Skip to main content

Advertisement

Log in

Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Modulation of the efficiency with which leaves convert absorbed light to photochemical energy [intrinsic efficiency of open photosystem II (PSII) centers, as the ratio of variable to maximal chlorophyll fluorescence] as well as leaf xanthophyll composition (interconversions of the xanthophyll cycle pigments violaxanthin and zeaxanthin) were characterized throughout single days and nights to entire seasons in plants growing naturally in contrasting light and temperature environments. All pronounced decreases of intrinsic PSII efficiency took place in the presence of zeaxanthin. The reversibility of these PSII efficiency changes varied widely, ranging from reversible-within-seconds (in a vine experiencing multiple sunflecks under a eucalypt canopy) to apparently permanently locked-in for entire seasons (throughout the whole winter in a subalpine conifer forest at 3,000 m). While close association between low intrinsic PSII efficiency and zeaxanthin accumulation was ubiquitous, accompanying features (such as trans-thylakoid pH gradient, thylakoid protein composition, and phosphorylation) differed among contrasting conditions. The strongest and longest-lasting depressions in intrinsic PSII efficiency were seen in the most stress-tolerant species. Evergreens, in particular, showed the most pronounced modulation of PSII efficiency and thermal dissipation, and are therefore suggested as model species for the study of photoprotection. Implications of the responses of field-grown plants in nature for mechanistic models are discussed.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adams WW III, Barker DH (1998) Seasonal changes in xanthophyll cycle-dependent energy dissipation in Yucca glauca Nuttall. Plant Cell Environ 21:501–512

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Adams WW III, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92:451–458

    Article  CAS  Google Scholar 

  • Adams WW III, Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18:117–127

    Article  Google Scholar 

  • Adams WW III, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 583–604

    Google Scholar 

  • Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990a) 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 180:166–174

    Article  CAS  Google Scholar 

  • Adams WW III, Winter K, Schreiber U, Schramel P (1990b) Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal leaf senescence. Plant Physiol 92:1184–1190

    Article  PubMed  CAS  Google Scholar 

  • Adams WW III, Volk M, Hoehn A, Demmig-Adams B (1992) Leaf orientation and the response of the xanthophyll cycle to incident light. Oecologia 90:404–410

    Article  Google Scholar 

  • Adams WW III, Demmig-Adams B, Lange OL (1993) Carotenoid composition and metabolism in green and blue–green algal lichens in the field. Oecologia 94:576–584

    Article  Google Scholar 

  • Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995a) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276

    Article  CAS  Google Scholar 

  • Adams WW III, Hoehn A, Demmig-Adams B (1995b) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22:75–85

    Article  CAS  Google Scholar 

  • Adams WW III, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent 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 22:125–136

    Article  CAS  Google Scholar 

  • 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. Photosynth Res 67:51–62

    Article  PubMed  CAS  Google Scholar 

  • Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biol 4:545–557

    Article  Google Scholar 

  • Adams WW III, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49

    Article  Google Scholar 

  • Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Advances in photosynthesis and respiration, vol 21. Springer, Dordrecht, pp 49–64

    Chapter  Google Scholar 

  • Allen JF, Mullineaux CW (2004) Probing the mechanism of state transitions in oxygenic photosynthesis by chlorophyll fluorescence spectroscopy, kinetics and imaging. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 447–461

    Google Scholar 

  • Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS, 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 25:95–103

    Article  CAS  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Article  Google Scholar 

  • Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106:12311–12316

    Article  PubMed  CAS  Google Scholar 

  • Brugnoli E, Björkman O (1992) Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbency changes related to ΔpH and zeaxanthin formation. Photosynth Res 32:23–35

    Article  CAS  Google Scholar 

  • Chen X, Han H, Jiang P, Nie L, Bao H, Fan P, Lv S, Feng J, Li Y (2011) Transformation of β-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant Cell Physiol 52:909–921

    Article  PubMed  CAS  Google Scholar 

  • Cleland RE, Demmig-Adams B, Adams WW III, Winter K (1990) Phosphorylation state of the light-harvesting chlorophyll–protein complexes of photosystem II and chlorophyll fluorescence characteristics in Monstera deliciosa Liebm. and Glycine max (L.) Merill in response to light. Aust J Plant Physiol 17:580–599

    Google Scholar 

  • Davidson PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance of Arabidopsis. Nature 418:203–206

    Article  Google Scholar 

  • Demmig B, 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 171:171–184

    Article  CAS  Google Scholar 

  • Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84:218–224

    Article  PubMed  CAS  Google Scholar 

  • Demmig B, Winter K, Krüger A, Czygan F-C (1988) Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. Plant Physiol 87:17–24

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1990) The carotenoid zeaxanthin and “high-energy-state quenching” of chlorophyll fluorescence. Photosynth Res 25:187–197

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15:411–419

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal dissipation. New Phytol 172:11–21

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Winter K, Meyer A, Schreiber U, Pereira JS, Krüger A, Czygan F-C, Lange OL (1989a) Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the “midday depression” of net CO2 uptake in Arbutus unedo growing in Portugal. Planta 177:377–387

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989b) Light response of CO2 assimilation, dissipation of excess excitation energy, and zeaxanthin content of sun and shade leaves. Plant Physiol 90:881–886

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Czygan F-C (1989c) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2 % O2, 0 % CO2. Plant Physiol 90:887–893

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Cygan F-C (1989d) Zeaxanthin synthesis, energy dissipation, and photoprotection of photosystem II at chilling temperatures. Plant Physiol 90:894–898

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Winkelmann E, Krüger A, Czygan F-C (1989e) Photosynthetic characteristics and the ratios of chlorophyll, β-carotene, and the components of the xanthophyll cycle upon a sudden increase in growth light regime in several plant species. Bot Acta 102:112–125

    Google Scholar 

  • Demmig-Adams B, Adams WW III, Czygan F-C, Schreiber U, Lange OL (1990a) Differences in the capacity for radiationless energy dissipation in green and blue–green algal lichens associated with differences in carotenoid composition. Planta 180:582–589

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Green TGA, Czygan F-C, Lange OL (1990b) Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the xanthophyll cycle. Oecologia 84:451–456

    Google Scholar 

  • Demmig-Adams B, Adams WW III, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W, Björkman O (1990c) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92:293–301

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Máguas C, Adams WW III, Meyer A, Kilian E, Lange OL (1990d) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue–green phycobionts. Planta 180:400–409

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible PSII efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Verhoeven AS, Bowling DR (1996) Using chlorophyll fluorescence to assess the allocation of absorbed light to thermal dissipation of excess excitation. Physiol Plant 98:253–264

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, 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. Physiol Plant 127:670–680

    Article  CAS  Google Scholar 

  • Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the β-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1302–1318

    Google Scholar 

  • Ebbert V, Demmig-Adams B, Adams WW III, Mueh KE, Staehelin LA (2001) Association between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynth Res 67:63–78

    Article  PubMed  CAS  Google Scholar 

  • 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 Environ 28:232–240

    Article  CAS  Google Scholar 

  • Falbel TG, Staehelin LA, Adams WW III (1994) Analysis of xanthophyll cycle carotenoids and chlorophyll fluorescence in light intensity-dependent chlorophyll-deficient mutants of wheat and barley. Photosynth Res 42:191–202

    Article  CAS  Google Scholar 

  • Förster B, Pogson BJ, Osmond CB (2011) Lutein from deepoxidation of lutein epoxide replaces zeaxanthin to sustain an enhanced capacity for nonphotochemical quenching in avocado leaves in the dark. Plant Physiol 156:393–403

    Article  PubMed  Google Scholar 

  • Gao S, Han H, Feng H-L, Zhao S-J, Meng Q-W (2010) Overexpression and suppression of violaxanthin de-epoxidase affects the sensitivity of photosystem II photoinhibition to high light and chilling stress in transgenic tobacco. J Integr Plant Biol 52:332–339

    Article  PubMed  CAS  Google Scholar 

  • Gilmore AM, Björkman O (1995) Temperature-sensitive coupling and uncoupling of ATPase-mediated, nonradiative energy-dissipation—similarities between chloroplasts and leaves. Planta 197:646–654

    Article  CAS  Google Scholar 

  • Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in plants. Fischer, Stuttgart, pp 57–79

    Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574

    Article  PubMed  CAS  Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    Article  PubMed  CAS  Google Scholar 

  • Jin ES, Yokhongwattana K, Polle JEW, Melis A (2003) Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiol 132:352–364

    Article  PubMed  CAS  Google Scholar 

  • Keren N, Krieger-Liszkay A (2011) Photoinhibition: molecular mechanisms and physiological significance. Physiol Plant 142:1–5

    Article  PubMed  CAS  Google Scholar 

  • Kilb B, Wietoska H, Godde D (1996) Changes in the expression of photosynthetic genes precede loss of photosynthetic activities and chlorophyll when glucose is supplied to mature spinach leaves. Plant Sci 115:225–235

    Article  CAS  Google Scholar 

  • Kim CH, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signaling in plants. EMBO Rep 9:435–439

    Article  PubMed  CAS  Google Scholar 

  • Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978

    Article  PubMed  CAS  Google Scholar 

  • Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115

    Article  PubMed  CAS  Google Scholar 

  • Krapp A, 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 195:313–323

    Article  CAS  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 463–495

    Google Scholar 

  • Li XP, 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. J Biol Chem 279:22866–22874

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812

    Article  PubMed  CAS  Google Scholar 

  • Liao P-N, Bode S, Wilk L, Hafi N, Walla PJ (2010) Correlation of electronic carotenoid–chlorophyll interactions and fluorescence quenching with the aggregation of native LHC II and chlorophyll deficient mutants. Chem Phys 373:50–55

    Article  CAS  Google Scholar 

  • Logan BA, Adams WW III, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Funct Plant Biol 34:853–859

    Article  CAS  Google Scholar 

  • Melis A (1999) Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • 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 Biol 8:459–478

    Article  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    Article  PubMed  CAS  Google Scholar 

  • Oguchi R, Terashima I, Kou J, Chow WS (2011) Operation of dual mechanisms that both lead to photoinactivation of Photosystem II in leaves by visible light. Physiol Plant 142:47–55

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Berg A, Berkowicz SM, Kaplan A, Keren N (2011) Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiol Plant 142:79–86

    Article  PubMed  CAS  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355

    Article  PubMed  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 1–24

    Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field—quintessential inefficiencies of the light and dark reactions of photosynthesis. J Exp Bot 46:1351–1362

    CAS  Google Scholar 

  • Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400

    Article  PubMed  CAS  Google Scholar 

  • Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    Article  PubMed  CAS  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81

    Article  PubMed  CAS  Google Scholar 

  • Stitt M, von Schaewen A, Willmitzer L (1991) Sink regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin cycle enzymes and an increase of glycolytic enzymes. Planta 183:40–50

    CAS  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  PubMed  CAS  Google Scholar 

  • Tikkanen M, Aro E-M (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817:232–238

    Article  PubMed  CAS  Google Scholar 

  • Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’. Trends Plant Sci 16:126–131

    Article  PubMed  CAS  Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 1817:209–217

    Article  PubMed  CAS  Google Scholar 

  • Vener AV (2007) Environmentally modulated phosphorylation and dynamics of proteins in photosynthetic membranes. Biochim Biophys Acta 1767:449–457

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Przybyla D, Camp ROD, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185

    Article  PubMed  CAS  Google Scholar 

  • Wahadoszamen M, Berera R, Ara AM, Romero E, von Grondelle R (2012) Identification of two emitting sites in the dissipative state of the major light harvesting antenna. Phys Chem Chem Phys 14:759–766

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Li B, Feng H-L, Zhang Q-Y, Yang X-H, Meng Q-W (2010) Anti-sense mediated suppression of tomato zeaxanthin epoxidase alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. Photosynthetica 48:409–416

    Article  CAS  Google Scholar 

  • Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51:639–648

    Article  CAS  Google Scholar 

  • Zarter CR, Adams WW III, Ebbert V, Cuthbertson D, Adamska I, Demmig-Adams B (2006a) Winter downregulation of intrinsic photosynthetic capacity coupled with upregulation of Elip-like proteins and persistent energy dissipation in a subalpine forest. New Phytol 172:272–282

    Article  PubMed  CAS  Google Scholar 

  • Zarter CR, Adams WW III, Ebbert V, Adamska I, Jansson S, Demmig-Adams B (2006b) Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant Cell Environ 29:869–878

    Article  PubMed  CAS  Google Scholar 

  • Zarter CR, Demmig-Adams B, Ebbert V, Adamska I, Adams WW III (2006c) Photosynthetic capacity and light harvesting efficiency during the winter-to-spring transition in subalpine conifers. New Phytol 172:283–292

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Science Foundation (Award Numbers IOS-0841546 and DEB-1022236) and the University of Colorado at Boulder.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara Demmig-Adams.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Demmig-Adams, B., Cohu, C.M., Muller, O. et al. Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113, 75–88 (2012). https://doi.org/10.1007/s11120-012-9761-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-012-9761-6

Keywords

Navigation