Continuous Turnover of Carotenes and Chlorophyll a in Mature Leaves of Arabidopsis Revealed by 14CO2 Pulse-Chase Labeling[OA]

Carotenoid turnover was investigated in mature leaves of Arabidopsis (Arabidopsis thaliana) by 14CO2 pulse-chase labeling under control-light (CL; 130 μmol photons m−2 s−1) and high-light (HL; 1,000 μmol photons m−2 s−1) conditions. Following a 30-min 14CO2 administration, photosynthetically fixed 14C was quickly incorporated in β-carotene (β-C) and chlorophyll a (Chl a) in all samples during a chase of up to 10 h. In contrast, 14C was not detected in Chl b and xanthophylls, even when steady-state amounts of the xanthophyll-cycle pigments and lutein increased markedly, presumably by de novo synthesis, in CL-grown plants under HL. Different light conditions during the chase did not affect the 14C fractions incorporated in β-C and Chl a, whereas long-term HL acclimation significantly enhanced 14C labeling of Chl a but not β-C. Consequently, the maximal 14C signal ratio between β-C and Chl a was much lower in HL-grown plants (1:10) than in CL-grown plants (1:4). In lut5 mutants, containing α-carotene (α-C) together with reduced amounts of β-C, remarkably high 14C labeling was found for α-C while the labeling efficiency of Chl a was similar to that of wild-type plants. The maximum 14C ratios between carotenes and Chl a were 1:2 for α-C:Chl a and 1:5 for β-C:Chl a in CL-grown lut5 plants, suggesting high turnover of α-C. The data demonstrate continuous synthesis and degradation of carotenes and Chl a in photosynthesizing leaves and indicate distinct acclimatory responses of their turnover to changing irradiance. In addition, the results are discussed in the context of photosystem II repair cycle and D1 protein turnover.

[1]  B. Pogson,et al.  Source to sink: regulation of carotenoid biosynthesis in plants. , 2010, Trends in plant science.

[2]  W. Sakamoto,et al.  Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. , 2009, Journal of biochemistry.

[3]  J. Keasling,et al.  Lutein Accumulation in the Absence of Zeaxanthin Restores Nonphotochemical Quenching in the Arabidopsis thaliana npq1 Mutant[W][OA] , 2009, The Plant Cell Online.

[4]  L. Tian,et al.  The evolution and function of carotenoid hydroxylases in Arabidopsis. , 2009, Plant & cell physiology.

[5]  K. Winter,et al.  Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. , 2009, Functional plant biology : FPB.

[6]  B. Pogson,et al.  De Novo Synthesis and Degradation of Lx and V Cycle Pigments during Shade and Sun Acclimation in Avocado Leaves1 , 2008, Plant Physiology.

[7]  W. Schwab,et al.  Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. , 2008, Journal of agricultural and food chemistry.

[8]  Yoshikazu Tanaka,et al.  Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. , 2008, The Plant journal : for cell and molecular biology.

[9]  K. Winter,et al.  Lutein epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga. , 2008, Plant, cell & environment.

[10]  P. Beyer,et al.  Metabolic engineering of carotenoid biosynthesis in plants. , 2008, Trends in biotechnology.

[11]  A. Fiore,et al.  Different Roles of α- and β-Branch Xanthophylls in Photosystem Assembly and Photoprotection* , 2007, Journal of Biological Chemistry.

[12]  C. Osmond,et al.  The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. , 2007, Functional plant biology : FPB.

[13]  W. Chow,et al.  The stoichiometry of the two photosystems in higher plants revisited. , 2007, Biochimica et biophysica acta.

[14]  B. Pogson,et al.  Regulation of lutein biosynthesis and prolamellar body formation in Arabidopsis. , 2007, Functional plant biology : FPB.

[15]  W. Vermaas,et al.  Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. , 2007, Biochimica et biophysica acta.

[16]  A. Ohmiya,et al.  Carotenoid Cleavage Dioxygenase (CmCCD4a) Contributes to White Color Formation in Chrysanthemum Petals1[OA] , 2006, Plant Physiology.

[17]  P. Fraser,et al.  Elucidation of the β‐carotene hydroxylation pathway in Arabidopsis thaliana , 2006 .

[18]  H. Klee,et al.  Plant carotenoid cleavage oxygenases and their apocarotenoid products. , 2006, Current opinion in plant biology.

[19]  B. Pogson,et al.  Vitamin synthesis in plants: tocopherols and carotenoids. , 2006, Annual review of plant biology.

[20]  H. Klee,et al.  Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. , 2006, The Plant journal : for cell and molecular biology.

[21]  D. DellaPenna,et al.  Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Jan Kern,et al.  Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II , 2005, Nature.

[23]  A. Telfer Too much light? How β-carotene protects the photosystem II reaction centre , 2005, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[24]  R. Tanaka,et al.  Effects of Chlorophyllide a Oxygenase Overexpression on Light Acclimation inArabidopsis thaliana , 2005, Photosynthesis Research.

[25]  E. Larsen,et al.  Simple saponification method for the quantitative determination of carotenoids in green vegetables. , 2005, Journal of agricultural and food chemistry.

[26]  W. Gruszecki,et al.  Carotenoids as modulators of lipid membrane physical properties. , 2005, Biochimica et biophysica acta.

[27]  R. Tanaka,et al.  The N-Terminal Domain of Chlorophyllide a Oxygenase Confers Protein Instability in Response to Chlorophyll b Accumulation in Arabidopsis , 2005, The Plant Cell Online.

[28]  T. Morosinotto,et al.  Stoichiometry of LHCI antenna polypeptides and characterization of gap and linker pigments in higher plants Photosystem I. , 2004, European journal of biochemistry.

[29]  C. Nichol,et al.  Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may 'lock-in' lutein-based photoprotection during acclimation to strong light. , 2004, Journal of experimental botany.

[30]  S. Cuiné,et al.  The Effect of Zeaxanthin as the Only Xanthophyll on the Structure and Function of the Photosynthetic Apparatus in Arabidopsis thaliana* , 2004, Journal of Biological Chemistry.

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

[32]  Jie He,et al.  The rate coefficient of repair of photosystem II after photoinactivation , 2003 .

[33]  E. Baena-González,et al.  Biogenesis, assembly and turnover of photosystem II units. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  W. Chow,et al.  The role of inactive photosystem-II-mediated quenching in a last-ditch community defence against high light stress in vivo. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  K. Winter,et al.  Acclimation of tropical tree seedlings to excessive light in simulated tree‐fall gaps , 2001 .

[36]  S. Allakhverdiev,et al.  Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery , 2001, The EMBO journal.

[37]  J. Hirschberg,et al.  Carotenoid biosynthesis in flowering plants. , 2001, Current opinion in plant biology.

[38]  B. Milborrow The pathway of biosynthesis of abscisic acid in vascular plants: a review of the present state of knowledge of ABA biosynthesis. , 2001, Journal of experimental botany.

[39]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[40]  W. Chow,et al.  Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves , 2001, Planta.

[41]  B. Pogson,et al.  Genetic manipulation of carotenoid biosynthesis and photoprotection. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  K. Niyogi,et al.  The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[43]  K. V. van Wijk,et al.  Co-translational Assembly of the D1 Protein into Photosystem II* , 1999, The Journal of Biological Chemistry.

[44]  Hartmut K. Lichtenthaler,et al.  THE 1-DEOXY-D-XYLULOSE-5-PHOSPHATE PATHWAY OF ISOPRENOID BIOSYNTHESIS IN PLANTS. , 1999, Annual review of plant physiology and plant molecular biology.

[45]  A. Melis,et al.  Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage ? , 1999, Trends in plant science.

[46]  W. Vermaas,et al.  Chlorophyll a availability affects psbA translation and D1 precursor processing in vivo in Synechocystis sp. PCC 6803. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B. Demmig‐Adams,et al.  Survey of Thermal Energy Dissipation and Pigment Composition in Sun and Shade Leaves , 1998 .

[48]  A. Trebst,et al.  β‐Carotene to zeaxanthin conversion in the rapid turnover of the D1 protein of photosystem II , 1998, FEBS letters.

[49]  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.

[50]  A. Trebst,et al.  Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii , 1997, FEBS letters.

[51]  J. Feierabend,et al.  Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction-center protein D1 in mature rye leaves , 1996, Planta.

[52]  G. Britton,et al.  Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. , 1996, The Plant cell.

[53]  E. Tyystjärvi,et al.  The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. Robinson,et al.  Photosystem II Regulation and Dynamics of the Chloroplast D1 Protein in Arabidopsis Leaves during Photosynthesis and Photoinhibition , 1995, Plant physiology.

[55]  J. Thornber,et al.  Analysis of the Pigment Stoichiometry of Pigment-Protein Complexes from Barley (Hordeum vulgare) (The Xanthophyll Cycle Intermediates Occur Mainly in the Light-Harvesting Complexes of Photosystem I and Photosystem II) , 1995, Plant physiology.

[56]  J. Anderson,et al.  Recovery from Photoinhibition in Peas (Pisum sativum L.) Acclimated to Varying Growth Irradiances (Role of D1 Protein Turnover) , 1994, Plant physiology.

[57]  J. Kim,et al.  Chlorophyll Regulates Accumulation of the Plastid-Encoded Chlorophyll Proteins P700 and D1 by Increasing Apoprotein Stability , 1994, Plant physiology.

[58]  J. Anderson,et al.  Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. , 1993, The Journal of biological chemistry.

[59]  R. Bassi,et al.  Carotenoid-binding proteins of photosystem II. , 1993, European journal of biochemistry.

[60]  E. Tyystjärvi,et al.  Slow degradation of the d1 protein is related to the susceptibility of low-light-grown pumpkin plants to photoinhibition. , 1992, Plant physiology.

[61]  W. W. Adams,et al.  Carotenoid composition in sun and shade leaves of plants with different life forms , 1992 .

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

[63]  J. Snel,et al.  The use of chlorophyll fluorescence nomenclature in plant stress physiology , 1990, Photosynthesis Research.

[64]  O. Björkman,et al.  Leaf Xanthophyll content and composition in sun and shade determined by HPLC , 1990, Photosynthesis Research.

[65]  W. Chow,et al.  Thylakoid Membrane Organisation in Sun/Shade Acclimation , 1988 .

[66]  J. Anderson,et al.  Biosynthesis and Possible Functional Relationships Among the Carotenoids; and Between Chlorophyll a and Chlorophyll b. , 1959, Plant physiology.

[67]  H. Lichtenthaler,et al.  Incorporation of 14CO2 in photosynthetic pigments of Chlorella pyrenoidosa , 2004, Planta.

[68]  H. Frank,et al.  Carotenoid photooxidation in photosystem II. , 2001, Archives of biochemistry and biophysics.

[69]  P. Bramley Inhibition of carotenoid biosynthesis , 1993 .