Nitrogen fertilisation influences low CO2 effects on plant performance
André G. Duarte
A E , Fred J. Longstaffe A B and Danielle A. Way A C D
+ Author Affiliations
- Author Affiliations
A Department of Biology, The University of Western Ontario, 1151 Richmond St., N6A 3K7, London, Canada.
B Department of Earth Sciences, The University of Western Ontario, 1151 Richmond St., N6A 3K7, London, Canada.
C Nicholas School of the Environment, Duke University, 9 Circuit Dr., 27710, Durham, USA.
D Present address: Division of Plant Sciences, Research School of Biology, The Australian National University, 134 Linnaeus Way, ACT 2601, Canberra, Australia.
E Corresponding author. Email: aduarte4@uwo.ca.
Functional Plant Biology 47(2) 134-144 https://doi.org/10.1071/FP19151
Submitted: 26 May 2019 Accepted: 27 September 2019 Published: 6 January 2020
Abstract
Low atmospheric CO2 conditions prevailed for most of the recent evolutionary history of plants. Such concentrations reduce plant growth compared with modern levels, but low-CO2 effects on plant performance may also be affected by nitrogen availability, since low leaf nitrogen decreases photosynthesis, and CO2 concentrations influence nitrogen assimilation. To investigate the influence of N availability on plant performance at low CO2, we grew Elymus canadensis at ambient (~400 μmol mol–1) and subambient (~180 μmol mol–1) CO2 levels, under four N-treatments: nitrate only; ammonium only; a full and a half mix of nitrate and ammonium. Growth at low CO2 decreased biomass in the full and nitrate treatments, but not in ammonium and half plants. Low CO2 effects on photosynthetic and maximum electron transport rates were influenced by fertilisation, with photosynthesis being most strongly impacted by low CO2 in full plants. Low CO2 reduced stomatal index in half plants, suggesting that the use of this indicator in paleo-inferences can be influenced by N availability. Under low CO2 concentrations, nitrate plants discriminated more against 15N whereas half plants discriminated less against 15N compared with the full treatment, suggesting that N availability should be considered when using N isotopes as paleo-indicators.
Additional keywords: Paleoecology, subambient CO2, δ15N, stomatal index, nitrogen assimilation.
References
Alt DS, Doyle JW, Malladi A (2017) Nitrogen-source preference in blueberry (Vaccinium sp.): enhanced shoot nitrogen assimilation in response to direct supply of nitrate. Journal of Plant Physiology 216, 79–87.| Nitrogen-source preference in blueberry (Vaccinium sp.): enhanced shoot nitrogen assimilation in response to direct supply of nitrate.Crossref | GoogleScholarGoogle Scholar | 28578080PubMed |
Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochemical Cycles 17,
| Global patterns of the isotopic composition of soil and plant nitrogen.Crossref | GoogleScholarGoogle Scholar |
BassiriRad H, Griffin KL, Reynolds JF, Strain BR (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.
| Changes in root NH4+ and NO3– absorption rates of loblolly and ponderosa pine in response to CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |
Becklin KM, Walker SM, Way DA, Ward JK (2017) CO2 studies remain key to understanding a future world. New Phytologist 214, 34–40.
| CO2 studies remain key to understanding a future world.Crossref | GoogleScholarGoogle Scholar | 27891618PubMed |
Beerling DJ (2005) Evolutionary responses of land plants to atmospheric CO2. In ‘A history of atmospheric CO2 and its effects on plants, animals, and ecosystems’. (Ed. I Baldwin) pp. 114–132. (Springer: New York)
Beerling DJ, Royer DL (2002) Reading a CO2 signal from fossil stomata. New Phytologist 153, 387–397.
| Reading a CO2 signal from fossil stomata.Crossref | GoogleScholarGoogle Scholar |
Bloom AJ, Burger M, Rubio Asensio JS, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899–903.
| Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20466933PubMed |
Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA (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.
| CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants.Crossref | GoogleScholarGoogle Scholar | 22624317PubMed |
Bloom AJ, Burger M, Kimball BA, Pinter PJ (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nature Climate Change 4, 477–480.
| Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat.Crossref | GoogleScholarGoogle Scholar |
Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology Evolution and Systematics 42, 411–440.
| On the use of stable isotopes in trophic ecology.Crossref | GoogleScholarGoogle Scholar |
Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nature Plants 4, 46–54.
| Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway.Crossref | GoogleScholarGoogle Scholar | 29229957PubMed |
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330, 192–196.
| The evolution and future of Earth’s nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 20929768PubMed |
Casey MM, Post DM (2011) The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106, 131–148.
| The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals.Crossref | GoogleScholarGoogle Scholar |
Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337, 1084–1087.
| Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2.Crossref | GoogleScholarGoogle Scholar | 22936776PubMed |
Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell & Environment 21, 427–435.
| Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar |
Cowling SA, Sykes MT (1999) Physiological significance of low atmospheric CO2 for plant–climate interactions. Quaternary Research 52, 237–242.
| Physiological significance of low atmospheric CO2 for plant–climate interactions.Crossref | GoogleScholarGoogle Scholar |
Cramer MD, Lewis OAM (1993) The influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants. Annals of Botany 72, 359–365.
| The influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants.Crossref | GoogleScholarGoogle Scholar |
Cunniff J, Jones G, Charles M, Osborne CP (2017) Yield responses of wild C3 and C4 crop progenitors to subambient CO2: a test for the role of CO2 limitation in the origin of agriculture. Global Change Biology 23, 380–393.
| Yield responses of wild C3 and C4 crop progenitors to subambient CO2: a test for the role of CO2 limitation in the origin of agriculture.Crossref | GoogleScholarGoogle Scholar | 27550721PubMed |
Dier M, Meinen R, Erbs M, Kollhorst L, Baillie C-K, Kaufholdt D, Kücke M, Weigel H-J, Zörb C, Hänsch R, Manderscheid R (2017) 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, e40–e54.
| Effects of free air carbon dioxide enrichment (FACE) on nitrogen assimilation and growth of winter wheat under nitrate and ammonium fertilization.Crossref | GoogleScholarGoogle Scholar | 28715112PubMed |
Duursma RA (2015) Plantecophys – an R package for analysing and modelling leaf gas exchange data. PLoS One 10, e0143346
| Plantecophys – an R package for analysing and modelling leaf gas exchange data.Crossref | GoogleScholarGoogle Scholar | 26581080PubMed |
Ehleringer JR, Cerling TE, Dearing MD (2005) ‘A history of atmospheric CO2 and its effects on plants, animals, and ecosystems.’ (Springer: Salt Lake City, UT, USA)
Elliott-Kingston C, Haworth M, Yearsley JM, Batke SP, Lawson T, McElwain JC (2016) Does size matter? Atmospheric CO2 may be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO2. Frontiers of Plant Science 7, 1253
| Does size matter? Atmospheric CO2 may be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO2.Crossref | GoogleScholarGoogle Scholar |
Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (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.
| Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert.Crossref | GoogleScholarGoogle Scholar |
Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.
| Physiological mechanisms influencing plant nitrogen isotope composition.Crossref | GoogleScholarGoogle Scholar | 11239611PubMed |
Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR (1996) Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant, Cell & Environment 19, 1317–1323.
| Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition.Crossref | GoogleScholarGoogle Scholar |
Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275.
| Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, von Caemmerer S (1982) Modelling of photosynthetic response to environmental conditions. In ‘Physiological plant ecology II’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 549–587. (Springer: Berlin)
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 24306196PubMed |
Fatichi S, Leuzinger S, Körner C (2014) Moving beyond photosynthesis: From carbon source to sink-driven vegetation modeling. New Phytologist 201, 1086–1095.
| Moving beyond photosynthesis: From carbon source to sink-driven vegetation modeling.Crossref | GoogleScholarGoogle Scholar | 24261587PubMed |
Foyer CH, Noctor G (2006) ‘Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism.’ (Springer Science & Business Media: New York)
Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 537–546.
| Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations.Crossref | GoogleScholarGoogle Scholar | 22232765PubMed |
Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N, Norby RJ, Tissue DT, von Caemmerer S (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytologist 197, 1077–1094.
| Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century.Crossref | GoogleScholarGoogle Scholar | 23346950PubMed |
Garten CT, Hanson PJ, Todd DE, Lu BB, Brice DJ (2008) Natural 15N- and 13C-abundance as indicators of forest nitrogen status and soil carbon dynamics. In ‘Stable isotopes in ecology and environmental science’. 2nd edn. (Eds R Michener, K Lajtha) pp. 61–82. (Blackwell Publishing: Hobeken, NJ, USA)
Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytologist 188, 674–695.
| Plant responses to low [CO2] of the past.Crossref | GoogleScholarGoogle Scholar | 20840509PubMed |
Griffin KL, Tissue DT, Turnbull MH, Whitehead D (2000) The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D.Don. after 4 years. Plant, Cell & Environment 23, 1089–1098.
| The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D.Don. after 4 years.Crossref | GoogleScholarGoogle Scholar |
Guo S, Zhou Y, Li Y, Gao Y, Shen Q (2008) Effects of different nitrogen forms and osmotic stress on water use efficiency of rice (Oryza sativa). Annals of Applied Biology 153, 127–134.
| Effects of different nitrogen forms and osmotic stress on water use efficiency of rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Hachiya T, Sakakibara H (2016) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants. Journal of Experimental Botany 68, erw449
| Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants.Crossref | GoogleScholarGoogle Scholar |
Hoagland DR, Arnon DI (1950) ‘The water-culture method for growing plants without soil.’ (College of Agriculture, University of California: Berkeley, CA, USA).
Hogberg P (1997) 15N natural abundance in soil–plant systems. New Phytologist 137, 179–203.
| 15N natural abundance in soil–plant systems.Crossref | GoogleScholarGoogle Scholar |
Jasso-Chaverria C, Hochmuth GJ, Hochmuth RC, Sargent SA (2005) Fruit yield, size and color responses of two greenhouse cucumber types to nitrogen fertilization in perlite soilless culture. HortTechnology 15, 565–571.
| Fruit yield, size and color responses of two greenhouse cucumber types to nitrogen fertilization in perlite soilless culture.Crossref | GoogleScholarGoogle Scholar |
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Plant Biology 25, 115–122.
| Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces.Crossref | GoogleScholarGoogle Scholar |
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379.
| Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed.Crossref | GoogleScholarGoogle Scholar | 18409427PubMed |
Lewis JD, Ward JK, Tissue DT (2010) Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations. New Phytologist 187, 438–448.
| Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations.Crossref | GoogleScholarGoogle Scholar | 20524990PubMed |
Maherali H, Reid CD, Polley HW, Johnson HB, Jackson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant, Cell & Environment 25, 557–566.
| Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland.Crossref | GoogleScholarGoogle Scholar |
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.
| Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age.Crossref | GoogleScholarGoogle Scholar |
Monnin E, Indermühle A, Dällenbach A, Flückiger J, Stauffer B, Stocker TF, Raynaud D, Barnola JM (2001) Atmospheric CO2 concentrations over the last glacial termination. Science 291, 112–114.
| Atmospheric CO2 concentrations over the last glacial termination.Crossref | GoogleScholarGoogle Scholar | 11141559PubMed |
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (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.
| CO2 enhancement of forest productivity constrained by limited nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 20974944PubMed |
Pace GM, Volk RJ, Jackson WA (1990) Nitrate reduction in response to CO2-limited photosynthesis. Plant Physiology 92, 286–292.
| Nitrate reduction in response to CO2-limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 16667273PubMed |
Pavlik BM (1983) Nutrient and productivity relations of the dune grasses Ammophila arenaria and Elymus mollis. I. Blade photosynthesis and nitrogen use efficiency in the laboratory and field. Oecologia 57, 227–232.
| Nutrient and productivity relations of the dune grasses Ammophila arenaria and Elymus mollis. I. Blade photosynthesis and nitrogen use efficiency in the laboratory and field.Crossref | GoogleScholarGoogle Scholar | 28310179PubMed |
Perry L, Quigg JM (2011) Starch remains and stone boiling in the Texas Panhandle. Part II: Identifying Wildrye (Elymus spp.). Plains Anthropologist 56, 109–119.
| Starch remains and stone boiling in the Texas Panhandle. Part II: Identifying Wildrye (Elymus spp.).Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Raynaud D, Basile I, Chappellaz J, Ritz C, Delmotte M, Legrand M, Lorius C, Pe L (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436.
| Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica.Crossref | GoogleScholarGoogle Scholar |
Pinto H, Sharwood RE, Tissue DT, Ghannoum O (2014) Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2. Journal of Experimental Botany 65, 3669–3681.
| Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2.Crossref | GoogleScholarGoogle Scholar | 24723409PubMed |
Policy HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361, 61–64.
| Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations.Crossref | GoogleScholarGoogle Scholar |
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
| Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 6 December 2019]
Rachmilevitch S, Cousins AB, Bloom AJ (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.
| Nitrate assimilation in plant shoots depends on photorespiration.Crossref | GoogleScholarGoogle Scholar | 15272076PubMed |
Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922–925.
| Nitrogen limitation constrains sustainability of ecosystem response to CO2.Crossref | GoogleScholarGoogle Scholar | 16612381PubMed |
Ripley BS, Cunniff J, Osborne CP (2013) Photosynthetic acclimation and resource use by the C3 and C4 subspecies of Alloteropsis semialata in low CO2 atmospheres. Global Change Biology 19, 900–910.
| Photosynthetic acclimation and resource use by the C3 and C4 subspecies of Alloteropsis semialata in low CO2 atmospheres.Crossref | GoogleScholarGoogle Scholar | 23504846PubMed |
Robinson D (2001) δ15N as an integrator of the nitrogen. Trends in Ecology & Evolution 16, 153–162.
| δ15N as an integrator of the nitrogen.Crossref | GoogleScholarGoogle Scholar |
Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of Palaeobotany and Palynology 114, 1–28.
| Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 11295163PubMed |
Sage RF (1995) Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture? Global Change Biology 1, 93–106.
| Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture?Crossref | GoogleScholarGoogle Scholar |
Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends in Plant Science 6, 18–24.
| Effects of low atmospheric CO2 on plants: more than a thing of the past.Crossref | GoogleScholarGoogle Scholar | 11164373PubMed |
Sage RF, Cowling SA (1999) Implications of stress in low CO2 atmospheres of the past: are today’s plants too conservative for a high CO2 world? In ‘Carbon dioxide and environmental stress’. (Eds Y Luo, HA Mooney) pp. 289–304. (Academic Press: San Diego, CA, USA)
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Shimshi D (1970) The effect of nitrogen supply on transpiration and stomatal behaviour of beans (Phaseolus vulgaris L.). New Phytologist 69, 405–412.
| The effect of nitrogen supply on transpiration and stomatal behaviour of beans (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Stevenson FJ, Stevenson EJ, Cole MA (1999) ‘Cycles of soils: carbon, nitrogen, phosphorus, sulfur, micronutrients.’ (John Wiley & Sons Ltd: Hoboken, NJ, USA)
Tcherkez G, Farquhar GD (2006) Viewpoint: isotopic fractionation by plant nitrate reductase, twenty years later. Functional Plant Biology 33, 531
| Viewpoint: isotopic fractionation by plant nitrate reductase, twenty years later.Crossref | GoogleScholarGoogle Scholar |
Temme AA, Cornwell WK, Cornelissen JHC, Aerts R (2013) Meta-analysis reveals profound responses of plant traits to glacial CO2 levels. Ecology and Evolution 3, 4525–4535.
| Meta-analysis reveals profound responses of plant traits to glacial CO2 levels.Crossref | GoogleScholarGoogle Scholar | 24340192PubMed |
Temme AA, Liu JC, Cornwell WK, Cornelissen JHC, Aerts R (2015) Winners always win: growth of a wide range of plant species from low to future high CO2. Ecology and Evolution 5, 4949–4961.
| Winners always win: growth of a wide range of plant species from low to future high CO2.Crossref | GoogleScholarGoogle Scholar | 26640673PubMed |
Tissue D, Griffin K, Thomas R, Strain B (1995) Effects of low and elevated CO2 on C3 and C4 annuals – II. Photosynthesis and leaf biochemistry. Oecologia 101, 21–28.
| Effects of low and elevated CO2 on C3 and C4 annuals – II. Photosynthesis and leaf biochemistry.Crossref | GoogleScholarGoogle Scholar | 28306971PubMed |
Tissue DT, Griffin KL, Ball JT (1999) Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevate CO2. Tree Physiology 19, 221–228.
| Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevate CO2.Crossref | GoogleScholarGoogle Scholar | 12651564PubMed |
Tyson RV, Simonne EH, Davis M, Lamb EM, White JM, Treadwell DD (2007) Effect of nutrient solution, nitrate-nitrogen concentration, and pH on nitrification rate in perlite medium. Journal of Plant Nutrition 30, 901–913.
| Effect of nutrient solution, nitrate-nitrogen concentration, and pH on nitrification rate in perlite medium.Crossref | GoogleScholarGoogle Scholar |
Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant, Cell & Environment 20, 254–260.
| Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations.Crossref | GoogleScholarGoogle Scholar |
Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123, 330–341.
| Is atmospheric CO2 a selective agent on model C3 annuals?Crossref | GoogleScholarGoogle Scholar | 28308587PubMed |
Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biological Reviews of the Cambridge Philosophical Society 67, 321–358.
| A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil.Crossref | GoogleScholarGoogle Scholar |
Weil RR, Brady NC (2016) ‘The nature and properties of soils.’ (Pearson Australia: Melbourne, Vic.)
Yoneyama T, Omata T, Nakata S, Yazaki J (1991) Fractionation of nitrogen isotopes during the uptake and assimilation of ammonia by plants. Plant & Cell Physiology 32, 1211–1217.
Zazula GD, Schweger CE, Beaudoin AB, McCourt GH (2006) Macrofossil and pollen evidence for full-glacial steppe within an ecological mosaic along the Bluefish River, eastern Beringia. Quaternary International 142–143, 2–19.
| Macrofossil and pollen evidence for full-glacial steppe within an ecological mosaic along the Bluefish River, eastern Beringia.Crossref | GoogleScholarGoogle Scholar |
