Abstract
We analyzed the response of potted strawberry tree (Arbutus unedo L.) seedlings exposed to water stress by withholding water for 10 d (WS). Leaf water potential, net CO2 assimilation, and stomatal conductance decreased with increasing water deficit. A 30 % reduction of chlorophyll (Chl) content in the antenna complexes was observed in WS-plants. Simultaneously, a decline of photochemical efficiency (Fv/Fm) occurred as a result of an excess of solar radiation energy when carbon assimilation was limited by stomata closure due to soil water deficit. The non-photochemical quenching of Chl fluorescence (ΦNPQ) significantly increased, as well as the leaf contents of zeaxanthin (Z) and antheraxanthin (A) at the expense of violaxanthin during the WS-period. Elevated predawn contents of de-epoxidized xanthophyll cycle components were associated with a sustained lowering of predawn photosystem 2 efficiency; this suggested an engagement of Z+A in a state primed for energy dissipation. Thus, the ability of strawberry trees to maintain the functionality of the xanthophyll cycle during the Mediterranean summer is an efficient mechanism to prevent irreversible damages to the photosynthetic machinery through thermal energy dissipation in the antenna and the reduction in photochemical efficiency.
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Abbreviations
- A:
-
antheraxanthin
- C:
-
control leaves
- ΔF/Fm′:
-
photochemical efficiency of photosystem 2 in the light
- Fm :
-
maximal fluorescence in the dark
- Fv/Fm :
-
photochemical efficiency of PS2 in the dark
- F0 :
-
minimal fluorescence in the dark
- g s :
-
stomatal conductance
- HPLC:
-
high-performance liquid chromatography
- PFD:
-
photon flux density
- PS2:
-
photosystem 2
- QB :
-
secondary plastoquinone acceptors of PS2
- RC:
-
reaction centre
- V:
-
violaxanthin
- VAZ:
-
total amount of xanthophyll cycle components
- VPD:
-
vapour pressure deficit
- WS:
-
water-stressed leaves
- Z:
-
zeaxanthin
- Φf,D :
-
sum of fluorescence and constitutive thermal dissipation
- ΦNPQ :
-
quantum yield of xanthophyll-regulated thermal energy dissipation
- ΦPS2 :
-
quantum yield of photochemistry
References
Adams, W.W., III, Demmig-Adams, B.: Carotenoid composition and down regulation of photosystem II in three conifer species during the winter.-Physiol. Plant. 92: 451–458, 1994.
Adams, W.W., III, Demmig-Adams, B.: The xanthophyll cycle and sustained thermal dissipation activity in Vinca minor and Euonymus kiautschovicus in winter.-Plant Cell Environ. 18: 117–127, 1995.
Adams, W.W., III, Demmig-Adams, B., Verhoeven, A.S., Barker, D.H.: Photoinhibition during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation.-Aust. J. Plant Physiol. 22: 261–276, 1995.
Aro, E.-M., McCaffery, S., Anderson, J.M.: Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances.-Plant Physiol. 103: 835–843, 1993
Barber, J.: Molecular basis of photoinhibition.-In: Mathis, P. (ed.): Photosynthesis, From Light to Biosphere. Vol. IV. Pp. 159–164. Kluwer Academic Publ., Dordrecht-Boston-London 1995.
Barker, D.H., Adams, W.W., III, Demmig-Adams, B., Logan, B.A., Verhoeven, A.S., Smith, S.D.: 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, 2002.
Barker, D.H., Adams, W.W., III, Logan, B.A., Demmig-Adams, B.: Photochemistry and xanthophyll cycle-dependent energy dissipation in differently oriented cladodes of Opuntia stricta during the winter.-Aust. J. Plant Physiol. 25: 95–104, 1998.
Bertamini, M., Nedunchezhian, N.: Photoinhibition and recovery of photosynthesis in leaves of Vitis berlandieri and Vitis rupestris.-J. Plant Physiol. 161: 203–210, 2004.
Björkman, O.: High-irradiance stress in higher plants and interaction with other stress factors.-In: Biggins, J. (ed.): Progress in Photosynthesis Research. Vol. 4. Pp. 11–18. Martin Nijhoff, Dordrecht-Boston-Lancaster 1987.
Björkman, O., Demmig-Adams, B.: Regulation of photosynthetic light energy capture, conversion and dissipation in leaves of higher plants.-In: Schulze, E.D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17–47. Springer-Verlag, Berlin 1994.
Carpentier, R.: Influence of high light intensity on photosynthesis: photoihibition and energy dissipation.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis. Pp. 443–450. Marcel Dekker, New York-Basel-Hong Kong 1995.
Choudhury, N.K., Behera, R.K.: Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents.-Photosynthetica 39: 481–488, 2001.
Comstock, J.P., Mahall, B.E.: Drought and changes in leaf orientation for two California chaparral shrubs: Ceanothus megacarpus and Ceanothus crassifolius.-Oecologia 65: 531–535, 1985.
de las Rivas, J., Abadía, A., Abadía, J.: A new reversed phase-HPLC method resolving all major higher plant photosynthetic pigments.-Plant Physiol. 91: 190–192, 1989.
Demmig, B., Björkman, O.: Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants.-Planta 171: 171–184, 1987.
Demmig, B., Winter, K., Krüger, A., Czygan, F.-C.: Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress.-Plant Physiol. 84: 17–24, 1988.
Demmig-Adams, B., Adams, W.W., III: Photoprotection and other responses of plants to high light stress.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 599–626, 1992.
Demmig-Adams, B., Adams, W.W., III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species.-Planta 198: 460–470, 1996a.
Demmig-Adams, B., Adams, W.W., III: The role of xanthophyll cycle carotenoids in the protection of photosynthesis.-Trends Plant Sci. 1: 21–26, 1996b.
Demmig-Adams, B., Adams, W.W., III, Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.-Physiol. Plant. 98: 253–264, 1996a.
Demmig-Adams, B., Adams, W.W., III, Winter, K., Meyer, A., Schreiber, U., Pereira, J.S., Krüger, A., Czygan, F.-C., Lange, O.L.: Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the midday depression and net CO2 uptake in Arbutus unedo growing in Portugal.-Planta 177: 377–387, 1989.
Demmig-Adams, B., Gilmore, A.M., Adams, W.W., III: In vivo functions of carotenoids of higher plants.-FASEB J. 10: 403–412, 1996b.
di Castri, F.: Mediterranean-type shrublands of the word.-In: di Castri, F., Goodall, D.W., Specht, R.L. (ed.): Mediterranean-Type Shrublands. Pp. 1–52. Elsevier, Amsterdam 1981.
Faria, T., Silvério, D., Breia, E., Cabral, R., Abadia, A., Pereira, J.S., Chaves, M.M.: Differences in the response of carbon assimilation to summer stress (water deficits, high light and temperature) in four Mediterranean tree species.-Physiol. Plant. 102: 419–428, 1998.
García-Plazaola, J.I., Artetxe, U., Becerril, J.M.: Diurnal changes in antioxidant and carotenoid composition in the Mediterranean sclerophyll tree Quercus ilex (L) during winter.-Plant Sci. 143: 125–133, 1999.
García-Plazaola, J.I., Becerril, J.M.: A rapid high-performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: Simultaneous determination of carotenoids and tocopherols.-Phytochem. Anal. 10: 307–313, 1999.
Giardi, M.T., Cona, A., Geiken, B., Kučera, T., Masojídek, J., Mattoo, A.K.: Long-term drought stress induces structural and functional reorganization of photosystem II.-Planta 199: 118–125, 1996.
Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.-Physiol. Plant. 99: 197–209, 1997.
Greer, D.H., Berry, J.A., Björkman, O.: Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery.-Planta 168: 253–260, 1986.
Hendrickson, L., Furbank, R.T., Chow, W.S.: A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence.-Photosynth. Res. 82: 73–81, 2004.
Kaiser, W.M.: Effects of water deficit on photosynthetic capacity.-Physiol. Plant. 71: 142–149, 1987.
Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis — the basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.
Kyle, D.J., Kuang, T.-Y., Watson, J.L., Arntzen, C.J.: Movement of a sub-population of the light-harvesting complex (LHCII) from grana to stroma lamellae as a consequence of its phosphorylation.-Biochim. biophys. Acta 765: 89–96, 1984.
Lavergne, J., Briantais, J.-M.: Photosystem II heterogeneity.-In: Ort, D.R., Yocum, C.F. (ed.): Oxygen Photosynthesis: the Light Reactions. Pp. 265–287. Kluwer Academic Publ., Dordrecht-Boston-London 1996.
Levizou, E., Petropoulou, E., Manetas, Y.: Carotenoid composition of peridermal twigs does not fully conform to a shade acclimation hypothesis.-Photosynthetica 42: 591–596, 2004.
Logan, B.A., Grace, S.C., Adams, W.W., III, Demmig-Adams, B.: Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments.-Oecologia 116: 9–17, 1998.
Long, S.P., Humphries, S., Falkowski, P.G.: Photoinhibition of photosynthesis in nature.-Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 633–662, 1994.
Masojídek, J., Trivedi, S., Halshaw, L., Alexiou, A., Hall, D.O.: Synergistic effect of drought and light stress in sorghum and pearl millet.-Plant Physiol. 96: 198–207, 1991.
Mooney, H.A.: Primary production in Mediterranean-climate regions.-In: Di Castri, F., Goodall, D.W., Specht, R.L. (ed.): Mediterranean-Type Shrublands. Pp. 249–256. Elsevier, Amsterdam 1981.
Müller, M., Hernández, I., Alegre, L., Munné-Bosch, S.: Enhanced α-tocopherol quinone levels and xanthophyll cycle deepoxidation in rosemary plants exposed to water deficit during a Mediterranean winter.-J. Plant Physiol. 163: 601–606, 2006.
Munné-Bosch, S., Alegre, L.: Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants.-Planta 210: 925–931, 2000.
Munné-Bosch, S., Peñuelas, J.: Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions.-Plant Sci. 166: 1105–1110, 2004.
Murata, N., Takahashi, S., Nishiyama, Y., Allakhverdiev, S.I.: Photoinhibition of photosystem II under environmental stress.-Biochim. biophys. Acta 1767: 414–421, 2007.
Nahal, I.: The Mediterranean climate from a biological viewpoint.-In: di Castri, F., Goodall, D.W., Specht, R.L. (ed.): Mediterranean-Type Shrublands. Pp. 63–86. Elsevier, Amsterdam 1981.
Niinemets, Ü., Bilger, W., Kull, O., Tenhunen, J.D.: Acclimation to high irradiance in temperate deciduous trees in the field: changes in xanthophyll cycle pool size and in photosynthetic capacity along a canopy light gradient.-Plant Cell Environ. 21: 1205–1218, 1998.
Niyogi, K.K., Grossman, A.R., Björkman, O.: Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion.-Plant Cell 10: 1121–1134, 1998.
Osmond, C.B.: What is photoinhibition? Some insights from comparisons of shade and sun plants.-In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photosynthesis, from Molecular Mechanisms to the Field. Pp. 1–24. Bios Scientific Publishers, Oxford 1994.
Pfündel, E., Bilger, W.: Regulation and possible function of the violaxanthin cycle.-Photosynth. Res. 42: 89–109, 1994.
Powles, S.B.: Photoinhibition of photosynthesis induced by visible light.-Annu. Rev. Plant Physiol. 35: 15–44, 1984.
Richardson, A.D., Duigan, S.P., Berlyn, G.P.: An evaluation of noninvasive methods to estimate foliar chlorophyll content.-New Phytol. 153: 185–194, 2002.
Saccardy, K., Pineau, B., Roche, O., Cornic, G.: Photochemical efficiency of Photosystem II and xanthophyll cycle components in Zea mays leaves exposed to water stress and high light.-Photosynth. Res. 56: 57–66, 1998.
Smirnoff, N.: The role of active oxygen in the response of plants to water deficit and desiccation.-New Phytol. 125: 27–58, 1993.
Tyystjärvi, E., Aro, E.M.: The rate constant of photoinhibition, measured in lincomycin-treated, is directly proportional to light intensity.-Proc. nat. Acad. Sci. USA 93: 2213–2218, 1996.
Varone, L., Gratani, L.: Physiological response of eight Mediterranean maquis species to low air temperature during winter.-Photosynthetica 45: 385–391, 2007.
Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress.-Physiol. Plant. 96: 567–576, 1996.
Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: Two forms of sustained xanthophyll-cycle dependent energy dissipation in overwintering Euonymus kiautschovicus.-Plant Cell Environ. 21: 893–903, 1998.
Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress.-Oecologia 118: 277–287, 1999.
Werner, C., Correia, O., Beyschlag, W.: Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought.-Acta oecol. 20: 15–23, 1999.
Zarco-Tejada, P.J., Miller, J.R., Mohammed, G.H., Noland, T.L.: Chlorophyll fluorescence effects on vegetation apparent reflectance: I. Leaf-level measurements and model simulation.-Remote Sensing Environ. 74: 582–595, 2000.
Zhu, X.-G., Govindjee, Baker, N.R., deSturler, E., Ort, D.R., Long, S.P.: Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II.-Planta 223: 114–133, 2005.
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Baraldi, R., Canaccini, F., Cortes, S. et al. Role of xanthophyll cycle-mediated photoprotection in Arbutus unedo plants exposed to water stress during the Mediterranean summer. Photosynthetica 46, 378–386 (2008). https://doi.org/10.1007/s11099-008-0069-x
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DOI: https://doi.org/10.1007/s11099-008-0069-x