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Role of xanthophyll cycle-mediated photoprotection in Arbutus unedo plants exposed to water stress during the Mediterranean summer

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Photosynthetica

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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bertamini, M., Nedunchezhian, N.: Photoinhibition and recovery of photosynthesis in leaves of Vitis berlandieri and Vitis rupestris.-J. Plant Physiol. 161: 203–210, 2004.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Choudhury, N.K., Behera, R.K.: Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents.-Photosynthetica 39: 481–488, 2001.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Demmig-Adams, B., Gilmore, A.M., Adams, W.W., III: In vivo functions of carotenoids of higher plants.-FASEB J. 10: 403–412, 1996b.

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.-Physiol. Plant. 99: 197–209, 1997.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kaiser, W.M.: Effects of water deficit on photosynthetic capacity.-Physiol. Plant. 71: 142–149, 1987.

    Article  CAS  Google Scholar 

  • Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis — the basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Long, S.P., Humphries, S., Falkowski, P.G.: Photoinhibition of photosynthesis in nature.-Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 633–662, 1994.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Murata, N., Takahashi, S., Nishiyama, Y., Allakhverdiev, S.I.: Photoinhibition of photosystem II under environmental stress.-Biochim. biophys. Acta 1767: 414–421, 2007.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Pfündel, E., Bilger, W.: Regulation and possible function of the violaxanthin cycle.-Photosynth. Res. 42: 89–109, 1994.

    Article  Google Scholar 

  • Powles, S.B.: Photoinhibition of photosynthesis induced by visible light.-Annu. Rev. Plant Physiol. 35: 15–44, 1984.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Smirnoff, N.: The role of active oxygen in the response of plants to water deficit and desiccation.-New Phytol. 125: 27–58, 1993.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Varone, L., Gratani, L.: Physiological response of eight Mediterranean maquis species to low air temperature during winter.-Photosynthetica 45: 385–391, 2007.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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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

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