Free air CO2 enrichment (FACE) improves water use efficiency and moderates drought effect on N2 fixation of Pisum sativum L.

Parvin, Shahnaj; Uddin, Shihab; Fitzgerald, Glenn J.; Tausz-Posch, Sabine; Armstrong, Roger; Tausz, Michael

doi:10.1007/s11104-019-03949-7

Free air CO₂ enrichment (FACE) improves water use efficiency and moderates drought effect on N₂ fixation of Pisum sativum L.

Regular Article
Published: 26 January 2019

Volume 436, pages 587–606, (2019)
Cite this article

Plant and Soil Aims and scope Submit manuscript

Shahnaj Parvin ORCID: orcid.org/0000-0001-7241-1712^1,2,
Shihab Uddin^2,3,
Glenn J. Fitzgerald^3,4,
Sabine Tausz-Posch^3,5,
Roger Armstrong^4,6 &
…
Michael Tausz^1,7

795 Accesses
19 Citations
Explore all metrics

Abstract

Background and aims

Legume N₂ fixation is highly sensitive to drought. Elevated [CO₂] (e[CO₂]) decreases stomatal conductance (g_s) and improves water use efficiency (WUE), which may result in soil water conservation and allow N₂ fixation to continue longer under drought. Using a Free-Air CO₂ Enrichment (FACE) approach, this study aimed to elucidate whether e[CO₂] improves N₂ fixation of Pisum sativum L. under drought.

Methods

In a FACE system, plants were grown in ambient [CO₂] (~400 ppm) or e[CO₂] (~550 ppm) and subjected to either terminal drought or well-watered treatments. Measurements were taken of photosynthesis, soil water dynamics, water soluble carbohydrates (WSC), amino acids (AA) and N₂ fixation.

Results

Lower g_s under e[CO₂] increased water use efficiency at leaf and plant level, and this translated to slower soil water depletion during drought. Elevated [CO₂] increased WSC and decreased total AA concentrations in nodules, and increased nodule activity under drought. N₂ fixation was stimulated (+51%) by e[CO₂] in proportion to biomass changes. Under e[CO₂] a greater proportion of plant total N was derived from fixed N₂ and a smaller proportion from soil N uptake compared to a[CO₂].

Conclusion

This study suggests that e[CO₂] increased WUE and this resulted in slower soil water depletion, allowing pea plants to maintain greater nodule activity under drought and resulting in appreciable increases in N₂ fixation. Our results suggest that growth under e[CO₂] can mitigate drought effects on N₂ fixation and reduce dependency on soil N resources especially in water-limited agro-ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Environmental variables controlling biological nitrogen fixation in soybean

Article 28 March 2024

Examining the soil bacterial community under the combined influence of water-absorbing polymer and plant subjected to drought stress

Article 16 April 2024

Effects of soil water content at freezing, thaw temperature, and snowmelt infiltration on N2O emissions and denitrifier gene and transcript abundance during a single freeze-thaw event

Article Open access 11 April 2024

Abbreviations

FACE:: Free-Air CO₂ Enrichment
[CO₂]:: CO₂ concentration
e[CO₂]:: Elevated [CO₂]
a[CO₂]:: Ambient [CO2]
WUE:: Water use efficiency
[N]:: N concentration
%Ndfa:: Percentage of N₂ derived from atmosphere
%Nds:: Percentage of N derived from soil
NO₃ ⁻ :: Nitrate
W:: Water regimes
A_sat :: Light saturated net CO₂ assimilation rate
g_s :: Stomatal conductance
WUEi:: Intrinsic water use efficiency
WUE_biomass :: Water-use efficiency based on biomass
RWC:: Relative water content
WSC:: Water soluble carbohydrate
AA:: Amino acids
WW:: Well-watered
DT:: Drought

References

Ainsworth EA, Rogers A, Nelson R, Long SP (2004) Testing the "source-sink" hypothesis of down-regulation of photosynthesis in elevated CO₂ in the field with single gene substitutions in Glycine max. Agric For Meteorol 122:85–94. https://doi.org/10.1016/j.agrformet.2003.09.002
Article Google Scholar
Angus JF, van Herwaarden AF (2001) Increasing water use and water use efficiency in dryland wheat. Agron J 93:290–298
Article Google Scholar
Aranjuelo I, Irigoyen JJ, Nogués S, Sánchez-Díaz M (2009) Elevated CO₂ and water-availability effect on gas exchange and nodule development in N₂-fixing alfalfa plants. Environ Exp Bot 65:18–26. https://doi.org/10.1016/j.envexpbot.2008.06.006
Article CAS Google Scholar
Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 171:1076–1090. https://doi.org/10.1016/j.jplph.2014.04.002
Article CAS PubMed Google Scholar
Bahrami H, De Kok LJ, Armstrong R, Fitzgerald GJ, Bourgault M, Henty S, Tausz M, Tausz-Posch S (2017) The proportion of nitrate in leaf nitrogen, but not changes in root growth, are associated with decreased grain protein in wheat under elevated [CO₂]. J Plant Physiol 216:44–51. https://doi.org/10.1016/j.jplph.2017.05.011.
Article CAS PubMed Google Scholar
Bernacchi CJ, Kimball BA, Quarles DR, Long SP, Ort DR (2007) Decreases in stomatal conductance of soybean under open-air elevation of CO₂ are closely coupled with decreases in ecosystem evapotranspiration. Plant Physiol 143:134–144. https://doi.org/10.1104/pp.106.089557
Article CAS PubMed PubMed Central Google Scholar
Bloom AJ, Burger M, Kimball BA, Pinter JPJ (2014) Nitrate assimilation is inhibited by elevated CO₂ in field-grown wheat. Nat Clim Chang 4:477–480. https://doi.org/10.1038/nclimate2183
Article CAS Google Scholar
Bourgault M, Brand J, Tausz M, Fitzgerald GJ (2016) Yield, growth and grain nitrogen response to elevated CO₂ of five field pea (Pisum sativum L.) cultivars in a low rainfall environment. Field Crop Res 196:1–9. https://doi.org/10.1016/j.fcr.2016.04.011.
Article Google Scholar
Burkart S, Manderscheid R, Wittich KP, Loepmeier FJ, Weigel HJ (2011) Elevated CO₂ effects on canopy and soil water flux parameters measured using a large chamber in crops grown with free-air CO₂ enrichment. Plant Biol 13:258–269. https://doi.org/10.1111/j.1438-8677.2010.00360.x
Article CAS PubMed Google Scholar
Butterly CR, Armstrong R, Chen D, Tang C (2015) Carbon and nitrogen partitioning of wheat and field pea grown with two nitrogen levels under elevated CO₂. Plant Soil 391:367–382. https://doi.org/10.1007/s11104-015-2441-5
Article CAS Google Scholar
Butterly CR, Armstrong R, Chen DL, Tang CX (2016a) Free-air CO₂ enrichment (FACE) reduces the inhibitory effect of soil nitrate on N₂ fixation of Pisum sativum. Ann Bot 117:177–185. https://doi.org/10.1093/aob/mcv140
Article CAS PubMed Google Scholar
Butterly CR, Phillips LA, Wiltshire JL, Franks AE, Armstrong RD, Chen DL, Mele PM, Tang CX (2016b) Long-term effects of elevated CO₂ on carbon and nitrogen functional capacity of microbial communities in three contrasting soils. Soil Biol Biochem 97:157–167. https://doi.org/10.1016/j.soilbio.2016.03.010
Article CAS Google Scholar
Cabrerizo PM, González EM, Aparicio-Tejo PM, Arrese-Igor C (2001) Continuous CO₂ enrichment leads to increased nodule biomass, carbon availability to nodules and activity of carbon-metabolising enzymes but does not enhance specific nitrogen fixation in pea. Physiol Plant 113:33–40. https://doi.org/10.1034/j.1399-3054.2001.1130105.x
Article CAS Google Scholar
Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO₂ leads to loss of soil carbon. Proc Natl Acad Sci U S A 104:4990–4995. https://doi.org/10.1073/pnas.0610045104
Article CAS PubMed PubMed Central Google Scholar
Conroy JP, Virgona JM, Smillie RM, Barlow EW (1988) Influence of drought acclimation and CO₂ enrichment on osmotic adjustment and chlorophyll a fluorescence of sunflower during drought. Plant Physiol 86:1108–1115
Article CAS PubMed PubMed Central Google Scholar
Darroch BA, Baker RJ (1990) Grain filling in three spring wheat genotypes: statistical analysis. Crop Sci 30:525–529. https://doi.org/10.2135/cropsci1990.0011183X003000030009x
Article Google Scholar
De Luis I, Irigoyen JJ, Sánchez-Díaz M (1999) Elevated CO₂ enhances plant growth in droughted N₂-fixing alfalfa without improving water status. Physiol Plant 107:84–89. https://doi.org/10.1034/j.1399-3054.1999.100112.x
Article Google Scholar
Drigo B, Kowalchuk GA, Knapp BA, Pijl AS, Boschker HTS, van Veen JA (2013) Impacts of 3 years of elevated atmospheric CO₂ on rhizosphere carbon flow and microbial community dynamics. Glob Chang Biol 19:621–636. https://doi.org/10.1111/gcb.12045
Article PubMed Google Scholar
Durand JL, Sheehy JE, Minchin FR (1987) Nitrogenase activity, photosynthesis and nodule water potential in soybean plants experiencing water-deprivation. J Exp Bot 38:311–321. https://doi.org/10.1093/jxb/38.2.311
Article CAS Google Scholar
Erice G, Irigoyen JJ, Pérez P, Martínez-Carrasco R, Sánchez-Díaz M (2006) Effect of elevated CO₂, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle. Physiol Plant 126:458–468. https://doi.org/10.1111/j.1399-3054.2006.00599.x
Article CAS Google Scholar
Erskine W, Sarker A, Kumar S (2011) Crops that feed the world 3. Investing in lentil improvement toward a food secure world. Food Sec 3:127–139. https://doi.org/10.1007/s12571-011-0124-5
Article Google Scholar
Feng ZZ, Rutting T, Pleijel H, Wallin G, Reich PB, Kammann CI, Newton PCD, Kobayashi K, Luo YJ, Uddling J (2015) Constraints to nitrogen acquisition of terrestrial plants under elevated CO₂. Glob Chang Biol 21:3152–3168. https://doi.org/10.1111/gcb.12938
Article PubMed Google Scholar
Fischinger SA, Hristozkova M, Mainassara ZA, Schulze J (2010) Elevated CO₂ concentration around alfalfa nodules increases N₂ fixation. J Exp Bot 61:121–130. https://doi.org/10.1093/jxb/erp287
Article CAS PubMed Google Scholar
Fitzgerald GJ, Tausz M, O'Leary G, Mollah MR, Tausz-Posch S, Seneweera S, Mock I, Low M, Partington DL, McNeil D, Norton RM (2016) Elevated atmospheric CO₂ can dramatically increase wheat yields in semi-arid environments and buffer against heat waves. Glob Chang Biol 22:2269–2284. https://doi.org/10.1111/gcb.13263
Article PubMed Google Scholar
Fitzpatrick E (1970) The expectancy of deficient winter rainfall and the potential for severe drought in the southwest of Western Australia. In ‘Miscellaneous Publication’ Vol. 70/1. pp. 37. (The University of Western Australia, Institute of Agriculture, Agronomy Dept: Perth)
Gil-Quintana E, Larrainzar E, Arrese-Igor C, González EM (2013) Is N-feedback involved in the inhibition of nitrogen fixation in drought-stressed Medicago truncatula? J Exp Bot 64:281–292. https://doi.org/10.1093/jxb/ers334
Article CAS PubMed Google Scholar
Gray SB, Brady SM (2016) Plant developmental responses to climate change. Dev Biol 419:64–77. https://doi.org/10.1016/j.ydbio.2016.07.023
Article CAS PubMed Google Scholar
Gray SB, Dermody O, Klein SP, Locke AM, McGrath JM, Paul RE, Rosenthal DM, Ruiz-Vera UM, Siebers MH, Strellner R, Ainsworth EA, Bernacchi CJ, Long SP, Ort DR, Leakey ADB (2016) Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean. Nat Plants 2:16132. https://doi.org/10.1038/nplants.2016.132
Article CAS PubMed Google Scholar
Guo HJ, Sun YC, Li YF, Liu XH, Ren Q, Zhu-Salzman K, Ge F (2013) Elevated CO₂ modifies N acquisition of Medicago truncatula by enhancing N₂ fixation and reducing nitrate uptake from soil. PLoS One 8. https://doi.org/10.1371/journal.pone.0081373
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18. https://doi.org/10.1007/s11104-008-9668-3
Article CAS Google Scholar
Houshmandfar A, Fitzgerald GJ, Macabuhay AA, Armstrong R, Tausz-Posch S, Low M, Tausz M (2016) Trade-offs between water-use related traits, yield components and mineral nutrition of wheat under free-air CO₂ enrichment (FACE). Eur J Agron 76:66–74. https://doi.org/10.1016/j.eja.2016.01.018
Article CAS Google Scholar
Hungria M, Vargas MAT (2000) Environmental factors affecting N₂ fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crop Res 65:151–164. https://doi.org/10.1016/S0378-4290(99)00084-2
Article Google Scholar
Hussain MZ, Vanloocke A, Siebers MH, Ruiz-Vera UM, Markelz RJC, Leakey ADB, Ort DR, Bernacchi CJ (2013) Future carbon dioxide concentration decreases canopy evapotranspiration and soil water depletion by field-grown maize. Glob Chang Biol 19:1572–1584. https://doi.org/10.1111/gcb.12155
Article PubMed Google Scholar
IPCC (2014) Climate Change 2014: Synthesis report. Contribution of working groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, RK Pachauri, LA Meyer (eds) Geneva: IPCC
Isbell RF (2002) The Australian soil classification. CSIRO Publishing Collingwood, Collingwood
Book Google Scholar
Jagadish SVK, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PVV, Craufurd PQ (2016) Implications of high temperature and elevated CO₂ on flowering time in plants. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00913
Jin J, Tang CX, Armstrong R, Sale P (2012) Phosphorus supply enhances the response of legumes to elevated CO₂ (FACE) in a phosphorus-deficient vertisol. Plant Soil 358:86–99. https://doi.org/10.1007/s11104-012-1270-z
Article CAS Google Scholar
Jin J, Lauricella D, Armstrong R, Sale P, Tang C (2015) Phosphorus application and elevated CO₂ enhance drought tolerance in field pea grown in a phosphorus-deficient vertisol. Ann Bot 116:975–985. https://doi.org/10.1093/aob/mcu209
Article CAS PubMed Google Scholar
Kimball BA (2016) Crop responses to elevated CO₂ and interactions with H₂O, N, and temperature. Curr Opin Plant Biol 31:36–43. https://doi.org/10.1016/j.pbi.2016.03.006
Article CAS PubMed Google Scholar
King CA, Purcell LC (2005) Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137:1389–1396
Knott CM (1987) A key for stages of development of the pea (Pisum sativum). Ann Appl Biol 111:233–245. https://doi.org/10.1111/j.1744-7348.1987.tb01450.x
Article Google Scholar
Lam SK, Hao X, Lin E, Han X, Norton R, Mosier AR, Seneweera S, Chen D (2012) Effect of elevated carbon dioxide on growth and nitrogen fixation of two soybean cultivars in northern China. Biol Fertil Soils 48:603–606. https://doi.org/10.1007/s00374-011-0648-z
Article CAS Google Scholar
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO₂ effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876. https://doi.org/10.1093/jxb/erp096
Article CAS PubMed Google Scholar
Lecoeur J (2010) Vegetative development: the morphogenesis of plantorgans. In: Munier-Jolain N, Biarnès V, Chaillet I, Lecoeur J, Jeuffroy MH (eds) Physiology of the pea crop. CRC Press, Enfield, pp 3–43
Chapter Google Scholar
Leport L, Turner NC, French RJ, Barr MD, Duda R, Davies SL, Tennant D, Siddique KHM (1999) Physiological responses of chickpea genotypes to terminal drought in a Mediterranean-type environment. Eur J Agron 11:279–291. https://doi.org/10.1016/S1161-0301(99)00039-8
Article Google Scholar
Li DX, Liu HL, Qiao YZ, Wang YN, Cai ZM, Dong BD, Shi CH, Liu YY, Li X, Liu MY (2013) Effects of elevated CO₂ on the growth, seed yield, and water use efficiency of soybean (Glycine max (L.) Merr.) under drought stress. Agric Water Manag 129:105–112. https://doi.org/10.1016/j.agwat.2013.07.014
Article Google Scholar
Li Y, Li H, Li Y, Zhang S (2017) Improving water-use efficiency by decreasing stomatal conductance and transpiration rate to maintain higher ear photosynthetic rate in drought-resistant wheat. Crop J 5:231–239. https://doi.org/10.1016/j.cj.2017.01.001
Article Google Scholar
Lopez FB, Johansen C, Chauhan YS (1996) Effects of timing of drought stress on phenology, yield and yield components of short-duration pigeonpea. J Agron Crop Sci 177:311–320. https://doi.org/10.1111/j.1439-037X.1996.tb00251.x
Article Google Scholar
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
Article PubMed Google Scholar
Luo D, Ganesh S, Koolaard J (2014) predictmeans: Calculate predicted means for linear models. R package version 0.99. https://CRAN.R-project.org/package=predictmeans. Accessed 20 Sept 2018
Manderscheid R, Erbs M, Weigel H-J (2014) Interactive effects of free-air CO₂ enrichment and drought stress on maize growth. Eur J Agron 52:11–21. https://doi.org/10.1016/j.eja.2011.12.007
Article CAS Google Scholar
McGrath JM, Lobell DB (2013) Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO₂ concentrations. Plant Cell Environ 36:697–705. https://doi.org/10.1111/pce.12007
Article CAS PubMed Google Scholar
Minchin FR, Sheehy JE, Minguez MI, Witty JF (1985) Characterization of the resistance to oxygen diffusion in legume nodules. Ann Bot 55:53–60. https://doi.org/10.1093/oxfordjournals.aob.a086877
Article Google Scholar
Mollah M, Norton R, Huzzey J (2009) Australian grains free-air carbon dioxide enrichment (AGFACE) facility: design and performance. Crop Pasture Sci 60:697–707. https://doi.org/10.1071/cp08354
Article CAS Google Scholar
Mollah M, Partington D, Fitzgerald G (2011) Understand distribution of carbon dioxide to interpret crop growth data: Australian grains free-air carbon dioxide enrichment experiment. Crop Pasture Sci 62:883–891. https://doi.org/10.1071/cp11178
Article CAS Google Scholar
Mouhouche B, Ruget F, Delécolle R (1998) Effects of water stress applied at different phenological phases on yield components of dwarf bean (Phaseolus vulgaris L.). Agronomie 18:197–205
Article Google Scholar
Nagar S, Ramakrishnan S, Singh VP, Singh GP, Dhakar R, Umesh DK, Arora A (2015) Cytokinin enhanced biomass and yield in wheat by improving N-metabolism under water limited environment. Indian J Plant Physiol 20:31–38. https://doi.org/10.1007/s40502-014-0134-3
Article CAS Google Scholar
Naudin C, Corre-Hellou G, Voisin A-S, Oury V, Salon C, Crozat Y, Jeuffroy M-H (2011) Inhibition and recovery of symbiotic N₂ fixation by peas (Pisum sativum L.) in response to short-term nitrate exposure. Plant Soil 346:275–287. https://doi.org/10.1007/s11104-011-0817-8
Article CAS Google Scholar
Naya L, Ladrera R, Ramos J, González EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 144:1104–1114. https://doi.org/10.1104/pp.107.099648
Article CAS PubMed PubMed Central Google Scholar
Nebiyu A, Huygens D, Upadhayay HR, Diels J, Boeckx P (2014) Importance of correct B value determination to quantify biological N₂ fixation and N balances of faba beans (Vicia faba L.) via ¹⁵N natural abundance. Biol Fertil Soils 50:517–525. https://doi.org/10.1007/s00374-013-0874-7
Article CAS Google Scholar
Parvin S, Uddin S, Bourgault M, Roessner U, Tausz-Posch S, Armstrong R, O'Leary G, Fitzgerald G, Tausz M (2018) Water availability moderates N₂ fixation benefit from elevated [CO₂]: a 2-years free-air CO₂ enrichment study on lentil (Lens culinaris MEDIK.) in a water limited agroecosystem. Plant Cell Environ 41:2418–2434. https://doi.org/10.1111/pce.13360
Article CAS PubMed Google Scholar
Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob Chang Biol 24:1–12. https://doi.org/10.1111/gcb.13850.
Article PubMed Google Scholar
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2017) nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–131, <URL: https://CRAN.R-project.org/package=nlme>
Pleijel H, Uddling J (2012) Yield vs. quality trade-offs for wheat in response to carbon dioxide and ozone. Glob Chang Biol 18:596–605. https://doi.org/10.1111/j.1365-2486.2011.2489.x
Article Google Scholar
Prudent M, Vernoud V, Girodet S, Salon C (2016) How nitrogen fixation is modulated in response to different water availability levels and during recovery: a structural and functional study at the whole plant level. Plant Soil 399:1–12. https://doi.org/10.1007/s11104-015-2674-3
Article CAS Google Scholar
Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, De Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165: 683–701. https://doi.org/10.1111/j.1469-8137.2004.01285.x
Purcell LC, Sinclair TR (1994) An osmotic hypothesis for the regulation of oxygen permeability in soybean nodules. Plant Cell Environ 17:837–843. https://doi.org/10.1111/j.1365-3040.1994.tb00178.x
Article Google Scholar
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Retrieved from https://www.R-project.org/
Google Scholar
Rab MA, Chandra S, Fisher PD, Robinson NJ, Kitching M, Aumann CD, Imhof M (2011) Modelling and prediction of soil water contents at field capacity and permanent wilting point of dryland cropping soils. Soil Res 49:389–407. https://doi.org/10.1071/sr10160
Article Google Scholar
Robredo A, Perez-Lopez U, de la Maza HS, Gonzalez-Moro B, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2007) Elevated CO₂ alleviates the impact of drought on barley improving water status by lowering stomatal conductance and delaying its effects on photosynthesis. Environ Exp Bot 59:252–263. https://doi.org/10.1016/j.envexpbot.2006.01.001
Article CAS Google Scholar
Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658. https://doi.org/10.1111/j.1365-3040.2006.01549.x
Article CAS PubMed Google Scholar
Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016. https://doi.org/10.1104/pp.109.144113
Article CAS PubMed PubMed Central Google Scholar
Sadras VO, Lake L, Chenu K, McMurray LS, Leonforte A (2012) Water and thermal regimes for field pea in Australia and their implications for breeding. Crop Pasture Sci 63:33–44. https://doi.org/10.1071/cp11321
Article Google Scholar
Schortemeyer M, Atkin OK, McFarlane N, Evans JR (2002) N₂ fixation by Acacia species increases under elevated atmospheric CO₂. Plant Cell Environ 25:567–579. https://doi.org/10.1046/j.1365-3040.2002.00831.x
Article CAS Google Scholar
Schulze J, Adgo E, Merbach W (1999) Carbon costs associated with N₂ fixation in Vicia faba L. and Pisum sativum L. over a 14-days period. Plant Biol 1:625–631. https://doi.org/10.1055/s-2007-978565
Article Google Scholar
Serraj R, Sinclair TR (2003) Evidence that carbon dioxide enrichment alleviates ureide‐induced decline of nodule nitrogenase activity. Ann Bot 91(1):85–89. https://doi.org/10.1093/aob/mcg012
Serraj R, Sinclair TR, Allen LH (1998) Soybean nodulation and N₂ fixation response to drought under carbon dioxide enrichment. Plant Cell Environ 21:491–500. https://doi.org/10.1046/j.1365-3040.1998.00298.x
Article Google Scholar
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N₂ fixation response to drought. J Exp Bot 50:143–155. https://doi.org/10.1093/jxb/50.331.143
Article CAS Google Scholar
Shrestha MK, Recknagel F, Frizenschaf J, Meyer W (2017) Future climate and land uses effects on flow and nutrient loads of a Mediterranean catchment in South Australia. Sci Total Environ 590:186–193. https://doi.org/10.1016/j.scitotenv.2017.02.197
Article CAS PubMed Google Scholar
Sinclair TR, Serraj R (1995) Legume nitrogen fixation and drought. Nature 378:344. https://doi.org/10.1038/378344a0
Article CAS Google Scholar
StatSoft (2013) Electronic Statistics Textbook. StatSoft Inc, Tulsa http://www.statsoft.com/Textbook. Accessed Dec 2018
Google Scholar
Streeter JG (1993) Translocation - a key factor limiting the efficiency of nitrogen fixation in legume nodules. Physiol Plant 87:616–623. https://doi.org/10.1111/j.1399-3054.1993.tb02514.x
Article CAS Google Scholar
Streeter JG (2003) Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ 26:1199–1204. https://doi.org/10.1046/j.1365-3040.2003.01041.x
Article CAS Google Scholar
Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO₂? A critical examination of the hypotheses. J Integr Plant Biol 50:1365–1374. https://doi.org/10.1111/j.1744-7909.2008.00754.x
Article CAS PubMed Google Scholar
Tausz-Posch S, Dempsey RW, Seneweera S, Norton RM, Fitzgerald G, Tausz M (2015) Does a freely tillering wheat cultivar benefit more from elevated CO₂ than a restricted tillering cultivar in a water-limited environment? Eur J Agron 64:21–28. https://doi.org/10.1016/j.eja.2014.12.009
Article Google Scholar
Tissue DT, Megonigal JP, Thomas RB (1996) Nitrogenase activity and N₂ fixation are stimulated by elevated CO₂ in a tropical N₂-fixing tree. Oecologia 109:28–33. https://doi.org/10.1007/s004420050054
Article CAS PubMed Google Scholar
Uddin S, Löw M, Parvin S, Fitzgerald G, Bahrami H, Tausz-Posch S, Armstrong R, O’Leary G, Tausz M (2018) Water use and growth responses of dryland wheat grown under elevated [CO₂] are associated with root length in deeper, but not upper soil layer. Field Crop Res 224:170–181. https://doi.org/10.1016/j.fcr.2018.05.014
Article Google Scholar
Unkovich M, Pate J, Sanford P, Armstrong E (1994) Potential precision of the δ¹⁵N natural abundance method in field estimates of nitrogen fixation by crop and pasture legumes in south-West Australia. Aust J Agric Res 45:119–132. https://doi.org/10.1071/AR9940119
Article Google Scholar
Voisin AS, Bourion V, Duc G, Salon C (2007) Using an ecophysiological analysis to dissect genetic variability and to propose an ideotype for nitrogen nutrition in pea. Ann Bot 100:1525–1536. https://doi.org/10.1093/aob/mcm241
Article CAS PubMed PubMed Central Google Scholar
Wang JY, Wang C, Chen NN, Xiong ZQ, Wolfe D, Zou JW (2015) Response of rice production to elevated CO₂ and its interaction with rising temperature or nitrogen supply: a meta-analysis. Clim Chang 130:529–543. https://doi.org/10.1007/s10584-015-1374-6
Article CAS Google Scholar
Yemm EW, Cocking EC (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–213. https://doi.org/10.1039/an9558000209
Article CAS Google Scholar
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.1042/bj0570508
Article CAS PubMed PubMed Central Google Scholar
Zanetti S, Hartwig UA, Luscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nosberger J (1996) Stimulation of symbiotic N₂ fixation in Trifolium repens L under elevated atmospheric CO₂ in a grassland ecosystem. Plant Physiol 112:575–583
Article CAS PubMed PubMed Central Google Scholar

Download references

Acknowledgements

The SoilFACE facility was part of the Australian Grains Free Air CO₂ Enrichment (AGFACE) program, which was jointly run by Agriculture Victoria and the University of Melbourne with funding from the Grains Research and Development Corporation and the Australian Commonwealth Department of Agriculture and Water Resources. We gratefully acknowledge Mahabubur Mollah (Agriculture Victoria) for operating the FACE technology and Sam Henty, Russel Argall, Mel Munn and other field team members for managing the field experiments. We are thankful to Shu Kee Lam for pre-submission review of the manuscript and useful comments, Maryse Bourgault for helpful suggestions during the experiment, Markus Löw for assisting with statistical analysis using R and Samuel Poynter for stable isotope analysis using the platform of Trace Analysis for Chemical, Earth and Environmental Science (TrACEES, University of Melbourne). First author acknowledges support by a Melbourne International Research Scholarship.

Author information

Authors and Affiliations

School of Ecosystem and Forest Sciences, The University of Melbourne, Creswick, VIC, Australia
Shahnaj Parvin & Michael Tausz
Department of Agronomy, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh
Shahnaj Parvin & Shihab Uddin
Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Creswick, VIC, Australia
Shihab Uddin, Glenn J. Fitzgerald & Sabine Tausz-Posch
Department of Economic Development, Jobs, Transport and Resources, Horsham, VIC, Australia
Glenn J. Fitzgerald & Roger Armstrong
School of Biosciences, University of Birmingham, Birmingham, UK
Sabine Tausz-Posch
Department of Animal, Plant and Soil Sciences, La Trobe University, Melbourne, VIC, Australia
Roger Armstrong
Birmingham Institute of Forest Research, University of Birmingham, Birmingham, UK
Michael Tausz

Authors

Shahnaj Parvin
View author publications
You can also search for this author in PubMed Google Scholar
Shihab Uddin
View author publications
You can also search for this author in PubMed Google Scholar
Glenn J. Fitzgerald
View author publications
You can also search for this author in PubMed Google Scholar
Sabine Tausz-Posch
View author publications
You can also search for this author in PubMed Google Scholar
Roger Armstrong
View author publications
You can also search for this author in PubMed Google Scholar
Michael Tausz
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shahnaj Parvin.

Additional information

Responsible Editor: Euan K. James.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1.43 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parvin, S., Uddin, S., Fitzgerald, G.J. et al. Free air CO₂ enrichment (FACE) improves water use efficiency and moderates drought effect on N₂ fixation of Pisum sativum L.. Plant Soil 436, 587–606 (2019). https://doi.org/10.1007/s11104-019-03949-7

Download citation