Lower photorespiration in elevated CO <subscript>2</subscript> reduces leaf N concentrations in mature Eucalyptus trees in the field. - OpacWWW

Szczegóły
Abstrakt

Tytuł:: Lower photorespiration in elevated CO 2 reduces leaf N concentrations in mature Eucalyptus trees in the field.
Autorzy:: Wujeska-Klause A; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
Crous KY; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
Ghannoum O; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.; Translational Photosynthesis Centre of Excellence, Western Sydney University, Penrith, New South Wales, Australia.
Ellsworth DS; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
Źródło:: Global change biology [Glob Chang Biol] 2019 Apr; Vol. 25 (4), pp. 1282-1295. Date of Electronic Publication: 2019 Feb 20.
Typ publikacji:: Journal Article
Język:: English
Imprint Name(s):: Publication: : Oxford : Blackwell Pub.
Original Publication: Oxford, UK : Blackwell Science, 1995-
References:: Ainsworth, E. A., & Long, S. P. (2005). What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist, 165, 351-371. https://doi.org/10.1111/j.1469-8137.2004.01224.x.
Ainsworth, E. A., & Rogers, A. (2007). The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant, Cell and Environment, 30, 258-270. https://doi.org/10.1111/j.1365-3040.2007.01641.x.
Andrews, M., Raven, J. A., & Lea, P. J. (2013). Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Annals of Applied Biology, 163, 174-199. https://doi.org/10.1111/aab.12045.
BassiriRad, H., Griffin, K. L., Reynolds, J. F., & Strain, B. R. (1997). Changes in root NH4+ and NO3− absorption rates of loblolly and ponderosa pine in response to CO2 enrichment. Plant and Soil, 190, 1-9. https://doi.org/10.1023/A:1004206624311.
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48.
Bauer, G. A., & Berntson, G. M. (2001). Ammonium and nitrate acquisition by plants in response to elevated CO2 concentration: The roles of root physiology and architecture. Tree Physiology, 21, 137-144. https://doi.org/10.1093/treephys/21.2-3.137.
Bloom, A. J. (2015a). Photorespiration and nitrate assimilation: A major intersection between plant carbon and nitrogen. Photosynthesis Research, 123, 117-128. https://doi.org/10.1007/s11120-014-0056-y.
Bloom, A. J. (2015b). The increasing importance of distinguishing among plant nitrogen sources. Current Opinion in Plant Biology, 25, 10-16. https://doi.org/10.1016/j.pbi.2015.03.002.
Bloom, A. J., Asensio, J. S. R., Randall, L., Rachmilevitch, S., Cousins, A. B., & Carlisle, E. A. (2012). CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology, 93, 355-367. https://doi.org/10.1890/11-0485.1.
Bloom, A. J., Burger, M., Asensio, J. S. R., & Cousins, A. B. (2010). Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science, 328, 899-902. https://doi.org/10.1126/science.1186440.
Bloom, A. J., Burger, M., Kimball, B. A., & Pinter, J. P. J. (2014). Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nature Climate Change, 4, 477-480. https://doi.org/10.1038/nclimate2183.
Cataldo, D. A., Maroon, M., Schrader, L. E., & Youngs, V. L. (2008). Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis, 6, 71-80. https://doi.org/10.1080/00103627509366547.
Crous, K. Y., & Ellsworth, D. S. (2004). Canopy position affects photosynthetic adjustments to long-term elevated CO2 concentration (FACE) in aging needles in a mature Pinus taeda forest. Tree Physiology, 24, 961-970. https://doi.org/10.1093/treephys/24.9.961.
Crous, K. Y., Ósvaldsson, A., & Ellsworth, D. S. (2015). Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant and Soil, 391, 293-305. https://doi.org/10.1007/s11104-015-2426-4.
Crous, K. Y., Quentin, A. G., Lin, Y. S., Medlyn, B. E., Williams, D. G., Barton, C. V., & Ellsworth, D. S. (2013). Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Global Change Biology, 19, 3790-3807. https://doi.org/10.1111/gcb.12314.
Dier, M., Meinen, R., Erbs, M., Kollhorst, L., Baillie, C. K., Kaufholdt, D., … Manderscheid, R. (2018). Effects of free air carbon dioxide enrichment (FACE) on nitrogen assimilation and growth of winter wheat under nitrate and ammonium fertilization. Global Change Biology, 24, 40-54. https://doi.org/10.1111/gcb.13819.
Dovis, V. L., Hippler, F. W. R., Silva, K. I., Ribeiro, R. V., Machado, E. C., & Mattos, D. (2014). Optimization of the nitrate reductase activity assay for citrus trees. Brazilian Journal of Botany, 37, 383-390. https://doi.org/10.1007/s40415-014-0083-0.
Drake, B. G., Gonzàlez-Meler, M. A., & Long, S. P. (1997). More efficient plants: A consequence of rising atmospheric CO2? Annual Review of Plant Physiology & Plant Molecular Biology, 48, 609-639.
Duursma, R. A., Gimeno, T. E., Boer, M. M., Crous, K. Y., Tjoelker, M. G., & Ellsworth, D. S. (2016). Canopy leaf area of a mature evergreen Eucalyptus woodland does not respond to elevated atmospheric [CO2] but tracks water availability. Global Change Biology, 22, 1666-1676. https://doi.org/10.1111/gcb.13151.
Ebell, L. F. (1969). Variation in total soluble sugars of conifer tissues with method of analysis. Phytochemistry, 8, 227-233. https://doi.org/10.1016/S0031-9422(00)85818-5.
Ellsworth, D. S., Crous, K. Y., Lambers, H., & Cooke, J. (2015). Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species. Plant, Cell and Environment, 38, 1142-1156. https://doi.org/10.1111/pce.12468.
Ellsworth, D. S., Reich, P. B., Naumburg, E. S., Koch, G. W., Kubiske, M. E., & Smith, S. D. (2004). Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology, 10, 2121-2138. https://doi.org/10.1111/j.1365-2486.2004.00867.x.
Ellsworth, D., Anderson, I., Crous, K., Cooke, J., Drake, J., Gherlenda, A., … Reich, P. (2017). Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nature Climate Change, 7, 279-282. https://doi.org/10.1038/nclimate3235.
Evans, J. R. (1989). Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 78, 9-19. https://doi.org/10.1007/BF00377192.
Evans, J. R., & Seemann, J. R. (1989). The allocation of protein nitrogen in the photosynthetic apparatus: Costs, consequences, and control. New York, NY: A.R. Liss.
Farquhar, G. D., Caemmerer, S. V., & Berry, J. A. (1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149, 78-90. https://doi.org/10.1007/BF00386231.
Feng, Z., Rütting, T., Pleijel, H., Wallin, G., Reich, P. B., Kammann, C. I., … Uddling, J. (2015). Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Global Change Biology, 21, 3152-3168. https://doi.org/10.1111/gcb.12938.
Finzi, A. C., DeLucia, E. H., Hamilton, J. G., Richter, D. D., & Schlesinger, W. H. (2002). The nitrogen budget of a pine forest under free air CO2 enrichment. Oecologia, 132, 567-578. https://doi.org/10.1007/s00442-002-0996-3.
Finzi, A. C., Jackson, R. B., Moore, D. J. P., Kim, H.-S., Delucia, E. H., Lichter, J., … Schlesinger, W. H. (2006). Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology, 87, 15-25. https://doi.org/10.1890/04-1748.
Fox, J., & S. Weisberg (Eds.) (2011). An R companion to applied regression. Thousand Oaks, CA: Sage.
Gherlenda, A. N., Crous, K. Y., Moore, B. D., Haigh, A. M., Johnson, S. N., & Riegler, M. (2016). Precipitation, not CO2 enrichment, drives insect herbivore frass deposition and subsequent nutrient dynamics in a mature Eucalyptus woodland. Plant and Soil, 399, 29-39. https://doi.org/10.1007/s11104-015-2683-2.
Gimeno, T. E., Crous, K. Y., Cooke, J., O'Grady, A. P., Ósvaldsson, A., Medlyn, B. E., & Ellsworth, D. S. (2016). Conserved stomatal behaviour under elevated CO2 and varying water availability in a mature woodland. Functional Ecology, 30, 700-709. https://doi.org/10.1111/1365-2435.12532.
Gimeno, T. E., McVicar, T. R., O'Grady, A. P., Tissue, D. T., & Ellsworth, D. S. (2018). Elevated CO2 did not affect the hydrological balance of a mature native Eucalyptus woodland. Global Change Biology, 24, 3010-3024. https://doi.org/10.1111/gcb.14139.
Hasegawa, S., Macdonald, C. A., & Power, S. A. (2016). Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited Eucalyptus woodland. Global Change Biology, 22, 1628-1643. https://doi.org/10.1111/gcb.13147.
Hikosaka, K. (2005). Leaf canopy as a dynamic system: Ecophysiology and optimality in leaf turnover. Annals of Botany, 95, 521-533. https://doi.org/10.1093/aob/mci050.
Hikosaka, K., & Terashima, I. (1996). Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Functional Ecology, 10, 335-343. https://doi.org/10.2307/2390281.
Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346-363. https://doi.org/10.1002/bimj.200810425.
Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y., & Field, C. B. (2003). Nitrogen and climate change. Science, 302, 1512-1513. https://doi.org/10.1126/science.1091390.
Koyama, L., Tokuchi, N., Fukushima, K., Terai, M., & Yamamoto, Y. (2008). Seasonal changes in nitrate use by three woody species: The importance of the leaf-expansion period. Trees, 22, 851-859. https://doi.org/10.1007/s00468-008-0246-3.
Lewin, K. F., Nagy, J., Robert Nettles, W., Cooley, D. M., & Rogers, A. (2009). Comparison of gas use efficiency and treatment uniformity in a forest ecosystem exposed to elevated [CO2] using pure and prediluted free-air CO2 enrichment technology. Global Change Biology, 15, 388-395. https://doi.org/10.1111/j.1365-2486.2008.01748.x.
Lillo, C. (2008). Signalling cascades integrating light-enhanced nitrate metabolism. Biochemical Journal, 415, 11-19. https://doi.org/10.1042/BJ20081115.
Lillo, C., Meyer, C., Lea, U. S., Provan, F., & Oltedal, S. (2004). Mechanism and importance of post-translational regulation of nitrate reductase. Journal of Experimental Botany, 55, 1275-1282. https://doi.org/10.1093/jxb/erh132.
Luo, Y., Field, C. B., & Mooney, H. A. (1994). Predicting responses of photosynthesis and root fraction to elevated [CO2]a: Interactions among carbon, nitrogen, and growth. Plant, Cell and Environment, 17, 1195-1204. https://doi.org/10.1111/j.1365-3040.1994.tb02017.x.
Luo, Y., Hui, D., & Zhang, D. (2006). Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: A meta-analysis. Ecology, 87, 53-63. https://doi.org/10.1890/04-1724.
Luo, Y., Su, B., Currie, W. S., Dukes, J. S., Finzi, A., Hartwig, U., … Field, C. B. (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience, 54, 731-739.
Nicholas, J. C., Harper, J. E., & Hageman, R. H. (1976). Nitrate reductase activity in soybeans (Glycine max [L.] Merr.). Plant Physiology, 58, 731-735. https://doi.org/10.1104/pp.58.6.731.
Nicodemus, M. A., Salifu, K. F., & Jacobs, D. F. (2008). Nitrate reductase activity and nitrogen compounds in xylem exudate of Juglans nigra seedlings: Relation to nitrogen source and supply. Trees, 22, 685-695. https://doi.org/10.1007/s00468-008-0226-7.
Niinemets, Ü. (1997). Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees, 11, 144-154. https://doi.org/10.1007/PL00009663.
Niinemets, Ü. (2016). Leaf age dependent changes in within-canopy variation in leaf functional traits: A meta-analysis. Journal of Plant Research, 129, 313-338. https://doi.org/10.1007/s10265-016-0815-2.
Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E., & McMurtrie, R. E. (2010). CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences of the United States of America, 107, 19368-19373. https://doi.org/10.1073/pnas.1006463107.
Norby, R. J., Wullschleger, S. D., Gunderson, C. A., Johnson, D. W., & Ceulemans, R. (1999). Tree responses to rising CO2 in field experiments: Implications for the future forest. Plant, Cell and Environment, 22, 683-714. https://doi.org/10.1046/j.1365-3040.1999.00391.x.
Pathare, V. S., Crous, K. Y., Cooke, J., Creek, D., Ghannoum, O., & Ellsworth, D. S. (2017). Water availability affects seasonal CO2-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland. Global Change Biology, 23, 5164-5178. https://doi.org/10.1111/gcb.13778.
Poorter, H., Berkel, Y. V., Baxter, R., Hertog, J. D., Dijkstra, P., Gifford, R. M., … Wong, S. C. (1997). The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant, Cell and Environment, 20, 472-482. https://doi.org/10.1046/j.1365-3040.1997.d01-84.x.
Quentin, A. G., Pinkard, E. A., Ryan, M. G., Tissue, D. T., Baggett, L. S., Adams, H. D., … Woodruff, D. R. (2015). Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiology, 35, 1146-1165. https://doi.org/10.1093/treephys/tpv073.
Rachmilevitch, S., Cousins, A. B., & Bloom, A. J. (2004). Nitrate assimilation in plant shoots depends on photorespiration. Proceedings of the National Academy of Sciences of the United States of America, 101, 11506-11510. https://doi.org/10.1073/pnas.0404388101.
Reich, P. B., Walters, M. B., & Ellsworth, D. S. (1991). Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in maple and oak trees. Plant, Cell and Environment, 14, 251-259. https://doi.org/10.1111/j.1365-3040.1991.tb01499.x.
Reich, P. B., Hobbie, S. E., Lee, T., Ellsworth, D. S., West, J. B., Tilman, D., … Trost, J. (2006). Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature, 440, 922-925. https://doi.org/10.1038/nature04486.
Sharkey, T. D. (1988). Estimating the rate of photorespiration in leaves. Physiologia Plantarum, 73, 147-152. https://doi.org/10.1111/j.1399-3054.1988.tb09205.x.
Stitt, M., & Krapp, A. (1999). The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background. Plant, Cell and Environment, 22, 583-621. https://doi.org/10.1046/j.1365-3040.1999.00386.x.
Taub, D. R., & Wang, X. (2008). Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology, 50, 1365-1374. https://doi.org/10.1111/j.1744-7909.2008.00754.x.
von Caemmerer, S. (2000). Biochemical models of leaf photosynthesis. Collingwood, Vic., Australia: CSIRO Publishing.
Walker, B. J., Strand, D. D., Kramer, D. M., & Cousins, A. B. (2014). The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Physiology, 165, 453-462.
Walker, B. J., VanLoocke, A., Bernacchi, C. J., & Ort, D. R. (2016). The costs of photorespiration to food production now and in the future. Annual Review of Plant Biology, 67, 107-129. https://doi.org/10.1146/annurev-arplant-043015-111709.
Yin, X. (2002). Responses of leaf nitrogen concentration and specific leaf area to atmospheric CO2 enrichment: A retrospective synthesis across 62 species. Global Change Biology, 8, 631-642. https://doi.org/10.1046/j.1365-2486.2002.00497.x.
Zaehle, S., Jones, C. D., Houlton, B., Lamarque, J.-F., & Robertson, E. (2015). Nitrogen availability reduces CMIP5 projections of twenty-first-century land carbon uptake. Journal of Climate, 28, 2494-2511. https://doi.org/10.1175/jcli-d-13-00776.1.
Grant Information:: DE160101484 Australian Research Council; DP160102452 Australian Research Council
Contributed Indexing:: Keywords: EucFACE; carbohydrates; leaf age; nitrate; nitrate reductase; nitrogen assimilation; photorespiration; photosynthesis
Entry Date(s):: Date Created: 20190222 Latest Revision: 20230201
Update Code:: 20240104
DOI:: 10.1111/gcb.14555
PMID:: 30788883
: Czasopismo naukowe

Full Text Finder

Rising atmospheric CO 2 concentrations is expected to stimulate photosynthesis and carbohydrate production, while inhibiting photorespiration. By contrast, nitrogen (N) concentrations in leaves generally tend to decline under elevated CO 2 (eCO 2 ), which may reduce the magnitude of photosynthetic enhancement. We tested two hypotheses as to why leaf N is reduced under eCO 2 : (a) A "dilution effect" caused by increased concentration of leaf carbohydrates; and (b) inhibited nitrate assimilation caused by reduced supply of reductant from photorespiration under eCO 2 . This second hypothesis is fully tested in the field for the first time here, using tall trees of a mature Eucalyptus forest exposed to Free-Air CO 2 Enrichment (EucFACE) for five years. Fully expanded young and mature leaves were both measured for net photosynthesis, photorespiration, total leaf N, nitrate ( N O 3 - ) concentrations, carbohydrates and N O 3 - reductase activity to test these hypotheses. Foliar N concentrations declined by 8% under eCO 2 in new leaves, while the N O 3 - fraction and total carbohydrate concentrations remained unchanged by CO 2 treatment for either new or mature leaves. Photorespiration decreased 31% under eCO 2 supplying less reductant, and in situ N O 3 - reductase activity was concurrently reduced (-34%) in eCO 2 , especially in new leaves during summer periods. Hence, N O 3 - assimilation was inhibited in leaves of E. tereticornis and the evidence did not support a significant dilution effect as a contributor to the observed reductions in leaf N concentration. This finding suggests that the reduction of N O 3 - reductase activity due to lower photorespiration in eCO 2 can contribute to understanding how eCO 2 -induced photosynthetic enhancement may be lower than previously expected. We suggest that large-scale vegetation models simulating effects of eCO 2 on N biogeochemistry include both mechanisms, especially where N O 3 - is major N source to the dominant vegetation and where leaf flushing and emergence occur in temperatures that promote high photorespiration rates.
(© 2019 John Wiley & Sons Ltd.)

Informacja

Lower photorespiration in elevated CO 2 reduces leaf N concentrations in mature Eucalyptus trees in the field.