Skip to main content
SpringerLink
Log in

Hydroxycinnamic acids in sunflower leaves serve as UV-A screening pigments

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Flavonoids and hydroxycinnamic acid derivatives, which are located in the upper epidermis of plants, are well known to screen ultraviolet radiation, thus protecting the underlying tissue from these harmful wavelengths. Both classes of secondary products complement each other over the UV spectral region according to their absorption spectra: flavonoids are most efficient as UV-A attenuators while hydroxycinnamates (HCAs) screen well within the UV-B region. Analysis of epidermal transmittance revealed a substantial UV-A screen in Helianthus annuus L. cv. Peredovick. Identifying responsible pigments by HPLC-MS, we found surprisingly low amounts of flavonoids but dominant abundance of the HCA derivatives chlorogenic and di-caffeoyl quinic acid. Both display low UV-A absorbance and thus, should contribute only a little to UV-A protection. However, growth at high light led to a decrease of epidermal transmittance at 366 nm of up to 90%. Underpinning the screening role, HCA autofluorescence microscopy revealed storage to occur predominantly in vacuoles of the upper epidermis. UV-A treatment in the absence of D1-repair resulted in photosystem II inactivation proportional to epidermal UV-A transmittance. Our findings suggest that UV-A protection can be achieved solely with HCAs, apparently through accumulation of high amounts of these compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Y. Jiang, M. Rabbi, M. Kim, C. Ke, W. Lee, R. L. Clark, et al., UVA generates pyrimidine dimers in DNA directly, Biophys.J., 2009, 96, 1151–1158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. I. Vass, E. Turcsányi, E. Touloupakis, D. Ghanotakis and V. Petrouleas, The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence, Biochemistry, 2002, 41, 10200–10208.

    Article  CAS  PubMed  Google Scholar 

  3. E. Turcsányi and I. Vass, Inhibition of photosynthetic electron transport by UV-A radiation targets the photosystem II complex, Photochem. Photobiol., 2000, 72, 513–520.

    Article  PubMed  Google Scholar 

  4. U.S. Department, of Energy (DOE)/NREL/ALLIANCE. ASTM G173-03 Reference Spectra Derived from SMARTS v. 2.9.2 [Internet]. Available from: https://www.nrel.gov/grid/solar-resource/spectra-am1.5.html.

  5. D. Verdaguer, M. A. K. Jansen, L. Llorens, L. O. Morales and S. Neugart, UV-A radiation effects on higher plants: Exploring the known unknown, Plant Sci., 2017, 255, 72–81.

    Article  CAS  PubMed  Google Scholar 

  6. M. Hakala, Photoinhibition of manganese enzymes: insights into the mechanism of photosystem II photoinhibition, J. Exp. Bot., 2006, 57, 1809–1816.

  7. M. Hakala, I. Tuominen, M. Keränen, T. Tyystjärvi and E. Tyystjärvi, Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II, Biochim. Biophys. Acta, 2005, 1706, 68–80.

    Article  CAS  PubMed  Google Scholar 

  8. S. Takahashi, S. E. Milward, W. Yamori, J. R. Evans, W. Hillier and M. R. Badger, The solar action spectrum of photosystem II damage, Plant Physiol., 2010, 153, 988–993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. P. Sarvikas, M. Hakala, E. Pätsikkä, T. Tyystjärvi and E. Tyystjärvi, Action spectrum of photoinhibition in leaves of wild type and npq1–2 and npq4-1 mutants of Arabidopsis thaliana, Plant Cell Physiol., 2006, 47, 391–400.

    Article  CAS  PubMed  Google Scholar 

  10. L. W. Jones and B. Kok, Photoinhibition of chloroplast reactions. I. Kinetics and action spectra, Plant Physiol., 1966, 41, 1037–1043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. T. A. Day, T. C. Vogelmann and E. H. DeLucia, Are some plant life forms more effective than others in screening out ultraviolet-B radiation?, Oecologia, 1992, 92, 513–519.

    Article  CAS  PubMed  Google Scholar 

  12. C. S. Cockell, Ultraviolet radiation, evolution and the π-electron system, Biol. J. Linn. Soc., 1998, 63, 449–457.

  13. K. G. Ryan, E. E. Swinny, K. R. Markham and C. Winefield, Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves, Phytochemistry, 2002, 59, 23–32.

    Article  CAS  PubMed  Google Scholar 

  14. L. G. Landry, C. Chapple and R. L. Last, Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage, Plant Physiol., 1995, 109, 1159–1166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. R. Lois and B. B. Buchanan, Severe sensitivity to ultraviolet radiation in an Arabidopsis mutant deficient in flavonoid accumulation: II. Mechanisms of UV-resistance in Arabidopsis, Planta, 1994, 194, 504–509.

    Article  Google Scholar 

  16. J. Li, T. M. Ou-Lee, R. Raba, R. G. Amundson and R. L. Last, Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation, Plant Cell, 1993, 5, 171–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. G. Agati and M. Tattini, Multiple functional roles of flavonoids in photoprotection, New Phytol., 2010, 186, 786–793.

    Article  CAS  PubMed  Google Scholar 

  18. M. Tattini, C. Galardi, P. Pinelli, R. Massai, D. Remorini and G. Agati, Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress, New Phytol., 2004, 163, 547–561.

    Article  CAS  PubMed  Google Scholar 

  19. G. Agati, C. Brunetti, M. Di Ferdinando, F. Ferrini, S. Pollastri and M. Tattini, Functional roles of flavonoids in photoprotection: New evidence, lessons from the past, Plant Physiol. Biochem., 2013, 72, 35–45.

    Article  CAS  PubMed  Google Scholar 

  20. P. Mølgaard and H. Ravn, Evolutionary aspects of caffeoyl ester distribution in dicotyledons, Phytochemistry, 1988, 27, 2411–2421.

    Article  Google Scholar 

  21. T. Okuda, T. Yoshida, T. Hatano, M. Iwasaki, M. Kubo, T. Orime, et al., Hydrolysable tannins as chemotaxonomic markers in the rosaceae, Phytochemistry, 1992, 31, 3091–3096.

    Article  CAS  Google Scholar 

  22. C. Clé, L. M. Hill, R. Niggeweg, C. R. Martin, Y. Guisez, E. Prinsen, et al., Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance, Phytochemistry, 2008, 69, 2149–2156.

    Article  CAS  PubMed  Google Scholar 

  23. L. Mondolot-Cosson, C. Andary, G.-H. Dai and J.-L. Roussel, Histolocalisation de substances phénoliques intervenant lors d’interactions plante-pathogène chez le tournesol et la vigne, Acta Bot. Gallica, 1997, 144, 353–362.

    Article  Google Scholar 

  24. D. Saftić-Panković, S. Veljović-Jovanović, M. Pucarević, N. Radovanović and A. Mijić, Phenolic compounds and peroxidases in sunflower near-isogenic lines after downy mildew infection, Helia, 2006, 29, 33–42.

    Article  Google Scholar 

  25. L. H. Rieseberg, D. E. Soltis and D. Arnold, Variation and localization of flavonoid aglycones in Helianthus annuus (Compositae), Am. J. Bot., 1987, 74, 224–233.

    Article  CAS  Google Scholar 

  26. O. Zsiros, S. I. Allakhverdiev, S. Higashi, M. Watanabe, Y. Nishiyama and N. Murata, Very strong UV-A light temporally separates the photoinhibition of photosystem II into light-induced inactivation and repair, Biochim. Biophys. Acta, 2006, 1757, 123–129.

    Article  CAS  PubMed  Google Scholar 

  27. G. Navarra, M. Moschetti, V. Guarrasi, M. R. Mangione, V. Militello and M. Leone, Simultaneous determination of caffeine and chlorogenic acids in green coffee by UV/Vis spectroscopy, J. Chem., 2017.

  28. S. C. Grace, B. A. Logan and W. W. Adams, Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repens, Plant, Cell Environ., 1998, 21, 513–521.

    Article  CAS  Google Scholar 

  29. F. Pescheck, H. Campen, L. Nichelmann and W. Bilger, Relative sensitivity of DNA and photosystem II in Ulva intestinalis (Chlorophyta) under natural solar irradiation, Mar. Ecol.: Prog. Ser., 2016, 555, 95–107.

    Article  CAS  Google Scholar 

  30. W. Bilger, T. Johnsen and U. Schreiber, UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants, J. Exp. Bot., 2001, 52, 2007–2014.

    Article  CAS  PubMed  Google Scholar 

  31. L. Nichelmann, M. Schulze, W. B. Herppich and W. Bilger, A simple indicator for non-destructive estimation of the violaxanthin cycle pigment content in leaves, Photosynth. Res., 2016, 128, 183–193.

    Article  CAS  PubMed  Google Scholar 

  32. L. Nichelmann and W. Bilger, Quantification of light screening by anthocyanins in leaves of Berberis thunbergii, Planta, 2017, 246, 1069–1082.

    Article  CAS  PubMed  Google Scholar 

  33. B. Harbaum, E. M. Hubbermann, Z. Zhu and K. Schwarz, Free and bound phenolic compounds in leaves of pak choi (Brassica campestris L. ssp. chinensis var. communis) and Chinese leaf mustard (Brassica juncea Coss), Food Chem., 2008, 110, 838–846.

    Article  CAS  PubMed  Google Scholar 

  34. A. Oertel, A. Matros, A. Hartmann, P. Arapitsas, K. J. Dehmer, S. Martens, et al., Metabolite profiling of red and blue potatoes revealed cultivar and tissue specific patterns for anthocyanins and other polyphenols, Planta, 2017, 246, 281–297.

    Article  CAS  PubMed  Google Scholar 

  35. D. Brauch, A. Porzel, E. Schumann, K. Pillen and H.-P. Mock, Changes in isovitexin-O-glycosylation during the development of young barley plants, Phytochemistry, 2018, 148, 11–20.

    Article  CAS  PubMed  Google Scholar 

  36. M. Lang, F. Stober and H. K. Lichtenthaler, Fluorescence emission spectra of plant leaves and plant constituents, Radiat. Environ. Biophys., 1991, 30, 333–347.

    Article  CAS  PubMed  Google Scholar 

  37. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, et al., Fiji: an open-source platform for biological-image analysis, Nat. Methods, 2012, 9, 676–682.

    Article  CAS  PubMed  Google Scholar 

  38. K. M. Bachmann, V. Ebbert, W. W. Adams III, A. S. Verhoeven, B. A. Logan and B. Demmig-Adams, Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery, Funct. Plant Biol., 2004, 31, 803–813.

    Article  CAS  PubMed  Google Scholar 

  39. J. L. Willems, M. M. Khamis, W. Mohammed Saeid, R. W. Purves, G. Katselis, N. H. Low, et al., Analysis of a series of chlorogenic acid isomers using differential ion mobility and tandem mass spectrometry, Anal. Chim. Acta, 2016, 933, 164–174.

    Article  CAS  PubMed  Google Scholar 

  40. P. Miketova, K. H. Schram, J. Whitney, E. H. Kearns and B. N. Timmermann, Mass spectrometry of 3,5- and 4,5-dicaffeoylquinic acids and selected derivatives, J. Mass Spectrom., 1999, 34, 1240–1252.

    Article  CAS  PubMed  Google Scholar 

  41. L. Mondolot, P. La Fisca, B. Buatois, E. Talansier, A. De Kochko and C. Campa, Evolution in caffeoylquinic acid content and histolocalization during Coffea canephora leaf development, Ann. Bot., 2006, 98, 33–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. R. del Moral, On the variability of chlorogenic acid concentration, Oecologia, 1972, 9, 289–300.

  43. T. Iwashina, The structure and distribution of the flavonoids in plants, J. Plant Res., 2000, 113, 287–299.

  44. B. Bohm, Chapter Three - Occurrence and distribution of flavonoids, in, Introduction to flavonoids, Harwood Academic Publishers, Amsterdam, 1998, pp. 117–173.

  45. J. Harborne, Chapter two - Phenolic compounds, in, Phytochemical methods: A guide to modern techniques of plant analysis, Chapman and Hall Ltd, London, 1973, pp. 33–88.

  46. J. B. Harborne and D. M. Smith, Anthochlors and other flavonoids as honey guides in the compositae, Biochem. Syst. Ecol., 1978, 6, 287–291.

    Article  CAS  Google Scholar 

  47. C. Sando, Anthocyanin formation in Helianthus annuus, J. Biol. Chem., 1925, 71–74.

  48. C. Rice-Evans, N. Miller and G. Paganga, Antioxidant properties of phenolic compounds, Trends Plant Sci., 1997, 2, 152–159.

    Article  Google Scholar 

  49. R. Niggeweg, A. J. Michael and C. Martin, Engineering plants with increased levels of the antioxidant chlorogenic acid, Nat. Biotechnol., 2004, 22, 746–754.

    Article  CAS  PubMed  Google Scholar 

  50. J. J. Sheahan, Sinapate esters provide greater UV-B attenuation than flavonoids in Arabidopsis thaliana (Brassicaceae), Am. J. Bot., 1996, 679–686.

  51. R. D. Hartley and P. J. Harris, Phenolic constituents of the cell walls of dicotyledons, Biochem. Syst. Ecol., 1981, 9, 189–203.

    Article  CAS  Google Scholar 

  52. P. J. Harris and R. D. Hartley, Phenolic constituents of the cell walls of monocotyledons, Biochem. Syst. Ecol., 1980, 8, 153–160.

    Article  CAS  Google Scholar 

  53. C. A. Kolb, U. Schreiber, R. Gademann and E. E. Pfündel, UV-A screening in plants determined using a new portable fluorimeter, Photosynthetica, 2005, 43, 371–377.

    Article  Google Scholar 

  54. C. A. Kolb, M. A. Käser, J. Kopecky, G. Zotz, M. Riederer and E. E. Pfundel, Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves, Plant Physiol., 2001, 127, 863–875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. T. A. Day, G. Martin and T. C. Vogelmann, Penetration of UV-B radiation in foliage: evidence that the epidermis behaves as a non-uniform filter, Plant, Cell Environ., 1993, 16, 735–741.

    Article  Google Scholar 

  56. G. Karabourniotis, Epicuticular phenolics over guard cells: Exploitation for in situ stomatal counting by fluorescence microscopy and combined image analysis, Ann. Bot., 2001, 87, 631–639.

  57. G. Liakopoulos, Analysis of epicuticular phenolics of Prunus persica and Olea europaea leaves: Evidence for the chemical origin of the UV-induced blue fluorescence of stomata, Ann. Bot., 2001, 87, 641–648.

  58. R. G. Riley and P. E. Kolattukudy, Evidence for covalently attached p-coumaric acid and ferulic acid in cutins and suberins, Plant Physiol., 1975, 56, 650–654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. P. Krauss, C. Markstädter and M. Riederer, Attenuation of UV radiation by plant cuticles from woody species, Plant, Cell Environ., 1997, 20, 1079–1085.

    Article  Google Scholar 

  60. S. S. Thayer and O. Björkman, Leaf Xanthophyll content and composition in sun and shade determined by HPLC, Photosynth. Res., 1990, 23, 331–343.

    Article  CAS  PubMed  Google Scholar 

  61. F. Pescheck and W. Bilger, High impact of seasonal temperature changes on acclimation of photoprotection and radiation-induced damage in field grown Arabidopsis thaliana, Plant Physiol. Biochem., 2019, 134, 129–136.

    Article  CAS  PubMed  Google Scholar 

  62. P. Burchard, W. Bilger and G. Weissenböck, 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., 2000, 23, 1373–1380.

    Article  CAS  Google Scholar 

  63. E. E. Pfündel, N. Ben Ghozlen, S. Meyer and Z. G. Cerovic, Investigating UV screening in leaves by two different types of portable UV fluorimeters reveals in vivo screening by anthocyanins and carotenoids, Photosynth, Res., 2007, 93, 205–221.

    Article  CAS  Google Scholar 

  64. P. Jahns and A. R. Holzwarth, The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II, Biochim. Biophys. Acta, Bioenerg., 2012, 1817, 182–193.

    Article  CAS  Google Scholar 

  65. S. I. Allakhverdiev and N. Murata, Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803, Biochim. Biophys. Acta, 2004, 1657, 23–32.

    Article  CAS  PubMed  Google Scholar 

  66. C. S. Cockell and J. Knowland, Ultraviolet radiation screening compounds, Biol. Rev. Cambridge Philos. Soc., 1999, 74, 311–345.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Roderich Roemhild

    Present address: Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, 75123, Sweden

Authors and Affiliations

  1. Department of Ecophysiology of Plants, Botanical Institute, Christian-Albrechts University Kiel, Kiel, 24118, Germany

    Jana Stelzner & Wolfgang Bilger

  2. Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts University Kiel, Kiel, 24118, Germany

    Roderich Roemhild

  3. Department of Physiology and Cell Biology, Leibniz Institute for Plant Genetics and Crop Plant Research, Gatersleben, 06466, Germany

    Adriana Garibay-Hernández & Hans-Peter Mock

  4. Department of Food Technology, Institute of Human Nutrition and Food Science, Christian-Albrechts University Kiel, Kiel, 24118, Germany

    Britta Harbaum-Piayda

Authors
  1. Jana Stelzner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roderich Roemhild
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adriana Garibay-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Britta Harbaum-Piayda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hans-Peter Mock
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolfgang Bilger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jana Stelzner.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c8pp00440d

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stelzner, J., Roemhild, R., Garibay-Hernández, A. et al. Hydroxycinnamic acids in sunflower leaves serve as UV-A screening pigments. Photochem Photobiol Sci 18, 1649–1659 (2019). https://doi.org/10.1039/c8pp00440d

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c8pp00440d

Search

Navigation