Winter down-regulation of intrinsic photosynthetic capacity coupled with up-regulation of Elip-like proteins and persistent energy dissipation in a subalpine forest

New Phytologist

Volumn 172, Issue 2, 2006, Pages 272-282

  Zarter, C Ryan ^a   Adams III, William W ^a   Ebbert, Volker ^a   Cuthbertson, Daniel J ^a   Adamska, Iwona ^b   Demmig Adams, Barbara ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Conifers; Elips; Energy dissipation; Photoprotection; Photosystem II; PsbS; Winter stress; Zeaxanthin

Indexed keywords

ARABIDOPSIS PROTEIN; ELIP PROTEIN, ARABIDOPSIS; ELIP PROTEIN, PLANT; PSBS PROTEIN, PLANT; VEGETABLE PROTEIN; XANTHOPHYLL;

ANTIBODY; CONIFEROUS TREE; DISSIPATION; PHOTOPROTECTION; PHOTOSYNTHESIS; PROTEIN; SUBALPINE ENVIRONMENT;

ALTITUDE; ARTICLE; COLD; CONIFER; ECOSYSTEM; GENE; GENE EXPRESSION REGULATION; METABOLISM; MULTIGENE FAMILY; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; PLANT GENE; PONDEROSA PINE; SEASON; SUNLIGHT; TREE;

ALTITUDE; ARABIDOPSIS PROTEINS; COLD; COLD TEMPERATURE; CONIFEROPHYTA; ECOSYSTEM; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MULTIGENE FAMILY; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PINUS PONDEROSA; PLANT PROTEINS; SEASONS; SUNLIGHT; TREES; XANTHOPHYLLS;

CONIFEROPHYTA; PINUS PONDEROSA;

EID: 33747584898     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2006.01815.x     Document Type: Article

References (47)

1. Adams WW 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.
2. Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V. 2002. Photosynthesis and photoprotection in overwintering plants. Plant Biology 4: 545-557.
3. Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V. 2001. Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynthesis Research 67: 51-62.
4. Adams WW III, Zarter CR, Ebbert V, Demmig-Adams B. 2004. Photoprotective strategies of overwintering evergreens. Bioscience 54: 41-49.
5. Adamska I. 2001. The Elip family of stress proteins in the thylakoid membranes of pro- and eukaryota. In: Aro E-M, Andersson B, eds. Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, Vol. 11. Kluwer. Dordrecht, the Netherlands: Academic Publishers, 487-505.
6. Adamska I, Kloppstech K. 1991. Evidence for an association of the early light-inducible protein (ELIP) of pea with photosystem II. Plant Molecular Biology 16: 209-223.
7. Adamska I, Kloppstech K, Ohad I. 1993. Early light-inducible protein in pea is stable during light stress but is degraded during recovery at low light intensity. Journal of Biological Chemistry 268: 5438-5444.
8. Banet G, Pick U, Zamir A. 2000. Light-harvesting complex II pigments in association with Cbr, a homolog of higher-plant early light-inducible proteins in the unicellular green alga Dunaliella. Planta 210: 947-955.
9. Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, Niyogi KK. 2004. Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. Journal of Biological Chemistry 279: 6337-6344.
10. Bei-ParaskevopoulouT, Kloppstech K. 1999. The expression of early light-inducible proteins (ELIPs) under high-light stress as defense marker in Northern and Southern European cultivars of barley (Hordeum vulgare). Physiologia Plantarum 106: 105-111.
11. Delieux T, Walker DA. 1981. Polarographic measurement of photosynthetic oxygen evolution by leaf discs. New Phytologist 89: 165-178.
12. Demmig-Adams B, Adams WW III. 1996. The role of the xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1: 21-26.
13. Demmig-Adams B, Ebbert V, Mellmann DL, Schaffer L, Funk C, Zarter CR, Adamska I, Jansson S, Adams WW III. 2006. Modulation of PsbS and flexible versus sustained energy dissipation by light environment in different species. Physiologia Plantarum. (In press.)
14. Demmig-Adams B, Gilmore AM, Adams WW III. 1996. In vivo functions of carotenoids in high plants. FASEB Journal 10: 403-412.
15. Ebbert V, Adams WW III, Mattoo AK, Sokolenko A, Demmig-Adams B. 2005. Upregulation of a PSII core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir. Plant, Cell & Environment 28: 232-240.
16. Ensminger I, Sceshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O, Öquist G. 2004. Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests. Global Change Biology 10: 995-1008.
17. Gilmore AM, Ball MC. 2000. Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences USA 97: 11 098-11 101.
18. Gilmore AM, Yamamoto HY. 1991. Resolution of lutein and zeaxanthin using a non-encapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. Journal of Chromatography 543: 137-145.
19. Green BR, Durnford DG. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 47: 685-714.
20. Havaux M, Guedeney G, He QF, Grossman AR. 2003. Elimination of high-light-inducible polypeptides related to eukaryotic chlorophll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochimica et Biophysica Acta 1557: 21-33.
21. Havaux M, Niyogi KK. 1999. The violoaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences USA 96: 8762-8767.
22. He Q, Dolganov N, Björkman O, Grossman AR. 2001. The high light-inducible polypeptides in Synechocystis PCC6803. Journal of Biological Chemistry 276: 306-314.
23. Heddad M, Adamska I. 2000. Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding family. Proceedings of the National Academy of Sciences USA 97: 3741-3746.
24. Heddad M, Adamska I. 2002. The evolution of light stress proteins in photosynthetic organisms. Comparative and Functional Genomics 3: 504-510.
25. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR. 2005. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307: 433-436.
26. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M. 2003. Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences USA 100: 4921-4926.
27. Jansson S. 1999. A guide to the Lhc genes and their relatives in Arabidopsis. Trends in Plant Science 4: 236-240.
28. Jansson S, Andersson J, Kim SJ, Jackowski G. 2000. An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Molecular Biology 42: 345-351.
29. Jin ES, Polle JEW, Melis A. 2001. Involvement of zeaxanthin and of the Cbr protein in the repair of photosystem II from photoinhibition in the green alga Dunaliella salina. Biochimica et Biophysica Acta 1506: 244-259.
30. Jin ES, Yokthongwattana K, Polle JEW, Melis A. 2003. Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiology 132: 352-364.
31. Król M, Maxwell DP, Huner NPA. 1997. Exposure of Dunaliella salina to low temperature mimics the high light-induced accumulation of carotenoids and the carotenoid binding protein (Cbr). Plant and Cell Physiology 38: 213-216.
32. Lee Y, Tsai J, Sunkara S, Karamycheva S, Pertea G, Sultana R, Antonescu V, Chan A, Cheung F, Quackenbush J. 2005. The TIGR Gene Indices: clustering and assembling EST and known genes and integration with eukaryotic genomes. Nucleic Acids Research 33: D71-D74.
33. Levy H, Tal T, Shaish A, Zamir A. 1993. Cbr, an algal homolog of plant early light-induced proteins, is a putative zeaxanthin binding-protein. Journal of Biological Chemistry 268: 20892-20896.
34. Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK. 2004. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. Journal of Biological Chemistry 279: 22 866-22 874.
35. Lindahl M, Funk C, Webster J, Bingsmark S, Adamska I, Andersson B. 1997. Expression of Elips and PSII-S protein in spinach during acclimative reduction of the photosystem II antenna in response to increased light intensities. Photosynthesis Research 54: 227-236.
36. Lloyd J, Shibistova O, Zolotoukhine D, Kolle O, Arneth A, Wirth C, Styles JM, Tchebakova NM, Schulze E-D. 2002. Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest. Tellus 54B: 590-610.
37. 2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest. Oecologia 146: 130-147.
38. Monson RK, Turnipseed AA, Sparks JP, Harley PC, Scott-Denton LE, Sparks K, Huxman TE. 2002. Carbon sequestration in a high-elevation, subalpine forest. Global Change Biology 8: 459-478.
39. Montané M-H, Kloppstech K. 2000. The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258: 1-8.
40. Niyogi KK. 2000. Safety valves for photosynthesis. Current Opinion in Plant Biology 3: 455-560.
41. 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 & Environment 26: 245-253.
42. Öquist G, Huner NPA. 2003. Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology 54: 329-355.
43. Ottander C, Campbell D, Öquist G. 1995. Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197: 176-183.
44. Sigrist M, Staehelin LA. 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. Verhoeven AS, Adams WW III, Demmig-Adams B. 1998. Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant, Cell & Environment 21: 893-903.
46. Verhoeven AS, Adams WW III, Demmig-Adams B. 1999. The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118: 277-287.
47. Zarter CR, Adams WW III, Ebbert V, Adamska I, Jansson S, Demmig-Adams B. 2006. Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant, Cell, & Environment 29: 869-878.