Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP09098
RESEARCH ARTICLE
Contents Vol 36(12)

Interactive effects of high irradiance and moderate heat on photosynthesis, pigments, and tocopherol in the tree-fern Dicksonia antarctica

Liubov Volkova A C , Michael Tausz A , Lauren T. Bennett A and Erwin Dreyer A B
+ Author Affiliations
- Author Affiliations

A Department of Forest and Ecosystem Science, Melbourne School of Land and Environment, The University of Melbourne, Water Street, Creswick, Vic. 3363, Australia.

B INRA, Nancy-Université, UMR 1137 ‘Ecologie et Ecophysiologie Forestières’, F-54280 Champenoux, France.

C Corresponding author. Email: l.volkova@pgrad.unimelb.edu.au

Functional Plant Biology 36(12) 1046-1056 https://doi.org/10.1071/FP09098
Submitted: 5 May 2009  Accepted: 31 July 2009   Published: 3 December 2009

Abstract

Effects of high irradiance and moderate heat on photosynthesis of the tree-fern Dicksonia antarctica (Labill., Dicksoniaceae) were examined in a climate chamber under two contrasting irradiance regimes (900 and 170 µmol photons m–2 s–1) and three sequential temperature treatments (15°C; 35°C; back to 15°C). High irradiance led to decline in predawn quantum yield of photochemistry, Fv/Fm (0.73), maximal Rubisco activity (Vcmax; from 37 to 29 µmol m–2s–1), and electron transport capacity (Jmax; from 115 to 67 µmol m–2 s–1). Temperature increase to 35°C resulted in further decreases in Fv/Fm (0.45) and in chlorophyll bleaching of high irradiance plants, while Vcmax and Jmax were not affected. Critical temperature for thylakoid stability (Tc) of D. antarctica was comparable with other higher plants (c. 47°C), and increases of Tc with air temperature were greater in high irradiance plants. Increased Tc was not associated with accumulation of osmotica or zeaxanthin formation. High irradiance increased the xanthophyll cycle pigment pool (V+A+Z, 91 v. 48 mmol mol–1 chlorophyll–1), de-epoxidation state (56% v. 4%), and α-tocopherol. Temperature increase to 35°C had no effect on V+A+Z and de-epoxidation state in both light regimes, while lutein, β-carotene and α-tocopherols increased, potentially contributing to increased membrane stability under high irradiance.

Additional keywords: α-tocopherols, β-carotene, critical temperature, de-epoxidation state, Jmax, light regime, lutein, osmolality, photoinhibition, Vcmax, temperature, xanthophyll pigments.


Acknowledgements

Liubov Volkova acknowledges support by a Melbourne Research Scholarship and by an S.F. Pond Trust Travelling Scholarship for 2006. The work was in part supported by a research contract with the Victorian Department of Sustainability and Environment and by an internal grant of the University of Melbourne to M Tausz. Thanks to Andrew Merchant for useful hints on the experimental design, to all the kind and helpful staff of INRA Nancy, in particular to Christophe Bailly for ensuring smooth operation of the climate chamber during the experiment, Jean Marie Gioria for growing the tree-ferns, and to Jacqueline Marchand for N quantification in the fronds. Damien L. Callahan, School of Botany, University of Melbourne, is personally thanked for help with operating the HPLC.


References


Arens NC (1997) Responses of leaf anatomy to light environment in the tree fern Cyathea caracasana (Cyatheaceae) and its application to some ancient seed ferns. Palaios 12, 84–94.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Bannister P, Wildish KL (1982) Light compensation points and specific leaf areas in some New-Zealand ferns. New Zealand Journal of Botany 20, 421–424. open url image1

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 31, 491–543. open url image1

Callister AN, Arndt SK, Adams MA (2006) Comparison of four methods for measuring osmotic potential of tree leaves. Physiologia Plantarum 127, 383–392.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Department of Natural Resources and Environment (2002) ‘Victorian tree fern management plan.’ (Department of Natural Resources and Environment: East Melbourne, Australia)

Downton WJS, Berry JA, Seemann JR (1984) Tolerance of photosynthesis to high temperature in desert plants. Plant Physiology 74, 786–790.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiology 21, 223–232.
|  CAS |
open url image1

Ducruet JM, Peeva V, Havaux M (2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynthesis Research 93, 159–171.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126, 345–354.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer-Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Froux F, Ducrey M, Epron D, Dreyer E (2004) Seasonal variations and acclimation potential of the thermostability of photochemistry in four Mediterranean conifers. Annals of Forest Science 61, 235–241.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

García-Plazaola JI, Becerril JM (1999) A rapid high performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochemical Analysis 10, 307–313.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ghouil H, Montpied P, Epron D, Ksontini M, Hanchi B, Dreyer E (2003) Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings. Tree Physiology 23, 1031–1039.
|  CAS |
open url image1

Haldimann P (1999) How do changes in temperature during growth affect leaf pigment composition and photosynthesis in Zea mays genotypes differing in sensitivity to low temperature? Journal of Experimental Botany 50, 543–550.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Havaux M, Gruszecki WI (1993) Heat-induced and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin – indications of a regulatory effect of zeaxanthin on thylakoid membrane fluidity. Photochemistry and Photobiology 58, 607–614.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: Possible involvement of xanthophyll cycle pigments. Planta 198, 324–333.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hennessy KJ , Fitzharris B , Bates BC , Harvey N , Howden SM , Hughes L , Salinger J , Warrick R (2007) Australia and New Zealand. In ‘Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds ML Parry, OF Canziani, JP Palutikof, PJ van der Linden, CE Hanson) pp. 507–540. (Cambridge University Press: Cambridge, UK)

Hunt MA, Davidson NJ, Unwin GL, Close DC (2002) Ecophysiology of the soft tree fern Dicksonia antarctica Labill. Austral Ecology 27, 360–368.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hüve K, Bichele I, Tobias M, Niinemets Ü (2006) Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential. Plant, Cell & Environment 29, 212–228.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Kirchgeßner HD, Reichert K, Hauff K, Steinbrecher R, Schnitzler JP, Pfündel EE (2003) Light and temperature, but not UV radiation, affect chlorophylls and carotenoids in Norway spruce needles (Picea abies (L.) Karst.). Plant, Cell & Environment 26, 1169–1179.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Lambers H , Chapin FS , Pons TL (2008) ‘Plant physiological ecology.’ (Springer: New York)

Large MF , Braggins JE (2004) ‘Tree ferns.’ (CSIRO Publishing: Collingwood, Vic.)

Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173–182.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lichtenthaler HK (1987) Chlorophylls and carotenoids – pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lindenmayer DB, Cunningham RB, Donnelly CF, Triggs BJ, Belvedere M (1994) The conservation of arboreal marsupials in the montane ash forests of the central highlands of Victoria, South-Eastern Australia. 5. Patterns of use and the microhabitat requirements of the mountain brushtail possum Trichosurus caninus ogilby in retained linear habitats (wildlife corridors). Biological Conservation 68, 43–51.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Llusià J, Peñuelas J, Munné-Bosch S (2005) Sustained accumulation of methyl salicylate alters antioxidant protection and reduces tolerance of holm oak to heat stress. Physiologia Plantarum 124, 353–361.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Lovelock CE, Kursar TA, Skillman JB, Winter K (1998) Photoinhibition in tropical forest understorey species with short- and long-lived leaves. Functional Ecology 12, 553–560.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Magrath R, Lill A (1983) The use of time and energy by the crimson rosella in a temperate wet forest in winter. Australian Journal of Zoology 31, 903–912.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Functional Plant Biology 36, 20–36.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

McCarthy PM (1998) ‘Ferns, gymnosperms and allied groups.’ (CSIRO Publishing: Melbourne, Australia)

Merchant A, Tausz M, Arndt SK, Adams MA (2006) Cyclitols and carbohydrates in leaves and roots of 13 Eucalyptus species suggest contrasting physiological responses to water deficit. Plant, Cell & Environment 29, 2017–2029.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Montpied P, Granier A, Dreyer E (2009) Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. Journal of Experimental Botany 60, 2407–2418.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. Journal of Plant Physiology 162, 743–748.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica Et Biophysica Acta – Bioenergetics 1767, 414–421.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Niyogi KK (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Nobel PS, Calkin HW, Gibson AC (1984) Influences of PAR, temperature and water vapor concentration on gas exchange by ferns. Physiologia Plantarum 62, 527–534.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

North HM, De Almeida A, Boutin JP, Frey A, To A, Botran L, Sotta B, Marion-Poll A (2007) The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. The Plant Journal 50, 810–824.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197, 176–183.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ough K, Murphy A (2004) Decline in tree-fern abundance after clearfell harvesting. Forest Ecology and Management 199, 153–163. open url image1

Robakowski P, Montpied P, Dreyer E (2002) Temperature response of photosynthesis of silver fir (Abies alba Mill.) seedlings. Annals of Forest Science 59, 163–170.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Roberts NR, Dalton PJ, Jordan GJ (2005) Epiphytic ferns and bryophytes of Tasmanian tree-ferns: a comparison of diversity and composition between two host species. Austral Ecology 30, 146–154.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Salvucci ME, Crafts-Brandner SJ (2004) Mechanism for deactivation of Rubisco under moderate heat stress. Physiologia Plantarum 122, 513–519.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Schreiber U, Berry JA (1977) Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of photosynthetic apparatus. Planta 136, 233–238.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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-carotene and β-carotene and their xanthophylls in green algae. Journal of Photochemistry and Photobiology. B, Biology 18, 273–279.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sinsawat V, Leipner J, Stamp P, Fracheboud Y (2004) Effect of heat stress on the photosynthetic apparatus in maize (Zea mays L.) grown at control or high temperature. Environmental and Experimental Botany 52, 123–129.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tallon C, Quiles MJ (2007) Acclimation to heat and high light intensity during the development of oat leaves increases the NADH DH complex and PTOX levels in chloroplasts. Plant Science 173, 438–445.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tausz M, Hietz P, Briones O (2001) The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of a Mexican cloud forest. Australian Journal of Plant Physiology 28, 775–783.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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 | CAS | open url image1

Tausz M, Warren CR, Adams MA (2005) Dynamic light use and protection from excess light in upper canopy and coppice leaves of Nothofagus cunninghamii in an old growth, cool temperate rainforest in Victoria, Australia. New Phytologist 165, 143–156.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tingey DT, Evans RC, Bates EH, Gumpertz ML (1987) Isoprene emissions and photosynthesis in 3 ferns – the influence of light and temperature. Physiologia Plantarum 69, 609–616.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

von Caemmerer S, Evans JR, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195, 88–97.
|  CAS |
open url image1

Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K , et al. (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynthesis Research 98, 589–608.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zsófi Z, Váradi G, Bálo B, Marschall M, Nagy Z, Dulai S (2009) Heat acclimation of grapevine leaf photosynthesis: mezo- and macroclimatic aspects. Functional Plant Biology 36, 310–322.
| Crossref | GoogleScholarGoogle Scholar | open url image1