Abstract
The aim of this work was to study the acclimation of photosynthesis in a boreal grass (Phalaris arundinacea L.) grown in controlled environment chambers under elevated temperature (ambient + 3.5°C) and CO2 (700 μmol mol−1) with varying soil water regimes. More specifically, we studied, during two development stages (early: heading; late: florescence completed), how the temperature response of light-saturated net photosynthetic rate (P sat), maximum rate of ribulose-1,5-bisphosphate carboxylase/oxygenase activity (V cmax) and potential rate of electron transport (J max) acclimatized to the changed environment. During the early growing period, we found a greater temperature-induced enhancement of P sat at higher measurement temperatures, which disappeared during the late stage. Under elevated growth temperature, V cmax and J max at lower measurement temperatures (5–15°C) were lower than those under ambient growth temperature during the early period. When the measurements were done at 20–30°C, the situation was the opposite. During the late growing period, V cmax and J max under elevated growth temperature were consistently lower across measurement temperatures. CO2 enrichment significantly increased P sat with higher intercellular CO2 compared to ambient CO2 treatment, however, elevated CO2 slightly decreased V cmax and J max across measurement temperatures, probably due to down-regulation acclimation. For two growing periods, soil water availability affected the variation in photosynthesis and biochemical parameters much more than climatic treatment did. Over two growing periods, V cmax and J max were on average 36.4 and 30.6%, respectively, lower with low water availability compared to high water availability across measurement temperatures. During the late growing period, elevated growth temperature further reduced the photosynthesis under low water availability. V cmax and J max declined along with the decrease in nitrogen content of leaves as growing period progressed, regardless of climatic treatment and water regime. We suggest that, for grass species, seasonal acclimation of the photosynthetic parameters under varying environmental conditions needed to be identified to fairly estimate the whole-life photosynthesis.
Similar content being viewed by others
Abbreviations
- C a :
-
CO2 concentration
- C c :
-
chloroplast CO2 concentration
- C i :
-
intercellular CO2 concentration
- CON:
-
ambient environment in chamber
- EC:
-
elevated CO2 concentration in chamber
- ET:
-
elevated temperature in chamber
- ETC:
-
chamber with combination of temperature and CO2 elevation
- g m :
-
mesophyll conductance
- g sat :
-
light-saturated stomatal conductance
- ΔH a :
-
enthalpy of activation
- ΔH d :
-
enthalpy of deactivation
- J :
-
rate of electron transport
- J max :
-
maximum rate of electron transport
- K c, K o :
-
Rubisco Michaelis constants for CO2, O2
- NL :
-
nitrogen content based on leaf area
- O :
-
O2 concentration
- P c :
-
Rubiscolimited rate of photosynthesis
- P j :
-
RuBP-regeneration-limited rate of photosynthesis
- P N :
-
net photosynthetic rate
- P sat :
-
light-saturated net photosynthetic rate
- PPFD:
-
photosynthetic photon flux densities
- R :
-
molar gas constant
- RCG:
-
reed canary grass
- R d :
-
mitochondrial respiration in light
- ΔS :
-
entropy of the desaturation equilibrium
- T opt :
-
optimal temperature
- V cmax :
-
maximum rate of carboxylation by Rubisco
- α:
-
quantum efficiency
- Γ*:
-
CO2 compensation point (absence of dark respiration)
- θ:
-
curvature of the light-response curve
References
Ainsworth, E.A., Rogers, A.: The response of photosynthesis and stomatal conductance to rising (CO2): mechanisms and environmental interactions. — Plant Cell Environ. 30: 258–270, 2007.
Alonso, A., Pérez, P., Morcuende, R., Martínez-Carrasco, R.: Future CO2 concentrations, though not warmer temperatures, enhance wheat photosynthesis temperature responses. — Physiol. Plant. 132: 102–112, 2008.
Alonso, A., Pérez, P., Martínez-Carrasco, R.: Growth in elevated CO2 enhances temperature response of photosynthesis in wheat. — Physiol. Plant. 135: 109–120, 2009.
Aranjuelo, I., Pérez, P., Hernández, L., Irigoyen, J.J., Zita, G., Martínez-Carrasco, R., Sánchez-Díaz, M.: The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic down-regulation. — Physiol. Plant. 123: 348–358, 2005.
Bernacchi, C.J., Singsaas, E.L., Pimentel, C., Portis, A.R., Long, S.P.: Improved temperature response functions for models of Rubisco-limited photosynthesis. — Plant Cell Environ. 24: 253–259, 2001.
Bernacchi, C.J., Portis, A.R., Nakano, H., von Caemmerer, S., Long, S.P.: Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. — Plant Physiol. 130: 1992–1998, 2002.
Crafts-Brandner, S.J., Salvucci, M.E.: Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. — Proc. Natl. Acad. Sci. USA 97: 13430–13435, 2000.
Drake, B.G., González-Meler, M.A., Long, S.P.: More efficient plants: a consequence of rising atmospheric CO2? — Annu. Rev. Plant Physiol. Mol. Biol. 48: 609–639, 1997.
Farquhar, G.D., von Caemmerer, S., Berry, J.A.: A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. — Planta 149: 78–90, 1980.
Farquhar, G.D., von Caemmerer, S.: Modelling of photosynthetic responses to environmental conditions. — In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (ed.): Physiological Plant Ecology. II. Encyclopedia of Plant Physiology. Vol. 12B. Pp. 548–577. Springer-Verlag, Berlin 1982.
Flexas, J., Bota, J., Loreto, F., Cornic, G., Sharkey, T.D.: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. — Plant Biol. 6: 269–279, 2004a.
Flexas, J., Bota, J., Cifre, J., Escalona, J.M., Galmes, J., Gulias, J., Lefi, E.K., Martinez-Canellas, S.F., Moreno, M.T., Ribas-Carbo, M., Riera, D., Sampol, B., Medrano, H.: Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management. — Ann. Appl. Biol. 144: 273–283, 2004b.
Flexas, J., Bota, J., Galmés, J., Medrano, H., Ribas-Carbo, M.: Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. — Physiol. Plant. 127: 343–352, 2006a.
Flexas, J., Ribas-Carbo, M., Bota, J., Galmés, J., Henkle, M., Martinez-Canellas, S., Medrano, H.: Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to condition of low stomatal conductance and chloroplast CO2 concentration. — New Phytol. 172: 73–82, 2006b.
Ge, Z.M., Zhou, X., Kellomäki, S., Wang, K.Y., Peltola, H., Martikainen, P.J.: Responses of leaf photosynthesis, pigments and chlorophyll fluorescence within canopy position in a boreal grass (Phalaris arundinacea L.) to elevated temperature and CO2 under varying water regimes. — Photosynthetica 49: 172–184, 2011.
Ge, Z.M., Zhou, X., Biasi, C., Kellomäki, S., Wang, K.Y., Peltola, H., Martikainen, P.J.: Carbon assimilation and allocation (13C labeling) in a boreal perennial grass (Phalaris arundinacea) subjected to elevated temperature and CO2 through a growing season. — Environ. Exp. Bot. 75: 150–158, 2012.
Gouasmi, M., Mordelet, P., Demarez, V., Gastellu-Etchegorry, J.P., Le Dantec, V., Dedieu, G., Menaut, J.C., Calvet, J.C., Lamaze, T.: Photosynthesis of a temperate fallow C3 herbaceous ecosystem: measurements and model simulations at the leaf and canopy levels. — Photosynthetica 47: 331–339, 2009.
Hikosaka, K.: Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. — Plant Cell Physiol. 46: 1283–1290, 2005.
Hikosaka, K., Ishikawa, K., Borjigidai, K., Muller, O., Onoda, Y.: Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. — J. Exp. Bot. 57: 291–302, 2006.
Hu, L.X., Wang, Z.L., Huang, B.R.: Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C3 perennial grass species. — Physiol. Plant. 139: 93–106, 2010.
Lawlor, D.W.: Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. — Ann. Bot. 89: 1–15, 2002.
Long, S.P., Bernacchi, C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. — J. Exp. Bot. 54: 2393–2401, 2003.
Long, S.P., Ainsworth, E.H., Rogers, A., Ort, D.R.: Rising atmospheric carbon dioxide: plants FACE the future. — Annu. Rev. Plant. Biol. 55: 591–628, 2004.
Medlyn, B.E., Loustau, D., Delzon, S.: Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). — Plant Cell Environ. 25: 1155–1165, 2002a.
Medlyn, B.E., Dreyer, E., Ellsworth, D., Forstreuter, M., Harley, P.C., Kirschbaum, M.U.F., Le Roux, X., Montpied, P., Stassenmeyer, J., Walcroft, A., Wang, K., Loustau, D.: Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. — Plant Cell Environ. 25: 1167–1179, 2002b.
Nowak, R.S., Ellsworth, D.S., Smith, S.D.: Functional responses of plants to elevated atmospheric CO2 — do photosynthetic and productivity data from FACE experiments support early predictions? — New Phytol. 162: 253–280, 2004.
Parry, M.A., Andraloj, P.J., Khan, S., Lea, P.J., Keys, A.J.: Rubisco activity: effects of drought stress. — Ann. Bot. 89: 833–839, 2002.
Pérez, P., Zita, G., Morcuende, R., Martínez-Carrasco, R.: Elevated CO2 and temperature differentially affect photosynthesis and resource allocation in flag and penultimate leaves of wheat. — Photosynthetica 45: 9–17, 2007.
Rogers, A., Gibon, Y., Stitt, M., Morgan, P.B., Bernacchi, C.J., Ort, D.R., Long, S.P.: Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. — Plant Cell Environ. 29: 1651–1658, 2006.
Salvucci, M.E., Crafts-Brandner, S.J.: Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. — Physiol. Plant. 120: 179–186, 2004.
Sahramaa, M., Jauhiainen, L.: Characterization of development and stem elongation of reed canary grass under northern conditions. — Ind. Crop Prod. 18: 155–169, 2003.
Schrader, S.M., Kane, H.J., Sharkey, T.D., von Caemmerer, S.: High temperature enhances inhibitor production but reduces fallover in tobacco Rubisco. Funct. Plant Biol. 33: 921–929, 2006.
Sharkey, T.D., Bernacchi, C.J., Farquhar, G.D., Singsaas, E.L.: Fitting photosynthetic carbon dioxide response curves for C3 leaves. — Plant Cell Environ. 30: 1035–1040, 2007.
Urban, O., Ač, A., Kalina, J., Priwitzer, T., Šprtová, M., Špunda, V., Marek, M.V. Temperature dependences of carbon assimilation processes in four dominant species from mountain grassland ecosystem. — Photosynthetica 45: 392–399, 2007.
von Caemmerer, S., Quick, P.W.: Rubisco, physiology in vivo. — In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (ed.): Photosynthesis: Physiology and Metabolism. Pp. 85–113. Kluwer Academic Publ., Dordrecht 2000.
Wullschleger, S.D., Gunderson, C.A., Hanson, P.J., Wilson, K.B., Norby, R.J.: Sensitivity of stomatal and canopy conductance to elevated CO2 concentration — interacting variables and perspectives of scale. — New Phytol. 153: 485–496, 2002a.
Wullschleger, S.D., Tschaplinski, T.J., Norby, R.J.: Plant water relations at elevated CO2 — implications for water-limited environments. — Plant Cell Environ. 25: 319–331, 2002b.
Yamori, W., Suzuki, K., Noguchi, K., Nakai, M., Terashima, I.: Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. — Plant Cell Environ. 29: 1659–1670, 2006.
Zhang, D.Y., Chen, G.Y., Chen, J., Yong, Z.H., Zhu, J.G., Xu, D.Q.: Photosynthetic acclimation to CO2 enrichment related to ribulose-1,5-bisphosphate carboxylation limitation in wheat. — Photosynthetica 47: 152–154, 2009.
Zhou, Y., Lam, H.M., Zhang, J.: Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. — J. Exp. Bot. 58: 1207–1217, 2007.
Zhou, X., Ge, Z.M., Kellomäki, S., Wang, K.Y., Peltola, H., Martikainen, P.: Effects of elevated CO2 and temperature on leaf characteristics, photosynthesis and carbon storage in aboveground biomass of a boreal bioenergy crop (Phalaris arundinacea L.) under varying water regimes. — Global Change Biol. Bioenerg. 3: 223–234, 2011.
Zhou, X., Ge, Z.M., Kellomäki, S., Wang, K.Y., Peltola, H., Martikainen, P., Lemettinen, M., Hassinen, A., Ikonen, R.: Multi-objective environment chamber system for studying plant responses to climate change. — Photosynthetica DOI: 10.1007/s11099-011-0063-6, 2012.
Xu, Z.Z, Zhou, G.S.: Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. — Planta 224: 1080–1090, 2006.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgments: This work was funded through the Finland Distinguished Professor Programme (FiDiPro) of the Academy of Finland (No. 127299-A5060-06) and the Finnish Network Graduate School in Forest Sciences of the Academy of Finland (No. 49996). Thanks are due to Matti Turpeinen of Vapo Ltd. for providing relevant logistical information on the field sites. The controlled environment chamber system was funded by European Regional Development Fund (ERDF) granted by the State Provincial Office of Eastern Finland. Matti Lemettinen, Alpo Hassinen, Risto Ikonen and Eine Ihanus at the Mekrijärvi Research Station, are thanked for their technical assistance. Dr. David Gritten is greatly thanked for revising the language of this paper.
Rights and permissions
About this article
Cite this article
Ge, Z.M., Zhou, X., Kellomäki, S. et al. Acclimation of photosynthesis in a boreal grass (Phalaris arundinacea L.) under different temperature, CO2, and soil water regimes. Photosynthetica 50, 141–151 (2012). https://doi.org/10.1007/s11099-012-0014-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-012-0014-x