Multiple light-harvesting II polypeptides from maize mesophyll chloroplasts are distinct gene products

Journal of Photochemistry and Photobiology B: Biology

Volumn 49, Issue 1, 1999, Pages 50-60

  De Luca, Claudio ^a,d   Varotto, Claudio ^b,e   Svendsen, Ib ^c   De Laureto, Patrizia Polverino ^a   Bassi, Roberto ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c CARLSBERG LABORATORY   (Denmark)

^d Max Plack Institut für Z ^*  (Italy)

^e MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Chlorophyll proteins; lhcb genes; Photosynthesis

Indexed keywords

APOPROTEIN; CHLOROPHYLL; GENE PRODUCT; PIGMENT; POLYPEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CHLOROPLAST; ISOELECTRIC FOCUSING; MAIZE; NONHUMAN; PHOTOSYSTEM II; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; SPECTROSCOPY;

AMINO ACID SEQUENCE; APOPROTEINS; ARABIDOPSIS; CONSENSUS SEQUENCE; DNA, COMPLEMENTARY; HORDEUM; LIGHT-HARVESTING PROTEIN COMPLEXES; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; ZEA MAYS;

EMBRYOPHYTA; ZEA MAYS;

EID: 0033103073     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1011-1344(99)00016-0     Document Type: Article

References (64)

1. [1] A. Melis, J.M. Andersson, Structural and functional organization of the photosystem in spinach chloroplast. Antenna size, relative electron-transport capacity, and chlorophyll composition, Biochim. Biophys. Acta 724 (1983) 473-484.
2. [2] S.W. McCauley, A. Melis, Quantitation of photosystem II in spinach chloroplasts, Biochim. Biophys. Acta 489 (1986) 175-182.
3. [3] R. Bassi, G. Hoyer-Hansen, R. Barbato, G.M. Giacometti, D.J. Simpson, Chlorophyll-proteins of the photosystem II antenna system, J. Biol. Chem. 262 (1987) 13333-13341.
4. [4] P. Dainese, R. Bassi, Subunit stoichiometry of the chloroplast photosystem II antenna system and aggregation state of the component chlorophyll a/b binding proteins, J. Biol. Chem. 266 (1991) 8136-8142.
5. [5] R. Bassi, P.A. Dainese, Supramolecular light harvesting complex from the chloroplast photosystem II membranes, Eur. J. Biochem. 204 (1991) 317-326.
6. [6] G.F. Peter, J.P. Thornber, Biochemical composition and organization of higher plant photosystem II light harvesting pigment proteins, J. Biol. Chem. 266 (1991) 16745-16754.
7. [7] E.L. Camm, B.R. Green, The chlorophyll-a/b complex CP29 is associated with the photosystem II reaction center core, Biochim. Biophys. Acta 974 (1980) 180-184.
8. [8] R. Bassi, F. Rigoni, R. Barbato, G. Giacometti, Light-harvesting chlorophyll a/b protein (LHCII) population in phosphorylated membranes, Biochim. Biophys. Acta 936 (1988) 29-38.
9. [9] M. Sigrist, L.A. Stahehelin, Identification of type I and type II light harvesting a/b binding protein using monospecific antibodies, Biochim. Biophys. Acta 1098 (1992) 191-200.
10. [10] M.L. Di Paolo, A. Peruffo dal Belin, R. Bassi, Immunological studies on chlorophyll a/b proteins and their location in chloroplast membrane domains, Planta 181 (1990) 275-286.
11. [11] R. Bassi, G.M. Giacometti, D. Simpson, Changes in the composition of stroma lamellae following state 1-state 2 transition, Biochim. Biophys. Acta 935 (1988) 152-165.
12. [12] U.K. Larsson, C. Sundby, B. Andersson, Characterization of two different subpopulation of spinach light-harvesting chlorophyll a/b protein complex (LHCII): Polypeptide composition, phosphorylation pattern and association with Photosystem II, Biochim. Biophys. Acta 894 (1987) 59-68.
13. [13] K. Islam, The rate and extent of phosphorylation of the two light harvesting chlorophyll a/b binding protein complex (LHCII) polypeptides in isolated spinach thylakoids, Biochim. Biophys. Acta 893 (1987) 333-341.
14. [14] P. Dunsmuir, The petunia chlorophyll-a/b binding protein genes: a comparison of CAB genes from different gene families, Nucleic Acid Res. 13 (1985) 2503-2518.
15. [15] S. Jansson, P. Gustaffson, Type I and Type II genes for the chlorophyll a/b binding protein in the gymnosperm Pinus sylvestris (Scots pine): cDNA cloning and sequence analysis, Plant Mol. Biol. 14 (1990) 287-296.
16. [16] B.D. Kohorn, E. Harel, P.R. Chitnis, J.P. Thornber, E.M. Tobin, Functional and mutational analysis of the light harvesting chlorophyll a/b protein of thylakoid membranes, J. Cell. Biol. 102 (1986) 972-981.
17. [17] K. Cline, Import of proteins into chloroplasts, J. Biol. Chem. 261 (1986) 10804-10810.
18. [18] C. Dahlin, K. Cline, Developmental regulation of the plastid protein import apparatus, The Plant Cell 3 (1991) 1131-1140.
19. [19] S. Jansson, E. Seltman, P. Gustafsson, The rapidly phosphorylated 25 kDa polypeptide of the light-harvesting complex of photosystem II is encoded by the cab-II gene, Biochim. Biophys. Acta 1019 (1990) 110-114.
20. [20] J. Bennett, Phosphorylation of chloroplast membrane polypeptides, Nature 269 (1977) 344-346.
21. [21] E. Bergantino, P. Dainese, Z. Cerovic, S. Sechi, R. Bassi, A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress, J. Biol. Chem. 270 (1995) 8474-8481.
22. [22] A.K. Matoo, M. Edelman, Intermembrane translocation and post-translational palmitoylation of the chloroplast 32 kDa herbicide-binding protein of maize, Proc. Natl. Acad. Sci. USA 84 (1987) 1497-1501.
23. [23] G.K. Lamppa, M.S. Abad, Processing of a wheat light harvesting chlorophyll a/b protein precursor by a soluble enzyme from higher plants chloroplast, J. Cell. Biol. 105 (1987) 2641-2648.
24. [24] J.Y. Sheen, L. Bogorad, Differential expression of six light harvesting chlorophyll a/b binding protein genes in maize leaf cell types, Proc. Natl. Acad. Sci. USA 83 (1986) 7811-7815.
25. [25] D.A. Berthold, G.T. Babcock, C.F. Yocum, A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron transport properties, FEBS Lett. 134 (1981) 231-234.
26. [26] T.G. Dunahay, L.A. Staehelin, M. Seibert, P.D. Ogilvie, S.P. Berg, Structural, biochemical and biophysical characterization of four oxygen-evolving photosystem II preparations from spinach, Biochim. Biophys. Acta 764 (1984) 179-193.
27. [27] R. Bassi, O. Machold, D.J. Simpson, Chlorophyll proteins of two photosystem I preparations from maize, Carlsberg Res. Comm. 50 (1985) 145-162.
28. [28] H. Schaeger, G. von Jagow, Tricine sodium dodecylsulfate polyacrilamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166 (1987) 368-379.
29. [29] M.W. Hunkapiller, L.E. Hood, Analysis of phenilthiohydantoins by ultrasensitive gradient high-performance liquid chromatography, Methods Enzymol. 91 (1983) 486-494.
30. [30] E. Gross, B. Witkop, Selective cleavage of the methionyl peptide bonds in ribonuclease with cyanogen bromide, J. Am. Chem. Soc. 83 (1961) 1510-1511.
31. [31] P. Madsudaira, Sequence from picomole quantities of protein electroblotted onto polyvinylidene-difluoride membranes, J. Biol. Chem. 262 (1987) 10035-10038.
32. [32] P.A. Edman, Method for the determination of the aminoacid sequence in peptides, Acta Chem. Scand. 4 (1950) 283-293.
33. [33] P. Dainese, G. Hoyer-Hansen, R. Bassi, The resolution of chlorophyll a/b binding proteins by a preparative method based on flat bed iso-electric focusing, Photochem. Photobiol. 51 (1990) 693-703.
34. [34] C. Santini, V. Tidu, G. Tognon, A.G. Magaldi, R. Bassi, Three-dimensional structure of the higher-plant photosystem II reaction center and evidence for its dimeric organization in vivo, Eur. J. Biochem. 221 (1994) 307-315.
35. [35] R.J. Porra, W.A. Thompson, P.E. Kriedemann, 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, Biochim. Biophys. Acta 975 (1989) 384-394.
36. [36] R. Bassi, B. Pineau, P. Dainese, J. Marquardt, Carotenoid-binding proteins of photosystem-II, Eur. J. Biochem. 212 (1993) 297-303.
37. [37] M.S. Abad, J.E. Oblong, G.K. Lamppa, Soluble chloroplast enzyme cleaves pre-LHCP made in Escherichia coli to a mature form lacking a basic N-terminal domain, Plant Physiol. 96 (1991) 1220-1227.
38. [38] B.I. Stepanov, A universal relation between the absorption and luminescence spectra of complex molecules, Sov. Phys. Dokl. 2 (1957) 81-84.
39. [39] G. Zucchelli, F. Garlaschi, R. Croce, R. Bassi, R.C. Jennings, A Stepanov relation analysis of the steady state absorption and fluorescence spectra in the isolated D1/D2/cytochrome b559 complex, Biochim. Biophys. Acta 1229 (1995) 59-63.
40. [40] M.A. Harrison, A. Melis, Organization and stability of polypeptides associated with the chlorophyll a/b light harvesting complex of photosystem II, Plant Cell Physiol. 33 (1992) 627-637.
41. [41] S. Jansson, E. Pichersky, R. Bassi, B.R. Green, M. Ikeuki, A. Melis, D.J. Simpson, M. Spangforth, L.A. Staehelin, J.P. Thornber, A nomenclature for the genes encoding the chlorophyll a/b binding proteins of higher plants, Plant Mol. Biol. Reporter 10 (1992) 242-253.
42. [42] D. Morishige, J.P. Thornber, Correlation of apoprotein with the genes of the major chlorophyll a/b binding proteins of photosystem II in Arabidopsis thaliana. Confirmation for the presence of a third member of the LHC IIb gene family, FEBS Lett. 293 (1991) 183-187.
43. [43] R. Bassi, P. Dainese, Reorganization of Thylakoid membrane lateral heterogeneity following state I-state II transition, in: J.H. Argyroudy-Akoyonoglou (Ed.), Regulation of Chloroplast Biogenesis, Plenum, New York, 1992, pp. 511-520.
44. [44] E. Schwarz, R. Stasys, R. Aebersold, J.M. McGrath, B.R. Green, E. Pichersky, Sequence of a tomato gene encoding a third type of LHCII chlorophyll a/b binding polypeptide, Plant Mol. Biol. 17 (1991) 923-925.
45. [45] J. Brandt, A.M. Skovgaard, V. Nielsen, H. Thordal-Christensen, D. Simpson, S. Oekkels, A barley cDNA clone encoding a type III chlorophyll a/b binding polypeptide of the light harvesting complex II, Plant Mol. Biol. 19 (1992) 699-703.
46. [46] M.S. Abad, J.E. Oblong, G.K. Lamppa, Properties of a chloroplast enzyme that cleaves the chlorophyll a/b binding protein precursor, Plant Physiol. 90 (1989) 117-124.
47. [47] I.M. Johansson, C. Forsman, Processing of the chloroplast transit peptide of pea carbonic anhydrase in chloroplasts and in Escherichia coli. Indication of two cleavage sites, FEBS Lett. 314 (1992) 232-236.
48. [48] M. Matsuoka, Y. Kano-Murakami, N. Yamamoto, Nucleotide sequence of cDNA encoding the light-harvesting chlorophyll-a/b binding protein from maize, Nucleic Acid Res. 15 (1987) 6302.
49. [49] T.D. Sullivan, A.H. Christensen, P.H. Quail, Isolation and characterization of a maize chlorophyll a/b binding protein gene that produces high levels of mRNA in the dark, Mol. Gen. Genet. 215 (1989) 431-440.
50. [50] J.F. Viret, M.L. Schantz, R. Schantz, Nucleotide sequence of maize cDNA coding for a Light Harvesting chlorophyll a/b binding protein of photosystem II, Nucleic Acid. Res. 18 (1990) 71-79.
51. [51] T.W. Becker, T.S. Templeman, J.F. Viret, L. Bogorad, The cab-m7 gene: a light inducible, mesophyll-specific gene of maize, Plant Mol. Biol. 20 (1992) 49-60.
52. [52] M.E. Knight, J.A. Ray, W. Schuch, Isolation of a gene from maize encoding a chlorophyll a/b binding protein, Plant Mol. Biol. 19 (1992) 533-536.
53. [53] D.S. Demmin, E.J. Stockinger, Y.C. Chang, L.L. Walling, Phylogenetic relationships between the chlorophyll a/b binding protein (Cab) multigene family: an intra-and inter-species study, J. Mol. Evol. 29 (1989) 266-279.
54. [54] J. Bennett, Chloroplast protein phosphorylation, Ann. Revs. Plant Physiol. Plant Mol. Biol. 42 (1991) 281-311.
55. [55] W. Kuhlbrandt, D.N. Wang, Three-dimensional structure of plant light-harvesting complex determined by electron crystallography, Nature 350 (1991) 130-135.
56. [56] J.F. Allen, Protein phosphorylation in regulation of photosynthesis, Biochim. Biophys. Acta 1098 (1992) 275-335.
57. [57] A. Nilsson, D. Stys, T. Drakenberg, M.D. Spangfort, S. Forsen, J.F. Allen, Phosphorylation controls the three-dimensional structure of plant light harvesting complex II, J. Biol. Chem. 272 (1997) 18350-18357.
58. [58] R. Van Grondelle, J.P. Dekker, T. Gillbro, V. Sundström, Energy transfer and trapping in photosynthesis, Biochim. Biophys. Acta 1187 (1994) 1-65.
59. [59] R.C. Jennings, R. Bassi, G. Zucchelli, Antenna structure and energy transfer in higher plant photosystems, in: J.D. Dunitz, K. Hafner, S. Ito, J.-M. Lehn, K.M. Raymond, C.W. Rees, J. Thiem, F. Vögtle (Eds.), Topics in Current Chemistry, vol. 177, Electron Transfer II, Springer, Berlin, 1996, pp. 147-181.
60. [60] W. Kühlbrandt, D.N. Wang, Y. Fujiyoshi, Atomic model of plant light-harvesting complex by electron crystallography, Nature 367 (1994) 614-621.
61. [61] E. Giuffra, G. Zucchelli, D. Sandonà, R. Croce, D. Cugini, F.M. Garlaschi, R. Bassi, R.C. Jennings, Analysis of some optical properties of a native and reconstituted photosystem II antenna complex, CP29: pigment binding sites can be occupied by chlorophyll a or chlorophyll b and determine spectral forms, Biochemistry 36 (1997) 12984-12993.
62. [62] A. Pagano, G. Cinque, R. Bassi, In vitro refolding of the recombinant photosystem II subunit CP24 (Lhcb6): identification of chlorophyll a and chlorophyll b absorptions, J. Biol. Chem. 273 (1998) 17154-17165.
63. [63] B. Demmig-Adams, W.W. Adams III, Carotenoid composition in sun and shade leaves of plants with different life forms, Plant Cell Environ. 15 (1992) 411-119.
64. [64] A.S. Verhoeven, W.W. Adams III, B. Demmig-Adams, R. Croce, R. Bassi, Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in low and high light-acclimated Vinca major, Plant Physiol. (1999) in press.