Skip to main content

Future Perspectives†

  • Chapter

Part of the Advances in Photosynthesis and Respiration book series (AIPH,volume 21)

Summary

The chloroplast-coded D1 protein of Photosystem II (PS II) is the major membrane protein synthesized within the plastid. It is involved in light-dependent electron transport, is a major target for photosynthesis herbicides and is universal to oxygenic phototrophs. The defining feature of D1 is its rapid turnover in spite of its being a structural component of the PS II reaction center core. Processing of nascent D1 precursor (33.5–34 kDa) occurs on unstacked stromal lamellae. The mature protein (32 kDa) then migrates to the grana where an initial scission occurs producing a 23 kDa N-terminal degradation fragment. Post-translational and reversible palmitoylation and phosphorylation accompany the protein along its life cycle. Both anabolism and catabolism of D1 are photoregulated, with synthesis coupled to phosphorylation but degradation coupled to PS II electron transport. Dephosphorylation of D1, in turn, is regulated by PS I excitation. Thus, the phosphorylation state of the protein is sensitive to the relative energy distribution between the two photosystems. Beyond redox regulation of D1 phosphorylation, an internal, circadian clock exerts overriding control. Two photosensitizers are involved in D1 degradation: chlorophyll pigments in the visible and far-red regions of the spectrum, and plastosemiquinone in the UV-B region. D1 degradation in visible light is a process only marginally overlapping with photoinhibition and overwhelmingly associated with fluences limiting for photosynthesis. Mixing physiological levels of visible and UV-B radiances leads to synergistic effects such that above a critical threshold of UV-B, the D1 as well as its sister protein, D2, both are targeted for accelerated degradation. These and other D1 protein studies, mainly carried out with intact Spirodela plants during the past 25 years in the authors’ laboratories, are presented in a historical perspective.

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (Canada)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (Canada)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andronis C, Kruse O, Deak Z, Vass I, Diner BA and Nixon PJ (1998) Mutation of residue threonine-2 of the D2 polypeptide and its effect on PS II function in Chlamydomonas reinhardtii. Plant Physiol 117: 515–524

    CrossRef  CAS  Google Scholar 

  • Aro E-M, Kettunen R and Tyystjärvi E (1992) ATP and light regulateD1protein modification and degradation: Role ofD1* in photoinhibition. FEBS Lett 297: 29–33

    Google Scholar 

  • Babu TS, Jansen MAK, Greenberg BM, Gaba V, Malkin S, Mattoo AK and Edelman M (1999) Amplified degradation of PS II D1 and D2 proteins under a mixture of photosynthetically active radiation and UV-B radiation: dependence on redox status of PS II. Photochem Photobiol 69: 553–559

    CrossRef  CAS  Google Scholar 

  • Bennett J (1984) Photosynthesis: Control of protein turnover by photosynthetic electron transport. Nature 310: 547–548

    CrossRef  Google Scholar 

  • Booij IS, Swegle M, Dube S, EdelmanMand Mattoo AK (1995) Photodegradation of D1-D2 PS II reaction center heterodimer. In: Mathis P (ed) Phostosynthesis: From Light to Biosphere, pp 487–490. Kluwer, Dordrecht

    Google Scholar 

  • Booij-James IS, Dube SK, Jansen MAK, EdelmanMand Mattoo AK (2000) Ultraviolet-B radiation impacts light-mediated turnover of the PS II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiol 124: 1275–1283

    CrossRef  PubMed  CAS  Google Scholar 

  • Booij-James IS, Swegle M, Edelman M and Mattoo AK (2002) Phosphorylation of the D1 PS II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiol 130: 2069–2075

    CrossRef  PubMed  CAS  Google Scholar 

  • Bustos SA, Schaefer MR and Golden SS (1990) Different and rapid responses of four cyanobacterial psbA transcripts to changes in light intensity. J Bacteriol 172: 1998–2004

    PubMed  CAS  Google Scholar 

  • Callahan FE, Wergin WP, Nelson N, Edelman M and Mattoo AK (1989) Distribution of thylakoid proteins between stromal and granal lamellae in Spirodela. Dual location of PS II components. Plant Physiol 91: 629–635

    PubMed  CAS  Google Scholar 

  • Callahan FE, Ghirardi ML, Sopory SK, Mehta AM, Edelman M and Mattoo AK (1990) A novel metabolic form of the 32kDa- D1 protein in the grana-localized reaction center of PS II. J Biol Chem 265: 15357–15360

    PubMed  CAS  Google Scholar 

  • Carpentier R and Allakhverdiev S (2004) Photosynthesis & Post Genomic Era: From Biophysics to Molecular Biology, a Path in the Research of PS II. Trois-Rivieres, Abstracts: pp 1–205

    Google Scholar 

  • Chen Y-B, Dominic B, Zani S, Mellon MT and Zehr JP (1999) Expression of photosynthesis genes in relation to nitrogen fixation in the diazo trophic filamentous nonheterocystous cyanobacterium Trichdesmium sp. IMS 101. Plant Mol Biol 41: 89–104

    CrossRef  PubMed  CAS  Google Scholar 

  • Chua N-H and Gilham NW (1977) The sites of synthesis of the principal thylakoid membrane polypeptides in Chlamydomonas reinhardtii. J Cell Biol 74: 441–452

    CrossRef  PubMed  CAS  Google Scholar 

  • Clarke AK, Soitamo A, Gustafsson P and Ö quist G (1993) Rapid interchange between two distinct forms of cyanobacterial PS II reaction center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973–9977

    CrossRef  PubMed  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 viridisat 3A resolution. Nature 318: 618–624

    CrossRef  Google Scholar 

  • Eaglesham ARJ and Ellis RJ (1974) Protein synthesis in chloroplasts. II. Light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochim Biophys Acta 335: 396–407

    CAS  Google Scholar 

  • Edelman M and Reisfeld A (1978) Characterization, translation and control of the 32,000 Dalton chloroplast membrane protein in Spirodela. In: Akoyunoglou G and Argyroudi- Akoyunoglou JH (eds) ChloroplastDevelopment, pp 641–652. Elsevier/North Holland, New York

    Google Scholar 

  • Edelman M and Reisfeld A (1980) Synthesis processing and functional probing of P-32000, the major membrane protein translated within the chloroplast. In: Leaver C (ed) Genome Organization and Expression in Plants, pp 353–362. Plenum, New York

    Google Scholar 

  • Edelman M, Hallick RB and Chua N-H (eds) (1982) Methods in Chloroplast Molecular Biology, Preface: pp v. Elsevier, Amsterdam

    Google Scholar 

  • Elich TD, Edelman, M and Mattoo AK (1992) Identification, characterization and resolution of the in vivo phosphorylated form of the D1 PS II reaction center protein. J Biol Chem 267: 3523–3529

    PubMed  CAS  Google Scholar 

  • Elich TD, Edelman M and Mattoo AK(1993) Dephosphorylation of PS II core proteins is light regulated in vivo. EMBO J 12: 4857–4862

    PubMed  CAS  Google Scholar 

  • Elich TD, Edelman M and Mattoo AK (1997) Evidence for lightdependent and light-independent protein dephosphorylation in chloroplasts. FEBS Lett 411: 236–238

    CrossRef  PubMed  CAS  Google Scholar 

  • Ellis RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Annu Rev Plant Physiol 32: 111–137

    CrossRef  CAS  Google Scholar 

  • Gaba V, Marder JB, Greenberg BM, Mattoo AK and Edelman M (1987) Degradation of the 32 kDa herbicide binding protein in far red light. Plant Physiol 84: 348–352

    PubMed  CAS  Google Scholar 

  • Garcia-Fernandez JM, Hess WR, Houmard J and Partensky F (1998) Expression of the psbA gene in the marine oxyphotobacteria ProchlorococcusSpp. Arch Biochem Biophys 359: 17–23

    CrossRef  PubMed  CAS  Google Scholar 

  • Ghirardi ML, Callahan FE, Sopory SK, Elich TD, Edelman M and Mattoo AK (1990) Cycling of the PS II reaction center core between grana and stromal lamellae. In: BaltschefsskyM (ed) Current Research in Photosynthesis, 2: 733–738, Kluwer, the Netherlands

    Google Scholar 

  • Ghirardi ML, Mahajan S, Sopory SK, Edelman M and Mattoo AK(1993) PS II reaction center particle from Spirodela stroma lamellae. J Biol Chem 268: 5357–5360

    PubMed  CAS  Google Scholar 

  • Golden SS (1995) Light responsive gene expression in cyanobacteria. J Bacteriol 177: 1651–1654

    PubMed  CAS  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: 734–746

    CrossRef  PubMed  CAS  Google Scholar 

  • Greenberg BM, Gaba V, Mattoo AK and Edelman M (1987) Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kDa protein of PS II.EMBOJ 6: 2865–2869

    CAS  Google Scholar 

  • Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK and Edelman M(1989) Separate photosynthesizers mediate degradation of the 32-kDa PS II reaction center protein in the visible and UV spectral regions. Proc Natl Acad Sci USA 86: 6617–6620

    CrossRef  PubMed  CAS  Google Scholar 

  • Hirschberg J, McIntosh L (1983) Molecular basis of herbicide resistance in Amaranthus hybridus. Science 222: 1346– 1349

    CrossRef  PubMed  CAS  Google Scholar 

  • Hoffman-Falk H, Mattoo AK, Marder JB, Edelman M and Ellis RJ (1982) General occurrence and structural similarity of the rapidly synthesized, 32,000-dalton protein of the chloroplast membrane. J Biol Chem 257: 4583–4587

    PubMed  CAS  Google Scholar 

  • Hwang S, Kawazoe R and Herrin DL (1996) Transcription of tufA and other chloroplast-encoded genes is controlled by a circadian clock in Chlamydomonas. Proc Natl Acad Sci USA 93: 996–1000

    CrossRef  PubMed  CAS  Google Scholar 

  • Jansen MAK, Driesenaar A, Kless H, Malkin S, Mattoo AK and Edelman M (1992) PS II inhibitor binding, QB-mediated electron flow and rapid degradation are separable properties of the D1 reaction center protein. In: Argyroudi-Akoyunoglou JH (ed) Regulation of Chloroplast Biogenesis, pp 303–311. Plenum, New York

    Google Scholar 

  • Jansen MAK, Depka B, Trebst A and Edelman M (1993) Engagement of specific sites in the plastoquinone niche regulates degradation of the D1 protein in PS II. J Biol Chem 268: 21246–21252

    PubMed  CAS  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM, Mattoo AK and Edelman M (1996a) Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of PS II. Plant J 9: 693– 699

    CrossRef  CAS  Google Scholar 

  • Jansen MAK, Greenberg BM, Edelman M, MattooAKand Gaba V (1996b) Accelerated degradation of the D2 protein of PS II under ultraviolet radiation. Photochem Photobiol 63: 814– 817

    Google Scholar 

  • Jansen MAK, Mattoo AK and Edelman M (1999) Photodynamics of D1-D2 protein catabolism in the chloroplast. Eur J Biochem 260: 527–532

    Google Scholar 

  • Jones LW and Kok B (1966) Photoinhibition of chloroplast reactions: kinetics and action spectra. Plant Physiol 41: 1037– 1043

    PubMed  CAS  Google Scholar 

  • Kawazoe R, Hwang S and Herrin DL (2000) Requirement for cytoplasmic protein synthesis during circadian peaks of transcription of chloroplast-encoded genes in Chlamydomonas. Plant Mol Biol 44: 699–709

    CrossRef  PubMed  CAS  Google Scholar 

  • Keren N, Berg A, van Kan PJM, Levanon H and Ohad I (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow. Proc Natl Acad Sci USA 94: 1579–1584

    CrossRef  PubMed  CAS  Google Scholar 

  • Kless H, Oren-Shamir M, Malkin S, McIntosh L and Edelman M (1994) The D-E region of theD1protein is involved in multiple quinone and herbicide interactions in PS II. Biochemistry 33: 10501–10507

    CrossRef  PubMed  CAS  Google Scholar 

  • Kulkarni RD and Golden SS (1994) Adaptation to high light intensity in Synechococcussp. strain PCC 7942: regulation of three psbA genes and two forms of D1 protein. J Bacteriol 176: 959–965

    PubMed  CAS  Google Scholar 

  • Kyle DJ, Ohad I and Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membrane. Proc Natl Acad Sci USA 81: 4070– 4074

    CrossRef  PubMed  CAS  Google Scholar 

  • Leto KJ, Bell E and McIntosh L (1985) Nuclear mutation leads to an accelerated turnover of chloroplast-encoded 48 kDa and 34.5 kDa polypeptides in thylakoids lacking PS II. EMBO J 4: 1645–1653

    PubMed  CAS  Google Scholar 

  • Liu Y, Golden SS, Kondo T, Ishiura M and Johnson CH (1995) Bacterial luciferase as a reporter of circadian gene expression in cyanobacteria. J Bacteriol 177: 2080–2086

    PubMed  CAS  Google Scholar 

  • Marder JB, Goloubinoff P and Edelman M (1984) Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II: Indications for COOH-terminal processing of a chloroplast membrane polypeptide. J Biol Chem 259: 3900–3908

    PubMed  CAS  Google Scholar 

  • Marder JB, Chapman DJ, Telfer A, Nixon PJ and Barber J (1987) Identification of psbA and psbD gene products, D1 and D2, as reaction centre proteins of PS II. Plant Mol Biol 9: 325–333

    CrossRef  CAS  Google Scholar 

  • Mattoo AK, Edelman M (1985) Photoregulation and metabolism of a thylakoidal herbicide-receptor protein. In: St John JB, Berlin E and Jackson PC (eds) Frontiers of Membrane Research in Agriculture, pp 23–34. Rowman & Allanheld, Totowa

    Google Scholar 

  • Mattoo AK and Edelman M(1987) Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA 84: 1497– 1501

    CrossRef  PubMed  CAS  Google Scholar 

  • Mattoo AK, Pick U, Hoffman-Falk H and Edelman M(1981) The rapidly metabolized 32,000-dalton polypeptide of the chloroplast is the "proteinaceous shield" regulating PS II electron transport and mediating diuron herbicide sensitivity. Proc Natl Acad Sci USA 78: 1572–1576

    CrossRef  PubMed  CAS  Google Scholar 

  • Mattoo AK, Hoffman-Falk H, Marder JB and Edelman M (1984a) Regulation of protein metabolism: Coupling of photosynthetic electron transport to in-vivo degradation of the rapidly metabolized 32 kDa protein of the chloroplast membrane. Proc Natl Acad Sci USA 81: 1380–1384

    CrossRef  CAS  Google Scholar 

  • Mattoo AK, St John JB and Wergin WP (1984b) Adaptive reorganization of protein and lipid components in chloroplast membranes as associated with herbicide binding. J Cellular Biochem 24: 163–175

    CrossRef  CAS  Google Scholar 

  • Mattoo AK, Marder JB and Edelman M(1989) Dynamics of the PS II reaction center. Cell 56: 241–246

    CrossRef  PubMed  CAS  Google Scholar 

  • Michel H, Hunt DF, Shabanowitz J and Bennett J (1988) Tandem mass spectrometry reveals that three photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem 263: 1123–1130

    PubMed  CAS  Google Scholar 

  • Mulo P, Tystjärvi T, Tystjärvi E, Govindjee, Maenpaa P and AroE-M (1997) Mutagenesis of the D-E loop of photosystem II reaction centre protein D1. Function and assembly of PS II. Plant Mol Biol 33: 1059–1071

    CrossRef  PubMed  CAS  Google Scholar 

  • Nanba O and Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112

    CrossRef  PubMed  CAS  Google Scholar 

  • Nixon PJ, Komenda J, Barber J, Deak Z, Vass I and Diner BA (1995) Deletion of the PEST-like region of PS II modifies the QB-binding pocket but does not prevent rapid turnover of D1. J Biol Chem 270: 14919–14927

    CrossRef  PubMed  CAS  Google Scholar 

  • Pfister K, Steinback KE, Gardner G and Arntzen CJ (1981) Photoaffinity labeling of an herbicide receptor protein in chloroplast membranes. Proc Natl Acad Sci USA 78: 981–985

    CrossRef  PubMed  CAS  Google Scholar 

  • Regitz G and Ohad I (1975) Changes in the protein organization in developing thylakoids of Chlamydomonas reinhardtii Y-1 as shown by sensitivity to trypsin. In: Avron M (ed) Proc 3rd Intl Congr Photosynthesis, 3: 1615–1625. Elsevier, Amsterdam

    Google Scholar 

  • Reisfeld A, Mattoo AK and Edelman M (1982) Processing of a chloroplast-translated membrane protein in vivo. Analysis of the rapidly synthesized 32000-dalton shield protein and its precursor in Spirodela oligorrhiza. Eur J Biochem 124: 125–129

    CrossRef  PubMed  CAS  Google Scholar 

  • Renger G (1976) Studies on the structural and functional organization of system II of photosynthesis. The use of trypsin as a structurally selective inhibitor at the outer surface of the thylakoid membrane. Biochim Biophys Acta 440: 287–300

    CrossRef  PubMed  Google Scholar 

  • Rintamäki E, Kettunen R, Tyystjärvi E and Aro, E-M (1995) Light dependent phosphorylation ofD1reaction centre protein of PS II: hypothesis for the functional role in vivo. Physiol Plant 93: 191–195

    CrossRef  Google Scholar 

  • Rochaix JD, Dron M, Rahire M and Malone P (1984) Sequence homology between the 32 kDa and the D2 chloroplast membrane polypeptide of Chlamydomonas reinhardii. Plant Mol Biol 3: 363–370

    CrossRef  CAS  Google Scholar 

  • Rogers S, Wells R and Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234: 364–368

    CAS  Google Scholar 

  • Rosner A, Jakob KM, Gressel J and Sagher D (1975) The early synthesis and possible function of a 0.5 x 106 Mr RNA after transfer of dark-grown Spirodela plants to light. Biochem Biophys Res Commun 67: 383–391

    CrossRef  PubMed  CAS  Google Scholar 

  • Sefton BM, Trowbridge IS, Cooper JA and Scolnik EM (1982) The transforming protein of Rous sarcoma virus, Harvey sarcoma virus and Abelson virus contain tightly bound lipid. Cell 31: 465–474

    CrossRef  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 

  • Sobolev V and Edelman M (1995) Modeling the quinone-B site of the PS II reaction center using notions of complementarity and contact surface between atoms. Proteins 21: 214– 225

    CrossRef  PubMed  CAS  Google Scholar 

  • Sopory SK, Greenberg BM, Mehta RA, Edelman M and Mattoo AK (1990) Free radical scavengers inhibit lightdependent degradation of the 32 kDa PS II reaction center protein. Z Naturforsch 45c: 412–417

    Google Scholar 

  • Teramura AH and Sullivan JH (1994) Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynth Res 39: 463–473

    CrossRef  CAS  Google Scholar 

  • Trebst A (1986) The topology of plastoquinone and herbicide binding peptides of PS II in the thylakoid membrane. Z Naturforsch 41c: 240–245

    Google Scholar 

  • Weinbaum SA, Gressel J, Resifeld A and Edelman M (1979) Characterization of the 32000 Dalton chloroplast membrane protein. III. Probing its biological function in Spirodela. Plant Physiol 64: 828–832

    CrossRef  PubMed  CAS  Google Scholar 

  • Wheeler AM and Hartley MR (1975) Major mRNA species from spinach chloroplasts do not contain poly(A). Nature 257: 66–67

    CrossRef  PubMed  CAS  Google Scholar 

  • Wilson MI and Greenberg BM (1993) Protection of the D1 PS II reaction center protein from degradation in ultraviolet radiation following adaptation of Brassica napusL. to growth in ultraviolet-B. Photochem Photobiol 57: 556–563

    CrossRef  CAS  Google Scholar 

  • Zurawski G, Bohnert HJ, Whitfeld PR and Bottomley W(1982) Nucleotide sequence of the gene for the Mr 32000 thylakoid protein from Spinacia oleraceaand Nicotiana debneyi predicts a totally conserved primary translation product of Mr 38950. Proc Natl Acad Sci USA 79: 7699–7703

    CrossRef  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Edelman, M., Mattoo, A.K. (2008). Future Perspectives†. In: Demmig-Adams, B., Adams, W.W., Mattoo, A.K. (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, vol 21. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3579-9_3

Download citation

Publish with us

Policies and ethics