Skip to main content
SpringerLink
Log in

Photosynthesis research: advances through molecular biology – the beginnings, 1975–1980s and on...

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Restriction endonuclease recognition sites and genes for rRNAs were first mapped on chloroplast chromosomes in 1975–1976. This marked the beginning of the application of molecular biology tools to photosynthesis research. In the first phase, knowledge about proteins involved in photosynthesis was used to identify plastid and nuclear genes encoding these proteins on cloned segments of DNA. Soon afterwards the DNA sequences of the cloned genes revealed the full primary sequences of the proteins. Knowledge of the primary amino acid sequences provided deeper understanding of the functioning of the protein and interactions among proteins of the photosynthetic apparatus. Later, as chloroplast DNA sequencing proceeded, genes were discovered that encoded proteins that had not been known to be part of the photosynthetic apparatus. This more complete knowledge of the composition of reaction centers and of the primary amino acid sequences of individual proteins comprising the reaction centers opened the way to determining the three-dimensional structures of reaction centers. At present, the availability of cloned genes, knowledge of the gene sequences and systems developed to genetically manipulate photosynthetic organisms is permitting experimental inquiries to be made into crucial details of the photosynthetic process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akoyunoglou G (ed) (1981) Photosynthesis, Vol V: Chloroplast Development. Balaban International Science Services, Philadelphia

  • Alt J, Westhoff P, Sears BB, Nelson N, Hurt E, Hauska G and Herrmann RG (1983) Genes and transcripts for the polypeptides of the cytochrome b 6 f complex from spinach thylakoid membranes. EMBO J 2: 979–986

    PubMed  CAS  Google Scholar 

  • Alt J, Morris J, Westhoff P and Herrmann RG (1984) Nucleotide sequence of the clustered genes for the 44 kD chlorophyll a apoprotein and the ‘32 kD-like’ protein of the Photosystem II reaction center in the spinach plastid chromosome. Curr Genet 8: 597–606

    Article  CAS  Google Scholar 

  • Amesz J (1998) The two photosystems of photosynthesis. In: Kung S-D and Yang S-F (eds) Discoveries in Plant Biology, Vol II, pp 1–14. World Scientific Publishing, Singapore

    Google Scholar 

  • Anderson JM (1975) The molecular organization of chloroplast thylakoids. Biochim Biophys Acta 416: 191–235

    PubMed  CAS  Google Scholar 

  • Anderson JM (2002) Changing concepts about the distribution of Photosystems I and II between grana-appressed and stromaexposed thylakoid membranes. Photosynth Res 73: 157–164

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Kloppstech K (1978) The plastid membranes of barley (Hordeum vulgare). Light-induced appearance of mRNAs coding for the apoprotein of the light-harvesting chlorophyll a/b protein. Eur J Biochem 85: 581–588

    Article  PubMed  CAS  Google Scholar 

  • Barry BA and Babcock GT (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 84: 7099–7103

    Article  PubMed  CAS  Google Scholar 

  • Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76: 35–52 (this issue)

    Article  PubMed  Google Scholar 

  • Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT and Calvin M(1954) The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J Am Chem Soc 76: 1760–1770

    Article  CAS  Google Scholar 

  • Bedbrook JR and Bogorad L (1976a) Endonuclease recognition sites mapped on Zea mays chloroplast DNA. Proc Natl Acad Sci USA 73: 4309–4313

    Article  PubMed  CAS  Google Scholar 

  • Bedbrook JR and Bogorad L (1976b) Physical and transcriptional mapping of Zea mays chloroplast DNA. In: Bucher TH, Neupert W, Sebald W and Werner S (eds) Genetics and Biogenesis of Chloroplasts and Mitochondria, pp 369–373. North-Holland Publishing, Amsterdam

    Google Scholar 

  • Bedbrook JR, Kolodner R and Bogorad L (1977) Zea mays chloroplast ribosomal RNA genes are part of a 22,000 base pair inverted repeat. Cell 11: 739–749

    Article  PubMed  CAS  Google Scholar 

  • Bedbrook JR, Link G, Coen DM, Bogorad L and Rich A (1978) Maize plastid gene expressed during photoregulated development. Proc Natl Acad Sci USA 75: 3060–3064

    Article  PubMed  CAS  Google Scholar 

  • Bedbrook JR, Coen DM, Beaton AR, Bogorad L and Rich A (1979) Location of the single gene for the large subunit of ribulose bisphosphate carboxylase on the maize chloroplast chromosome. J Biol Chem 254: 905–910

    PubMed  CAS  Google Scholar 

  • Bedbrook JR, Smith SM and Ellis RJ (1980) Molecular cloning and sequencing of cDNA encoding the precursor to the small subunit of chloroplast ribulose-1,5–bisphosphate carboxylase. Nature 287: 692–697

    Article  CAS  Google Scholar 

  • Bengis C and Nelson N (1975) Purification and properties of the Photosystem I reaction center from chloroplasts. J Biol Chem 250: 2783–2788

    PubMed  CAS  Google Scholar 

  • Bengis C. and Nelson N (1977) Subunit structure of chloroplast Photosystem I reaction center. J Biol Chem 252: 4584–4569

    PubMed  Google Scholar 

  • Benson AA (1998) The path of carbon in photosynthesis: 1942-1955. In: Kung SD and Yang SF (eds) Discoveries in Plant Biology, pp 97–213. World Scientific Publishing, Singapore

    Google Scholar 

  • Benson AA (2002) Following the path of carbon in photosynthesis: a personal story. Photosyn Res 73: 29–49

    Article  PubMed  CAS  Google Scholar 

  • Blowers AD, Bogorad L, Shark KB and Sanford JC (1989) Studies on Chlamydomonas chloroplast transformation: foreign DNA can be stably maintained in the chromosome. Plant Cell 1: 123–132

    Article  PubMed  CAS  Google Scholar 

  • Boardman NK and Anderson JM (1964) Isolation from spinach chloroplasts of particles containing different proportions of chlorophyll a and chlorophyll b and their possible role in the light reactions of photosynthesis. Nature 203: 166–167

    Article  CAS  Google Scholar 

  • Boardman NK, Linnane AW and Smillie RM (eds) (1971) Autonomy and Biogenesis of Mitochondria and Chloroplasts, p 511. North-Holland Publishing, Amsterdam

    Google Scholar 

  • Bogorad L (1975) Evolution of organelles and eukaryotic genomes. Science 188: 891–898

    PubMed  CAS  Google Scholar 

  • Bogorad L (1982) Regulation of intracellular gene flow in the evolution of eukaryotic genomes. In: Schiff, JA (ed) Origins of Chloroplasts, pp 277–295. Elsevier/North-Holland Publishing, Amsterdam

    Google Scholar 

  • Bogorad L (1998) Discovery of chloroplast DNA, genomes and genes. In: Kung S-D and Yang S-F (eds) Discoveries in Plant Biology, Vol II, pp 15–43. World Scientific Publishing, Singapore

    Google Scholar 

  • Bogorad L and Weil JH (eds) (1977a) Nucleic Acids and Protein Synthesis in Plants. Plenum Press, New York, 417 pp

    Google Scholar 

  • Bogorad L and Weil JH (eds) (1977b) Acids nucleiques et synthese des proteines chez les vegetaux. Editions du Centre National de la Recherche Scientifique, Paris

    Google Scholar 

  • Borisov A (2003) The beginnings of research on biophysics of photosynthesis and initial contributions made by Russian scientists to its development. Photosynth Res 76: 413–426 (this issue)

    Article  PubMed  CAS  Google Scholar 

  • Boynton JE, Gillham NW Harris EH, Hosier JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB and Sanford JC (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240: 1534–1538

    PubMed  CAS  Google Scholar 

  • Broglie R, Bellemare G, Bartlett S, Chua N-H and Cashmore AR (1981) Cloned DNA sequences complementary to mRNAs encoding precursors to the small subunit of ribulose-1,5–bisphosphate carboxylase and chlorophyll a/b binding polypeptide. Proc Natl Acad Sci USA 78: 7304–7308

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Xie D-L, Nelson H, Pinther W, Hauska G and Nelson N (1992) Photosynthetic reaction center genes in green sulfur bacteria and in Photosystem I are related. Proc Natl Acad Sci USA 89: 8135–8139

    Article  PubMed  Google Scholar 

  • Chan PH and Wildman SG (1972) Chloroplast DNA codes for the primary structure of the large subunit of fraction I protein. Biochim Biophys Acta 277: 677–680

    PubMed  CAS  Google Scholar 

  • Chitnis PR and Nelson N (1991) Photosystem I. In: Bogorad L and Vasil IK (eds) The Photosynthetic Apparatus. Molecular Biology and Operation, pp 177–224. Academic Press, San Diego, California

    Google Scholar 

  • Chitnis PR, Purvis D and Nelson N (1991) Molecular cloning and targeted mutagenesis of the gene psaF encoding subunit III of Photosystem I from the cyanobacterium Synechocystis sp PCC 6803. J Biol Chem 266: 20146–20151

    PubMed  CAS  Google Scholar 

  • Clayton RK (2002) Research on photosynthetic reaction centers from 1932 to 1987. Photosynth Res 73: 63–71

    Article  PubMed  CAS  Google Scholar 

  • Coen DM, Bedbrook JR, Bogorad L and Rich A (1977) Maize chloroplast DNA fragment encoding the large subunit of ribulose bisphosphate carboxylase. Proc Natl Acad Sci USA 74: 5487–5491

    Article  PubMed  CAS  Google Scholar 

  • Coruzzi G, Broglie R, Cashmore A and Chua N-H (1983) Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose 1,5–bisphosphate carboxylase and the major chlorophyll a/b-binding thylakoid polypeptide. J Biol Chem 258: 1399–1402

    PubMed  CAS  Google Scholar 

  • Crouse EJ, Schmitt JM, Bohnert HJ, Gordon K, Driesel A J and Hermann RG (1978) Intramolecular compositional heterogeneity of Spinacia andEuglena chloroplast DNAs. In: Akoyunoglou G and Argyroudi-Akoyunoglou JH (eds) Chloroplast Development, pp 565–572. Elsevier/North-Holland BioMed Press, Amsterdam

    Google Scholar 

  • Daniell H, Viveknanda J, Nielsen BL, Ye GN, Tewari KK and Sanford JC (1990) Transient foreign gene expression in chloroplasts of cultured tobacco cells after biolistic delivery of chloroplast vectors. Proc Natl Acad Sci USA 87: 88–92

    Article  PubMed  CAS  Google Scholar 

  • Davidson JN, Hanson MR and Bogorad L (1974) An altered chloroplast ribosomal protein in ery-M1 mutants of Chlamydomonas reinhardi. Mol Gen Genet 133: 119–129

    Google Scholar 

  • Debus RJ, Barry BA, Babcock GT and McIntosh L (1988a) Sitedirected mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430

    Article  PubMed  CAS  Google Scholar 

  • Debus RJ, Barry BA, Sithole I, Babcock GT and McIntosh L (1988b) Directed mutagenesis indicates that the donor to P+(680) in Photosystem II is tyrosine-161 of the D1 polypeptide Biochemistry 27: 9071–9074

    CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature (London) 318: 618–624

    Article  Google Scholar 

  • Deno H, Shinozaki K and Sugiura M (1983) Nucleotide sequence of tobacco chloroplast gene for the alpha subunit of protontranslocating ATPase. Nucleic Acids Res 11: 2185–2191

    PubMed  CAS  Google Scholar 

  • Dunsmuir P, Smith SM and Bedbrook J (1983) The major chlorophyll a/b binding protein of petunia is composed of several polypeptides encoded by a number of distinct nuclear genes. J Mol Appl Genet 2: 285–300

    PubMed  CAS  Google Scholar 

  • Dzelzkalns VA and Bogorad L (1988) Molecular analysis of a mutant defective in photosynthetic oxygen evolution and isolation of a complementing clone by a novel screening procedure. EMBO J 7: 333–338

    PubMed  CAS  Google Scholar 

  • Fish LE and Bogorad L (1986)Identification and analysis of the maize P700 chlorophyll a apoproteins PS I-A1 and PS I-A2 by high pressure liquid chromatography. Analysis and partial sequence determination. J Biol Chem 261: 8134–8139

    PubMed  CAS  Google Scholar 

  • Fish LE, Kuck U and Bogorad L (1985a) Two partially homologous adjacent light-inducible chloroplast genes encoding polypeptides of the P700 chlorophyll a-protein complex of Photosystem I. J Biol Chem 260: 1413–1421

    PubMed  CAS  Google Scholar 

  • Fish LE, Kuck U and Bogorad L (1985b) Analysis of the two partially homologous P700–chlorophyll a-proteins of maize Photosystem I: Predictions based on the primary sequences and features shared by other chlorophyll proteins. In: Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (eds) Molecular Biology of the Photosynthetic Apparatus, pp 111–120. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Golbeck J (1993) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci USA 90: 1642–1646

    Article  PubMed  CAS  Google Scholar 

  • Govindjee (2000) Milestones in Photosynthesis Research. In: Younis M, Pathre U and Mohanty P (ed) Probing Photosynthesis, pp 9–39. Taylor & Francis, New York

    Google Scholar 

  • Granick S (1938) Quantitative isolation of chloroplasts from higher plants. Am J Bot 25: 558–561

    Article  CAS  Google Scholar 

  • Gray PW and Hallick R (1976) Restriction endonuclease map of chloroplast DNA from Euglena gracilis. In: Bucher TH, Neupert W, Sebald W and Werner S (eds) Genetics and Biogenesis of Chloroplasts and Mitochondria, pp 347–350. North-Holland Publishing, Amsterdam

    Google Scholar 

  • Grebanier AE, Coen DM, Rich A and Bogorad L (1978) Membrane proteins synthesized but not processed by isolated maize chloroplasts. J Cell Biol 78: 734–764

    Article  PubMed  CAS  Google Scholar 

  • Grigorieva G and Shestakov S (1982) Transformation in the cyanobacterium Synechocystis sp 6803. FEMS Microbiol Lett 13:367–370

    Article  CAS  Google Scholar 

  • Guergova-Kuras M, Boudreaux B, Joliot A, Joliot P and Redding K (2001) Evidence for two active branches for electron transfer in Photosystem I. Proc Natl Acad Sci USA 98: 4437–4442

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR and Bogorad L (1977) Complementation analysis at the ery-m1 locus in Chlamydomonas reinhardi. Mol Gen Genet 153: 271–277

    Article  CAS  Google Scholar 

  • Heinemeyer W, Alt J, and Herrmann RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b6 and subunit 4 of the cytochrome b/f complex in the spinach plastid chromosome. Curr Genet 8: 543–549

    Article  CAS  Google Scholar 

  • Herrmann RG, Alt J, Schiller B, Widger WR and Cramer WA (1984) Nucleotide sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome: implications for the structure of the membrane protein. FEBS Lett 176: 239–244

    Article  CAS  Google Scholar 

  • Highfield PE and Ellis RJ (1978) Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424

    Article  PubMed  CAS  Google Scholar 

  • Holschuh K, Bottomley W and Whitfield PR (1984) Structure of the spinach chloroplast genes for the D2 and 44 kd reaction-centre proteins of Photosystem II and for tRNASer (UGA). Nucleic Acids Res 12: 8819–8834

    PubMed  CAS  Google Scholar 

  • Howe CJ, Bowman CM, Dyer TA and Gray JC (1982) Location and nucleotide sequence of the gene for the proton-translocating subunit of wheat chloroplast ATP synthase. Proc Natl Acad Sci USA 79: 6903–6907

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauss N (2001) Three-dimensional structure of cyanobacterial Photosystem I at 2.5 C resolution. Nature 411: 909–917

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136

    Article  PubMed  CAS  Google Scholar 

  • Kawashima N and Wildman SG (1972) Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim Biophys Acta 262: 42–49

    PubMed  CAS  Google Scholar 

  • Khakhina LN (1992) Concepts of Symbiogenesis: a Historical and Critical Study of the Research of Russian Botanists. Yale University Press, New Haven, Commecticut

    Google Scholar 

  • Kirsch W, Seyer P and Herrmann R G (1986) Nucleotide sequence of the clustered genes for two P700 chlorophyll apoproteins of the Photosystem I reaction center and the ribosomal protein S14 of the spinach plastid chromosome. Curr Genet 10: 843–855

    Article  CAS  Google Scholar 

  • Kislev S, Swift H and Bogorad L (1965) Nucleic acids of chloroplasts and mitochondria in Swiss chard. J Cell Biol 25: 327–344

    Article  PubMed  CAS  Google Scholar 

  • Kolodner R and Tewari KK (1975) The molecular size and conformation of the chloroplast DNA from higher plants. Biochim Biophys Acta 402: 372–390

    PubMed  CAS  Google Scholar 

  • Krebbers E, Larrinua IM, McIntosh L and Bogorad L (1982)The maize chloroplast genes for beta and ePS Ilon subunits of the photosynthetic coupling factor CF1 are fused. Nucleic Acid Res 10: 4985–5502

    PubMed  CAS  Google Scholar 

  • Lehmbeck J, Rasmussen OF, Bookjans GB, Jepsen BR, Stummann BM and Henningsen KW (1986) Sequence of two genes in pea chloroplast DNA coding for 84 and 82 kD polypeptides of the Photosystem I complex. Plant Mol Biol 7: 3–10

    Article  CAS  Google Scholar 

  • Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE and Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90: 7124–7128

    Article  PubMed  CAS  Google Scholar 

  • Manning JE and Richards OC (1972) Isolation and molecular weight of circular chloroplast DNA fromEuglena gracilis. Biochim Biophys Acta 259: 285–296

    PubMed  CAS  Google Scholar 

  • Manning JE, Wolstenholme DR, Ryan RS, Hunter JA and Richards OC (1971a) Circular chloroplast DNA from Euglena gracilis. Proc Natl Acad Sci USA 68: 1169–1173

    Article  PubMed  CAS  Google Scholar 

  • Manning JE, Wolstenholme DR, Ryan RS, Hunter JA and Richards OC (1971b) Circular chloroplast DNA molecules associated with chloroplasts of spinach, Spinacia oleracea. J Cell Biol 53: 594–601

    Article  Google Scholar 

  • McIntosh L, Poulsen C and Bogorad L (1980) Chloroplast gene sequence for the large subunit of ribulose bisphosphate carboxylase of maize. Nature 298: 556–560

    Article  Google Scholar 

  • Menke W (1938) Untersuchungen uber das protoplasma gruner pflanzenzellen. I. Isolierung von chloroplasten aus spinatblattern. Z Physiol Chem 257: 43–48

    CAS  Google Scholar 

  • Mets L and Bogorad L (1971) Mendelian and uniparental alterations in erythromycin binding by plastid ribosomes. Science 174: 707–709

    PubMed  CAS  Google Scholar 

  • Mets L and Bogorad L (1972) Altered chloroplast ribosomal proteins associated with erythromycin-resistant mutants in two genetic systems of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 69: 3779–3783

    Article  PubMed  CAS  Google Scholar 

  • Metz JG, Miles D and Rutherford AW (1983) Characterization of nuclear mutants of maize which lack the cytochrome f/b-563 complex. Plant Physiol 73: 452–459

    Article  PubMed  CAS  Google Scholar 

  • Metz JG, Nixon PJ, Roegner M, Brudvig GW and Diner BA (1989) Directed alteration of the D1 polypeptide of Photosystem II: evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron donor, P680. Biochemistry 28: 6960–6969

    Article  PubMed  CAS  Google Scholar 

  • Morris J and Herrmann RG (1984) Nucleotide sequence of the gene for the P680 chlorophyll a apoprotein of the Photosystem II reaction center from spinach. Nucleic Acids Res 12: 2837

    PubMed  CAS  Google Scholar 

  • Myers J (2002) In one era and out the other. Photosynth Res 73: 21–28

    Article  PubMed  CAS  Google Scholar 

  • Nelson N and Ben-Shem A (2002) Photosystem I reaction center: past and future. Photosynth Res 73: 193–206

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T (2003) Physical separation of chlorophyll-protein complexes. Photosynth Res 76: 227–232 (this issue)

    Article  PubMed  CAS  Google Scholar 

  • Ogren WL (2003) Affixing the O to Rubisco: discovering the source of photorespiratory glycolate and its regulation. Photosynth Res 76: 53–63 (this issue)

    Article  PubMed  CAS  Google Scholar 

  • Ohyama K, Fukuzawa H, Kochi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–547

    Article  CAS  Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: Structure and evolution. In: Bogorad L and Vasil IK (eds) TheMolecular Biology of Plastids, pp. 5–53. Academic Press, San Diego, California

    Google Scholar 

  • Puiseux-Dao S, Gibello D and Hoursiango-Neubrun D (1967) Techniques du mise en èvidence du DNA dans les plastes. Acad Sci Paris CR Ser D 265: 406–414

    CAS  Google Scholar 

  • Ris H and Plaut W (1962) The ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13: 383–391

    Article  PubMed  CAS  Google Scholar 

  • Rochaix J-D (2002) The three genomes of Chlamydomonas. Photosynth Res 73: 285–293

    Article  PubMed  CAS  Google Scholar 

  • Rochaix J-D, Dron M, Rahire M and Malnoe P (1984) Sequence homology between the 32K dalton and the D2 chloroplast membrane polypeptides of Chamydomonas reinhardii. PlantMol Biol 3: 363–370

    Article  CAS  Google Scholar 

  • Rodermel SR and Bogorad L (1985) Maize plastid photogenes: mapping and photoregulation of transcript levels during lightinduced development. J Cell Biol 100: 463–476

    Article  PubMed  CAS  Google Scholar 

  • Rousseau F, Setif P and Lagoutte B (1993) Evidence for the involvement of PS I-E subunit in the reduction of ferredoxin by Photosystem I. EMBO J 12: 1755–17765

    PubMed  CAS  Google Scholar 

  • Rutner AC and Lane MD (1967) Nonidentical subunits of ribulose diphosphate carboxylase. Biochem Biophys Res Commun 28: 531–537

    Article  PubMed  CAS  Google Scholar 

  • Sayre RT, Andersson B and Bogorad L (1986) The topology of a membrane protein: the orientation of the 32 kd Qb-binding chloroplast thylakoid membrane protein. Cell 47: 601–608

    Article  Google Scholar 

  • Shen G, Boussiba S and Vermaas WF (1993) Synechocystis sp PCC 6803 strains lacking Photosystem I and phycobilisome function. Plant Cell 5: 1853–1863

    Article  PubMed  CAS  Google Scholar 

  • Shestakov SV (2002) Gene-targeted and site-directed mutagenesis of photosynthesis genes in cyanobacteria. Photosynth Res 73: 279–284

    Article  PubMed  CAS  Google Scholar 

  • Shestakov SV and Khyen NT (1970) Evidence for genetic transformation in blue-green alga Anacystis nidulans. Mol Gen Genet 107: 372–375

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H and Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049

    PubMed  CAS  Google Scholar 

  • Smart LB and McIntosh L (1993) Genetic inactivation of the psaB gene in Synechocystis sp PCC 6803 disrupts assembly of Photosystem I. Plant Mol Biol 21: 177–180

    Article  PubMed  CAS  Google Scholar 

  • Smart LB, Warren PV, Golbeck JH and McIntosh L (1993) Mutational analysis of the structure and biogenesis of the Photosystem I reaction center in the cyanobacterium Synechocystis sp PCC 6803. Proc Natl Acad Sci USA 90: 1132–1136

    Article  PubMed  CAS  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517

    Article  PubMed  CAS  Google Scholar 

  • Steinback KE (1977) The Organization and Development of Chloroplast Thylakoid Membranes in Zea mays. PhD Thesis, Department of Biology, Harvard University, Cambridge, Massachusetts

    Google Scholar 

  • Steinback KE, McIntosh L, Bogorad L and Arntzen CJ (1981) Identification of the triazine receptor protein as a chloroplast gene product. Proc Natl Acad Sci USA 78: 7463–7467

    Article  PubMed  CAS  Google Scholar 

  • Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (eds) (1985) Molecular Biology of the Photosynthetic Apparatus. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sugiura M (2003) History of chloroplast genomics. Photosynth Res 76: 371–377 (this issue)

    Article  PubMed  CAS  Google Scholar 

  • Svab Z, Hajdukiewicz P and Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci USA 87: 8526–8530

    Article  PubMed  CAS  Google Scholar 

  • Thornber JP (1975) Chlorophyll-proteins: light-harvesting and reaction center components of plants. Ann Rev Plant Physiol 26: 127–158

    Article  CAS  Google Scholar 

  • Vermaas WFJ, Rutherford AW and Hansson O (1988) Site-directed mutagenesis in Photosystem II of the cyanobacterium Synechocystis sp PCC 6803: donor D is a tyrosine residue in the D2 protein. Proc Natl Acad Sci USA 85: 8477–8481

    Article  CAS  Google Scholar 

  • Webber AN, Gibbs PB, Ward JB and Bingham SE (1993) Sitedirected mutagenesis of the Photosystem I reaction center in chloroplasts. The proline-cysteine motif. J Biol Chem 268: 12990–12995

    PubMed  CAS  Google Scholar 

  • Weber K and Osborn M (1969) The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem 244: 4406–4012

    PubMed  CAS  Google Scholar 

  • Wessels JSC (1962) Separation of the two photochemical systems of photosynthesis by digitonin fragmentation of spinach chloroplasts. Biochim Biophys Acta 65: 561–564

    Article  PubMed  CAS  Google Scholar 

  • Wildman SG (2002) Along the trail from fraction 1 protein to Rubisco (ribulose bisphosphate carboxylase-oxygenase). Photosynth Res 73: 243–250

    Article  PubMed  CAS  Google Scholar 

  • Wildman SG and Bonner J (1947) The proteins of green leaves. I. Isolation enzymatic properties auxin content of spinach cytoplasmic proteins. Arch Biochem 14: 382–413

    Google Scholar 

  • Wildman SG, Chen K, Gray JC, Kung S-D, Kwaynen P and Sakano K (1975) Evolution of ferredoxin and fraction I protein in the genus Nicotiana. In: Birky CW, Pearlman PS and Byers TJ (eds) Genetics and Biogenesis of Mitochondria and Chloroplasts, pp 309–329. Ohio State University Press, Columbus, Ohio

    Google Scholar 

  • Willey DL, Auffret AD and Gray JC (1984) Structure and topology of cytochrome f in pea chloroplast membranes. Cell 36: 555–562

    Article  PubMed  CAS  Google Scholar 

  • Williams JC, Steiner LA, Ogden RC, Simon MI and Feher G (1983) Primary structure of the M subunit of the reaction center from Rhodopseudomaonas sphaeroides. Proc Natl Acad Sci USA 80: 6505–6509

    Article  PubMed  CAS  Google Scholar 

  • Youvan DC and Marrs BL (1985) Photosynthetic apparatus genes from Rhodopseudomonas capsulata. In: Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (eds) Molecular Biology of the Photosynthetic Apparatus, pp 173–181. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Youvan DC, Bylina EJ, Alberti M, Begusch H and Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides from R capsulata. Cell 37: 949–957

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Green BR and Cavalier-Smith T (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155–159

    Article  PubMed  CAS  Google Scholar 

  • Zurawski G, Bohnert HJ, Whitfield PR and Bottomley W (1982a) Nucleotide sequence of the gene for the Mr 32,000 thylakoid membrane protein from Spinacia oleracea and Nicotiana debneyi predicts a totally conserved primary translation product of Mr 38,950. Proc Natl Acad Sci USA 79: 7699–7703

    Article  PubMed  CAS  Google Scholar 

  • Zurawski G, Bottomley W and Whitfield PR (1982b) Structure of the genes for the beta and ePS Ilon subunits of spinach chloroplast ATPase indicates a dicistronic RNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79: 6260–6264

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Harvard University, The Biological Laboratories, 16 Divinity Ave., Cambridge, MA, 02138, USA

    Lawrence Bogorad

Authors
  1. Lawrence Bogorad
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bogorad, L. Photosynthesis research: advances through molecular biology – the beginnings, 1975–1980s and on.... Photosynthesis Research 76, 13–33 (2003). https://doi.org/10.1023/A:1024957602990

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024957602990

Search

Navigation