Skip to main content
Log in

May photoinhibition be a consequence, rather than a cause, of limited plant productivity?

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

Abstract

Photoinhibition in leaves in response to high and/or excess light, consisting of a decrease in photosynthesis and/or photosynthetic efficiency, is frequently equated to photodamage and often invoked as being responsible for decreased plant growth and productivity. However, a review of the literature reveals that photoinhibited leaves characterized for foliar carbohydrate levels were invariably found to possess high levels of sugars and starch. We propose that photoinhibition should be placed in the context of whole-plant source–sink regulation of photosynthesis. Photoinhibition may represent downregulation of the photosynthetic apparatus in response to excess light when (1) more sugar is produced in leaves than can be utilized by the rest of the plant and/or (2) more light energy is harvested than can be utilized by the chloroplast for the fixation of carbon dioxide into sugars.

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

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

    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

    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

    Google Scholar 

  • Adams WW III, Smith SD, Osmond CB (1987) Photoinhibition of the CAM succulent Opuntia basilaris growing in Death Valley: evidence from 77 K fluorescence and quantum yield. Oecologia 71:221–228

    Google Scholar 

  • Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180:166–174

    CAS  Google Scholar 

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

    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

    CAS  Google Scholar 

  • Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V, Brightwell AK, Barker DH, Zarter CR (2001a) Photosynthesis, xanthophylls, and D1 phosphorylation under winter stress. In PS2001 Proceedings: 12th International Congress on Photosynthesis, CSIRO Publishing, Melbourne. Available at http://www.publish.csiro.au/ps2001

  • Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001b) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res 67:51–62

    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

    Google Scholar 

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

    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

    Google Scholar 

  • Adams WW III, Watson AM, Mueh KE, Amiard V, Turgeon R, Ebbert V, Logan BA, Combs AF, Demmig-Adams B (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynth Res 94:455–466

    PubMed  CAS  Google Scholar 

  • Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition: a historical perspective. Photosynth Res 76:343–370

    PubMed  CAS  Google Scholar 

  • Alves PLDA, Magalhães ACN, Barja PR (2002) The phenomenon of photoinhibition of photosynthesis and its importance in reforestation. Bot Rev 68:193–208

    Google Scholar 

  • Baker NR, Bowyer JR (1994) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Baker NR, Farage PK, Stirling CM, Long SP (1994) Photoinhibition of crop photosynthesis in the field at low temperatures. In: Baker NR, Bowyer JR (eds) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 349–363

    Google Scholar 

  • Ball MC (1994) The role of photoinhibition during tree seedling establishment at low temperatures. In: Baker NR, Bowyer JR (eds) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 365–376

    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

    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

    Google Scholar 

  • Blennow K, Lang ARG, Dunne P, Ball MC (1998) Cold-induced photoinhibition and growth of seedling snow gum (Eucalyptus pauciflora) under differing temperature and radiation regimes in fragmented forests. Plant Cell Environ 21:407–416

    Google Scholar 

  • Brüggemann W (1992) Effects of long-term chilling under low irradiance on photosynthesis parameters of four Fabaceae species of different chilling tolerance. Photosynthetica 27:619–626

    Google Scholar 

  • Campbell DA, Tyystjärvi E (2012) Parameterization of photosystem II photoinactivation and repair. Biochim Biophys Acta 1817:258–265

    PubMed  CAS  Google Scholar 

  • Cheng J, Fan P, Liang Z, Wang Y, Niu N, Li W, Li S (2009) Accumulation of end products in source leaves affects photosynthetic rate in peach via alteration of stomatal conductance and photosynthetic efficiency. J Amer Soc Hort Sci 134:667–676

    Google Scholar 

  • Close DC, Beadle CL (2003) Chilling-induced photoinhibition, nutrition and growth analysis of Eucalyptus nitens seedlings during establishment. Tree Physiol 23:217–226

    PubMed  Google Scholar 

  • Critchley C (1994) D1 protein turnover: Response to photodamage or regulatory mechanism? In: Baker NR, Bowyer JR (eds) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 195–203

    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

    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

    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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Moeller DL, Logan BA, Adams WW III (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola. Planta 205:367–374

    CAS  Google Scholar 

  • Demmig-Adams B, Ebbert V, Zarter CR, Adams WW III (2006a) Characteristics and species-dependent employment of flexible versus sustained thermal dissipation and photoinhibition. In: Demmig-Adams B, Adams WW III, Adams WW III, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. advances in photosynthesis and respiration, vol 21. Springer, Dordrecht, pp 39–48

    Google Scholar 

  • Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, Schaffer L, Funk C, Zarter CR, Adamska I, Jansson S, Adams WW III (2006b) Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species. Physiol Plant 127:670–680

    CAS  Google Scholar 

  • Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88

    PubMed  CAS  Google Scholar 

  • Duan W, Fan PG, Wan LJ, Li WD, Yan ST, Li SH (2008) Photosynthetic response to low sink demand after fruit removal in relation to photoinhibition and photoprotection in peach trees. Tree Physiol 28:123–132

    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

    CAS  Google Scholar 

  • Edelman M, Mattoo AK (2006) The D1 protein: past and future perspectives. 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 23–38

    Google Scholar 

  • Einhorn KS, Rosenqvist E, Levernz JW (2004) Photoinhibition in seedlings of Fraxinus and Fagus under natural light conditions: implications for forest regeneration? Oecologia 140:241–251

    PubMed  Google Scholar 

  • 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 Biol 10:995–1008

    Google Scholar 

  • Falkowski PG, Greene R, Kolber Z (1994) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosyinthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 407–432

    Google Scholar 

  • Farage PR, Long SP (1991) The occurrence of photoinhibition in an over-wintering crop of oil-seed rape (Brassica napus L.) and its correlation with changes in crop growth. Planta 185:279–286

    Google Scholar 

  • Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 97:11098–11101

    PubMed  CAS  Google Scholar 

  • Godde D, Hefer M (1994) Photoinhibition and light-dependent turnover of the D1 reaction-centre polypeptide of photosystem II are enhanced by mineral-stress conditions. Planta 193:290–299

    CAS  Google Scholar 

  • Goh CH, Ko SM, Koh S, Kim YJ, Bae HJ (2012) Photosynthesis and environments: photoinhibition and repair mechanisms in plants. J Plant Biol 55:93–101

    CAS  Google Scholar 

  • Han S, Tang N, Jiang H-X, Yang L-T, Li Y, Chen L-S (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153

    CAS  Google Scholar 

  • Hymus GJ, Ellsworth DS, Baker NR, Long SP (1999) Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? A chlorophyll fluorescence study of mature loblolly pine. Plant Physiol 120:1183–1191

    PubMed  CAS  Google Scholar 

  • Hymus GJ, Dukstra P, Baker NR, Drake BG, Long SP (2001) Will rising CO2 protect plants from the midday sun? A study of photoinhibition of Quercus myrtifolia in a scrub-oak community in two seasons. Plant Cell Environ 24:1361–1368

    CAS  Google Scholar 

  • Jones PG, Lloyd JC, Raines CA (1996) Glucose feeding of intact wheat plants represses the expression of a number of Calvin cycle genes. Plant Cell Environ 19:231–236

    CAS  Google Scholar 

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

    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

    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

    PubMed  CAS  Google Scholar 

  • Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21:234–244

    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

    CAS  Google Scholar 

  • Krapp A, Quick WP, Stitt M (1991) Ribulose-1,5-bisphosphate carboxylase-oxygenase, other Calvin-cycle enzymes, and chlorophyll decrease when glucose is supplied to mature spinach leaves via the transpiration stream. Planta 186:58–69

    CAS  Google Scholar 

  • Krapp A, Hofmann B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3:817–828

    CAS  Google Scholar 

  • Krause GH, Gallé A, Virgo A, García M, Bucic P, Jahns P, Winter K (2006) High-light stress does not impair biomass accumulation of sun-acclimated tropical tree seedlings (Calophyllum longifolium Willd. and Tectona grandis L. f.). Plant Biol 8:31–41

    PubMed  CAS  Google Scholar 

  • Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81:4070–4074

    PubMed  CAS  Google Scholar 

  • Kyle DJ, Osmond CB, Arntzen CJ (1987) Photoinhibition. Topics in photosynthesis, vol 9. Elsevier, Amsterdam

    Google Scholar 

  • Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Berlin

    Google Scholar 

  • Layne DR, Flore JA (1993) Physiological responses of Prunus cerasus to whole-plant source manipulation. Leaf gas exchange, chlorophyll fluorescence, water relations and carbohydrate concentrations. Physiol Plant 88:44–51

    CAS  Google Scholar 

  • Logan BA, Barker DH, Adams WW III, 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 24:27–33

    Google Scholar 

  • Logan BA, Demmig-Adams B, Rosenstiel TN, Adams WW III (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–220

    PubMed  CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    CAS  Google Scholar 

  • Losciale P, Chow WS, Grappadelli LC (2010) Modulating the light environment with the peach ‘asymmetric orchard’: effects on gas exchange performances, photoprotection, and photoinhibition. J Exp Bot 61:1177–1192

    PubMed  CAS  Google Scholar 

  • Lundell R, Saarinen T, Aström H, Hänninen H (2008) The boreal dwarf shrub Vaccinium vitis-idaea retains its capacity for photosynthesis through the winter. Botany 86:491–500

    CAS  Google Scholar 

  • Makino A, Mae T (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol 40:999–1006

    CAS  Google Scholar 

  • Mondal MH, Brun WA, Brenner ML (1978) Effects of sink removal on photosysnthesis and senescence in leaves of soybean (Glycine max L.) plants. Plant Physiol 61:394–397

    PubMed  CAS  Google Scholar 

  • Monson RK, Turnipseed AA, Sparks JP, Harley PC, Scott-Denton LE, Sparks LK, Huxman TE (2002) Carbon sequestration in a high-elevation, subalpine forest. Glob Change Biol 8:459–478

    Google Scholar 

  • Morales F, Belkhodja R, Abadía A, Abadía J (2000) Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient, field-grown pear trees (Pyrus communis L.). Photosynth Res 63:9–21

    PubMed  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    PubMed  CAS  Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133

    PubMed  CAS  Google Scholar 

  • Myers DA, Thomas RB, DeLucia EH (1999) Photosynthetic responses of loblolly pine (Pinus taeda) needles to experimental reduction in sink demand. Tree Physiol 19:235–242

    PubMed  Google Scholar 

  • Naviaux RK (2012) Oxidative shielding or oxidative stress? Perspec Pharm 342:608–618

    CAS  Google Scholar 

  • Neale PJ (1987) Algal photoinhibition and photosynthesis in the aquatic environment. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 39–65

    Google Scholar 

  • Ögren E (1994) The significance of photoinhibition for photosynthetic productivity. In: Baker NR, Bowyer JR (eds) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 433–447

    Google Scholar 

  • Ögren E, Sjöström M (1990) Estimation of the effect of photoinhibition on the carbon gain in leaves of a willow canopy. Planta 181:560–567

    Google Scholar 

  • Oguchi R, Terashima I, Kou JC, 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

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibiiton 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

    PubMed  CAS  Google Scholar 

  • Pearcy RW (1987) Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments. Func Ecol 1:169–178

    Google Scholar 

  • Pearcy RW, Calkin HW (1983) Carbon dioxide exchange of C3 and C4 tree species in the understory of a Hawaiian forest. Oecologia 58:26–32

    Google Scholar 

  • Powles SB, Osmond CB, Thorne SW (1979) Photoinhibition of intact leaves of C3 plants illuminated in the absence of both carbon dioxide and of photorespiration. Plant Physiol 64:982–988

    PubMed  CAS  Google Scholar 

  • Quereix A, Dewar RC, Gaudillere JP, Dayau S, Valancogne C (2001) Sink feedback regulation of photosynthesis in vines: measurements and a model. J Exp Bot 52:2313–2322

    PubMed  CAS  Google Scholar 

  • Raven JA (1994) The cost of photoinhibition to plant communities. In: Baker NR, Bowyer JR (eds) Photoinhibiiton of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 449–464

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G (2012) Achieving yield gains in wheat. Plant Cell Environ 35:1799–1823

    PubMed  Google Scholar 

  • Rivas F, Gravina A, Agusti M (2007) Girdling effects on fruit set and quantum yield efficiency of PSII in two Citrus cultivars. Tree Physiol 27:527–535

    PubMed  CAS  Google Scholar 

  • Roden JS, 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 111:909–919

    PubMed  CAS  Google Scholar 

  • Roden JS, Egerton JJG, Ball MC (1999) Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring. Aust J Plant Physiol 26:37–46

    Google Scholar 

  • Savitch LV, Leonardos ED, Krol M, Jansson S, Grodzinski B, Huner NPA, Öquist G (2002) Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation. Plant Cell Environ 25:761–771

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Stitt M, von Schaewen A, Willmitzer L (1990) “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

    Google Scholar 

  • Strand Å, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene repression despite the accumulation of soluble carbohydrates. Plant J 12:605–614

    PubMed  CAS  Google Scholar 

  • Strand Å, Hurry V, Henkes S, Huner NPA, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376

    Google Scholar 

  • Tyystjärvi E (2013) Photoinhibition of photosystem II. Intl Rev Cell Mol Biol 300:243–303

    Google Scholar 

  • Urban L, Alphonsout L (2007) Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. Tree Physiol 27:345–352

    PubMed  CAS  Google Scholar 

  • Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111:505–514

    Google Scholar 

  • van Oosten J-J, Besford RT (1996) Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: climate of opinion. Photosynth Res 48:353–365

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Verhoeven AS, Adams WW III, Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96:567–576

    CAS  Google Scholar 

  • Verhoeven AS, Adams WW III, Demmig-Adams B (1998) Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant Cell Environ 21:893–903

    Google Scholar 

  • 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

    Google Scholar 

  • Way DA, Pearcy RW (2012) Sunflecks in tress and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:1066–1081

    PubMed  Google Scholar 

  • Werner C, Correia O (1996) Photoinhibition in cork-oak leaves under stress: influence of bark-stripping on the chlorophyll fluorescence emission in Quercus suber L. Trees 10:288–293

    Google Scholar 

  • Werner C, Ryel RJ, Correia O, Beyschlag W (2001) Effect of photoinhibition on whole-plant carbon gain assessed with a photosynthesis model. Plant Cell Environ 24:27–40

    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

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Zarter CR, Adams WW III, Ebbert V, Adamska I, Jansson S, Demmig-Adams B (2006c) 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

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work 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 William W. Adams III.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Adams, W.W., Muller, O., Cohu, C.M. et al. May photoinhibition be a consequence, rather than a cause, of limited plant productivity?. Photosynth Res 117, 31–44 (2013). https://doi.org/10.1007/s11120-013-9849-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9849-7

Keywords

Navigation