Soil Temperature and Phosphorus Supply Interactively Affect Physiological Responses of White Birch to CO2 Elevation


Phosphorus (P) is a common limiting nutrient element to plants and its supply and uptake by plants are strongly influenced by soil temperature. However, the interactive effects of the two factors on the physiological responses of plants to global change are poorly understood. In this study, we examined how P supply and Tsoil interacted in affecting physiological responses in white birch (Betula papyrifera) to [CO2]. We exposed seedlings to 7°C, 17°C and 27°C Tsoil, 0.1479, 0.3029 and 0.5847 mM P2O5, and 360 and 720 μmol·mol-1 [CO2] for four months. We have found that both the low soil temperature and CO2 elevation resulted in photosynthetic down regulation but the specific mechanisms of the down regulation were different between the two treatments, particularly the relative contributions of biochemical and photochemical capacity, mesophyll conductance and sink strength for carbohydrate utilization to the down regulation. Furthermore, our data suggest that morphological adjustments, such as reduced leaf size and total leaf area, were the primary form of responses in white birch to low phosphorus supply and no significant physiological acclimation to P supply was detected. Our results suggest that white birch will likely enhance water use efficiency under the projected future climate conditions with doubled carbon dioxide concentration, particularly at warmer soil temperatures. Although a trade-off between water use efficiency and nutrient use efficiency is widely accepted, our results suggest that there does not have to be a trade-off between the two, for instance, CO2 elevation increased both use efficiencies and low soil temperature and reduced nitrogen efficiency without affecting water use efficiency under elevated CO2.

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G. Danyagri and Q. Dang, "Soil Temperature and Phosphorus Supply Interactively Affect Physiological Responses of White Birch to CO2 Elevation," American Journal of Plant Sciences, Vol. 5 No. 2, 2014, pp. 219-229. doi: 10.4236/ajps.2014.52029.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] A. Rogers, B. U. Fischer, J. Bryant, M. Frehner, H. Blum, C. A. Raines and S. P. Long, “Acclimation of Photosynthesis to Elevated CO2 under Low Nitrogen Nutrition Is Affected by the Capacity for Assimilate Utilization. Perennial Ryegrass under Free-Air CO2 Enrichment,” Plant Physiology, Vol. 118, No. 2, 1998, pp. 683-689.
[2] H. Saxe, D. S. Ellsworth and J. Heath, “Tree and Forest Functioning in an Enriched CO2 Atmosphere,” New Phytologist, Vol. 139, No. 3, 1998, pp. 395-436.
[3] P. A. Davey, A. J. Parsons, L. Atkinson, K. Wadge and S. P. Long, “Does Photosynthetic Acclimation to Elevated CO2 Increase Photosynthetic Nitrogen-Use Efficiency? A Study of Three Native UK Grassland Species in Open-Top Chambers,” Functional Ecology, Vol. 13, No. S1, 1999, pp. 21-28.
[4] R. Liozon, F. W. Badeck, B. Genty, S. Meyer and B. Saugier, “Leaf Photosynthetic Characteristics of Beech (Fagus sylvatica) Saplings during Three Years of Exposure to Elevated CO2 Concentration,” Tree Physiology, Vol. 20, No. 4, 2000, pp. 239-247.
[5] S. Zhang and Q.-L. Dang, “Effects of Soil Temperature and Elevated Atmospheric CO2 Concentration on Gas Exchange, in Vivo Carboxylation and Chlorophyll Fluorescence in Jack Pine and White Birch Seedlings,” Tree Physiology, Vol. 25, No. 5, 2005, pp. 523-531.
[6] S. Zhang and Q.-L. Dang, “Effects of Carbon Dioxide Concentration and Nutrition on Photosynthetic Functions of White Birch Seedlings,” Tree Physiology, Vol. 26, No. 11, 2006, pp. 1457-1467.
[7] S. P. Long, E. A. Ainsworth, A. Rogers and D. R. Ort, “Rising Atmospheric Carbon Dioxide: Plants FACE the Future,” Annual Review of Plant Biology, Vol. 55, 2004, pp. 591-628.
[8] B. Cao, Q.-L. Dang and S. Zhang, “Relationship between Photosynthesis and Leaf Nitrogen Concentration in Ambient and Elevated [CO2] in White Birch Seedlings,” Tree Physiology, Vol. 27, No. 6, 2007, pp. 891-899.
[9] R. S. Nowak, D. S. Ellsworth and S. D. Smith, “Functional Responses of Plants to Elevated Atmospheric CO2: Do Photosynthetic and Productivity Data from FACE Experiments Support Early Predictions?” New Phytologist, Vol. 162, No. 2, 2004, pp. 253-280.
[10] S. Li, S. R. Pezeshki and S. Goodwin, “Effects of Soil Moisture Regimes on Photosynthesis and Growth in Cattail (Typha latifolia),” Acta Oecologica, Vol. 25, No. 1-2, 2004, pp. 17-22.
[11] K. Y. Crous, M. B. Walters and D. S. Ellsworth, “Elevated CO2 Concentration Affects Leaf Photosynthesis-Nitrogen Relationships in Pinus taeda over Nine Years in FACE,” Tree Physiology, Vol. 28, No. 4, 2008, pp. 607-614.
[12] C. Plassard and B. Dell, “Phosphorus Nutrition of Mycorrhizal Trees,” Tree Physiology, Vol. 30, No. 9, 2010, pp. 1129-1139.
[13] D. M. Oosterhuis, A. C. Bibi, E. D. Gonias and M. Mozaffari, “Effect of Phosphorus Deficiency on Cotton Physiology,” AAES Research Series 562, 2007, pp. 35-38.
[14] M. Chaudhary, J. Adu-Gyamfi, H. Saneoka, N. Nguyen, R. Suwa, S. Kanai, H. El-Shemy, D. Lightfoot and K. Fujita, “The Effect of Phosphorus Deficiency on Nutrient Uptake, Nitrogen Fixation and Photosynthetic Rate in Mashbean, Mungbean and Soybean,” Acta Physiologiae Plantarum, Vol. 30, No. 4, 2008, pp. 537-544.
[15] A. Brooks, “Effects of Phosphorus Nutrition on Ribulse1,5-Bisphosphate Carboxylase Activation, Photosynthetic Quantum Yield and Amounts of Some Calvin Cycle Metabolites in Spinach Leaves,” Australian Journal of Plant Physiology, Vol. 13, No. 2, 1986, pp. 221-237.
[16] J. Jacob and D. W. Lawlor, “Dependence of Photosynthesis of Sunflower and Maize Leaves on Phosphate Supply, Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activity, and Ribulose-1,5-Bisphosphate Pool Size,” Plant Physiology, Vol. 98, No. 3, 1992, pp. 801-807.
[17] M. Rao and N. Terry, “Leaf Phosphate Status, Photosynthesis, and Carbon Partitioning in Sugar Beet. IV. Changes with Time Following Increased Supply of Phosphate to Low-Phosphate Plants,” Plant Physiology, Vol. 107, No. 4, 1995, pp. 1313-1321.
[18] Z.-H. Lin, L.-S. Chen, R.-B. Chen, F.-Z. Zhang, H.-X. Jiang and N. Tang, “CO2 Assimilation, Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase, Carbohydrates and Photosynthetic Electron Transport Probed by the JIP-Test, of Tea Leaves in Response to Phosphorus Supply,” BMC Plant Biology, Vol. 9, 2009, p. 43.
[19] H. W. Heldt, C. J. Chon and G. H. Lorimer, “Phosphate requirement for the Light Activation of Ribulosc-1.5-Bisphosphate Carboxylase in Intact Spinach Chloroplast,” FEBS Letters, Vol. 92, No. 2, 1978, pp. 234-240.
[20] R. C. Leegood, D. A. Walker and C. H. Foyer, “Regulation of the Benson-Calvin Cycle,” In: N. Barber and R. Barker, Eds., Photosynthetic Mechanisms and the Environment, Elsevier, Amsterdam, 1985, pp. 189-258.
[21] U. I. Flügge, K. Fischer, A. Gross, W. Sebald, F. Lottspeich and C. Eckerskorn, “The Triose Phosphate-3-Phosphoglyceratephosphate Translocator from Spinach Chloroplasts: Nucleotide Sequence of a Full-Length cDNA Clone and Import of the in Vitro Synthesized Precursor Protein into Chloroplasts,” EMBO Journal, Vol. 8, No. 1, 1989, pp. 39-46.
[22] M. Rao and N. Terry, “Leaf Phosphate Status, Photosynthesis and Carbon Partitioning in Sugar Beet. I. Changes in Growth, Gas Exchange and Calvin Cycle Enzymes,” Plant Physiology, Vol. 90, No. 3, 1989, pp. 814-819.
[23] D. T. Tissue and J. D. Lewis, “Photosynthetic Responses of Cottonwood Seedlings Grown in Glacial through Future Atmospheric [CO2] Vary with Phosphorus Supply,” Tree Physiology, Vol. 30, No. 11, 2010, pp. 1361-1372.
[24] T. A. Day, S. A. Heckathorn and E. H. Delucia, “Limitations of Photosynthesis in Pinus taeda (Loblolly Pine) at Low Soil Temperatures,” Plant Physiology, Vol. 96, No. 4, 1991, pp. 1246-1254.
[25] H. Lambers, S. F. Chapin III and T. L. Pons, “Plant Physiological Eclogy,” Springer, New York, 2008.
[26] M. E. Gavito, P. S. Curtis, T. N. Mikkelsen and I. Jakobsen, “Interactive Effects of Soil Temperature, Atmospheric Carbon Dioxide and Soil N on Root Development, Biomass and Nutrient Uptake of Winter Wheat during Vegetative Growth,” Journal of Experimental Botany, Vol. 52, No. 362, 2001, pp. 1913-1923.
[27] T. F. Ambebe and Q.-L. Dang, “Low Moisture Availability Inhibits the Enhancing Effect of Increased Soil Temperature on Net Photosynthesis of White Birch (Betula papyrifera) Seedlings Grown under Ambient and Elevated Carbon Dioxide Concentrations,” Tree Physiology, Vol. 29, No. 11, 2009, pp. 1341-1348.
[28] T. F. Ambebe and Q.-L. Dang, “Low Moisture Availability Reduces the Positive Effect of Increased Soil Temperature on Biomass Production of White Birch (Betula papyrifera) Seedlings in Ambient and Elevated Carbon Dioxide Concentration,” Nordic Journal of Botany, Vol. 28, 2010, pp. 104-111.
[29] T. F. Ambebe, Q.-L. Dang and J. Marfo, “Low Soil Temperature Reduces the Positive Effects of High Nutrient Supply on the Growth and Biomass of White Birch Seedlings in Ambient and Elevated Carbon Dioxide Concentrations,” Botany, Vol. 87, No. 10, 2009, pp. 905-912.
[30] R. O. Teskey, T. M. Hinckley and C. C. Grier, “Effect of Interruption of Flow Path on Stomatal Conductance of Abies amabilis,” Journal of Experimental Botany, Vol. 34, No. 10, 1983, pp. 1251-1259.
[31] P. G. Blackman and W. J. Davies, “Root to Shoot Communication in Maize Plants of the Effects of Soil Drying,” Journal of Experimental Botany, Vol. 36, No. 1, 1985, pp. 39-48.
[32] J. Pastor, R. H. Gardner, V. H. Dale and W. M. Post, “Successional Changes in Nitrogen Availability as a Potential Factor Contributing to Spruce Declines in Boreal North America,” Canadian Journal of Forest Research, Vol. 17, No. 11, 1987, pp. 1394-1400.
[33] E. H. DeLucia, S. A. Heckathorn and T. A. Day, “Effects of Soil Temperature on Growth, Biomass Allocation and Resource Acquisition of Andropogon gerardii Vitman,” New Phytologist, Vol. 120, No. 4, 1992, pp. 543-549.
[34] D. Paré, Y. Bergeron and C. Camiré, “Changes in the Forest Floor of Canadian Southern Boreal Forest after Disturbance,” Journal of Vegetation Science, Vol. 4, No. 6, 1993, pp. 811-818.
[35] R. S. Folk, S. C. Grossnickle and J. H. Russell, “Gas Exchange, Water Relations and Morphology of Yellow-Cedar Seedlings and Stecklings before Planting and during Field Establishment,” New Forest, Vol. 9, No. 1, 1995, pp. 1-20.
[36] T. Domisch, L. Finér and T. Lehto, “Effects of Soil Temperature on Biomass and Carbohydrate Allocation in Scots Pine (Pinus sylvestris) Seedlings at the Beginning of the Growing Season,” Tree Physiology, Vol. 21, No. 7, 2001, pp. 465-472.
[37] P.J. Aphalo, M. Lahti, T. Lehto, T. Repo, A. Rummukainen, H. Mannerkoski and L. Finér, “Responses of Silver Birch Saplings to Low Soil Temperature,” Silva Fennica, Vol. 40, No. 3, 2006, pp. 429-442.
[38] G. B. Bonan and H. H. Shugart, “Environmental Factors and Ecological Processes in Boreal Forests,” Annual Review of Ecology and Systematics, Vol. 20, 1989, pp. 1-28.
[39] J. C. Zasada, A. G. Gordon, C. W. Slaughter and L. C. Duchesne, “Ecological Considerations for the Sustainable Management of the North American Boreal Forests,” IIASA Interim Report IR-97-024/July 67, 1997.
[40] R. Z. Man, G. J. Kayahara, Q.-L. Dang and J. A. Rice, “A Case of Severe Frost Damage Prior to Budbreak in Young Conifers in Northeastern Ontario: Consequence of Climate Change?” The Forestry Chronicle, Vol. 85, No. 3, 2009, pp. 453-462.
[41] T. Landis, R. Tinus, S. McDonald and J. Barnett, “The Container Nursery Manuals. Volume 2: Containers and Growing Media,” Agricultural Handbook 674, USDA Forest Service, Washington DC, 1993.
[42] S. Cheng, Q.-L. Dang and T.-B. Cai, “A Soil Temperature Control System for Ecological Research in Greenhouses,” Journal of Forest Research, Vol. 5, No. 3, 2000, pp. 205-208.
[43] R. M. Burns and B. H. Honkala, “Silvics of North America Volume 2, Hardwoods,” Agriculture Handbook 654, USDA Forest Service, Washington DC, 1990, 877p.
[44] D. A. Horneck and R. O. Miller, “Automated Combustion Method with LECO-CNS. Determination of Total Nitrogen in Plant Tissue,” In: Y. P. Kalra, Ed., Handbook of Reference Methods for Plant Analysis, CRC Press LLC, Boca Raton, 1998, pp. 75-83.
[45] R. C. Munter and R. A. Grande, “Plant Analysis and soil extracts by ICP-atomic emission spectrometry,” In: R. M. Barnes, Ed., Developments in Atomic Plasma Spectrochemical Analysis, Heyden and Son, Ltd., London, 1981, pp. 653-672.
[46] R. A. Miller, “Nitric-Perchloric Acid Wet Digestion in an Open Vessel,” In: Y. P. Kalra, Ed., Handbook of Reference Methods for Plant Analysis, CRC Press LLC, Boca Raton, 1998, pp. 57-61.
[47] C. R. Hicks and K. V. Turner, “Fundamental Concepts in the Design of Experiments,” 5th Edition, Oxford University Press, New York, 1999.
[48] M. Martin, K. Gavazov, C. Körner, S. Hättenschwiler and C. Rixen, “Reduced Early Growing Season Freezing Resistance in Alpine Treeline Plants under Elevated Atmospheric CO2,” Global Change Biology, Vol. 16, No. 3, 2010, pp. 1057-1070.
[49] D. A. Clark and D. B. Clark, “Life History Diversity of Canopy and Emergent Trees in a Neotropical Rain Forest,” Ecological Monographs, Vol. 62, No. 3, 1992, pp. 315-344.
[50] C. D. Canham, “Different Response to Gaps among Shade-Tolerance Tree Species,” Ecology, Vol. 70, No. 3, 1989, pp. 549-550.
[51] T. F. Ambebe, Q.-L. Dang and J. Li, “Low Soil Temperature Inhibits the Effect of High Nutrient Supply on Photosynthetic Response to Elevated Carbon Dioxide Concentration in White Birch Seedlings,” Tree Physiology, Vol. 30, No. 2, 2010, pp. 234-243.
[52] K. Y. Crous, P. B. Reich, M. D. Hunter and D. S. Ellsworth, “Maintenance of Leaf N Controls the Photosynthetic CO2 Response of Grassland Species Exposed to 9 Years of Free-Air CO2 Enrichment,” Global Change Biology, Vol. 16, No. 7, 2010, pp. 2076-2088.
[53] H.-M. Ro, P.-G. Kim, I.-B. Lee, M.-S. Yiem and S.-Y. Woo, “Photosynthetic Characteristics and Growth Responses of Dwarf Apple (Malus domestica Borkh. cv. Fuji) Saplings after 3 Years of Exposure to Elevated Atmospheric Carbon Dioxide Concentration and Temperature,” Trees, Vol. 15, No. 4, 2001, pp. 195-203.
[54] G. Orlander, P. Gemmel and J. Hunt, “Site Preparation: A Swedish Overview,” Government of Canada, Province of British Columbia, 1990, p. 62.
[55] D. M. Smith, B. C. Larson, M. J. Kelty and P. M. S. Ashton, “The Practice of Silviculture: Applied Forest Ecology,” 9th Edition, John Wiley and Sons, New York, 1997.
[56] A. Sellin and P. Kupper, “Effects of Light Availability versus Hydraulic Constraints on Stomatal Responses within a Crown of Silver Birch,” Oecologia, Vol. 142, No. 3, 2005, pp. 388-397.
[57] T. F. Ambebe, G. Danyagri and Q.-L. Dang, “Low Soil Temperature Inhibits the Stimulatory Effect of Elevated [CO2] on Height and Biomass Accumulation of White Birch Seedlings Grown under Three Non-Limiting Phosphorus Conditions,” Nordic Journal of Botany, Vol. 31, No. 2, 2013, pp. 239-246.

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