Skip to main content

Photosynthetic benefits of ultraviolet-A to Pimelea ligustrina, a woody shrub of sub-alpine Australia

Abstract

The definition of photosynthetically active radiation (Q) as the visible waveband (λ 400–700 nm) is a core assumption of much of modern plant biology and global models of carbon and water fluxes. On the other hand, much research has focused on potential mutation and damage to leaves caused by ultraviolet (UV) radiation (280–400 nm), and anatomical and physiological adaptations that help avoid such damage. Even so, plant responses to UV-A are poorly described and, until now, photosynthetic utilization of UV-A has not been elucidated under full light conditions in the field. We found that the UV-A content of sunlight increased photosynthetic rates in situ by 12 % in Pimelea ligustrina Labill., a common and indigenous woody shrub of alpine ecosystems of the Southern Hemisphere. Compared to companion shrubs, UV-A-induced photosynthesis in P. ligustrina resulted from reduced physical and chemical capacities to screen UV-A at the leaf surface (illustrated by a lack of cuticle and reduced phenol index) and the resulting ability of UV-A to excite chlorophyll (Chl) a directly, and via energy provided by the carotenoid lutein. A screening of 55 additional sub-alpine species showed that 47 % of the plant taxa also display Chl a fluorescence under UV-A. If Chl a fluorescence indicates potential for photosynthetic gain, continued exclusion of UV-A from definitions of Q in this ecosystem could result in underestimates of measured and modeled rates of photosynthesis and miscalculation of potential for carbon sequestration. We suggest that carbon gain for alpine environs across the globe could be similarly underestimated given that UV-A radiation increases with altitude and that the frequently dominant herb and grass life-forms often transmit UV-A through the epidermis.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Ålenius CM, Vogelmann TC, Bornman JF (1995) A three-dimensional representation of the relationship between penetration of UV-B radiation and UV-screening pigments in leaves of Brassica napus. New Phytol 131:297–302

    Article  Google Scholar 

  • Amthor JS (2010) Tansley review: from sunlight to phytomass: on the potential efficiency of converting solar radiation to phyto-energy. New Phytol 188:939–995. doi:10.1111/j.1469-8137.2010.03505.x

    PubMed  Article  CAS  Google Scholar 

  • American Society for Testing and Materials (ASTM) (2003) Standard tables for reference solar spectral irradiances: direct normal and hemispherical on 37 tilted surface. Standard G173-03. American Society for Testing and Materials, West Conshohocken

  • Barnes PW et al (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 et al (2008) Diurnal changes in epidermal UV transmittance of plants in naturally high UV environments. Physiol Plant 133:363–372. doi:10.1111/j.1399-3054.2008.01084.x

    PubMed  Article  CAS  Google Scholar 

  • Bidel LPR et al (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 Biol 88:163–179. doi:10.1016/j.jphotobiol.2007.06.002

    Article  CAS  Google Scholar 

  • Bilger W, Veit M, Schreiber L, Schreiber U (1997) Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiol Plant 101:754–763. doi:10.1034/j.1399-3054.1997.1010411.x

    Article  CAS  Google Scholar 

  • Bilger W, Rolland M, Nybakken L (2006) UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochem Photobiol Sci 6:190–195

    Article  Google Scholar 

  • Blumthaler M, Ambach W, Ellinger R (1997) Increase in solar UV radiation with altitude. J Photochem Photobiol B 39:130–134. doi:10.1016/S1011-1344(96)00018-8

    Article  CAS  Google Scholar 

  • Bornman JF, Vogelmann TC (1988) Leaf adaptation and penetration of blue and UV radiation measured by fiber optics in spruce and fir needles. Physiol Plant 72:699–705

    Article  Google Scholar 

  • Cadet E, Samson G (2011) Detection and discrimination of nutrient deficiencies in sunflower by blue-green and chlorophyll-a fluorescence imaging. J Plant Nutr 34:2114–2126

    Article  CAS  Google Scholar 

  • Caffarri S, Croce R, Breton J, Bassi R (2001) The major antenna complex of photosystem II as a xanthophyll binding site not involved in light harvesting. J Biol Chem 267:35924–35933

    Article  Google Scholar 

  • Caldwell MM (1968) Ultraviolet radiation as an ecological factor for alpine plants. Ecol Monogr 38:243–268

    Article  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 

  • Cerovic ZG, Ounis A, Cartelat A, Latouche G, Goulas Y, Meyer S, Moya I (2002) The use of chlorophyll fluorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves. Plant Cell Environ 25:1663–1676. doi:10.1046/j.1365-3040.2002.00942.x

    Article  CAS  Google Scholar 

  • Chen M et al (2010) A red-shifted chlorophyll. Science 329:1318–1319. doi:10.1126/science.1191127

    PubMed  Article  CAS  Google Scholar 

  • Connelly JP, Muller MG, Bassi R, Croce R, Holzwarth AR (1997) Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. Biochemistry 36:281–287

    PubMed  Article  CAS  Google Scholar 

  • Cork SJ, Krockenberger AK (1991) Methods and pitfalls of extracting condensed tannins and other phenolics from plants: insights from investigations on Eucalyptus leaves. J Chem Ecol 17:123–134. doi:10.1007/BF00994426

    Article  CAS  Google Scholar 

  • Croce R, Muller MG, Bassi R, Holzwarth AR (2001) Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophys J 80:901–915

    PubMed  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. doi:10.1007/BF00317843

    Article  Google Scholar 

  • Day TA, Howells BW, Ruhland CT (1996) Changes in growth and pigment concentrations with leaf age in pea under modulated UV-B radiation field treatments. Plant Cell Environ 19:101–108

    Article  CAS  Google Scholar 

  • Demotes-Mainard S et al (2008) Indicators of nitrogen status for ornamental woody plants based on optical measurements of leaf epidermal polyphenol and chlorophyll contents. Sci Hortic 115:377–385

    Article  CAS  Google Scholar 

  • Flint SD, Caldwell MM (2003a) A biological spectral weighting function for ozone depletion research with higher plants. Physiol Plant 117:137–144

    Article  CAS  Google Scholar 

  • Flint SD, Caldwell MM (2003b) Field testing of UV biological spectral weighting functions for higher plants. Physiol Plant 117:145–153

    Article  CAS  Google Scholar 

  • Flint SD, Jordan PW, Caldwell MM (1985) Plant protective response to enhanced UV-B radiation under field conditions: leaf optical properties and photosynthesis. Photochem Photobiol 41:95–99

    Article  CAS  Google Scholar 

  • Furuya M, Galston AW (1965) Flavonoid complexes in Pisum sativum L. I. Nature and distribution of the major components. Phytochemistry 4:285–296

    Article  CAS  Google Scholar 

  • Grammatikopoulos G, Petropoulou Y, Manetas Y (1999) Site-dependent differences in transmittance and UV-B-absorbing capacity of isolated leaf epidermis and mesophyll in Urginea maritime LL. Baker. J Exp Bot 50:517–521

    CAS  Google Scholar 

  • Halldal P (1964) Ultraviolet action spectra of photosynthesis and photosynthetic inhibition in a green and a red alga. Physiol Plant 17:414–421

    Article  Google Scholar 

  • Inada K (1976) Action spectra for photosynthesis in higher plants. Plant Cell Physiol 17:355–365

    Google Scholar 

  • Johnson GA, Day TA (2002) Enhancement of photosynthesis in Sorghum bicolor by ultraviolet radiation. Physiol Plant 116:554–562. doi:10.1034/j.1399-3054.2002.1160415.x

    Article  CAS  Google Scholar 

  • Karabourniotis G et al (1992) Ultraviolet-B radiation absorbing capacity of leaf hairs. Physiol Plant 86:414–418

    Article  Google Scholar 

  • Kolb C et al (2001) Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiol 127:863–875

    PubMed  Article  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Krause GH et al (2003) Capacity of protection against ultraviolet radiation in sun and shade leaves of tropical forest plants. Funct Plant Biol 30:533–542

    Article  CAS  Google Scholar 

  • Lang M, Lichtenthaler HK (1991) Changes in the blue-green and red fluorescence-emission spectra of beech leaves during the autumnal chlorophyll breakdown. J Plant Physiol 138:550–553

    Article  CAS  Google Scholar 

  • Lenk S, Buschmann C (2005) Distribution of UV-shielding of the epidermis of sun and shade leaves of the beech (Fagus sylvatica L.) as monitored by multi-colour fluorescence imaging. J Plant Physiol 163:1273–1283

    PubMed  Article  Google Scholar 

  • Liakoura V, Bornman JF, Karabourniotis G (2003) The ability of abaxial and adaxial epidermis of sun and shade leaves to attenuate UV-A and UV-B radiation in relation to the UV absorbing capacity of the whole leaf methanolic extracts. Physiol Plant 117:33–43. doi:10.1034/j.1399-3054.2003.1170104.x

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Barschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. Curr Protoc Food Analyt Chem, F4.3.1–F4.3.8

  • Lichtenthaler HK, Miehé JA (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320. doi:10.1016/S1360-1385(97)89954-2

    Article  Google Scholar 

  • Louis J et al (2009) Seasonal changes in optically assessed epidermal phenolic compounds and chlorophyll contents in leaves of sessile oak (Quercus petraea): towards signatures of phonological stage. Funct Plant Biol 36:732–741

    Article  CAS  Google Scholar 

  • Lubin D, Jensen EH, Gies HP (1998) Global surface ultraviolet radiation climatology from TOMS and ERBE data. J Geophys Res 103:26061–26091. doi:10.1029/98JD02308

    Article  Google Scholar 

  • Mantha SV, Johnson GA, Day TA (2001) Evidence from action and fluorescence spectra that UV-induced violet–blue–green fluorescence enhances leaf photosynthesis. Photochem Photobiol 73:249–256. doi:10.1562/0031-8655(2001)073<0249:EFAAFS>2.0.CO;2

    PubMed  CAS  Google Scholar 

  • Markstädter C et al (2001) Epidermal transmission of leaves of Vicia faba for UV radiation as determined by two different methods. Photosynth Res 67:17–25

    PubMed  Article  Google Scholar 

  • McCree KJ (1972a) The action spectrum, absorptance and quantum yield of photosynthesis in crop plants. Agric Meteorol 9:191–216

    Article  Google Scholar 

  • McCree KJ (1972b) Test of current definitions of photosynthetically active radiation against leaf photosynthesis data. Agric Meteorol 10:443–453

    Article  Google Scholar 

  • McCree KJ (1981) Photosynthetically active radiation. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology I. Springer, Berlin, pp 41–55

    Chapter  Google Scholar 

  • McCree KJ, Keener ME (1974) Effect of atmospheric turbidity on the photosynthetic rates of leaves. Agric Meteorol 13:349–357

    Article  Google Scholar 

  • McKenzie RL et al (1993) First Southern Hemisphere intercomparison of measured solar UV spectra. Geophys Res Lett 20:2223–2226. doi:10.1029/93GL02359

    Article  Google Scholar 

  • McLeod GC, Kanwisher J (1962) The quantum efficiency of photosynthesis in ultraviolet light. Physiol Plant 15:581–586

    Article  CAS  Google Scholar 

  • Miyashita H et al (1996) Chlorophyll d as a major pigment. Nature 383:402. doi:10.1038/383402a0

    Article  CAS  Google Scholar 

  • Morales LO et al (2011) Temporal variation in epidermal flavonoids due to altered solar UV radiation is moderated by the leaf position in Betula pendula. Physiol Plant 143:261–270

    PubMed  Article  CAS  Google Scholar 

  • Niinemets Ü, Tenhunen JD (1997) Carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866. doi:10.1046/j.1365-3040.1997.d01-133.x

    Article  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 

  • Ounis A et al (2001) Dual-excitation FLIDAR for the estimation of epidermal UV absorption in leaves and canopies. Remote Sens Environ 76:33–48

    Article  Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005) The long-wavelength limit of plant photosynthesis. FEBS Lett 579:4017–4019. doi:10.1016/j.febslet.2005.04.088

    PubMed  Article  CAS  Google Scholar 

  • Pfündel EE et al (2007) Investigating UV screening in leaves by two different types of portable UV fluorimeters reveals in vivo screening by anthocyanins and carotenoids. Photosynth Res 93:205–221

    PubMed  Article  Google Scholar 

  • Ren W et al (2010) UV light spectral response of photosynthetic photochemical efficiency in alpine mosses. J Plant Ecol 3:17–24. doi:10.1093/jpe/rtp029

    Article  Google Scholar 

  • Robberecht R, Caldwell MM (1978) Leaf epidermal transmittance of ultraviolet radiation and its implications for plant sensitivity to ultraviolet-radiation induced injury. Oecologia 32:277–287

    Article  Google Scholar 

  • Robberecht R, Caldwell MM, Billings WD (1980) Leaf ultraviolet optical properties along a latitudinal gradient in the arctic-alpine life zone. Ecology 61:612–619

    Article  Google Scholar 

  • Robinson N (1966) Solar radiation. Elsevier, Amsterdam, pp 171, 177

  • Takahashi S et al (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993. doi:10.1104/pp.110.155747

    PubMed  Article  CAS  Google Scholar 

  • Turcsányi E, Vass I (2000) Inhibition of photosynthetic electron transport by UV-A radiation targets the photosystem II complex. Photochem Photobiol 72:513–520. doi:10.1562/0031-8655(2000)072<0513:IOPETB>2.0.CO;2

    PubMed  Article  Google Scholar 

  • Vass I, Turcsányi E, Touloupakis E, Ghanotakis D, Petrouleas V (2002) The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Biochemistry 41:10200–10208. doi:10.1021/bi020272

    PubMed  Article  CAS  Google Scholar 

  • Vogelmann TC, Björn LO (1984) Measurement of light gradients and spectral regime in plant tissue with a fiber optic probe. Physiol Plant 60:361–368

    Article  Google Scholar 

  • Wagner H, Gilbert M, Wilhelm C (2003) Longitudinal leaf gradients of UV-absorbing screening pigments in barley (Hordeum vulgare). Physiol Plant 117:383–391

    PubMed  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 34:1401–1412

    PubMed  Article  CAS  Google Scholar 

  • Wollenweber E, Dietz VH (1981) Occurrence and distribution of free flavonoid aglycones in plants. Phytochemistry 20:869–893

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Barry Aitchison and Darval Dixon for site access, Michael Kemp for machining custom LiCor chamber and Assoc. Prof. Min Chen for assistance with fluorescence spectrophotometry.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tarryn L. Turnbull.

Additional information

Communicated by Ylo Niinemets.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 40 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Turnbull, T.L., Barlow, A.M. & Adams, M.A. Photosynthetic benefits of ultraviolet-A to Pimelea ligustrina, a woody shrub of sub-alpine Australia. Oecologia 173, 375–385 (2013). https://doi.org/10.1007/s00442-013-2640-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2640-9

Keywords

  • Photosynthetically active radiation spectrum
  • Ultraviolet radiation
  • Chlorophyll a fluorescence
  • Ultraviolet-A-induced photosynthesis