroplasts.We carried out the  rst systemat- ic characterisation of the lumen content and showed that it contained at least 25 proteins.These data changed the common understanding of the thylakoid lumen from being mainly proton storage for the generation of the proton motive force.We were able to show that the lumen instead plays an important role in the proper function of the photosynthetic complexes and the integrity of the thylakoid membrane.
Schroder bild1
We characterised several of the novel lumen proteins. As the genome for the model organism Arabidopsis thaliana was getting available we continued our research on this organism and published the  rst 2D-gels of Arabidopsis in 2000 and the complete map was published (Schubert et al. 2002). Our analysis showed that the thylakoid lumen of Arabidopsis contains at least 46 unique proteins. These include 11 immunophilins, Deg (P1, P5 and P8) proteases, 3 pentapeptiderepeat proteins, 10 PsbP domain proteins, 2 PsbQ-domain proteins, extra copies of the Photo- system II extrinsic proteins PsbO, P and Q,TL29,VDE and  ve proteins with unknown function. It is thus clear that there is a very speci c group of proteins that are localized in the thylakoid lumen.The “empty” space contains proteins and thus is bound to have various enzymatic activities important for the photosynthetic process. A large program for antibody produc- tion, overexpression, crystalisation and anti-sense of these lumen proteins is now in progress.The published maps of the thylakoid lumen content are used for analysis of various stress factors such as temperature, light and nutrition. The protein changes are quanti ed with the EttanTM DIGE, and DeCyderTM image analysis platform, in combination with various MS techniques.
sweden_greySvensk sammanfattning

Latest Publications

  1. Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases
    Plant Physiol. 2018 Feb;176(2):1199-1214
  2. Active-site plasticity revealed in the asymmetric dimer of AnPrx6 the 1-Cys peroxiredoxin and molecular chaperone from Anabaena sp. PCC 7210
    Sci Rep. 2017, 7(1):17151
  3. Establishment of photosynthesis is controlled by two distinct regulatory phases
    Plant Physiol. 2017 Jun 16 [Epub ahead of print]
  4. The PsbY protein of Arabidopsis Photosystem II is important for the redox control of Cytochrome b559
    Biochim Biophys Acta. 2016 May 21. pii: S0005-2728(16)30536-9 [Epub ahead of print]
  5. Functional Update of the Auxiliary Proteins PsbW, PsbY, HCF136, PsbN, TerC and ALB3 in Maintenance and Assembly of PSII
    Front Plant Sci. 2016, 7:423 eCollection, Review
  6. Metabolomic analysis of extreme freezing tolerance in Siberian spruce (Picea obovata)
    New Phytol. 2014, 204(3):545-555
  7. PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum
    Plant Cell. 2014, 26(3):1183-99
  8. Dark-adapted spinach thylakoid protein heterogeneity offers insights into the Photosystem II repair cycle
    Biochim Biophys Acta. 2014; 1837(9):1463-71
  9. Family-wide characterization of Matrix Metallo-proteinases from Arabidopsis thaliana reveals their distinct proteolytic activity and cleavage site specificity
    Biochem J. 2013 Oct 25. [Epub ahead of print]
  10. Proteomic amino-termini profiling reveals targeting information for protein import into complex plastids
    PLoS One. 2013 Sep 16;8(9):e74483
  11. Isolation of monomeric photosystem II that retains the subunit PsbS
    Photosynth Res. 2013; 118(3):199-207
  12. Jänkänpää HJ, Mishra Y, Schröder WP, Jansson S
    Metabolic profiling reveals metabolic shifts in Arabidopsis plants grown under different light conditions.
    Plant, Cell & Environment 2012 Online
  13. Mishra Y, Johansson Jankanpaa H, Kiss AZ, Funk C, Schroder WP, Jansson S
    Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components
    BMC Plant Biology 2012, 12:6
  14. Mishra Y, Hall M, Chaurasia N, Rai LC, Jansson S, Schröder WP, Sauer UH
    Expression, purification, crystallization and preliminary X-ray crystallographic studies of alkyl hydroperoxide reductase (AhpC) from the cyanobacterium Anabaena sp. PCC 7120
    Acta Cryst. : 2011 F67
  15. Lundberg E, Storm P, Schröder WP, Funk C
    Crystal structure of the TL29 protein from Arabidopsis thaliana: An APX homolog without peroxidase activity
    J Struct Biol.: 2011 176(1):24-31
  16. Hall M, Mishra Y, Schröder WP
    Preparation of stroma, thylakoid membrane, and lumen fractions from Arabidopsis thaliana chloroplasts for proteomic analysis
    Methods in Molecular Biology: 2011, 775:207-222
  17. Shi L, Hall M, Funk C, Schröder WP
    Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins
    Biochimica et Biophysica Acta - Bioenergetics: 1817 (2012), pp. 13-25
  18. Granlund I, Kieselbach T, Alm R, Schröder WP, Emanuelsson C
    Clustering of MS spectra for improved protein identification rate and screening for protein variants and modifications by MALDI-MS/MS
    J Proteomics.; 2011, 12;74(8):1190-200
  19. Ådén J, Wallgren M, Storm P, Weise CF, Christiansen A, Schröder WP, Funk C, Wolf-Watz M
    Extraordinary μs–ms backbone dynamics in Arabidopsis thaliana peroxiredoxin Q
    Biochimica et Biophysica Acta - Proteins & Proteomics: 1814, 1880-1890
  20. Shiryaeva L, Antti H, Schröder WP, Strimbeck R, Shiriaev AS
    Pair-wise multi-comparison and OPLS analyses of cold-acclimation phases in Siberian spruce
    Metabolomics 2011 April 11,
    Online first
  21. Kjellsen TD, Shiryaeva L, Schröder WP, Strimbeck RG
    Proteomics of Extreme Frost Tolerance in Siberian Spruce (Picea obovata)
    Journal of Proteomics (2010) 73:965
  22. Garcia-Cerdán JG, Kovács L, Tóth T, Kereiche S, Avseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP
    The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants
    The Plant Journal: 2011 65: 368-381

  23. info_16x16The photosystem II (PSII) complex, responsible for splitting water and releasing oxygen, is located mainly in the grana thylakoid membrane. The complex consists of more than 30 different protein subunits, and has a molecular mass of more than 700 kDa. Eighteen of the subunits are low molecular mass proteins (< 10 kDa), all of which contain a single transmembrane span and their protein sequences are highly conserved among photosynthetic organisms. Why are so many single-transmembrane spanning protein subunits found in the PSII complex?

    The light driven photosynthetic electron transport of green plants is mediated by chlorophyll-binding protein complexes located in the thylakoid membrane within the chloroplast. The thylakoid membrane has a complex structure, with lateral segregation of protein complexes into distinct regions referred to as the grana and stroma lamellae. The components involved in the light reactions are organized in five supracomplexes: Photosystem I (PSI) and II (PSII), light harvesting complex (LHCII), ATP-synthase and the cytochrome b6/f complex. For these entire complexes, we have medium to high resolution structural information, even though the location of several of the low molecular mass proteins still are unclear. Recently, it has become known that these complexes interact and form higher orders of association complexes, like mega-organized super-complexes within the membrane.
    It has been assumed, suggested and accepted that various protein complexes can migrate between the two thylakoid regions. For instance, the antenna protein complex LHCII has been shown to migrate out of the grana region upon phosphorylation. Also, turnover and assembly of the grana-located Photosystem II complex may need migration. On the other hand, the grana thylakoids are among the most protein-dense membranes found in living cells, with suggested 70-80% protein contents. Thus, the mechanism of protein diffusion in such a densely packed membrane is difficult to understand. The protein complexes in the thylakoid membrane must be organized in a manner that optimises migration and allows fast diffusion. How is this achieved? We think that a set of low molecular mass proteins are involved in this process.
    So far, isolation of various knock-out mutants of the small proteins has not given clear indications of the functions for several of them. However, recently we have obtained new data that have given us a breakthrough. The data clearly show that the characteristic phosphorylation pattern of the PSII reaction centre proteins is dramatically changed upon deletion of two small proteins. Furthermore, the structure of the thylakoid membrane was found to be changed, so that no PSII-LHCII super complex could be detected.
    sweden_greySvensk sammanfattning

    Key publications

    Lundberg E, Storm P, Schröder WP, Funk C (2011) Crystal structure of the TL29 protein from Arabidopsis thaliana: An APX homolog without peroxidase activity.
    J Struct Biol. 176(1):24-31

    Shi L, Hall M, Funk C, Schröder WP (2012) Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins.
    Biochimica et Biophysica Acta – Bioenergetics. 1817 (2012), pp. 13-25

    Garcia-Cerdán JG, Kovács L, Tóth T, Kereiche S, Avseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants.
    The Plant Journal. 65: 368-381

    Hall M, Mata-Cabana A, Åkerlund H-E, Florencio FJ, Schröder WP, Lindahl M, Kieselbach T (2010) Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function.
    Proteomics. 10:987-1001

    García-Cerdán JG, Sveshnikov D, Dewez D, Jansson S, Funk C, and Schröder WP. (2008) Antisense inhibition of the PsbX protein Affects PSII integrity in higher plant Arabidopsis thaliana. Plant Cell Physiol 50:1-12

    playExpand publications list
  24. Hall M, Mata-Cabana A, Åkerlund H-E, Florencio FJ, Schröder WP, Lindahl M, Kieselbach T
    Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function
    Proteomics: 2010 10:987-1001
  25. Granlund I, Storm P, Schubert M, Garcia-Cerdan JG, Funk C, Schröder WP
    The TL29 protein is lumen located associated with Photosystem II and not an ascorbate peroxidase
    Plant and Cell Physiology: 2009 50:1898-1910
  26. Pesaresi P, Scharfenberg M, Weigel M, Granlund I, Schroder WP, Finazzi G, Rappaport F, Masiero S, Furini A, Jahns P, Leister D
    Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: Fevised roles of plastocyanin on photosynthetic electron flow and thylakoid redox state
    Molecular Plant: 2009 2:236-248
  27. Cain P, Hall M, Schröder WP, Kieselbach T, Robinson C.
    A novel extended family of stromal thioredoxins
    Plant Mol Biol. 2009 Jun;70(3):273-81
  28. Granlund I, Hall M, Kieselbach T, Schröder WP
    Light induced changes in protein expression and uniform regulation of transcription in the thylakoid lumen of Arabidopsis thaliana
    Plos One: 2009 4:e5649
  29. Garcia-Cerdin JG, Sveshnikov D, Dewer D., Jansson S, Funk C, Schröder WP
    Antisense inhibition of the PsbX protein affects PSII integrity in higher plant Arabidopsis thaliana
    Plant and Cell Physiology: 2009 50(2):191-202
  30. Garcia-Cerdán JG, Sveshnikov D, Dewer D., Jansson S, Funk C, Schröder WP
    Antisense inhibition of the PsbX protein affects PSII integrity in higher plant Arabidopsis thaliana
    Plant and Cell Physiology: 2009 50(2):191-202
  31. Fey H, Piano D, Horn R, Fischer D, Schmidt M, Ruf S, Schröder WP, Bock R, Büchel C.
    Isolation of highly active photosystem II core complexes with a His-tagged Cyt b559 subunit from transplastomic tobacco plants
    Biochim Biophys Acta. ;1777(12):1501-9
  32. Sveshnikov D, Funk C, Schröder WP
    The PsbP-like protein (sll1418) of Synechocystis sp. PCC 6803 stabilises the donor side of Photosystem II
    Photosynthesis Research: 2008 93:101-109
  33. Hedman E, Widen C, Asadi A, Schröder WP, Gustavsson JÅ, Wikström AC
    Proteomics identification of glucocorticoid receptor interacting proteins
    Proteomics: 2006 6:3114-3126
  34. Edvardsson A, Shapiguzov A, Petersson UA, Schröder WP, Vener AV
    Immunophilin AtFKBP13 sustains all peptidyl- prolyl isomerase activity in the thylakoid lumen from Arabidopsis thaliana deficient in AtCYP20-2
    Biochemistry: 2007 46:9432-9442
  35. Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestrom P, Schroder W, Hurry V
    The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature
    Plant Journal: 2006 47:720-734
  36. Hedman E, Widen C, Asadi A, Dinnetz I, Schroder WP, Gustafsson JA, Wikstrom AC
    Proteomic identification of glucocorticoid receptor interacting proteins
    Proteomics: 2006 6:3114-3126
  37. Ishikawa Y, Schroder WP, Funk C
    Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp. PCC 6803
    Photosynth Res: 2005 84:257-262
  38. Shi LX, Schroder WP
    The low molecular mass subunits of the photosynthetic supracomplex, photosystem II
    Biochimica Et Biophysica Acta-Bioenergetics: 2004 1608:75-96
  39. Huang F, Hedman E, Funk C, Kieselbach T, Schroder WP, Norling B
    Isolation of outer membrane of Synechocystis sp PCC 6803 and its proteomic characterization
    Molecular & Cellular Proteomics: 2004 3:586-595
  40. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T
    Proteome map of the chloroplast lumen of Arabidopsis thaliana (vol 277, pg 8354, 2002)
    Journal of Biological Chemistry: 2003 278:13590-13590
  41. Kieselbach T, Schroder WP
    The proteome of the chloroplast lumen of higher plants
    Photosynth Res: 2003 78:249-264
  42. Schroder WP, Kieselbach T
    Update on chloroplast proteomics
    Photosynth Res: 2003 78:181-193
  43. Carlberg I, Hansson M, Kieselbach T, Schroder WP, Andersson B, Vener AV
    A novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes
    Proc Natl Acad Sci U S A: 2003 100:757-762
  44. Thidholm E, Lindstrom V, Tissier C, Robinson C, Schroder WP, Funk C
    Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer
    Febs Letters: 2002 513:217-222
  45. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T
    Proteome map of the chloroplast lumen of Arabidopsis thaliana
    J Biol Chem: 2002 277:8354-8365
  46. Funk C, Wiklund R, Schroder WP, Jansson C
    D1 ' centers are less efficient than normal photosystem II centers
    Febs Letters: 2001 505:113-117
  47. Kieselbach T, Bystedt M, Hynds P, Robinson C, Schroder WP
    A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen
    Febs Letters: 2000 480:271-276
  48. Shi LX, LorkoviÆ’a ZJ, Oelmuller R, Schroder WP
    The low molecular mass PsbW protein is involved in the stabilization of the dimeric photosystem II complex in Arabidopsis thaliana
    J Biol Chem: 2000 275:37945-37950
  49. Shi LX, Kim SJ, Marchant A, Robinson C, Schroder WP
    Characterisation of the PsbX protein from Photosystem II and light regulation of its gene expression in higher plants
    Plant Molecular Biology: 1999 40:737-744
  50. Mant A, Kieselbach T, Schroder WP, Robinson C
    Characterisation of an Arabidopsis thaliana cDNA encoding a novel thylakoid lumen protein imported by the Delta pH-dependent pathway
    Planta: 1999 207:624-627
  51. Kieselbach T, Mant A, Robinson C, Schroder WP
    Characterisation of an Arabidopsis cDNA encoding a thylakoid lumen protein related to a novel 'pentapeptide repeat' family of proteins
    FEBS Lett: 1998 428:241-244
  52. Funk C, Schroder WP, Salih G, Wiklund R, Jansson C
    Engineering of N-terminal threonines in the D1 protein impairs photosystem II energy transfer in Synechocystis 6803
    Febs Letters: 1998 436:434-438
  53. Kieselbach T, Hagman A, Andersson B, Schroder WP
    The thylakoid lumen of chloroplasts - Isolation and characterization
    Journal of Biological Chemistry: 1998 273:6710-6716
  54. Eckermann S, Schroder G, Schmidt J, Strack D, Edrada RA, Helariutta Y, Elomaa P, Kotilainen M, Kilpelainen I, Proksch P, Teeri TH, Schroder J
    New pathway to polyketides in plants
    Nature: 1998 396:387-390
  55. Hagman A, Shi LX, Rintamaki E, Andersson B, Schroder WP
    The nuclear-encoded PsbW protein subunit of photosystem II undergoes light-induced proteolysis
    Biochemistry: 1997 36:12666-12671
  56. Shi LX, Schroder WP
    Compositional and topological studies of the PsbW protein in spinach thylakoid membrane
    Photosynthesis Research: 1997 53:45-53
  57. Funk C, Schroder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B
    The Psii-S Protein of Higher-Plants - a New-Type of Pigment-Binding Protein
    Biochemistry: 1995 34:11133-11141
  58. Jegerschold C, Arellano JB, Schroder WP, Vankan PJM, Baron M, Styring S
    Copper(Ii) Inhibition of Electron-Transfer through Photosystem-Ii Studied by Epr Spectroscopy
    Biochemistry: 1995 34:12747-12754
  59. Irrgang KD, Shi LX, Funk C, Schroder WP
    A Nuclear-Encoded Subunit of the Photosystem-Ii Reaction-Center
    Journal of Biological Chemistry: 1995 270:17588-17593
  60. Helariutta Y, Elomaa P, Kotilainen M, Griesbach RJ, Schroder J, Teeri TH
    Chalcone Synthase-Like Genes Active During Corolla Development Are Differentially Expressed and Encode Enzymes with Different Catalytic Properties in Gerbera-Hybrida (Asteraceae)
    Plant Molecular Biology: 1995 28:47-60
  61. Lorkovic ZJ, Schroder WP, Pakrasi HB, Irrgang KD, Herrmann RG, Oelmuller R
    Molecular Characterization of Psbw, a Nuclear-Encoded Component of the Photosystem-Ii Reaction-Center Complex in Spinach
    Proceedings of the National Academy of Sciences of the United States of America: 1995 92:8930-8934
  62. Funk C, Schroder WP, Green BR, Renger G, Andersson B
    The Intrinsic 22 Kda Protein Is a Chlorophyll-Binding Subunit of Photosystem-Ii
    Febs Letters: 1994 342:261-266
  63. Schroder WP, Arellano JB, Bittner T, Baron M, Eckert HJ, Renger G
    Flash-Induced Absorption-Spectroscopy Studies of Copper Interaction with Photosystem-Ii in Higher-Plants
    Journal of Biological Chemistry: 1994 269:32865-32870
  64. Arellano JB, Schroder WP, Sandmann G, Chueca A, Baron M
    Removal of Nuclear Contaminants and of Nonspecifically Photosystem Ii-Bound Copper from Photosystem-Ii Preparations
    Physiologia Plantarum: 1994 91:369-374
  65. Messinger J, Schroder WP, Renger G
    Structure-Function Relations in Photosystem-Ii - Effects of Temperature and Chaotropic Agents on the Period 4 Oscillation of Flash-Induced Oxygen Evolution
    Biochemistry: 1993 32:7658-7668
  66. Vermaas WFJ, Styring S, Schroder WP, Andersson B
    Photosynthetic Water Oxidation - the Protein Framework
    Photosynthesis Research: 1993 38:249-263
  67. Schroder WP, Messinger J, Tremolieres A, Renger G
    On the Effects of Lipase Treatment on the Reaction Pattern of Ps-Ii
    Photosynthesis Research: 1992 34:140-140
  68. Schroder WP, Petit PX
    Flow-Cytometry of Spinach-Chloroplasts - Determination of Intactness and Lectin-Binding Properties of the Envelope and the Thylakoid Membranes
    Plant Physiology: 1992 100:1092-1102
  69. Henrysson T, Schroder WP, Spangfort M, Akerlund HE
    Isolation and Characterization of the Chlorophyll-a/B Protein Complex Cp29 from Spinach
    Biochimica Et Biophysica Acta: 1989 977:301-308
  70. Sundblad LG, Schroder WP, Akerlund HE
    S-State Distribution and Redox State of Qa in Barley in Relation to Luminescence Decay Kinetics
    Biochimica Et Biophysica Acta: 1989 973:47-52
  71. Schroder WP, Henrysson T, Akerlund HE
    Characterization of Low-Molecular Mass Proteins of Photosystem-Ii by N-Terminal Sequencing
    Febs Letters: 1988 235:289-292
  72. Sundblad LG, Schroder WP, Akerlund HE
    S-State Distribution and Redox State of Qb in Relation to Far Red Induced Luminescence Decay Kinetics of Intact Leaves, Protoplasts and Protoplast Extracts from Barley
    Physiologia Plantarum: 1988 73:A18-A18
  73. Schroder WP, Akerlund HE
    H2o2 Accessibility to the Photosystem-Ii Donor Side in Protein-Depleted inside-out Thylakoids Measured as Flash-Induced Oxygen Production
    Biochimica Et Biophysica Acta: 1986 848:359-363