Summary
Plastid development in ‘yellow-in-the-dark’ strains of Chlamydomonas reinhardtii provides a unique system to investigate assembly of light-harvesting complexes (LHC) in situ. The ultrastructure of the plastid in degreened cells exposed to only a few minutes of light at 38°C indicated that thylakoid membrane formation was initiated by expansion of the envelope. The kinetics of accumulation of LHCII were consistent with assembly of the complex concomitant with import of the apoproteins into the chloroplast. The initial fluorescence of newly formed LHCII was quenched within the first minute of greening as the energy transducing system also assembled within initial membranes. Most of the chlorophyll (Chl) in early greening cells was distributed in foci at the periphery of the chloroplast. In such cells, LHCII apoproteins were detected adjacent to the inner surface of the envelope by immunoelectron microscopy. Interestingly, LHCII apoproteins were also detected outside of the chloroplast in vacuoles, rather than in the chloroplast stroma, when synthesized in the absence of synthesis of Chl. Wall-deficient cw15 cells, grown in the light or dark at 28°C, contain large granules within these vacuoles that were immunoreactive to antibodies against LHCII apoproteins. In a Chl b-less strain, cbn1-113 arg2 y, which is an algal analogue of chlorina mutants of plants when grown in medium lacking acetate, LHCII apoproteins accumulated also in cytoplasmic vacuoles. The apoproteins were quantitatively recovered as the mature-sized species in each case, which suggested that even those outside of the chloroplast were processed. A possible interpretation of these results is that assembly of LHCII in the chloroplast envelope, by association of apoproteinswith Chl and xanthophylls, is required to prevent retrogrademovement of the proteins into the cytosol.
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Abbreviations
- CHL:
-
chlorophyll
- Chlide:
-
chlorophyllide
- LHC:
-
light-harvesting complexes
- LHCII:
-
light-harvesting
- Chl a/b:
-
protein complexes
- Pchlide:
-
protochlorophyllide
- PS I:
-
Photosystem I
- PS II:
-
Photosystem II
References
Allen KD and Staehelin LA (1994) Polypeptide composition, assembly and phosphorylation patterns of the Photosystem II antenna system of Chlamydomonas reinhardtii. Planta 194: 42–54
Bassi R and Wollman F-A (1991) The chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtii. Planta 183: 423–433
Bassi R, Soen SY, Grank, G, Zuber H and Rochaix J-D (1992) Characterization of chlorophyll a/b proteins of Photosystems I from Chlamydomonas reinhardtii. J Biol Chem 267: 25714–25721
Bellemare G, Bartlett SG and Chua N-H (1982) Biosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barley. J Biol Chem 257: 7762–7767
Bishop NI (1996) The β,ε-carolenoid, lutein, is specifically required for the formation of the oligomeric forms of the light harvesting complex in the green alga, Scenedesmus obliquus. J Photochem Photobiol B: Biol 36: 279–283
Booth PJ and Paulsen H (1996) Assembly of light-harvesting chlorophyll a/b complexes in vitro. Time-resolved fluorescence measurements. Biochemistry 35: 5103–5108
Cammarata KV, Schmidt V, Tamura W and Schmidt GW (1997) Reconstitution of partially-assembled light-harvesting complexes. Plant Physiol 114 (Suppl.): 206
Chitnis PR, Harel E, Kohorn BD, Tobin EM and Thornber JP (1986) Assembly of the precursor and processed light-harvesting chlorophyll a/b protein of Lemna into the light-harvesting complex II of barley etiochloroplasts. J Cell Biol 102: 982–988
Chory J, Chatterjee M, Cook RK, Elich T, Fankhauser C, Li J, Nagpal P, Neff M, Pepper A, Poole D., Reed J and Vitart V (1996) From seedgermination to flowering, light controls plant development via the pigment phytochrome. Proc Natl Acad Sci USA 93: 12066–12071
Chunaev AS, Mirnaya ON, Maslov VG and Boschetti A (1991) Chlorophyll b-and loroxanthin-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica 25: 291–301
Cline K and Henry R (1996) Import and routing of nucleus-encoded chloroplast proteins. Ann Rev Cell Devel Biol 12: 1–26
Cline K, Fulsom DR and Viitanen PV (1989) An imported thylakoid protein accumulates in the stroma when insertion into thylakoids is inhibited. J Biol Chem 264: 14225–14232
Connelly JP, Müller MG, Bassi R, Croce R and Holzwarth AR (1997) Femtosecond transient absorptionstudy of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of Photosystem II. Biochemistry 36: 281–288
Davies DR and Plaskitt A (1971) Genetic and structural analysis of cell-wallformation in Chlamydomonas reinhardi. Genet Res 17: 33–43
Douce R and Joyard J (1990) Biochemistry and function of the plastid envelope. Annu Rev Cell Biol 6: 173–216
Dreyfuss BW and Thornber JP (1994a) Assembly of thelight-harvesting complexes (LHCs) of Photosystem II. Plant Physiol 106: 829–839
Dreyfuss BW and Thornber JP (1994b) Organization of the light-harvesting complex of Photosystem I and its assembly during plastid development. Plant Physiol 106: 841–848
Green BR and Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47: 685–714
Hagen SJ, Hofrichter J, Szabo A and Eaton WA (1996) Diffusion-limited contact formation in unfolded cytochrome c: Estimating the maximum rate of protein folding. Proc Natl Acad Sci USA 93: 11615–11617
Heinze I, Pfündel E, Hühn M and Dau H (1997) Assembly of light-harvesting complexes II (LHC-II) in the absence of lutein. A study on the-carotenoid-free mutant C-2A′-34 of the green alga Scenedesmus obliquus. Biochim Biophys Acta 1320: 188–194
Henningsen KW and Boynton JE (1969) Macromolecular physiology of plastids. VII. The effect of a brief illumination on plastids of dark-grown barley leaves. J Cell Sci s5: 757–793
Henningsen KW and Boynton JE (1970) Macromolecular physiology of plastids. VIII. Pigment and membrane formation in plastids of barley greening under low light intensity. J Cell Biol 44: 290–304
Henningsen KW and Boynton JE (1974) Macromolecular physiology of plastids. IX. Development of plastid membranes during greening of dark-grown barley seedlings. J Cell Sci 15: 31–55
High S, Henry R, Mould RM, Valent Q, Meacock S, Cline K, Gray JC and Luirink J (1997) Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J Biol Chem 272: 11622–11628
Hobe S, Prytulla S, Kühlbrandt W and Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13: 3423–3429
Hobe S, Förster, Klinger J and Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34: 10224–10228
Hoober JK (1972) A major polypeptide of chloroplast membranes of Chlamydomonas reinhardi. J Cell Biol 52: 84–96
Hoober JK (1987) The molecular basis of chloroplast development. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, Vol 10, Photosynthesis, pp 1–74. Academic Press, San Diego
Hoober JK and Stegeman WH (1976) Kinetics and regulation of synthesis of the major polypeptides of thylakoid membranes in Chlamydomonas reinhardtii y-1 at elevated temperatures. J Cell Biol 70: 326–337
Hoober JK, Marks DB, Keller BJ and Margulies MM (1982) Regulation of accumulation of the major thylakoid polypeptides in Chlamydomonas reinhardtii y-1 at 25 °C and 38 °C. J Cell Biol 95: 552–558
Hoober JK, Boyd CO and Paavola LG (1991) Origin of thylakoid membranes in Chlamydomonas reinhardtii y-1 at 38 °C. Plant Physiol 96: 1321–1328
Hoober JK, Maloney MA, Asbury LR and Marks DB (1990) Accumulation of chlorophyll a/b-binding polypeptides in Chlamydomonas reinhardtii y-1 in the light or dark. Plant Physiol 92: 419–426
Hoober JK, White RA, Marks DB and Gabriel JL (1994) Biogenesis of thylakoid membranes with emphasis on the process in Chlamydomonas. Photosynth Res 39: 15–31
Hwang S and Herrin DL (1993) Characterization of a cDNA encoding the 20-kDa Photosystem I light-harvesting polypeptide of Chlamydomonas reinhardtii. Curr Genet 3: 512–517
Imbault P, Wittemer C, Johanningmeier U, Jacobs JD and Howell SH (1988) Structure of the Chlamydomonas reinhardtii cabII-1 gene encoding a chlorophyll-a/b-binding protein. Gene 73: 397–407
Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1–19
Kohorn BD, Harel E., Chitnis PR, Thornber JP and Tobin EM (1986) Functional and mutational analysis of the light-harvesting chlorophyll a/b protein of thylakoid membranes. J Cell Biol 102: 972–981
Komine Y, Park H, Wolfe GR and Hoober JK (1996) Secretory granules in the cytoplasm of a wall-less mutant of Chlamydomonas reinhardtii contain processed light-harvesting complex apoproteins and Hsp70. J Photochem Photobiol B: Biol 36: 301–306
Kühlbrandt W and Wang DN (1991) Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350: 130–134
Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621
Kuttkat A, Hartmann A, Kobe S and Paulsen H (1996) The C-terminal domain of light-harvesting chlorophyll-a/b-binding protein is involved in the stabilisation of trimeric light-harvesting complex. Eur J Biochem 242: 288–292
Li J and Timko MP (1996) The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH: protochlorophyllide oxidoreductase. Plant Mol Biol 30: 15–37
Li X, Henry R, Yuan J, Cline K and Hoffman NE (1995) A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a proteininto thylakoid membranes. Proc Natl Acad Sci USA 92: 3789–3793
Malnoe P, Mayfleld SP and Rochaix J-D (1988) Comparative analysis of the biogenesis of Photosystem II in the wild-type and y-1 mutant of Chlamydomonas reinhardtii. J Cell Biol 106: 609–616
Maloney MA, Hoober JK and Marks DB (1989) Kinetics of chlorophyll accumulation and formation of chlorophyll-protein complexesduringgreening of Chlamydomonas reinhardtii y-1 at 38 °C. Plant Physiol 91: 1100–1106
Marks DB, Keller BJ and Hoober JK (1985) In vitro processing of precursors of thylakoid membrane proteins of Chlamydomonas reinhardtii y-1. Plant Physiol 79: 108–113
Michel H, Tellenbach M and Boschetti A (1983) A chlorophyll b-less mutant of Chlamydomonas reinhardtii lacking in the light-harvesting chlorophyll a/b-protein complex but not in its apoproteins. Biochim Biophys Acta 725: 417–424
Nussberger S, Dörr K, Wang DN and Kühlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234: 347–356
Ohad I, Siekevitz P and Palade GE (1967a) Biogenesis of chloroplast membranes. I Plastid dedifferentiation of a dark-grown algal mutant (Chlamydomonas reinhardi). J Cell Biol 35: 521–552
Ohad I, Siekevitz P and Palade GE (1967b) Biogenesis of chloroplast membranes. II Plastid differentiation during greening of a dark-grown algalmutant (Chlamydomonas reinhardi). J Cell Biol 35: 553–584
Ohlrogge J and Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957–970
Park H and Hoober JK (1997) Chlorophyll synthesis modulates retention of LHCII apoproteins by the chloroplast in Chlamydomonas reinhardtii. Physiol Plant 101: 135–142
Payen LA and Cline K (1991) A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J Cell Biol 112: 603–613
Paulsen H, Finkenzeller B and Kühlein N (1993) Pigments induce folding of light-harvesting chlorophyll a/b-binding protein. Eur J Biochem 215: 809–816
Peter GF and Thornber JP (1991) Biochemical composition and organization of higher plant PhotosystemII light-harvesting pigment-proteins. J Biol Chem 266: 16745–16754
Plumley FG and Schmidt GW (1987) Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci USA 84: 146–150
Plumley FG and Schmidt GW (1995) Light-harvesting chlorophyll a/b complexes: Interdependent pigment synthesis and protein assembly. Plant Cell 7: 689–704
Plumley FG, Douglas SE, Branagan-Switzer A and Schmidt GW (1989) Nitrogen-dependent biogenesis of chlorophyll-protein complexes. In: Briggs WR (ed) Photosynthesis, pp 311–329. Alan R Liss, New York
Plumley FG, Martinson TA, Herrin DL, Ikeuchi M and Schmidt GW (1993) Structural relationships of the Photosystem I and Photosystem II chlorophyll a/b and a/c light-harvesting apoproteins of plants and algae. Photochem Photobiol 57: 143–151
Pogson B, McDonald DA, Truong M, Britton G and DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8: 1627–1639
Preiss S and Thornber JP (1995) Stability of the apoproteins of light-harvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant chlorina f2. Plant Physiol 107: 709–717
Rawyler A, Meylan-Bettex M and Siegenthaler PA (1995) (Galacto)lipid export from envelope to thylakoid membranes in intact chloroplasts. II A general process with a key role for the envelope in the establishment of lipid asymmetry in thylakoid membranes. Biochim Biophys Acta 1233: 123–133
Reed JE, Cline K, Stephens LC, Bacot KO and Viitanen PV (1990) Early events in the import/assembly pathway of an integral thylakoid protein. Eur J Biochem 194: 33–42
Sager R (1955) Inheritance in the green alga Chlamydomonas reinhardi. Genetics 40: 476–489
Sager R and Palade GE (1957) Structure and development of the chloroplast in Chlamydomonas, I. The normal green cell. J Biochem Biophys Cytol 3: 463–487
Sato N, Sonoike K, Kawaguchi A and Tsuzuki M (1996) Contribution of lowered unsaturation levels of chloroplast lipids to high temperature tolerance of photosynthesis in Chlamydomonas reinhardtii. J. Photochem Photobiol B: Biol 36: 333–337
Schnell DJ and Blobel G (1993) Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J Cell Biol 120: 103–115
Scott SV and Theg SM (1996) A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: Energetics and mechanistic implications. J Cell Biol 132: 63–75
Silva-Filho M de C, Wieërs M-C, Flügge U-I, Chaumont F and Boutry M (1997) Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane protein. J Biol Chem 272: 15264–15269
Su Q and Boschetti A (1993) Partial purification and properties of enzymes involved in the processing of a chloroplast import protein from Chlamydomonas reinhardtii. Eur J Biochem 17: 1039–1047
Terao T and Katoh S (1989) Synthesis and breakdown of the apoproteins of light-harvesting chlorophyll a/b proteins in chlorophyll b-deficient mutants of rice. Plant Cell Physio 30: 571–580
VanderVere PS, Bennett TM, Oblong JE and Lamppa GK (1995) A chloroplast processing enzyme involved in precursor maturation shares a zin c-binding motif with a recently recognized family of metalloendopeptidases. Proc Natl Acad Sci USA 92: 7177–7181
Wei N and Deng X-W (1996) The role of the COP/DET/FUS genes in light control of Arabidopsis seedling development. Plant Physiol 112: 871–878
Whatley JM, Hawes CR, Home JC and Kerr JDA (1982) The establishment of the plastid thylakoid system. New Phytol 90: 619–629
White RA and Hoober JK (1994) Biogenesis of thylakoid membranes in Chlamydomonas reinhardtii y1. A kinetic study of initial greening. Plant Physiol 106: 583–590
White RA, Wolfe GR, Komine Y and Hoober JK (1996) Localization of light-harvesting complex apoproteins in the chloroplast and cytoplasm during greening of Chlamydomonas reinhardtii at 38 °C. Photosynth Res 47: 267–280
Wolfe GR, Park H, Sharp WP and Hoober JK (1997) Light-harvesting complex apoproteins in cytoplasmic vacuoles in Chlamydomonas reinhardtii (Chlorophyta). J. Phycol 33: 377–386
Yuan J, Henry R and Cline K (1993) Stromal factor plays a essential role in protein integration into thylakoids that cannot be replaced by unfolding or by heat shock protein Hsp70. Proc Natl Acad Sci USA 90: 8552–8556
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Hoober, J.K., Park, H., Wolfe, G.R., Komine, Y., Eggink, L.L. (1998). Assembly of Light-Harvesting Systems. In: Rochaix, J.D., Goldschmidt-Clermont, M., Merchant, S. (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Advances in Photosynthesis and Respiration, vol 7. Springer, Dordrecht. https://doi.org/10.1007/0-306-48204-5_19
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