Photoprotective carotenoids and antioxidants are more affected by canopy position than by nitrogen supply in 21-year-old Pinus radiata
Sabine Posch A B E , Charles R. Warren C , Mark A. Adams D and Helmut Guttenberger BA School of Forest and Ecosystem Science, The University of Melbourne, Water Street, Creswick, Vic. 3363, Australia.
B Department for Plant Sciences, Karl-Franzens-University Graz, Schubertstraße 51, 8010 Graz, Austria.
C School of Biological Sciences, University of Sydney, Heydon-Laurence Building A08, Sydney, NSW 2006, Australia.
D School of Biological Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.
E Corresponding author. Email: sposch@unimelb.edu.au
F This paper originates from a presentation at EcoFIZZ 2007, Richmond, New South Wales, Australia, September 2007.
Functional Plant Biology 35(6) 470-482 https://doi.org/10.1071/FP08124
Submitted: 14 April 2008 Accepted: 4 June 2008 Published: 4 August 2008
Abstract
Photoprotection, light harvesting and light utilisation were investigated as a function of variation in N supply and canopy position in 21-year-old Pinus radiata D. Don. Chlorophyll fluorescence, gas exchange and photoprotective compounds were measured on lower, middle and upper canopy needles in trees receiving N fertiliser and in control trees not receiving N fertiliser. Irrespective of canopy height, additional N increased the light-harvesting capacity through greater contents of chlorophyll, neoxanthin and lutein, but did not affect light-utilisation processes, such as effective quantum yield of PSII or rates of net CO2 assimilation. Additional N fertiliser did not affect the concentrations of the measured photoprotective carotenoids (violaxanthin, antheraxanthin, zeaxanthin, α-carotene and β-carotene) or antioxidants (ascorbic acid, glutathione and α-tocopherol); however, carotenoids and antioxidants were strongly affected by canopy height and increased in concentration with increasing canopy height. The present study found that pools of photoprotective carotenoids and antioxidants were not driven by imbalances in light-harvesting and light-utilisation processes, but rather by gradients in light.
Additional keywords: α-tocopherol, ascorbic acid, chlorophyll a fluorescence, chloroplast pigments, gas exchange, glutathione.
Acknowledgements
We thank Hancock Victorian Plantations and Jörg Kruse for providing the plantation, Phil Gerschwitz for excellent assistance in the field and Klaus Remele for excellent technical support in the laboratory. Sabine Posch gratefully acknowledges financial support of a DOC scholarship from the Austrian Academy of Sciences.
Arena C,
Vitale L, De Sants AV
(2005) Photosynthetic response of Quercus ilex L. plants grown on compost and exposed to increasing photon flux densities and elevated CO2. Photosynthetica 43, 615–619.
| Crossref | GoogleScholarGoogle Scholar |
Asada K
(1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bettmann GT,
Ratnayaka HH,
Molin WT, Sterling TM
(2006) Physiological and antioxidant responses of cotton and spurred anoda (Anoda cristata) under nitrogen deficiency. Weed Science 54, 641–650.
| Crossref | GoogleScholarGoogle Scholar |
Chen LS, Cheng LL
(2003) Both xanthophyll cycle-dependent thermal dissipation and the antioxidant system are up-regulated in grape (Vitis labrusca L. cv. Concord) leaves in response to N limitation. Journal of Experimental Botany 54, 2165–2175.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen YZ,
Murchie EH,
Hubbart S,
Horton P, Peng SB
(2003) Effects of season-dependent irradiance levels and nitrogen-deficiency on photosynthesis and photoinhibition in field-grown rice (Oryza sativa). Physiologia Plantarum 117, 343–351.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cruz JL,
Mosquim PR,
Pelacani CR,
Araujo WL, DaMatta FM
(2003) Photosynthesis impairment in cassava leaves in response to nitrogen deficiency. Plant and Soil 257, 417–423.
| Crossref | GoogleScholarGoogle Scholar |
Dang QL,
Margolis HA,
Coyea MR,
Sy M, Collatz GJ
(1997) Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapor pressure difference. Tree Physiology 17, 521–535.
| PubMed |
Demmig-Adams B, Adams WW
(1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
| Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW
(2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. The New Phytologist 172, 11–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Easter MJ, Spies TA
(1994) Using hemispherical photography for estimating photosynthetic photon flux-density under canopies and in gaps in douglas-fir forests of the pacific-northwest. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 24, 2050–2058.
| Crossref | GoogleScholarGoogle Scholar |
Ehleringer JR
(1981) Leaf absorptances of Mohave and Sonoran desert plants. Oecologia 49, 366–370.
| Crossref | GoogleScholarGoogle Scholar |
Evans JR, Terashima I
(1987) Effect of nitrogen nutrition on electron transport components and photosynthesis in spinach. Australian Journal of Plant Physiology 14, 59–68.
Field C
(1983) Allocating leaf nitrogen for the maximization of carbon gain – leaf age as a control on the allocation program. Oecologia 56, 341–347.
| Crossref | GoogleScholarGoogle Scholar |
Fife DN, Nambiar EKS
(1997) Changes in the canopy and growth of Pinus radiata in response to nitrogen supply. Forest Ecology and Management 93, 137–152.
| Crossref | GoogleScholarGoogle Scholar |
Foyer C, Noctor G
(2000) Oxygen processing in photosynthesis: regulation and signalling. The New Phytologist 146, 359–388.
| Crossref | GoogleScholarGoogle Scholar |
Fryer MJ,
Andrews JR,
Oxborough K,
Blowers DA, Baker NR
(1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
García-Plazaola JI, Becerril JM
(2000) Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings from diverse climatic origins. Trees – Structure and Function 14, 339–343.
García-Plazaola JI,
Becerril JM,
Hernandez A,
Niinemets U, Kollist H
(2004) Acclimation of antioxidant pools to the light environment in a natural forest canopy. The New Phytologist 163, 87–97.
| Crossref | GoogleScholarGoogle Scholar |
Hansen U,
Fiedler B, Rank B
(2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees – Structure and Function 16, 354–364.
Hansen U,
Schneiderheinze J,
Stadelmann S, Rank B
(2003) The alpha-tocopherol content of leaves of pedunculate oak (Quercus robur L.) – variation over the growing season and along the vertical light gradient in the canopy. Journal of Plant Physiology 160, 91–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Herbinger K,
Then C,
Low M,
Haberer K, Alexous M , et al.
(2005) Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure. Environmental Pollution 137, 476–482.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kato MC,
Hikosaka K,
Hirotsu N,
Makino A, Hirose T
(2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant & Cell Physiology 44, 318–325.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kruse J, Adams MA
(2008) Three parameters comprehensively describe the temperature response of respiratory oxygen reduction. Plant, Cell & Environment 31, 954–967.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Logan BA,
Demmig-Adams B,
Rosenstiel TH, Adams WW
(1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209, 213–220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Logan BA,
Adams WW, Demmig-Adams B
(2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Functional Plant Biology 34, 853–859.
| Crossref | GoogleScholarGoogle Scholar |
Lundmark T,
Bergh J,
Strand M, Koppel A
(1998) Seasonal variation of maximum photochemical efficiency in boreal Norway spruce stands. Trees – Structure and Function 13, 63–67.
Maxwell K, Johnson GN
(2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Müller P,
Xiao-Ping L, Niyogi KK
(2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Munne-Bosch S, Alegre L
(2002) The function of tocopherols and tocotrienols in plants. Critical Reviews in Plant Sciences 21, 31–57.
Niinemets U,
Ellsworth DS,
Lukjanova A, Tobias M
(2001) Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. Tree Physiology 21, 1231–1244.
| PubMed |
Niinemets U,
Lukjanova A,
Turnbull MH, Sparrow AD
(2007) Plasticity in mesophyll volume fraction modulates light-acclimation in needle photosynthesis in two pines. Tree Physiology 27, 1137–1151.
| PubMed |
Niyogi KK
(2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Noctor G, Foyer CH
(1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palmroth S, Hari P
(2001) Evaluation of the importance of acclimation of needle structure, photosynthesis, and respiration to available photosynthetically active radiation in a Scots pine canopy. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 31, 1235–1243.
| Crossref | GoogleScholarGoogle Scholar |
Persson J,
Gardeström P, Näsholm T
(2006) Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. Journal of Experimental Botany 57, 2651–2659.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Poorter L,
Oberbauer SF, Clark DB
(1995) Leaf optical properties along a vertical gradient in a tropical rain forest canopy in Costa Rica. American Journal of Botany 82, 1257–1263.
| Crossref | GoogleScholarGoogle Scholar |
Pórte A, Loustau D
(1998) Variability of the photosynthetic characteristics of mature needles within the crown of a 25-year-old Pinus pinaster. Tree Physiology 18, 223–232.
| PubMed |
Posch S,
Warren CR,
Kruse J,
Guttenberger H, Adams MA
(2008) Nitrogen allocation and the fate of absorbed light in 21-year-old Pinus radiata. Tree Physiology 28, 375–384.
| PubMed |
Ramalho JC,
Campos PS,
Teixeira M, Nunes MA
(1998) Nitrogen dependent changes in antioxidant system and in fatty acid composition of chloroplast membranes from Coffea arabica L. plants submitted to high irradiance. Plant Science 135, 115–124.
| Crossref | GoogleScholarGoogle Scholar |
Richardson AD, Berlyn GP
(2002) Changes in foliar spectral reflectance and chlorophyll fluorescence of four temperate species following branch cutting. Tree Physiology 22, 499–506.
| PubMed |
Robakowski P
(2005) Species-specific acclimation to strong shade modifies susceptibility of conifers to photoinhibition. Acta Physiologiae Plantarum 27, 255–263.
| Crossref | GoogleScholarGoogle Scholar |
Sands PJ
(1995) Modelling Canopy Production. 1. Optimal distribution of photosynthetic resources. Australian Journal of Plant Physiology 22, 593–601.
Senger H,
Wagner C,
Hermsmeier D,
Hohl N,
Urbig T, Bishop NI
(1993) The influence of light intensity and wavelength on the contents of α- and β-carotene and their xanthophylls in green algae. Journal of Photochemistry and Photobiology. B, Biology 18, 273–279.
| Crossref | GoogleScholarGoogle Scholar |
Siefermann-Harms D
(1994) Light and temperature control of season-dependent changes in the α- and β-carotene content of spruce needles. Journal of Plant Physiology 143, 488–494.
Smirnoff N
(2000) The function and metabolism of ascorbic acid in plants. Current Opinion in Plant Biology 3, 229–235.
| PubMed |
Smirnoff N,
Todd P, Stewart GR
(1984) The occurrence of nitrate reduction in the leaves of woody plants. Annals of Botany 54, 363–374.
Tausz M,
Wonisch A,
Grill D,
Morales D, Jimenez MS
(2003) Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation. Journal of Experimental Botany 54, 1505–1510.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tausz M,
Loffler S,
Posch S,
Monschein S,
Grill D, Katzel R
(2005) Do photoprotective pigments and antioxidants in needles of Pinus sylvestris relate to high N or water availability at field plots in a dry year? Phyton-Annales Rei Botanicae 45, 107–116.
Van Kooten O, Snel JFH
(1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25, 147–150.
| Crossref | GoogleScholarGoogle Scholar |
Verhoeven AS,
Demmig-Adams B, Adams WW
(1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiology 113, 817–824.
| PubMed |
Warren CR, Adams MA
(2001) Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant, Cell & Environment 24, 597–609.
| Crossref | GoogleScholarGoogle Scholar |
Warren CR,
Dreyer E, Adams MA
(2003a) Photosynthesis–Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores. Trees – Structure and Function 17, 359–366.
Warren CR,
Ethier GJ,
Livingston NJ,
Grant NJ,
Turpin DH,
Harrison DL, Black TA
(2003b) Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant, Cell & Environment 26, 1215–1227.
| Crossref | GoogleScholarGoogle Scholar |
Wood GB
(1971) Shape of Pinus radiata fascicles and the implications for estimating needle surface area. Australian Forest Research 5, 31–36.
Young AJ
(1991) The photoprotective role of carotenoids in higher plants. Physiologia Plantarum 83, 702–708.
| Crossref | GoogleScholarGoogle Scholar |
