Advertisement

Energy Dissipation and Photoinhibition: A Continuum of Photoprotection

  • William W. Adams III
  • C. Ryan Zarter
  • Kristine E. Mueh
  • V’eronique Amiard
  • Barbara Demmig-Adams
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 21)

Keywords

Energy Dissipation Photosynthetic Electron Transport Plant Cell Environ Xanthophyll Cycle Evergreen Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams WW III and Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186: 390–398Google Scholar
  2. Adams WW III and Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18: 117–127CrossRefGoogle Scholar
  3. AdamsWWIII and Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC and Govindjee (eds) Chlorophyll a Fluorescence: A Probe of Photosynthesis, pp 583–604. Springer,CrossRefGoogle Scholar
  4. Dordrecht Adams WW III, D’\iaz M and Winter K (1989) Diurnal changes in photochemical efficiency, the reduction state of Q, radiationless energy dissipation, and non-photochemical fluorescence quenching in cacti exposed to natural sunlight in northern Venezuela. Oecologia 80: 553–561CrossRefGoogle Scholar
  5. Adams WW III, Demmig-Adams B, Winter K and Schreiber U (1990) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77K, as an indicator of the photon yield of photosynthesis. Planta 180: 166–174CrossRefGoogle Scholar
  6. Adams WW III, Demmig-Adams B, Verhoeven AS and Barker DH (1995a) ‘Photoinhibition’ during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22: 261–276CrossRefGoogle Scholar
  7. AdamsWWIII, Hoehn A and Demmig-Adams B (1995b) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22: 75–85CrossRefGoogle Scholar
  8. Adams WW III, Demmig-Adams B, Logan BA, Barker DH and Osmond CB (1999) Rapid changes in xanthophyll cycledependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant Cell Environ 22: 125–136CrossRefGoogle Scholar
  9. AdamsWWIII, Demmig-Adams B, Rosenstiel TN and EbbertV (2001a) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res 67: 51–62CrossRefGoogle Scholar
  10. Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V, Brightwell AK, Barker DH, Zarter CR (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/ps2001Google Scholar
  11. Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK and Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biol 4: 545–557CrossRefGoogle Scholar
  12. Adams WW III, Zarter CR, Ebbert V and Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. BioScience 54: 41–49CrossRefGoogle Scholar
  13. Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition – a historical perspective. Photosynth Res 76: 343–370Google Scholar
  14. Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem 2 – inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedCrossRefGoogle Scholar
  15. Bachmann KM, EbbertV, AdamsWWIII,Verhoeven AS, Logan BA and Demmig-Adams B (2004) Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery. Func Plant Biol 31: 803–813Google Scholar
  16. Baker NR and Bowyer JR (eds) (1994) Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field. Bios Scientific Publishers, Oxford Ball MC,Google Scholar
  17. Hodges VS and Laughlin GP (1991) Cold-induced photoinhibition limits regeneration of snow gum at tree-line. Funct Ecol 5: 663–668CrossRefGoogle Scholar
  18. Barber J (1995) Molecular basis of the vulnerability of photosystem II to damage by light. Aust J Plant Physiol 22: 201–208CrossRefGoogle Scholar
  19. Barber J and Andersson B (1992) Too much of a good thing – light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66PubMedCrossRefGoogle Scholar
  20. Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS and Smith SD (2002) Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species growing in the Mojave Desert. Plant Cell Environ 25: 95–103CrossRefGoogle Scholar
  21. Bilger W and Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of lightinduced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25: 173–185CrossRefGoogle Scholar
  22. Bilger W and Björkman O (1991) Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184: 226–234CrossRefGoogle Scholar
  23. Bilger W and Björkman O (1994) Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193: 238–246Google Scholar
  24. Björkman O (1987) Low-temperature chlorophyll fluorescence in leaves and its relationship to photon yield of photosynthesis in photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 123–144. Elsevier,Google Scholar
  25. Amsterdam Björkman O and Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origin. Planta 170: 489–504CrossRefGoogle Scholar
  26. Blennow K, Lang ARG, Dunne P and Ball MC (1998) Coldinduced photoinhibition and growth of seedling snow gum (Eucalyptus pauciflora) under differing temperature and radiation regimes in fragmented forests. Plant Cell Environ 21: 407–416CrossRefGoogle Scholar
  27. Braun E and Bachofen R (2004) Homoserine lactones and microcystin in cyanobacterial assemblages in Swiss lakes. Hydrobiol 522: 271–280CrossRefGoogle Scholar
  28. Cunningham FX Jr, Dennenberg RJ, Mustardy L, Jursinic PA and Gantt E (1989) Stoichiometry of photosystem I, photosystem II, and phycobilisomes in the red alga Porphyridium cruentum as a function of growth irradiance. Plant Physiol 91: 1179–1187CrossRefGoogle Scholar
  29. Demmig B and Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184CrossRefGoogle Scholar
  30. Demmig-Adams B and Adams WWIII (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15: 411–419CrossRefGoogle Scholar
  31. Demmig-Adams B and AdamsWWIII (1994a) Light stress and photoprotection related to the xanthophyll cycle. In: Foyer CH and MullineauxPM(eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, pp 105–126. CRC Press,Google Scholar
  32. Boca Raton Demmig-Adams B and Adams WW III (1994b) Capacity for energy dissipation in the pigment bed in leaves with different xanthophyll cycle pools. Aust J Plant Physiol 21: 575–588CrossRefGoogle Scholar
  33. Demmig-Adams B and Adams WWIII (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198: 460–470CrossRefGoogle Scholar
  34. Demmig-Adams B and Adams WW III (2003) Photoinhibition. In: Thomas B, Murphy D and Murray B (eds) Encyclopedia of Applied Plant Science, pp 707–714. Academic Press, LondonGoogle Scholar
  35. Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989a) Light response ofCO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol 90: 881–886CrossRefGoogle Scholar
  36. Demmig-Adams B, Winter K, Krüger A and Czygan F-C (1989b) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2 O 2, 0 CO2. Plant Physiol 90: 887–893CrossRefGoogle Scholar
  37. Demmig-Adams B, Adams WW III, Czygan F-C, Schreiber U and Lange OL (1990) Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180: 582–589CrossRefGoogle Scholar
  38. Demmig-Adams B, Adams WW III, Logan BA and Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible PS II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22: 249–260CrossRefGoogle Scholar
  39. Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Verhoeven AS and Bowling DR (1996a) Using chlorophyll fluorescence to assess the allocation of absorbed light to thermal dissipation or excess excitation. Physiol Plant 98: 253–264CrossRefGoogle Scholar
  40. Demmig-Adams B, Gilmore AM, Adams WW III (1996b) In vivo functions of carotenoids in higher plants. FASEB J 10: 403–412Google Scholar
  41. Demmig-Adams B, Moeller DL, Logan BA and AdamsWWIII (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205: 367–374Google Scholar
  42. Demmig-Adams B, Ebbert V, Zarter CR and Adams WW III (2005) Characteristics and species-dependent employment of flexible versus sustained thermal dissipation and photoinhibition. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 39–48. Springer,Google Scholar
  43. Dordrecht Dijkwel PP, Kock PAM, Bezemer R, Weisbeek PJ and Smeekens SCM (1996) Sucrose represses the developmentally controlled transient activation of the plastocyanin gene in Arabidopsis thaliana seedlings. Plant Physiol 110: 455–463Google Scholar
  44. Edelman M and Mattoo AK (2005) D1 protein retrospective: the sizzling ’80s. In: Demmig-Adams B, Adams WW III and MattooAK(eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 23–38. Springer,Google Scholar
  45. Dordrecht Endo T and Asada K (2005) Photosystem I and photoprotection: cyclic electron flow and water-water cycle. In: Demmig- Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 205–221. Springer,Google Scholar
  46. Dordrecht Ensminger I, Sveshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O and Ö quist G (2004) Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests. Glob Change Biol 10: 995–1008CrossRefGoogle Scholar
  47. Evens TJ, Kirkpatrick GJ, Millie DF, Chapman DF and Schofield OME (2001) Photophysiological response of the red-tide dinoflagellate Gymnodinium breve (Dinophyceae) under natural sunlight. J Plankton Res 23: 1177–1193CrossRefGoogle Scholar
  48. Fiekers JF, Marshal IB and Parsons RL (1979) Clindamycin and lincomycin alter miniature endplate current decay. Nature 281: 680–682PubMedCrossRefGoogle Scholar
  49. Gevaert F, Creach A, Davoult D, Migne A, Levavasseur G, Arzel P, Holl AC and Lemoine Y (2003) Laminaria saccharina photosynthesis measure in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar Ecol Prog Ser 247: 43–50CrossRefGoogle Scholar
  50. Gilmore AM (1997) Mechanistic aspects of xanthophyll cycledependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99: 197–209CrossRefGoogle Scholar
  51. Gilmore AM and Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 97: 11098–11101PubMedCrossRefGoogle Scholar
  52. Häder D-P (2005) Photoinhibition and UV response in the aquatic environment. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 87–105. Springer,Google Scholar
  53. Dordrecht Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in Plants, pp 57–79. Fischer, Stuttgart Huner NPA, Ivanov AG, Sane PV, Pocock T, Kr’ol M, Balserus A, Rosso D, Savitch LV, Hurry VM and Ö quist G (2005) Photoprotection of photosystem II: reaction center quenching versus antenna quenching. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 155–173. Springer,Google Scholar
  54. Hymus GJ, Ellsworth DS, Baker NR and Long SP (1999) Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? Achlorophyll fluorescence study of mature loblolly pine. Plant Physiol 120: 1183–1191PubMedCrossRefGoogle Scholar
  55. Jin ES, Yokthongwattana K, Polle JEW and Melis A (2003) Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiol 132: 352–364PubMedCrossRefGoogle Scholar
  56. Jung H-S and Niyogi KK (2005) Molecular analysis of photoprotection and photosynthesis. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 127–143. Springer,Google Scholar
  57. Dordrecht Kilb B, Wietoska H and Godde D (1996) Changes in the expression of photosynthetic genes precede the loss of photosynthetic activities and chlorophyll when glucose is supplied to mature spinach leaves. Plant Sci 115: 225–235CrossRefGoogle Scholar
  58. Kitajima M and Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105–115PubMedCrossRefGoogle Scholar
  59. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509–540PubMedCrossRefGoogle Scholar
  60. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21: 234–244PubMedCrossRefGoogle Scholar
  61. Krapp A and Stitt M (1995) An evaluation of direct and indirect mechanisms for the ‘sink-regulation’ of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195: 313–323CrossRefGoogle Scholar
  62. Külheim C, Agren J and Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91–93PubMedCrossRefGoogle Scholar
  63. Kyle DJ, Osmond CB and Arntzen CJ (eds) (1987) Photoinhibition. Elsevier, AmsterdamGoogle Scholar
  64. Lavaud J, Rousseau B and Etienne AL (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40: 130–137Google Scholar
  65. Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S and Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395PubMedCrossRefGoogle Scholar
  66. Li X-P, Phippard A, Pasari J and Niyogi KK (2002) Structure– function analysis of photosystem II subunit S (PsbS) in vivo. Func Plant Biol 29: 1131–1139CrossRefGoogle Scholar
  67. Logan BA, Barker DH, Adams WW III and Demmig-Adams B (1997) The response of xanthophyll cycle-dependent energy dissipation in Alocasia brisbanensis to sunflecks in a subtropical rainforest. Aust J Plant Physiol 24: 27–33CrossRefGoogle Scholar
  68. Logan BA, Demmig-Adams B, Rosenstiel TN and Adams WW III (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209: 213–220PubMedCrossRefGoogle Scholar
  69. Long SP, Humphries S and Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45: 633–662CrossRefGoogle Scholar
  70. Ma Y-Z, Holt NE, Li X-P, Niyogi KK and Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100: 4377–4382PubMedCrossRefGoogle Scholar
  71. Maher P and Schubert D (2000) Signaling by reactive oxygen species in the nervous system. Cell Mol Life Sci 57: 1287– 1305Google Scholar
  72. Marshall HL, Geider RJ and Flynn KJ (2000) A mechanistic model of photoinhibition. New Phytol 145: 347–359CrossRefGoogle Scholar
  73. Mattoo AK, Hoffman-Falk H, Marder JB and EdelmanM (1984) 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 81:1380–1384PubMedCrossRefGoogle Scholar
  74. Melis A (1999) Photosystem II damage and repair cycle in chloroplasts:what modulates the rate of photodamage in vivo? Trends Plant Sci 4: 130–135PubMedCrossRefGoogle Scholar
  75. Morales F, Abad’\ia A and Abad’\ia J (2005) Photoinhibition and photoprotection under nutrient deficiencies, drought, and salinity. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 65–85. Springer,Google Scholar
  76. Dordrecht Nishiyama Y, Allakhverdiev SI and Murata N (2005) Regulation by environmental conditions of the repair of photosystem II in cyanobacteria. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 193–203. Springer,Google Scholar
  77. Dordrecht Nor’en H, Svensson P, Stegmark R, Funk C, Adamska I and Andersson B (2003) Expression of early light-induced protein but not the PsbS protein is influenced by low temperature and depends on the development state of the plant in field-grown pea cultivars. Plant Cell Environ 26: 245–253CrossRefGoogle Scholar
  78. Okada K, Satoh K and Katoh S (1991) Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett 295: 155–158PubMedCrossRefGoogle Scholar
  79. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field, pp 1–24. Bios Scientific Publishers, OxfordGoogle Scholar
  80. Osmond CB and Förster B (2005) Photoinhibition: then and now. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 11–22. Springer,Google Scholar
  81. Dordrecht Osmond CB and Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field. Quintessential inefficiencies of the light and dark reactions of photosynthesis. J Exp Bot 46: 1351–1362Google Scholar
  82. OsmondCB, Badger M, Maxwell K, Björkman O and Leegood R (1997) Too many photons: Photorespiration, photoinhibition and photooxidation. Trends Plant Sci 2: 119–121CrossRefGoogle Scholar
  83. Paul MJ and Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52: 1383–1400PubMedCrossRefGoogle Scholar
  84. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44CrossRefGoogle Scholar
  85. Prior C, Fiekers JF, Henderson F, Dempster J, Marshall IG and Parsons RL (1990) End-plate ion channel block produced by lincosamide antibiotics and their chemical analogs. J Pharm Exp Ther 255: 1170–1176Google Scholar
  86. Roden JS and Ball MC (1996) The effect of elevated [CO2] on growth and photosynthesis of two Eucalyptus species exposed to high temperatures and water deficits. Plant Physiol 111: 909–919PubMedGoogle Scholar
  87. Roden JS, Egerton JJ and Ball MC (1999) Effect of elevated (CO2) on photosynthesis and growth of snowgum (Eucalyptus pauciflora) seedlings during winter and spring. Aust J Plant Physiol 26: 37–46CrossRefGoogle Scholar
  88. Schreiber U, BilgerWand Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D and CaldwellMM(eds) Ecophysiology of Photosynthesis, pp 49–70. Springer,Google Scholar
  89. Berlin Sopory SK, Greenberg BM, Mehta RA, Edelman M and Mattoo AK (1990) Free radical scavengers inhibit light-dependent degradation of the 32 kDa PS II reaction center protein. Z Naturforsch 45c: 412–417Google Scholar
  90. Telfer A, Oldham TC, Phillips D and Barber J (1999) Singlet oxygen formation detected by near-infrared emission from isolated photosystem II reaction centres: direct correlation between P680 triplet decay and luminescence rise kinetics and its consequences for photoinhibition. J Photochem Photobiol B Biol 48: 89–96CrossRefGoogle Scholar
  91. Teplitski M, Chen HC, Rajamani S, Gao MS, Merighi M, Sayre RT, Robinson JB, Rolfe BG and Bauer WD (2004) Chamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol 134: 137–146PubMedCrossRefGoogle Scholar
  92. Uhrmacher S, Hanelt D and Nultsch W (1995) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma. Mar Biol 123: 159– 165CrossRefGoogle Scholar
  93. Ursi S, Pedersen M, Plastino E and Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Mar Biol 142: 997–1007Google Scholar
  94. Verhoeven AS, Adams WW III and Demmig-Adams B (1996) Close relationship between the state of the xanthophyll pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96: 567–576CrossRefGoogle Scholar
  95. Verhoeven AS, Demmig-Adams B and Adams WW III (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol. 113: 817–824PubMedGoogle Scholar
  96. Verhoeven AS, Adams WW III and Demmig-Adams B (1998) Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant Cell Environ 21: 893–903CrossRefGoogle Scholar
  97. Verhoeven AS, Adams WW III and Demmig-Adams B (1999) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118: 277–287CrossRefGoogle Scholar
  98. Weindruch R and Sohal RS (1997) Caloric intake and aging. New Engl J Med 337: 986–994Google Scholar
  99. Werner C, Ryel RJ, Correia O and Beyschlag W (2001) Effects of photoinhibition on whole-plant carbon gain assessed with a photosynthesis model. Plant Cell Environ 24: 27–40CrossRefGoogle Scholar
  100. Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51: 639–648CrossRefGoogle Scholar
  101. Yamamoto HY (2005) Arandomwalk to and through the xanthophyll cycle. In: Demmig-AdamsB, Adams WWIII and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 1–10. Springer,Google Scholar
  102. Dordrecht Yokthongwattana K and Melis A (2005) Photoinhibition and recovery in oxygenic photosynthesis: Mechanism of a photosystem-II damage and repair cycle. In: Demmig-Adams B, Adams WWIII and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 175–191. Springer,Google Scholar
  103. Dordrecht Zhu XG, Ort DR, Whitmarsh J and Long SP (2004) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to lowlight may cause large losses in carbon gain by crop canopies: a theoretical analysis. J Exp Bot 55: 1167–1175CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • William W. Adams III
    • 1
  • C. Ryan Zarter
    • 1
  • Kristine E. Mueh
    • 1
  • V’eronique Amiard
    • 1
  • Barbara Demmig-Adams
    • 1
  1. 1.Department of Ecology & Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations