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.
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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
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
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
Bennett J (1984) Photosynthesis: Control of protein turnover by photosynthetic electron transport. Nature 310: 547–548
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Edelman M, Hallick RB and Chua N-H (eds) (1982) Methods in Chloroplast Molecular Biology, Preface: pp v. Elsevier, Amsterdam
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
Elich TD, Edelman M and Mattoo AK(1993) Dephosphorylation of PS II core proteins is light regulated in vivo. EMBO J 12: 4857–4862
Elich TD, Edelman M and Mattoo AK (1997) Evidence for lightdependent and light-independent protein dephosphorylation in chloroplasts. FEBS Lett 411: 236–238
Ellis RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Annu Rev Plant Physiol 32: 111–137
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
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
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
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
Golden SS (1995) Light responsive gene expression in cyanobacteria. J Bacteriol 177: 1651–1654
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
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
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
Hirschberg J, McIntosh L (1983) Molecular basis of herbicide resistance in Amaranthus hybridus. Science 222: 1346– 1349
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
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
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
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
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
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
Jansen MAK, Mattoo AK and Edelman M (1999) Photodynamics of D1-D2 protein catabolism in the chloroplast. Eur J Biochem 260: 527–532
Jones LW and Kok B (1966) Photoinhibition of chloroplast reactions: kinetics and action spectra. Plant Physiol 41: 1037– 1043
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Mattoo AK, Marder JB and Edelman M(1989) Dynamics of the PS II reaction center. Cell 56: 241–246
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
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
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
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
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
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
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
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
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
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
Rogers S, Wells R and Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234: 364–368
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
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
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
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
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
Teramura AH and Sullivan JH (1994) Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynth Res 39: 463–473
Trebst A (1986) The topology of plastoquinone and herbicide binding peptides of PS II in the thylakoid membrane. Z Naturforsch 41c: 240–245
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
Wheeler AM and Hartley MR (1975) Major mRNA species from spinach chloroplasts do not contain poly(A). Nature 257: 66–67
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
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
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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
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