Skip to main content
Log in

Diurnal adjustment in ultraviolet sunscreen protection is widespread among higher plants

  • Physiological ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The accumulation of ultraviolet (UV)-absorbing compounds (flavonoids and related phenylpropanoids) in the epidermis of higher plants reduces the penetration of solar UV radiation to underlying tissues and is a primary mechanism of acclimation to changing UV conditions resulting from ozone depletion and climate change. Previously we reported that several herbaceous plant species were capable of rapid, diurnal adjustments in epidermal UV transmittance (T UV), but how widespread this phenomenon is among plants has been unknown. In the present study, we tested the generality of this response by screening 37 species of various cultivated and wild plants growing in four locations spanning a gradient of ambient solar UV and climate (Hawaii, Utah, Idaho and Louisiana). Non-destructive measurements of adaxial T UV indicated that statistically significant midday decreases in T UV occurred in 49 % of the species tested, including both herbaceous and woody growth forms, and there was substantial interspecific variation in the magnitude of these changes. In general, plants in Louisiana exhibited larger diurnal changes in T UV than those in the other locations. Moreover, across all taxa, the magnitude of these changes was positively correlated with minimum daily air temperatures but not daily UV irradiances. Results indicate that diurnal changes in UV shielding are widespread among higher plants, vary both within and among species and tend to be greatest in herbaceous plants growing in warm environments. These findings suggest that plant species differ in their UV protection “strategies” though the functional and ecological significance of this variation in UV sunscreen protection remains unclear at present.

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

Similar content being viewed by others

References

  • Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45. doi:10.1016/j.plaphy.2013.03.014

    Article  CAS  PubMed  Google Scholar 

  • Albert A, Sareedenchai V, Heller W, Seidlitz HK, Zidorn C (2009) Temperature is the key to altitudinal variation of phenolics in Arnica montana L. cv. ARBO. Oecologia 160:1–8. doi:10.1007/s00442-009-1277-1

    Article  PubMed  Google Scholar 

  • Albert KR, Mikkelsen TN, Ro-Poulsen H, Arndal MF, Michelsen A (2011) Ambient UV-B radiation reduces PSII performance and net photosynthesis in High Arctic Salix arctica. Environ Exp Bot 73:10–18. doi:10.1016/j.envexpbot.2011.08.003

    Article  CAS  Google Scholar 

  • Austin AT, Vivanco L (2006) Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature 442:555–558

    Article  CAS  PubMed  Google Scholar 

  • Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363. doi:10.1146/annurev-arplant-050213-040145

    Article  PubMed  Google Scholar 

  • Ballaré CL, Caldwell MM, Flint SD, Robinson SA, Bornman JF (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochem Photobiol Sci 10:226–241. doi:10.1039/c0pp90035d

    Article  PubMed  Google Scholar 

  • Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci 213:98–105. doi:10.1016/j.plantsci.2013.09.003

    Article  CAS  PubMed  Google Scholar 

  • Barnes PW, Searles PS, Ballaré CL, Ryel RJ, Caldwell MM (2000) Non-invasive measurements of leaf epidermal transmittance of UV radiation using chlorophyll fluorescence: field and laboratory studies. Physiol Plant 109:274–283

    Article  CAS  Google Scholar 

  • Barnes PW, Shinkle JR, Flint SD, Ryel RJ (2005) UV-B radiation, photomorphogenesis and plant-plant interactions. Prog Bot 66:313–340

    Article  Google Scholar 

  • Barnes PW, Flint SD, Slusser JR, Gao W, Ryel RJ (2008) Diurnal changes in epidermal UV transmittance of plants in naturally high UV environments. Physiol Plant 133:363–372

    Article  CAS  PubMed  Google Scholar 

  • Barnes PW, Flint SD, Ryel RJ, Tobler MA, Barkley AE, Wargent JJ (2015) Rediscovering leaf optical properties: new insights into plant acclimation to solar UV radiation. Plant Physiol Biochem 93:94–100. doi:10.1016/j.plaphy.2014.11.015

    Article  CAS  PubMed  Google Scholar 

  • Barnes PW, Tobler MA, Keefover-Ring K, Flint SD, Barkley AE, Ryel RJ, Lindroth RL (2016) Rapid modulation of UV-shielding in plants is influenced by solar UV radiation and linked to alterations in flavonoids. Plant Cell Environ 39:222–230. doi:10.1111/pce.12609

    Article  CAS  PubMed  Google Scholar 

  • Bidel LPR, Meyer S, Goulas Y, Cadot Y, Cerovic ZG (2007) 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 88:163–179. doi:10.1016/j.jphotobiol.2007.06.002

    Article  CAS  PubMed  Google Scholar 

  • Bilger W, Rolland M, Nybakken L (2007) UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochem Photobiol Sci 6:190–195

    Article  CAS  PubMed  Google Scholar 

  • Bornman JF, Barnes PW, Robinson SA, Ballaré CL, Flint SD, Caldwell MM (2015) Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems. Photochem Photobiol Sci 14:88–107. doi:10.1039/c4pp90034k

    Article  CAS  PubMed  Google Scholar 

  • Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Physiol Plant Mol Biol 47:75–100

    Article  CAS  PubMed  Google Scholar 

  • Caldwell MM (1971) Solar UV irradiation and the growth and development of higher plants. Photophysiol 6:131–177

    Article  CAS  Google Scholar 

  • Caldwell MM, Robberecht R, Flint SD (1983) Internal filters: prospects for UV-acclimation in higher plants. Physiol Plant 58:445–450

    Article  CAS  Google Scholar 

  • Day TA, Vogelmann TC, DeLucia EH (1992) Are some plant life forms more effective than others in screening out ultraviolet-B radiation? Oecologia 92:513–519

    Article  Google Scholar 

  • Flint SD, Searles PS, Caldwell MM (2004) Field testing of biological spectral weighting functions for induction of UV-absorbing compounds in higher plants. Photochem Photobiol 79:399–403. doi:10.1111/j.1751-1097.2004.tb00026.x

    Article  CAS  PubMed  Google Scholar 

  • Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 17:230–237. doi:10.1016/j.tplants.2012.01.007

    Article  CAS  PubMed  Google Scholar 

  • Hideg E, Jansen MAK, Strid Å (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115. doi:10.1016/j.tplants.2012.09.003

    Article  CAS  PubMed  Google Scholar 

  • Hofmann RW, Jahufer MZZ (2011) Tradeoff between biomass and flavonoid accumulation in white clover reflects contrasting plant strategies. PLoS ONE 6:e18949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen MAK, Bornman JF (2012) UV-B radiation: from generic stressor to specific regulator. Physiol Plant 145:501–504. doi:10.1111/j.1399-3054.2012.01656.x

    Article  CAS  PubMed  Google Scholar 

  • Jansen MAK, Coffey AM, Prinsen E (2012) UV-B induced morphogenesis: four players or a quartet? Plant Signal Behav 7:1185–1187. doi:10.4161/psb.21260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26:21–37. doi:10.1105/tpc.113.119446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan BR (2002) Molecular response of plant cells to UV-B stress. Funct Plant Biol 29:909–916

    Article  CAS  Google Scholar 

  • Julkunen-Tiitto R, Nenadis N, Neugart S, Robson M, Agati G, Vepsäläinen J, Zipoli G, Nybakken L, Winkler B, Jansen MAK (2015) Assessing the response of plant flavonoids to UV radiation: an overview of appropriate techniques. Phytochem Rev 14:273–297. doi:10.1007/s11101-014-9362-4

    Article  CAS  Google Scholar 

  • King JY, Brandt LA, Adair EC (2012) Shedding light on plant litter decomposition: advances, implications and new directions in understanding the role of photodegradation. Biogeochemistry 111:57–81. doi:10.1007/s10533-012-9737-9

    Article  Google Scholar 

  • Kolb CA, Schreiber U, Gademann R, Pfündel EE (2005) UV-A screening in plants determined using a new portable fluorimeter. Photosynthetica 43:371–377

    Article  Google Scholar 

  • König S, Feussner K, Kaever A, Landesfeind M, Thurow C, Karlovsky P, Gatz C, Polle A, Feussner I (2014) Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytol 202:823–837. doi:10.1111/nph.12709

    Article  PubMed  Google Scholar 

  • Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Funct Plant Biol 31:743–756

    Article  Google Scholar 

  • Kuhlmann F, Müller C (2010) UV-B impact on aphid performance mediated by plant quality and plant changes induced by aphids. Plant Biol 12:676–684. doi:10.1111/j.1438-8677.2009.00257.x

    CAS  PubMed  Google Scholar 

  • Kuhn BM, Geisler M, Bigler L, Ringli C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 156:585–595. doi:10.1104/pp.111.175976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landry LG, Chapple CCS, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109:1159–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lautenschlager-Fleury D (1955) Über die Ultraviolettdurchläessigkeit von Blattepidermen. Ber Schweiz Bot Ges 65:343–386

    CAS  Google Scholar 

  • Markstadter C, Queck I, Baumeister J, Riederer M, Schreiber U, Bilger W (2001) Epidermal transmittance of leaves of Vicia faba for UV radiation as determined by two different methods. Photosynth Res 67:17–25

    Article  CAS  PubMed  Google Scholar 

  • Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122:117–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClung CR (2001) Circadian rhythms in plants. Annu Rev Plant Physiol Plant Mol Biol 52:139–162

    Article  CAS  PubMed  Google Scholar 

  • Morales LO, Brosché M, Vainonen J, Jenkins GI, Wargent JJ, Sipari N, Strid A, Lindfors AV, Tegelberg R, Aphalo PJ (2013) Multiple roles for UV RESISTANCE LOCUS8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar ultraviolet radiation. Plant Physiol 161:744–759. doi:10.1104/pp.112.211375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neugart S, Fiol M, Schreiner M, Rohn S, Zrenner R, Kroh LW, Krumbein A (2013) Low and moderate photosynthetically active radiation affects the flavonol glycosides and hydroxycinnamic acid derivatives in kale (Brassica oleracea var. sabellica) dependent on two low temperatures. Plant Physiol Biochem 72:161–168. doi:10.1016/j.plaphy.2013.04.002

    Article  CAS  PubMed  Google Scholar 

  • Nullet D, Juvik JO (1997) Measured altitudinal profiles of UV-B iradiance in Hawai’i. Phys Geogr 18:335–345

    Google Scholar 

  • Nybakken L, Aubert S, Bilger W (2004) Epidermal UV-screening of arctic and alpine plants along a latitudinal gradient in Europe. Polar Biol 27:391–398

    Article  Google Scholar 

  • Pfündel EE, Ben Ghozlen N, Meyer S, Cerovic ZG (2007) Investigating UV screening in leaves by two different types of portable UV fluorimeter reveals in vivo screening by anthocyanins and carotenoids. Photosynth Res 93:205–221. doi:10.1007/s11120-007-9135-7

    Article  PubMed  Google Scholar 

  • Rizzini L, Favory J-J, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schaefer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106. doi:10.1126/science.1200660

    Article  CAS  PubMed  Google Scholar 

  • Schenke D, Bottcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant Cell Environ 34:1849–1864. doi:10.1111/j.1365-3040.2011.02381.x

    Article  CAS  PubMed  Google Scholar 

  • Searles PS, Flint SD, Caldwell MM (2001) A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127:1–10

    Article  Google Scholar 

  • Siipola SM, Kotilainen T, Sipari N, Morales LO, Lindfors AV, Robson TM, Aphalo PJ (2015) Epidermal UV-A absorbance and whole-leaf flavonoid composition in pea respond more to solar blue light than to solar UV radiation. Plant Cell Environ 38:941–952. doi:10.1111/pce.12403

    Article  CAS  PubMed  Google Scholar 

  • Song X, Peng C, Jiang H, Zhu Q, Wang W (2013) Direct and indirect effects of UV-B exposure on litter decomposition: a meta-analysis. PLoS ONE 8:e68858. doi:10.1371/journal.pone.0068858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan JH, Gitz DC, Liu-Gitz L, Xu CP, Gao W, Slusser J (2007) Coupling short-term changes in ambient UV-B levels with induction of UV-screening compounds. Photochem Photobiol 83:863–870. doi:10.1111/j.1751-1097.2007.00138.x

    Article  CAS  PubMed  Google Scholar 

  • Turnbull TL, Barlow AM, Adams MA (2013) Photosynthetic benefits of ultraviolet-A to Pimelea ligustrina, a woody shrub of sub-alpine Australia. Oecologia 173:375–385. doi:10.1007/s00442-013-2640-9

    Article  PubMed  Google Scholar 

  • Veit M, Bilger T, Muhlbauer T, Brummet W, Winter K (1996) Diurnal changes in flavonoids. J Plant Physiol 148:478–482

    Article  CAS  Google Scholar 

  • Wargent JJ, Elfadly EM, Moore JP, Paul ND (2011) Increased exposure to UV-B radiation during early development leads to enhanced photoprotection and improved long-term performance in Lactuca sativa. Plant Cell Environ 34:1401–1413. doi:10.1111/j.1365-3040.2011.02342.x

    Article  CAS  PubMed  Google Scholar 

  • Williamson CE, Zepp RG, Lucas RM, Madronich S, Austin AT, Ballaré CL, Norval M, Sulzberger B, Bais AF, McKenzie RL, Robinson SA, Häder D-P, Paul ND, Bornman JF (2014) Solar ultraviolet radiation in a changing climate. Nat Clim Change 4:434–441. doi:10.1038/nclimate2225

    Article  Google Scholar 

Download references

Acknowledgments

The research described here was supported, in part, by funds from the Louisiana Board of Regents [SURE/NSF grant LEQSF-EPS (2013)-SURE-85 to Loyola University], the US Department of Agriculture UV-Monitoring Program (USDA-CSREES no. 2008-34263-19485 to Utah State University via subcontract with Colorado State University), the Utah Agricultural Experiment Station, and the Loyola University J. H. Mullahy Endowment in Environmental Biology. We thank M. Grabner, D. Hackenburg, I. Bottger, and B. Burnet for their assistance. The authors declare no competing financial or other interests.

Author contribution statement

P. W. B., S. D. F. and R. J. R. conceived and designed the experiments. S. D. F., M. A. T. and R. J. R. performed the experiments. P. W. B., S. D. F. and M. A. T. analyzed the data; P. W. B. wrote the manuscript; other authors provided editorial advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul W. Barnes.

Additional information

Communicated by Caroline Müller.

Ronald J. Ryel: Deceased 20 October 2015.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 842 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barnes, P.W., Flint, S.D., Tobler, M.A. et al. Diurnal adjustment in ultraviolet sunscreen protection is widespread among higher plants. Oecologia 181, 55–63 (2016). https://doi.org/10.1007/s00442-016-3558-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3558-9

Keywords

Navigation