Abstract
We examined the dynamics of phenolic compounds (PheCs) and carotenoids (Cars) in the leaves of wild type (WT) spring barley (Hordeum vulgare L.) and its mutant lacking chlorophyll b Chlorina f2 (Clo f2) grown from seeds at high irradiance (8 d at 1 000 μmol m-2 s-1; HI) during 9 d of acclimation to low irradiance (50 μmol m-2 s-1; LI). Our results show that a leaf epidermal flavonoid UV-shielding index remained rather constant after transfer of plants from HIto LIconditions and that it was significantly lower in Clo f2 compared to WTplants. This suggests that HIpretreated plants can be well protected against excessive UVfor at least 9 d, as supported also by the constant absorbance of leaf PheCs extracts in the UV-A region (at 335 nm). In contrast, absorbance in the UV-B region (at 270 nm) was reduced, particularly during the initial days of LItreatment, indicating specific changes in PheC profile. High-performance liquid chromatography of soluble PheCs revealed stable content of the major PheC saponarin during LIacclimation, whereas luteolin and feruloylquinic acid content decreased, particularly in WTplants. We also observed a pronounced decrease in Car relative content, particularly a reduction in the xanthophyll cycle pigments (violaxanthin, antheraxanthin, and zeaxanthin, VAZ) pool and diminution of their de-epoxidation state (DEPS) in dark-adapted leaves. As both VAZ and DEPS were higher in HI-acclimated Clo f2 plants than they were in WTplants, the presence of a significant VAZ pool within the lipid phase of thylakoid membrane is indicated. That can contribute to antioxidant capacity particularly in Clo f2 plants. We can therefore conclude that there is a tendency to retain the PheCs responsible for UVshielding during LIacclimation. Meanwhile, the accumulation of both PheCs and zeaxanthin serving as effective antioxidants is considerably downregulated within 9 d.
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Abbreviations
- A:
-
absorbance at respective nm
- AOX:
-
antioxidant activity
- Car x+c :
-
spectrophotometrically determined total carotenoid content
- Car:
-
carotenoid
- Chl a :
-
chlorophyll a
- Clo f2 :
-
chlorophyll b-less mutant of spring barley (Chlorina f2)
- DEPS:
-
de-epoxidation state of xanthophyll cycle pigments
- HI:
-
high irradiance
- HPLC:
-
high-performance liquid chromatography
- LHC:
-
light-harvesting complex
- LI:
-
low irradiance
- PAR:
-
photosynthetically active radiation
- PheC:
-
phenolic compound
- PS II:
-
photosystem II
- ROS:
-
reactive oxygen species
- Rt:
-
retention time
- UV:
-
ultraviolet radiation
- VAZ:
-
sum of violaxanthin, antheraxanthin, and zeaxanthin
- VIS:
-
visible light
- WT:
-
wild type.
References
Agati, G., Azzarello, E., Pollastri, S., Tattini, M.: Flavonoids as antioxidants in plants: location and functional significance. - Plant Sci. 196: 67–76, 2012.
Agati, G., Cerovic, Z.G., Pinelli, P., Tattini, M.: Light-induced accumulation of ortho-dihydroxylated flavonoids as nondestructively monitored by chlorophyll fluorescence excitation techniques. - Environ. exp. Bot. 73: 3–9, 2011.
Agati, G., Matteini, P., Goti, A., Tattini, M.: Chloroplastlocated flavonoids can scavenge singlet oxygen. - New Phytol. 174: 77–89, 2007.
Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391–396, 2006.
Barnes, P.W., Flint, S.D., Slusser, J.R., Gao, W., Ryel, R.J.: Diurnal changes in epidermal UVtransmittance of plants in naturally high UVenvironments. - Physiol. Plant. 133: 363–372, 2008.
Barnes, P.W., Kersting, A.R., Flint, S.D., Beyschlag, W., Ryel, R.J.: Adjustments in epidermal UV-transmittance of leaves in sun-shade transitions. - Physiol. Plant. 149: 200–213, 2013.
Bidel, L.P.R., Meyer, S., Goulas, Y., Cadot, Y., Cerovic, Z.G.: Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species. - J. Photochem. Photobiol. B-Biol. 88: 163–179, 2007.
Bilger, W., Johnsen, T., Schreiber, U.: UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. - J. exp. Bot. 52: 2007–2014, 2001.
Burchard, P., Bilger, W., Weissenbock, G.: Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. - Plant Cell Environ. 23: 1373–1380, 2000.
Cazzaniga, S., Li, Z., Niyogi, K.K., Bassi, R., Dall’Osto, L.: The Arabidopsis szl1 mutant reveals a critical role of betacarotene in photosystem I photoprotection. - Plant Physiol. 159: 1745–1758, 2012.
Dall’Osto, L., Cazzaniga, S., Havaux, M., Bassi, R.: Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. - Mol. Plants 3: 576–593, 2010.
Demidchik, V.: Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. - Environ. exp. Bot. 109: 212–228, 2015.
Demmig-Adams, B.: Survey of thermal energy dissipation and pigment composition in sun and shade leaves. - Plant Cell Physiol. 39: 474–482, 1998.
Demmig-Adams, B., Adams, W.W.: Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. - New Phytol. 172: 11–21, 2006.
Demmig-Adams, B., Cohu, C.M., Muller, O., Adams, W.W.: Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. - Photosynth. Res. 113: 75–88, 2012.
Edreva, A.: The importance of non-photosynthetic pigments and cinnamic acid derivatives in photoprotection. - Agr. Ecosyst. Environ. 106: 135–146, 2005.
Färber, A., Jahns, P.: The xanthophyll cycle of higher plants: influence of antenna size and membrane organization. - Biochim. biophys. Acta 1363: 47–58, 1998.
Förster, B., Osmond, C.B., Pogson, B.J.: De novo synthesis and degradation of Lx and V cycle pigments during shade and sun acclimation in avocado leaves. - Plant Physiol. 149: 1179–1195, 2009.
Guidi, L., Degl’Innocenti, E., Remorini, D., Biricolti, S., Fini, A., Ferrini, F., Nicese, F.P., Tattini, M.: The impact of UVradiation on the physiology and biochemistry of Ligustrum vulgare exposed to different visible-light irradiance. - Environ. exp. Bot. 70: 88–95, 2011.
Havaux, M., Dall’Osto, L., Bassi, R.: 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, 2007.
Havaux, M., Tardy, F.: Thermostability and photostability of photosystem IIin leaves of the Chlorina-f2 barley mutant deficient in light-harvesting chlorophyll a/b protein complexes. - Plant Physiol. 113: 913–923, 1997.
Heim, K.E., Tagliaferro, A.R., Bobilya, D.J.: Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. - J. Nutr. Biochem. 13: 572–584, 2002.
Hernández, I., Alegre, L., Van Breusegem, F., Munné-Bosch, S.: How relevant are flavonoids as antioxidants in plants? - Trends Plant Sci. 14: 125–132, 2009.
Hideg, E., Jansen, M.A.K., Strid, A.: UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? - Trends Plant Sci. 18: 107–115, 2013.
Horton, P., Johnson, M.P., Perez-Bueno, M.L., Kiss, A.Z., Ruban, A.V.: Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem IIin higher plant grana membranes regulate light harvesting states? - FEBS J. 275: 1069–1079, 2008.
Humbeck, K., Krupinska, K.: The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCl of barley (Hordeum vulgare L.) during leaf senescence is controlled by light. - J. exp. Bot. 54: 375–383, 2003.
Jahns, P., Holzwarth, A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II.- Biochim. biophys. Acta 1817: 182–193, 2012.
Kaspar, S., Matros, A., Mock, H. P.: Proteome and flavonoid analysis reveals distinct response of epidermal tissue and whole leaves upon UV-B radiation of barley (Hordeum vulgare L.) seedlings. - J. Proteome Res. 9: 2402–2411, 2010.
Klem, K., Ac, A., Holub, P., Kovác, D., Špunda, V., Robson, T.M., Urban, O.: Interactive effects of PAR and UVradiation on the physiology, morphology and leaf optical properties of two barley varieties. - Environ. exp. Bot. 75: 52–64, 2012.
Klem, K., Holub, P., Štroch, M., Nezval, J., Špunda, V., Tríska, J., Jansen, M.A.K., Robson, T.M., Urban, O.: Ultraviolet and photosynthetically active radiation can both induce photoprotective capacity allowing barley to overcome high radiation stress. - Plant Physiol. Biochem. 93: 74–83, 2015.
Kolb, C.A., Pfündel, E.E.: Origins of non-linear and dissimilar relationships between epidermal UVabsorbance and UVabsorbance of extracted phenolics in leaves of grapevine and barley. - Plant Cell Environ. 28: 580–590, 2005.
Kurasová, I., Cajánek, M., Kalina, J., Urban, O., Špunda, V.: Characterization of acclimation of Hordeum vulgare to high irradiation based on different responses of photosynthetic activity and pigment composition. - Photosynth. Res. 72: 71–83, 2002.
Kurasová, I., Kalina, J., Urban, O., Štroch, M., Špunda, V.: Acclimation of two distinct plant species, spring barley and Norway spruce, to combined effect of various irradiance and CO2 concentration during cultivation in controlled environment. - Photosynthetica 41: 513–523, 2003.
Liakoura, V., Bornman, J.F., Karabourniotis, G.: The ability of abaxial and adaxial epidermis of sun and shade leaves to attenuate UV-A and UV-B radiation in relation to the UVabsorbing capacity of the whole leaf methanolic extracts. - Physiol. Plant. 117: 33–43, 2003.
Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Methods Enzymol. 148: 350–382, 1987.
Liu, L., Gitz, D.C., McClure, J.W.: Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. - Physiol. Plant. 93: 725–733, 1995.
Mondolot, L., La Fisca, P., Buatois, B., Talansier, E., De Kochko, A., Campa, C.: Evolution in caffeoylquinic acid content and histolocalization during Coffea canephora leaf development. - Ann. Bot. 98: 33–40, 2006.
Mozzo, M., Dall’Osto, L., Hienerwadel, R., Bassi, R., Croce, R.: Photoprotection in the antenna complexes of Photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. - J. biol. Chem. 283: 6184–6192, 2008.
Pfündel, E.E., Ben Ghozlen, N., Meyer S., Cerovic Z.G.: Investigating UVscreening in leaves by two different types of portable UVfluorimeters reveals in vivo screening by anthocyanins and carotenoids. - Photosynth. Res. 93: 205–221, 2007.
Rice-Evans, C.A., Miller, N.J., Paganga, G.: Structureantioxidant activity relationships of flavonoids and phenolic acids. - Free Radicals Biol. Med. 20: 933–956, 1996.
Solovchenko, A.E., Merzlyak, M.N.: Screening of visible and UVradiation as a photoprotective mechanism in plants. - Russ. J. Plant Physiol. 55: 719–737, 2008.
Štroch, M., Cajánek, M., Kalina, J., Špunda, V.: Regulation of the excitation energy utilization in the photosynthetic apparatus of chlorina f2 barley mutant grown under different irradiances. - J. Photochem. Photobiol. B-Biol. 75: 41–50, 2004a.
Štroch, M., Špunda, V., Kurasová, I.: Non-radiative dissipation of absorbed excitation energy within photosynthetic apparatus of higher plants. - Photosynthetica 42: 323–337, 2004b.
Štroch, M., Kuldová, K., Kalina, J., Špunda, V.: Dynamics of the xanthophyll cycle and non-radiative dissipation of absorbed light energy during exposure of Norway spruce to high irradiance. - J. Plant Physiol. 165: 612–622, 2008a.
Štroch, M., Lenk, S., Navrátil, M., Špunda, V., Buschmann, C.: Epidermal UV-shielding and photosystem IIadjustment in wild type and chlorina f2 mutant of barley during exposure to increased PAR and UVradiation. - Environ. exp. Bot. 64: 271–278, 2008b.
Takahashi, S., Badger, M.R.: Photoprotection in plants: a new light on photosystem IIdamage. - Trends Plant Sci. 16: 53–60, 2011.
Tattini, M., Galardi, C., Pinelli, P., Massai, R., Remorini, D., Agati, G.: Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. - New Phytol. 163: 547–561, 2004.
Telfer, A.: What is beta-carotene doing in the photosystem IIreaction centre? - Phil. Tran. roy. Soc. London B 357: 1431–1439, 2002.
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Acknowledgements: This work was supported by the University of Ostrava (SGS09/PřF/2015, SGS11/PřF/2016) and by the Ministry of Education, Youth and Sports of the Czech Republic through projects LO1208 and LO1415 of the National Programme for Sustainability and COST (no. LD14005).
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Nezval, J., Štroch, M., Materová, Z. et al. Phenolic compounds and carotenoids during acclimation of spring barley and its mutant Chlorina f2 from high to low irradiance. Biol Plant 61, 73–84 (2017). https://doi.org/10.1007/s10535-016-0689-0
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DOI: https://doi.org/10.1007/s10535-016-0689-0