Up-regulation of a photosystem II core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir

Plant, Cell and Environment

Volumn 28, Issue 2, 2005, Pages 232-240

  Ebbert, V ^a   Adams III, W W ^a   Mattoo, A K ^b   Sokolenko, A ^c   Demmig Adams, B ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

D1; Energy dissipation; Phosphorylation; Photoprotection; Photosynthesis; PsbS; TLP40; Winter stress; Zeaxanthin

Indexed keywords

PHOTOSYNTHESIS;

ABIES; CONIFEROPHYTA; PSEUDOTSUGA; PSEUDOTSUGA MENZIESII;

EID: 13444278789     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2004.01267.x     Document Type: Article

References (51)

1. Adams W.W. III & Barker D.H. (1998) Seasonal changes in xanthophyll cycle-dependent energy dissipation in Yucca glauca Nuttall. Plant, Cell and Environment 21, 501-512.
2. Adams W.W. III & Demmig-Adams B. (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186, 390-398.
3. Adams W.W. III & Demmig-Adams B. (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiologia Plantarum 92, 451-458.
4. Adams W.W. III & Demmig-Adams B. (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant, Cell and Environment 18, 117-127.
5. Adams W.W. III, Demmig-Adams B., Verhoeven A.S. & Barker D.H. (1995) 'Photoinhibition' during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Australian Journal of Plant Physiology 22, 261-276.
6. Adams W.W. III, Demmig-Adams B., Rosenstiel T.N. & Ebbert V. (2001a) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynthesis Research 67, 51-62.
7. Adams W.W. III, Demmig-Adams B., Rosenstiel T.N., Ebbert V., Brightwell A.K., Barker D.H. & Zarter C.R. (2001b) Photosynthesis, xanthophylls, and D1 phosphorylation under winter stress. In: PS2001 Proceedings: 12th International Congress on Photosynthesis. CSIRO Publishing, Melbourne, Australia. Available at. http://www.publish.csiro.au/ps2001.
8. Adams W.W. III, Demmig-Adams B., Rosenstiel T.N., Brightwell A.K. & Ebbert V. (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biology 4, 545-557.
9. Adams W.W. III, Zarter C.R., Ebbert V. & Demmig-Adams B. (2004) Photoprotective strategies of overwintering evergreens. BioScience 54, 41-49.
10. Allen J.F. (1992) Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta 1098, 275-335.
11. Baena-Gonzalez E., Barbato R. & Aro E.-M. (1999) Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta 208, 196-204.
12. Bennett J. (1991) Protein phosphorylation in green plant chloroplasts. Annual Review of Plant Physiology and Plant Molecular Biology 42, 281-311.
13. Booij-James I.S., Swegle W.M., Edelman M. & Mattoo A.K. (2002) Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiology 130, 2069-2075.
14. Cleland R.E., Demmig-Adams B., Adams W.W. III & Winter K. (1990) Phosphorylation state of the light-harvesting chlorophyll-protein complex of photosystem II and chlorophyll fluorescence characteristics in Monstera deliciosa Liebm. & Glycine max (L.) Merrill in response to light. Australian Journal of Plant Physiology 17, 589-599.
15. Demmig-Adams B. & Adams W.W. III (1996) The role of the xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21-26.
16. Demmig-Adams B., Adams W.W. III, Barker D.H., Logan B.A., Bowling D.R. & Verhoeven A.S. (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98, 253-264.
17. Ebbert V. & Godde D. (1996) Phosphorylation of PS II polypeptides inhibits D1 protein-degradation and increases PS II stability. Photosynthesis Research 50, 257-269.
18. Ebbert V., Demmig-Adams B., Adams W.W. III, Mueh K.E. & Staehelin L.A. (2001) Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynthesis Research 67, 63-78.
19. Elich T.D., Edelman M. & Mattoo A.K. (1992) Identification, characterization and resolution of the in vivo phosphorylated form of the D1 photosystem II reaction center protein. Journal of Biological Chemistry 267, 3523-3529.
20. Ensminger I., Sceshnikov D., Campbell D.A., Funk C., Jansson S., Lloyd J., Shibistova O. & Öquist G. (2004) Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine foresets. Global Change Biology 10, 995-1008.
21. Fulgosi H., Vener A.V., Altschmied L., Herrmann R.G. & Andersson B. (1998) A novel multi-functional chloroplast protein: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO Journal 17, 1577-1587.
22. Gilmore A.M. & Ball M.C. (2000) Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences of the USA 97, 11098-11101.
23. Gilmore A.M., Matsubara S., Ball M.C., Barker D.H. & Itoh S. (2003) Excitation energy flow at 77 K in the photosynthetic apparatus of overwintering evergreens. Plant, Cell and Environment 26, 1021-1034.
24. Haldrup A., Jensen P.E., Lunde C. & Scheller H.V. (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends in Plant Science 6, 301-305.
25. Külheim C., Agren J. & Jansson S. (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91-93.
26. Li X.-P., Björkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S. & Niyogi K.K. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395.
27. Li X.-P., Phippard A., Pasari J. & Niyogi K.K. (2002) Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Functional Plant Biology 29, 1131-1139.
28. Logan B.A., Grace S.C., Adams W.W. III & Demmig-Adams B. (1998) Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments. Oecologia 116, 9-17.
29. Martinsuo P., Pursiheimo S., Aro E.-M. & Rintamäki E. (2003) Dithol oxidant and disulfide reductant dynamically regulate the phosphorylation of light-harvesting complex II proteins in thylakoid membranes. Plant Physiology 133, 37-46.
30. Matsubara S., Gilmore A.M., Ball M.C., Anderson J.M. & Osmond C.B. (2002) Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Functional Plant Biology 29, 1157-1169.
31. Misra A.N. & Biswal A.K. (2000) Thylakoid membrane protein kinase activity as a signal transduction pathway in chloroplasts. Photosynthetica 38, 323-332.
32. Niyogi K.K. (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455-560.
33. Norén H., Svensson P., Stegmark R., Funk C., Adamska I. & Andersson B. (2003) Expression of the early light-induced protein but not the PsbS protein is influenced by low temperature and depends on the developmental stage of the plant in field-grown pea cultivars. Plant, Cell and Environment 26, 245-253.
34. Oberhuber W. & Bauer H. (1991) Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees. Planta 185, 545-553.
35. Öquist G. & Huner N.P.A. (2003) Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology 54, 329-355.
36. Ottander C. & Öquist G. (1991) Recovery of photosynthesis in winter-stressed Scots pine. Plant, Cell and Environment 14, 345-349.
37. Ottander C., Campbell D. & Öquist G. (1995) Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197, 176-183.
38. Pursiheimo S., Rintamäki E., Baena-González E. & Aro E.-M. (1998) Thylakoid protein phosphorylation in evolutionarily divergent species with oxygenic photosynthesis. FEBS Letters 423, 178-182.
39. Rintamäki E., Salonen M., Suoranta U.-M., Carlberg I., Andersson B. & Aro E.-M. (1997) Phosphorylation of light-harvesting complex II and Photosystem II core proteins shows different irradiance-dependent regulation in vivo - Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. Journal of Biological Chemistry 272, 30476-30482.
40. Rokka A., Aro E.-M., Herrmann R.G., Andersson B. & Vener A.V. (2000) Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiology 123, 1525-1535.
41. Salonen M., Aro E.-M. & Rintamäki E. (1998) Reversible phosphorylation and turnover of the D1 protein under various redox states of Photosystem II induced by low temperature photoinhibition. Photosynthesis Research 58, 143-151.
42. B. Journal of Biological Chemistry 277, 32739-32745.
43. Savitch L.V., Leonardos E.D., Król M., Jansson S., Grodzinski B., Huner N.P.A. & Öquist G. (2002) Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation. Plant, Cell and Environment 25, 761-771.
44. Sigrist M. & Staehelin L.A. (1994) Appearance of type 1, 2, and 3 light-harvesting complex II and light-harvesting complex I proteins during light-induced greening of barley (Hordeum vulgare) etioplasts. Plant Physiology 104, 135-145.
45. Vener A.V., Ohad I. & Andersson B. (1998) Protein phosphorylation and redox sensing in chloroplast thylakoids. Current Opinion in Plant Biology 1, 217-223.
46. Vener A.V., Rokka A., Fulgosi H., Andersson B. & Herrmann R.G. (1999) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38, 14955-14965.
47. Verhoeven A.S., Adams W.W. III & Demmig-Adams B. (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiologia Plantarum 96, 567-576.
48. Verhoeven A.S., Adams W.W. III & Demmig-Adams B. (1998) Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant, Cell and Environment 21, 893-903.
49. Verhoeven A.S., Adams W.W. III & Demmig-Adams B. (1999a) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118, 277-287.
50. Verhoeven A.S., Adams W.W. III, Demmig-Adams B., Croce R. & Bassi R. (1999b) Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiology 120, 727-737.
51. Yang D.H., Webster J., Adam Z., Lindahl M. & Andersson B. (1998) Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiology 118, 827-834.