Skip to main content
SpringerLink
Log in

D1 polypeptide degradation may regulate psbA gene expression at transcriptional and translational levels in Synechocystis sp. PCC 6803

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Light has been suggested to regulate both synthesis and degradation of the Photosystem II (PS II) reaction centre polypeptide D1, encoded by the psbA gene. The modified degradation rate of the D1 polypeptide in site-directed Synechocystis sp PCC 6803 D1 mutants CA1 [del(E242-E244);Q241H], E243K and E229D has provided a tool to determine whether the rate of D1 polypeptide synthesis is directly regulated by light-intensity-related factors or by a control mechanism mediated by light-dependent degradation of the D1 polypeptide. In vivo accumulation of [35S] methionine into the D1 polypeptide was found to correlate with D1 polypeptide degradation rather than with incident irradiance. This suggests that the degradation rate of the D1 polypeptide regulates its own synthesis at translational level. Furthermore, several fold differences in the psbA mRNA levels were measured between D1 mutant strains, indicating that the psbA gene transcription is not solely under light control.

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

Abbreviations

Chl:

chlorophyll

DCBQ:

2,6-dichloro-p-benzoquinone

MW:

molecular weight

SDS-PAGE:

sodium dodecyl sulfate polyacrylamide gel electrophoresis

PPFD:

photosynthetic photon flux density

PS II:

Photosystem II

References

  • Adir N, Shochat S and Ohad I (1990) Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. Reaction center II serves as an acceptor for the D1 precursor. J Biol Chem 265: 12563–12568

    PubMed  Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II inactivation, protein damage and turnover. BBA 1143: 113–134

    PubMed  Google Scholar 

  • Baumgartner BJ, Rapp JC and Mullet JE (1993) Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development. Plant Physiol 101: 781–791

    PubMed  Google Scholar 

  • Bustos S, Schaefer MR and Golden SS (1990) Different and rapid responses of four cyanobacterial psbA transcripts to changes in light intensity. J Bacteriol 171: 3973–3981

    Google Scholar 

  • Danon A and Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene spesific mRNA binding proteins. EMBO J 10: 3993–4001

    PubMed  Google Scholar 

  • Danon A and Mayfield SP (1994a) ADP-dependent phosphorylation regulates RNA-binding in vitro implications in light-modulated translation. EMBO J 13: 2227–2235

    PubMed  Google Scholar 

  • Danon A and Mayfield SP (1994b) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 26: 1717–1719

    Google Scholar 

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

    PubMed  Google Scholar 

  • Deng X-W and Gruissem W (1987) Control of plastid gene expression during development: The limited role of transcriptional regulation. Cell 49: 379–387

    Article  PubMed  Google Scholar 

  • Erickson JM and Rochaix J-D (1992) The molecular biology of Photosystem II. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, Topics in Photosynthesis, pp 101–177. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Fromm H, Devic M, Fluhr R and Edelman M (1985) Control of psbA gene expression; in mature Spirodela chloroplsts light regulation of 32-kd protein synthesis is indepenent of transcript level. EMBO J 4: 291–295

    Google Scholar 

  • Gamble PG and Mullet JE (1989) Translation and stability of proteins encoded by the plastid psbA and psbB genes are regulated by a nuclear gene during light-induced chloroplast development in barley. J Biol Chem 264: 7236–7243

    PubMed  Google Scholar 

  • Girard-Bascou J, Pierre Y and Drapier D (1992) A nuclear mutation affects the synthesis of the chloroplast psbA gene production Clamydomonas reinhardtii. Curr Genet 22: 47–52

    PubMed  Google Scholar 

  • Golden SS Brusslan J and Haselkorn R (1986) Expression of a family of psbA gene encoding a Photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798

    PubMed  Google Scholar 

  • Greenberg BM, Gaba V, Mattoo AK and Edelman M (1987) Identification of a primary in vivo degradation product of the rapidlyturning-over 32 kd protein of Photosystem II. EMBO J 6: 2865–2869

    PubMed  Google Scholar 

  • Greer DH, Berry JA and Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: Role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 181: 253–260

    Google Scholar 

  • Inagaki N and Satoh K (1992) Accumulation of a translation intermediate of D1 protein by light-dark transition in isolated spinach chloroplasts. FEBS Lett 300: 5–8

    Article  PubMed  Google Scholar 

  • Kanervo E, Mäenpää P and Aro E-M (1993) D1 protein degradation and psbA transcript levels in Synechocystis PCC 6803 during photoinhibition in vivo. J Plant Physiol 142: 669–675

    Google Scholar 

  • Kawaguchi H, Fukuda I, Shiina T and Toyoshima Y (1992) Dynamical behavior of psb gene transcripts in greening wheat seedlings. I. Time course of accumulation of the psbA through psbN gene transcripts during light-induced greening. Plant Mol Biol 20: 695–704

    PubMed  Google Scholar 

  • Kettunen R, Tyystjärvi E and Aro E-M (1991) D1 protein degradation during photoinhibition of intact leaves. A modification of the D1 protein precedes degradation. FEBS Lett 290: 153–156

    Article  PubMed  Google Scholar 

  • Kim J, Eichacker LA, Rudiger W and Mullet JE (1994a) Chlorophyll regulates accumulation of the plastid-encded chloropyll proteins P700 and D1 by incresing apoprotein stability. Plant Physiol 104: 907–916

    Article  PubMed  Google Scholar 

  • Kim J, Klein PG and Mullet JE (1994b) Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts. Plant Mol Biol 25: 459–467

    PubMed  Google Scholar 

  • Kim J, Klein P G, and Mullet JE (1994c) Synthesis and turnover of Photosystem II reaction center protein D1. J Biol Chem 269: 17918–17923

    PubMed  Google Scholar 

  • Klaff P and Gruissem W (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell 3: 517–529

    Article  PubMed  Google Scholar 

  • Klein RR and Mullet JE (1986) Regulation of chloroplst-encoded chlorophyll-binding protein translation during higher plant chloroplst biogenesis. J Biol Chem 261: 11138–11145

    PubMed  Google Scholar 

  • Koenig F (1990) Anacystis mutants with different tolerance to DCMU-type herbicides show differences in architecture and dynamics of the photosynthetic apparatus, depending on site and mode of the amino acid exhanges in the D1 protein. Z Naturforsch. 45c: 446–451

    Google Scholar 

  • Kulkarni RD, Schaefer MS and Golden SS (1992) Transcriptional and posttranscriptional components of psbA response to high light intensity in Synechococcus sp. strain PCC 7942. J Bacteriology 174: 3775–3781

    Google Scholar 

  • Kuroda H, Inagaki N and Satoh K (1992) The level of stromal ATP regulates translation of the D1 protein in isolated chloroplasts. Plant Cell Physiol 33: 33–39

    Google Scholar 

  • Li R and Golden SS (1993) Enhancer activity of light-responsive regulatory elements in the untranslated leader regions of cyanobacterial psbA genes. Proc Natl Acad Sci USA 90: 11678–11682

    PubMed  Google Scholar 

  • Mohamed A and Jansson C (1989) Influence of light in accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13: 693–700

    PubMed  Google Scholar 

  • Mohamed A, Eriksson J, Osiewacz HD, Jansson C (1993) Differntial expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238: 161–168

    PubMed  Google Scholar 

  • Mullet JE, Klein PG and Klein R (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc Natl Acad Sci USA 87: 4038–4042

    PubMed  Google Scholar 

  • Mäenpää P, Kallio T, Mulo P, Salih GF, Aro E-M, Tyystjärvi E and Jansson C (1993) Site-specific mutations in the D1 polypeptide affect the susceptibility of Synechocystis 6803 cells to photoinhibiton. Plant Mol Biol 22: 1–12

    PubMed  Google Scholar 

  • Mäenpää P, Miranda T, Tyystjärvi E, Tyystjärvi T, Govindjee, Ducruet JM, Etienne A-L and Kirilovsky D (1995) A mutation in the D-DE loop of D1 modifies the stability of the S2 QA- and S2QB-states in Photosystem II. Plant Physiol 107: 187–197

    PubMed  Google Scholar 

  • Nixon PJ, Rögner P and Diner BA (1991) Expression of a higher plant psbA gene in Synechocystis 6803 yields a functional hybrid Photosystem II reaction center complex. Plant Cell 3: 383–395

    Article  PubMed  Google Scholar 

  • Prasil O, Adir N, and Ohad I (1992) Dynamics of Photosystem II: Mechanism of photoinhibition and recovery processes. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, Topics in Photosynthesis, pp 295–348. Elsevier Science Publishers, Amsterdam

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Salvador ML, Klein U and Bogorad L (1993) Light-regulated and endogenous fluctuations of chloroplast transript levels in Chlamydomonas. Regulation by transcription and RNA degradation. Plant J 3: 213–219

    Article  PubMed  Google Scholar 

  • Schaefer MR and Golden SS (1989a) Differential expression of members of a cyanobacterial psbA gene family in response to light. J Bacteriol 171: 3973–3981

    PubMed  Google Scholar 

  • Schaefer MR and Golden SS (1989b) Light availability influences the ratio of two forms of D1 in cyanobacterial thylakoids. J Biol Chem 264: 7412–7417

    PubMed  Google Scholar 

  • Soitamo AJ, Zhou G, Clarke AK, Öquist G, Aro E-M and Gustafsson P (1994) Over-production of the D1 protein of Photosystem II reaction centre in the cyanobacterium Synechococcus sp. PCC 7942. Plant Mol Biol 26: 709–721

    Article  PubMed  Google Scholar 

  • Staub JM and Maliga P (1993) Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J 12: 601–606

    PubMed  Google Scholar 

  • Staub JM and Maliga P (1994) Translation of psbA mRNA is regulated by light via the 5′-untranslated region in tobacco plastids. Plant J 6: 547–553

    Article  PubMed  Google Scholar 

  • Tae GS and Cramer WA (1992) Truncation of the COOH-terminal domain of the psbE gene product in Synechocystis sp. PCC 6803: Requirements for Photosystem II assembly and function. Biochemistry 31: 4066–4074

    PubMed  Google Scholar 

  • Taniguchi M, Kuroda H and Satoh K (1993) ATP-dependent protein synthesis in isolated pea chloroplasts. Evidence for accumulation of a translation intermediate of the D1 protein. FEBS Lett 317: 57–61

    Article  PubMed  Google Scholar 

  • Tomioka N, Shinozaki K and Sugiura M (1981) Molecular cloning and characterization of ribosomal RNA genes from a blue-green alga, Anacystis nidulans. Mol Gen Genet 184: 359–363

    Google Scholar 

  • Tyystjärvi E (1993) Photoinhibition-struggle between damage and repair of Photosystem II. PhD thesis, Univ of Turku, Turku, Finland

  • Tyystjärvi T, Aro E-M, Jansson C and Mäenpää P (1994) Changes of amino acid sequence in PEST-like area and QEEET motif affect degradation rate of d1 polypeptide in Photosystem II. Plant Mol Biol 25: 517–526

    PubMed  Google Scholar 

  • Zer H, Prasil O and Ohad I (1994) Role of plastoquinol oxidoreduction in regulation of photochemical reaction center IID1 protein turnover in vivo. J Biol Chem 269: 17670–17676

    PubMed  Google Scholar 

  • Zurawski G, Bohnert HH, Whitfeld P R and Bottomley W (1982) Nucleotide sequence of the gene for Mr 32,000 thylakoid membane 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Turku, BioCity A 6th floor, Tykistökatu 6, FIN-20520, Turku, Finland

    Taina Tyystjärvi, Paula Mulo, Pirkko Mäenpää & Eva-Mari Aro

Authors
  1. Taina Tyystjärvi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Mulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pirkko Mäenpää
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eva-Mari Aro
    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

Tyystjärvi, T., Mulo, P., Mäenpää, P. et al. D1 polypeptide degradation may regulate psbA gene expression at transcriptional and translational levels in Synechocystis sp. PCC 6803. Photosynth Res 47, 111–120 (1996). https://doi.org/10.1007/BF00016174

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00016174

Key words

Search

Navigation