Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts[OA]

The photosystem II (PSII) light-harvesting antenna in higher plants contains a number of highly conserved gene products whose function is unknown. Arabidopsis thaliana plants depleted of one of these, the CP24 light-harvesting complex, have been analyzed. CP24-deficient plants showed a decrease in light-limited photosynthetic rate and growth, but the pigment and protein content of the thylakoid membranes were otherwise almost unchanged. However, there was a major change in the macroorganization of PSII within these membranes; electron microscopy and image analysis revealed the complete absence of the C2S2M2 light-harvesting complex II (LHCII)/PSII supercomplex predominant in wild-type plants. Instead, only C2S2 supercomplexes, which are deficient in the LHCIIb M-trimers, were found. Spectroscopic analysis confirmed the disruption of the wild-type macroorganization of PSII. It was found that the functions of the PSII antenna were disturbed: connectivity between PSII centers was reduced, and maximum photochemical yield was lowered; rapidly reversible nonphotochemical quenching was inhibited; and the state transitions were altered kinetically. CP24 is therefore an important factor in determining the structure and function of the PSII light-harvesting antenna, providing the linker for association of the M-trimer into the PSII complex, allowing a specific macroorganization that is necessary both for maximum quantum efficiency and for photoprotective dissipation of excess excitation energy.

[1]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[2]  J. Briantais,et al.  A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. , 1979, Biochimica et biophysica acta.

[3]  C. Bustamante,et al.  Theory of the interaction of light with large inhomogeneous molecular aggregates. I. Absorption , 1986 .

[4]  C. Bustamante,et al.  Theory of the interaction of light with large inhomogeneous molecular aggregates. II. Psi‐type circular dichroism , 1986 .

[5]  C. Bustamante,et al.  Helically organized macroaggregates of pigment-protein complexes in chloroplasts: evidence from circular intensity differential scattering. , 1988, Biochemistry.

[6]  C. Bustamante,et al.  Direct observation of large chiral domains in chloroplast thylakoid membranes by differential polarization microscopy. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[7]  B. Green,et al.  The chlorophyll ab complex, CP29, is associated with the Photosystem II reaction centre core , 1989 .

[8]  R. J. Porra,et al.  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 , 1989 .

[9]  N. W. Horne.  Changes of light , 1989 .

[10]  Barbara Demmig-Adams,et al.  Carotenoids and photoprotection in plants : a role for the xanthophyll zeaxanthin , 1990 .

[11]  G. Peter,et al.  Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. , 1991, The Journal of biological chemistry.

[12]  J. Allen,et al.  Protein phosphorylation in regulation of photosynthesis. , 1992, Biochimica et biophysica acta.

[13]  G. Garab,et al.  Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. , 1994, Biochemistry.

[14]  S. Jansson.  The light-harvesting chlorophyll a/b-binding proteins. , 1994, Biochimica et biophysica acta.

[15]  H. Trissl,et al.  Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. , 1995, Biophysical journal.

[16]  B. Green,et al.  THE CHLOROPHYLL-CAROTENOID PROTEINS OF OXYGENIC PHOTOSYNTHESIS. , 1996, Annual review of plant physiology and plant molecular biology.

[17]  P. Horton,et al.  Identification of proton-active residues in a higher plant light-harvesting complex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  F. Wollman,et al.  Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii , 1996 .

[19]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[20]  K. Niyogi,et al.  Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching. , 1997, The Plant cell.

[21]  V Barzda,et al.  Isolation of lamellar aggregates of the light-harvesting chlorophyll a/b protein complex of photosystem II with long-range chiral order and structural flexibility. , 1997, Analytical biochemistry.

[22]  A. Young,et al.  Dynamics of Xanthophyll-Cycle Activity in Different Antenna Subcomplexes in the Photosynthetic Membranes of Higher Plants (The Relationship between Zeaxanthin Conversion and Nonphotochemical Fluorescence Quenching) , 1997, Plant physiology.

[23]  Tardy,et al.  Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance , 1998, Plant physiology.

[24]  Wilko Keegstra,et al.  Automation of specimen selection and data acquisition for protein electron crystallography , 1998 .

[25]  D. Kaftan,et al.  Flash fluorescence induction: a novel method to study regulation of Photosystem II , 1999 .

[26]  E. Boekema,et al.  Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. , 1999, European journal of biochemistry.

[27]  E. Boekema,et al.  Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. , 1999, Biochemistry.

[28]  Lazăr,et al.  Chlorophyll a fluorescence induction1 , 1999, Biochimica et biophysica acta.

[29]  E. Boekema,et al.  Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. , 2000, Journal of molecular biology.

[30]  Stefan Jansson,et al.  A pigment-binding protein essential for regulation of photosynthetic light harvesting , 2000, Nature.

[31]  A. Ruban,et al.  Xanthophylls of the major photosynthetic light‐harvesting complex of plants: identification, conformation and dynamics , 2000, FEBS letters.

[32]  H. Scheller,et al.  Balance of power: a view of the mechanism of photosynthetic state transitions. , 2001, Trends in plant science.

[33]  P. Horton,et al.  Antisense Inhibition of the Photosynthetic Antenna Proteins CP29 and CP26: Implications for the Mechanism of Protective Energy Dissipation , 2001, Plant Cell.

[34]  J F Allen,et al.  Molecular recognition in thylakoid structure and function. , 2001, Trends in plant science.

[35]  H. Scheller,et al.  Supermolecular organization of photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana. , 2001, European journal of biochemistry.

[36]  P. Gustafsson,et al.  The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. , 2001, Plant physiology.

[37]  K. Niyogi,et al.  A Major Light-Harvesting Polypeptide of Photosystem II Functions in Thermal Dissipation Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002154. , 2002, The Plant Cell Online.

[38]  A. Holzenburg,et al.  Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. , 2002, Biochemistry.

[39]  E. Boekema,et al.  The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. , 2003, Biochemistry.

[40]  S. Taneva,et al.  Structural rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect. , 2003, Biochemistry.

[41]  P. Horton,et al.  Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. , 2003, The Plant journal : for cell and molecular biology.

[42]  E. Boekema,et al.  Plants lacking the main light-harvesting complex retain photosystem II macro-organization , 2003, Nature.

[43]  E. Stauber,et al.  Proteomics of Chlamydomonas reinhardtii Light-Harvesting Proteins , 2003, Eukaryotic Cell.

[44]  Zhenfeng Liu,et al.  Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution , 2004, Nature.

[45]  E. Boekema,et al.  Solubilization of green plant thylakoid membranes with n-dodecyl-α,D-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b6 f complexes , 2004, Photosynthesis Research.

[46]  Graham R Fleming,et al.  Toward an understanding of the mechanism of nonphotochemical quenching in green plants. , 2004, Biochemistry.

[47]  D. Kaftan,et al.  On the relationship between the non-photochemical quenching of the chlorophyll fluorescence and the Photosystem II light harvesting efficiency. A repetitive flash fluorescence induction study , 2004, Photosynthesis Research.

[48]  Wah Soon Chow,et al.  The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues , 1995, Photosynthesis Research.

[49]  C. Külheim,et al.  Is Each Light-Harvesting Complex Protein Important for Plant Fitness?1[w] , 2004, Plant Physiology.

[50]  K. Niyogi,et al.  Regulation of Photosynthetic Light Harvesting Involves Intrathylakoid Lumen pH Sensing by the PsbS Protein* , 2004, Journal of Biological Chemistry.

[51]  P. Horton,et al.  The functional significance of the monomeric and trimeric states of the photosystem II light harvesting complexes. , 2004, Biochemistry.

[52]  R. Bassi,et al.  Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls , 2004, Photosynthesis Research.

[53]  Bruno Robert,et al.  Molecular basis of photoprotection and control of photosynthetic light-harvesting , 2005, Nature.

[54]  P. Horton,et al.  Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. , 2004, Journal of experimental botany.

[55]  P. Horton,et al.  Control of the light harvesting function of chloroplast membranes: The LHCII‐aggregation model for non‐photochemical quenching , 2005, FEBS letters.

[56]  Egbert J Boekema,et al.  Supramolecular organization of thylakoid membrane proteins in green plants. , 2005, Biochimica et biophysica acta.

[57]  H. Scheller,et al.  Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. , 2005, Biochemistry.

[58]  Pam Lee,et al.  Plasticity in the Composition of the Light Harvesting Antenna of Higher Plants Preserves Structural Integrity and Biological Function* , 2006, Journal of Biological Chemistry.

[59]  J. Minagawa,et al.  Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[60]  P. Horton,et al.  PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin , 2006, FEBS letters.

[61]  J. Barber,et al.  Environmentally Modulated Phosphoproteome of Photosynthetic Membranes in the Green Alga Chlamydomonas reinhardtii*S , 2006, Molecular & Cellular Proteomics.

[62]  D. Leister,et al.  Abundantly and Rarely Expressed Lhc Protein Genes Exhibit Distinct Regulation Patterns in Plants1[W] , 2006, Plant Physiology.

[63]  Thermo-Optic Effects , 2006 .