Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures.

Chromoplast development in ripening bell pepper fruits is characterized by a massive synthesis of carotenoid pigments, resulting in their distinctive red color. We have shown that 95% of these pigments accumulate in chromoplasts in specific lipoprotein fibrils. In addition to carotenoids, purified fibrils contain galactolipids, phospholipids, and a single, 32-kD protein, designated fibrillin, which has antigenically related counterparts in other species. Fibrils were reconstituted in vitro when purified fibrillin was combined with carotenoids and polar lipids in the same stoichiometric ratio found in fibrils in vivo. Antibodies directed against fibrillin were used to isolate a fibrillin cDNA clone and, in immunological studies, to follow its accumulation during the chloroplast-to-chromoplast transition under different conditions. A model for fibril architecture is proposed wherein carotenoids accumulate in the center of the fibrils and are surrounded by a layer of polar lipids, which in turn are surrounded by an outer layer of fibrillin. Topological analysis of purified fibrils verified this structure. Collectively, these results suggest that the process of fibril self-assembly in chromoplasts is an example of a general phenomenon shared among cells that target excess membrane lipids into deposit structures to avoid their destabilizing or toxic effects. In addition, we have shown that abscisic acid stimulates this phenomenon in chromoplasts, whereas gibberellic acid and auxin delay it.

[1]  G. Bahr Osmium tetroxide and ruthenium tetroxide and their reactions with biologically important substances. Electron stains. III. , 1954, Experimental cell research.

[2]  A. Frey-wyssling,et al.  The submicroscopic development of chromoplasts in the fruit of Capsicum annuum L. , 1958, Journal of ultrastructure research.

[3]  Y. Ben-Shaul,et al.  Development and Structure of Carotene Bodies in Carrot Roots , 1965, Botanical Gazette.

[4]  J. Thiery Mise en evidence des polysaccharides sur coupes fines en microscopie electronique , 1967 .

[5]  A. Spurr,et al.  ULTRASTRUCTURE OF CHLOROPLASTS AND CHROMOPLASTS IN CAPSICUM ANNUUM I. THYLAKOID MEMBRANE CHANGES DURING FRUIT RIPENING , 1968 .

[6]  A. Spurr,et al.  CHROMOPLASTS OF TOMATO FRUITS. II. THE RED TOMATO , 1969 .

[7]  A. Spurr,et al.  CHROMOPLASTS OF TOMATO FRUITS. I. ULTRASTRUCTURE OF LOW‐PIGMENT AND HIGH‐BETA MUTANTS. CAROTENE ANALYSES , 1969 .

[8]  C. Coggins,et al.  Lycopene Accumulation Induced by 2-(4-Chlorophenylthio)-Triethylamine Hydrochloride , 1970, Science.

[9]  H. Kuhn Chemismus, Struktur und Entstehung der Carotinkriställchen in der Nebenkrone von Narcissus poeticus L. var. ‘La Riante’ , 1970 .

[10]  A. Scanu Structural studies on serum lipoproteins , 1972 .

[11]  Jeng-Sheng Huang,et al.  RECONSTITUTION OF A MEMBRANE‐LIKE STRUCTURE WITH STRUCTURAL PROTEINS AND LIPIDS ISOLATED FROM TOBACCO THYLAKOID MEMBRANES , 1973 .

[12]  A. Benson,et al.  Isolation and properties of the envelope of spinach chloroplasts. , 1973, The Journal of biological chemistry.

[13]  A. Spurr,et al.  CHROMOPLAST ULTRASTRUCTURE AS AFFECTED BY GENES CONTROLLING GRANA RETENTION AND CAROTENOIDS IN FRUITS OF CAPSICUM ANNUUM , 1973 .

[14]  P. K. Jensen,et al.  Isolation of lipid particles from baker's yeast , 1974, FEBS letters.

[15]  D. Simpson,et al.  Chemical Regulation of Plastid Development. II.* Effect of CPTA on the Ultrastructure and Carotenoid Composition of Chromoplasts of Capsicum annuum Cultivars , 1974 .

[16]  M. Baqar,et al.  Ultrastructure and Carotenoid Composition of Chromoplasts of the Sepals of Strelitzia reginae Aiton during Floral Development , 1975 .

[17]  H. Wuttke Chromoplasts in Rosa rugosa: Development and Chemical Characterization of Tubular Elements , 1976 .

[18]  T. H. Lee,et al.  The fine structure and formation of fibrils of Capsicum annuum L. chromoplasts , 1976 .

[19]  M. Baqar,et al.  Chromoplast ultrastructure of Capsicum carotenoid Mutants I. Ultrastructure and carotenoid composition of a new mutant , 1977 .

[20]  M. Baqar,et al.  Fine Structure and Carotenoid Composition of the Fibrillar Chromoplasts of Asparagus officinalis L. , 1977 .

[21]  N. Ljubešić The Formation of Chromoplasts in Fruits of Cucurbita maxima Duch. 'Turbaniformis' , 1977, Botanical Gazette.

[22]  L. W. Parks,et al.  Metabolic interconversion of free sterols and steryl esters in Saccharomyces cerevisiae , 1978, Journal of bacteriology.

[23]  B. Camara,et al.  Free and esterified carotenoids in green and red fruits of Capsicum annuum , 1978 .

[24]  J. M. Whatley,et al.  Development of Nongreen Plastids , 1980 .

[25]  K. Miller,et al.  Addition of lipid to the photosynthetic membrane: effects on membrane structure and energy transfer , 1981, The Journal of cell biology.

[26]  T. Takagi,et al.  Biochemical studies on carotenoids. part X. Further studies on the acquisition of novel optical activity on interaction of lutein and other carotenoids with proteins. , 1981 .

[27]  T. Takagi,et al.  Further Studies on the Acquisition of Novel Optical Activity on Interaction of Lutein and Other Carotenoids with Proteins , 1981 .

[28]  A. Ben‐Amotz,et al.  ACCUMULATION OF β‐CAROTENE IN HALOTOLERANT ALGE: PURIFICATION AND CHARACTERIZATION OF β‐CAROTENE‐RICH GLOBULES FROM DUNALIELLA BARDAWIL (CHLOROPHYCEAE) 1 , 1982 .

[29]  S. Golden,et al.  Cloning of Photosynthesis Genes from the Cyanobacterium Anacystis Nidulans R2 , 1984 .

[30]  B. Camara [31] Prenylation of chlorophyllide a in Capsicum plastids , 1985 .

[31]  B. Camara [28] Carotene synthesis in Capsicum chromoplasts , 1985 .

[32]  L. Sherman,et al.  Identification of a carotenoid-binding protein in the cytoplasmic membrane from the heterotrophic cyanobacterium Synechocystis sp. strain PCC6714 , 1986, Journal of bacteriology.

[33]  H. Riethman,et al.  Isolation and Characterization of a Carotenoid-Associated Thylakoid Protein from the Cyanobacterium Anacystis nidulans R2. , 1987, Plant physiology.

[34]  A. Huang,et al.  The major protein from lipid bodies of maize. Characterization and structure based on cDNA cloning. , 1987, The Journal of biological chemistry.

[35]  H F Kern,et al.  Selection of AUG initiation codons differs in plants and animals. , 1987, The EMBO journal.

[36]  G. Schmidt,et al.  Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Y. Meyer,et al.  Preparation by two‐dimensional electrophoresis of proteins for antibody production: Antibodies against proteins whose synthesis is reduced by auxin in tobacco mesophyll protoplasts , 1988, Electrophoresis.

[38]  C. Price,et al.  Chromoplast-Specific Proteins in Capsicum annuum. , 1988, Plant physiology.

[39]  L. Newman,et al.  Synthesis of Two Chromoplast-Specific Proteins During Fruit Development in Capsicum annuum. , 1989, Plant physiology.

[40]  L. Newman,et al.  ChrA Is a Carotenoid-Binding Protein in Chromoplasts of Capsicum annuum. , 1990, Plant physiology.

[41]  Y. Lai,et al.  Oleosin isoforms of high and low molecular weights are present in the oil bodies of diverse seed species. , 1990, Plant physiology.

[42]  J. Labavitch,et al.  Comparison of ripening processes in intact tomato fruit and excised pericarp discs. , 1990, Plant physiology.

[43]  J. Rivas,et al.  ISOLATION OF A YELLOW CAROTENOPROTEIN FROM CARROT , 1991 .

[44]  E. Krejci,et al.  Cholinesterase-like domains in enzymes and structural proteins: functional and evolutionary relationships and identification of a catalytically essential aspartic acid. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Ginsberg,et al.  Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. , 1991, Trends in biochemical sciences.

[46]  F. Tablin,et al.  Bovine platelets contain a 280 kDa microtubule-associated protein antigenically related to brain MAP 2. , 1991, European journal of cell biology.

[47]  J. Erdman,et al.  Isolation and partial characterization of .alpha.- and .beta.-carotene-containing carotenoprotein from carrot (Daucus carota L.) root chromoplasts , 1992 .

[48]  J. Tzen,et al.  Surface structure and properties of plant seed oil bodies , 1992, The Journal of cell biology.

[49]  M. Kuntz,et al.  Cysteine synthase from Capsicum annuum chromoplasts. Characterization and cDNA cloning of an up-regulated enzyme during fruit development. , 1992, The Journal of biological chemistry.

[50]  L. J. Smith,et al.  Secondary structures of a new class of lipid body proteins from oilseeds. , 1992, The Journal of biological chemistry.

[51]  M. Kuntz,et al.  Identification of a cDNA for the plastid-located geranylgeranyl pyrophosphate synthase from Capsicum annuum: correlative increase in enzyme activity and transcript level during fruit ripening. , 1992, The Plant journal : for cell and molecular biology.

[52]  J. Battey,et al.  Regulation of chlorophyll apoprotein expression and accumulation. Requirements for carotenoids and chlorophyll. , 1992, The Journal of biological chemistry.

[53]  C. Dahlin Import of nuclear‐encoded proteins into carotenoid‐deficient young etioplasts , 1993 .

[54]  Laurence Gondet Caracterisation biochimique et cytochimique d'un mutant de tabac (nicotiana tabacum l. ) surproducteur de sterols , 1993 .

[55]  M. Kuntz,et al.  Expression of the genes encoding the early carotenoid biosynthetic enzymes in Capsicum annuum. , 1993, Biochemical and biophysical research communications.

[56]  B. Camara [32] Plant phytoene synthase complex: Component enzymes, immunology, and biogenesis , 1993 .

[57]  R. Croteau,et al.  Terpenoid metabolism. , 1995, The Plant cell.