Skip to main content
Log in

Nitric oxide donor-mediated inhibition of phosphorylation shows that light-mediated degradation of photosystem II D1 protein and phosphorylation are not tightly linked

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

An outcome of the photochemistry during oxygenic photosynthesis is the rapid turn over of the D1 protein in the light compared to the other proteins of the photosystem II (PS II) reaction center. D1 is a major factor of PS II instability and its replacement a primary event of the PS II repair cycle. D1 also undergoes redox-dependent phosphorylation prior to its degradation. Although it has been suggested that phosphorylation modulates D1 metabolism, reversible D1 phosphorylation was reported not to be essential for PS II repair in Arabidopsis. Thus, the involvement of phosphorylation in D1 degradation is controversial. We show here that nitric oxide donors inhibit in vivo phosphorylation of the D1 protein in Spirodela without inhibiting degradation of the protein. Thus, D1 phosphorylation is not tightly linked to D1 degradation in the intact plant.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

CAM:

Crassulacean acid metabolism

NaF:

Sodium fluoride

NO:

Nitric oxide

PS II:

Photosystem II

SIN-1:

3-Morpholinosydnonimine

SNOC:

S-Nitrosocysteine

References

  • Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata—ribulose-1, 5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J 275:2862–2872

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    Article  PubMed  CAS  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Sci 172:876–887

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, Kettunen R, Tyystjärvi E (1992) ATP and light regulate D1 protein modification and degradation: role of D1 in photoinhibition. FEBS Lett 297:29–33

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    Article  PubMed  CAS  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bustos SA, Schaefer MR, 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 

  • Drapier JC, Pellat C, Henry Y (1991) Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells cocultured with activated macrophages. J Biol Chem 266:10162–10167

    PubMed  CAS  Google Scholar 

  • Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620. doi:10.1007/s11120-008-9342-x

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Allen JF (2003) Lessons from redox signaling in plants. Antioxid Redox Signal 5:3–5

    Article  PubMed  CAS  Google Scholar 

  • Giardi MT (1993) Phosphorylation and disassembly of photosystem II core as an early stage of photoinhibition. Planta 190:107–113

    Article  CAS  Google Scholar 

  • Gopalakrishna R, Chen ZH, Gundimeda U (1993) Nitric oxide and nitric oxide-generating agents induce a reversible inactivation of protein kinase C activity and phorbol ester binding. J Biol Chem 268:27180–27185

    PubMed  CAS  Google Scholar 

  • Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H (2004) Biological significance of nitric oxide-mediated protein modifications. Am J Physiol Lung Cell Mol Physiol 287:L262–L268

    Article  PubMed  CAS  Google Scholar 

  • Harrison MA, Allen JF (1991) Light-dependent phosphorylation of photosystem II polypeptides maintains electron transport at high light intensity: separation from effects of phosphorylation of LHC-II. Biochim Biophys Acta 1058:289–296

    Article  CAS  Google Scholar 

  • Ignarro LJ (1990) Biosynthesis and metabolism of endothelial-derived nitric oxide. Annu Rev Pharmacol Toxicol 30:535–560

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jansen MAK, Mattoo AK, Edelman M (1999) D1–D2 protein degradation in the chloroplast: complex light saturation kinetics. Eur J Biochem 260:527–532

    Article  PubMed  CAS  Google Scholar 

  • Kolpakov V, Gordon D, Kulik TJ (1995) Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. Circ Res 76:305–309

    PubMed  CAS  Google Scholar 

  • Le Brun NE, Andrews SC, Moore GR, Thomson AJ (1997) Interaction of nitric oxide with non-haem iron sites of Escherichia coli bacterioferritin: reduction of nitric oxide to nitrous oxide and oxidation of iron(II) to iron(III). Biochem J 326:173–179

    PubMed  CAS  Google Scholar 

  • Lei SZ, Pan Z-H, Aggarwal SK, Chen H-SV, Hartman J, Sucher NJ, Lipton SA (1992) Effect of nitric oxide production on the redox regulatory site of the NMDA receptor–channel complex. Neuron 8:1087–1099

    Article  PubMed  CAS  Google Scholar 

  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mehta RA, Fawcett TW, Porath D, Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1, 5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810–2816

    PubMed  CAS  Google Scholar 

  • Nanba O, 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

    Article  PubMed  CAS  Google Scholar 

  • Nelson N, Yocum CF (2006) Structure and function of Photosystems I and II. Annu Rev Plant Biol 57:521–565

    Article  PubMed  CAS  Google Scholar 

  • Osakada F, Hashino A, Kume T, Katsuki H, Kaneko S, Akaike A (2003) Neuroprotective effects of α-tocopherol on oxidative stress in rat striatal cultures. Eur J Pharmacol 465:15–22

    Article  PubMed  CAS  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  PubMed  CAS  Google Scholar 

  • Park H-S, Huh S-H, Kim M-S, Lee SH, Choi E-J (2000) Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc Natl Acad Sci USA 97:14382–14387

    Article  PubMed  CAS  Google Scholar 

  • Posner HB (1967) Aquatic vascular plants. In: Witt FA, Wessels NK (eds) Methods in developmental biology. Crowell, New York, pp 301–317

    Google Scholar 

  • Rintamäki E, Kettunen R, Tyystjärvi E, Aro E-M (1995a) Light-dependent phosphorylation of D1 reaction centre protein of photosystem II: hypothesis for the functional role in vivo. Physiol Plant 93:191–195

    Article  Google Scholar 

  • Rintamaki E, Salo R, Lehtonen E, Aro E-M (1995b) Regulation of D1 protein degradation during photoinhibition of photosystem II in vivo: phosphorylation of the D1 protein in various plant groups. Planta 195:379–386

    Article  CAS  Google Scholar 

  • Takahashi S, Yamasaki H (2002) Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett 512:145–148

    Article  PubMed  CAS  Google Scholar 

  • Wodala B, Deák Z, Vass I, Erdei L, Altorjay I, Horváth F (2008) In vivo target sites of nitric oxide in photosynthetic electron transport as studied by chlorophyll fluorescence in pea leaves. Plant Physiol 146:1920–1927

    Article  PubMed  CAS  Google Scholar 

  • Yokthongwattana K, Melis A (2006) Photoinhibition and recovery in oxygenic photosynthesis: mechanism of a photosystem II damage and repair cycle. In: Demmig-Adams B, Adams WWIII, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, The Netherlands, pp 175–191

    Chapter  Google Scholar 

Download references

Acknowledgments

Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Autar K. Mattoo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Booij-James, I.S., Edelman, M. & Mattoo, A.K. Nitric oxide donor-mediated inhibition of phosphorylation shows that light-mediated degradation of photosystem II D1 protein and phosphorylation are not tightly linked. Planta 229, 1347–1352 (2009). https://doi.org/10.1007/s00425-009-0914-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0914-6

Keywords

Navigation