Abstract
Purpose
Belowground carbon (C) allocation for nitrogen (N) acquisition plays a crucial role in determining primary productivity and plant competitiveness in legume-grass mixtures, but beyond modeling and qualitative assessments, this remains poorly understood, especially with regard to drought stress and interspecific interactions.
Methods
We grew a legume (Trifolium repens) and a grass (Lolium perenne) in monocultures and as a 50:50 mixture (with same plant density), at 70% and 50% soil water holding capacity representing non-drought and drought conditions, for 104 days in a growth chamber experiment. By using continuous 13CO2 labelling and 15N pulse soil-labelling, we analyzed how drought and interspecific interaction affected belowground C allocation (including root biomass, root respiration and rhizodeposition) and N acquisition through soil N uptake and biological N fixation.
Results
Drought increased belowground C allocation per unit of N acquisition in the legume, but not in the grass. Drought significantly reduced biological N fixation in the legume, so that the legume allocated relatively more C to take up soil N. Interspecific competition increased belowground C allocation per unit of N acquisition, which could be attributed to a reduction in biological N fixation by the legume and an increased abundance of the grass.
Conclusions
We highlight that drought and interspecific competition for N strongly alter C allocation towards biological N fixation and soil N uptake. Our measurements provide important process-based information to improve modeling drought effects on productivity and composition in legume-grass mixtures.
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Data availability
The data that support the findings of this study will be made available from Dryad Digital Repository.
References
Adams MA, Buchmann N, Sprent J, Buckley TN, Turnbull TL (2018) Crops, nitrogen, water: are legumes friend, foe, or misunderstood ally? Trends Plant Sci 23:539–550
Almagro M, Jorge L, Boix-Fayos C, Albaladejo J, Martínez-Mena M (2010) Belowground carbon allocation patterns in a dry Mediterranean ecosystem: a comparison of two models. Soil Biol Biochem 42:1549–1557
Arndal MF, Schmidt IK, Kongstad J, Beier C, Michelsen A (2014) Root growth and N dynamics in response to multi-year experimental warming, summer drought and elevated CO2 in a mixed heathland-grass ecosystem. Funct Plant Biol 41:1–10
Bahn M, Knapp M, Garajova Z, Pfahringer N, Cernusca A (2006) Root respiration in temperate mountain grasslands differing in land use. Glob Change Biol 12:995–1006
Balogh J, Papp M, Pintér K, Fóti S, Posta K, Eugster W, Nagy Z (2016) Autotrophic component of soil respiration is repressed by drought more than the heterotrophic one in dry grasslands. Biogeosciences 13:5171–5182
Canarini A, Dijkstra FA (2015) Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol Biochem 81:195–203
Chomel M, Lavallee J, Alvarez-Segura N, de Castro F, Rhymes J, Caruso T, Vries F, Baggs E, Emmerson M, Bardgett R, Johnson D (2019) Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity. Glob Change Biol 25:3549–3561
Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533
Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G (2013) Long-term climate change: projections, commitments and irreversibility. Climate Change 2013-The Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press
Craine JM, Ocheltree TW, Nippert JB, Towne EG, Skibbe AM, Kembel SW, Fargione JE (2013) Global diversity of drought tolerance and grassland climate-change resilience. Nat Clim Chang 3:63–67
Daryanto S, Wang L, Jacinthe P-A (2017) Global synthesis of drought effects on cereal, legume, tuber and root crops production: a review. Agric Water Manag 179:18–33
de Vries FT, Brown C, Stevens CJ (2016) Grassland species root response to drought: consequences for soil carbon and nitrogen availability. Plant Soil 409:297–312
Deng L, Peng C, Kim D-G, Li J, Liu Y, Hai X, Liu Q, Huang C, Shangguan Z, Kuzyakov Y (2021) Drought effects on soil carbon and nitrogen dynamics in global natural ecosystems. Earth-Sci Rev 214:103501
Dijkstra FA, Cheng W (2007) Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecol Lett 10:1046–1053
Dijkstra FA, Bader NE, Johnson DW, Cheng W (2009) Does accelerated soil organic matter decomposition in the presence of plants increase plant N availability? Soil Biol Biochem 41:1080–1087
Dijkstra FA, Morgan JA, Blumenthal D, Follett RF (2010) Water limitation and plant inter-specific competition reduce rhizosphere-induced C decomposition and plant N uptake. Soil Biol Biochem 42:1073–1082
Divito GA, Sadras VO (2014) How do phosphorus, potassium and Sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. Field Crops Res 156:161–171
Dovrat G, Sheffer E (2019) Symbiotic dinitrogen fixation is seasonal and strongly regulated in water-limited environments. New Phytol 221:1866–1877
Evans PS (1977) Comparative root morphology of some pasture grasses and clovers. N Z J Agric Res 20:331–335
Eziz A, Yan Z, Tian D, Han W, Tang Z, Fang J (2017) Drought effect on plant biomass allocation: a meta-analysis. Ecol and Evol 7:11002–11010
Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler PB, Blumenthal DM, Buckley YM, Chu C, Cleland EE, Collins SL, Davies KF, Du G, Feng X et al (2015) Grassland productivity limited by multiple nutrients. Nature Plants 1:15080
Fisher J, Sitch S, Malhi Y, Fisher R, Huntingford C, Tan SY (2010) Carbon cost of plant nitrogen acquisition: a mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation. Glob Biogeochem Cycles 24:1–17
Fornara D, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol 96:314–322
Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927
Gill AL, Finzi AC (2016) Belowground carbon flux links biogeochemical cycles and resource-use efficiency at the global scale. Ecol Lett 19:1419–1428
Goh K, Bruce G (2005) Comparison of biomass production and biological nitrogen fixation of multi-species pastures (mixed herb leys) with perennial ryegrass-white clover pasture with and without irrigation in Canterbury, New Zealand. Agric Ecosyst Environ 110:230–240
Gomez-Casanovas N, Matamala R, Cook DR, Gonzalez-Meler MA (2012) Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands. Glob Change Biol 18:2532–2545
Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127
Hazard C, Gosling P, Van Der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. The ISME J 7:498–508
Holz M, Zarebanadkouki M, Kaestner A, Kuzyakov Y, Carminati A (2018) Rhizodeposition under drought is controlled by root growth rate and rhizosphere water content. Plant Soil 423:429–442
Isbell R (2016) The Australian soil classification. CSIRO publishing
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480
Karlowsky S, Augusti A, Ingrisch J, Akanda MKU, Bahn M, Gleixner G (2018) Drought-induced accumulation of root exudates supports post-drought recovery of microbes in mountain grassland. Front Plant Sci 9:1593
Keller A, Phillips R (2019) Relationship between belowground carbon allocation and nitrogen uptake in saplings varies by plant mycorrhizal type. Front For Glob Change 2:81
Klumpp K, SchÄUfele R, LÖTscher M, Lattanzi F, Feneis W, Schnyder H (2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant Cell Environ 28:241–250
Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Ledgard S, Steele K (1992) Biological nitrogen fixation in mixed legume/grass pastures. Plant Soil 141:137–153
Ledgard SF, Sprosen MS, Penno JW, Rajendram GS (2001) Nitrogen fixation by white clover in pastures grazed by dairy cows: temporal variation and effects of nitrogen fertilization. Plant Soil 229:177–187
Louarn G, Pereira-Lopès E, Fustec J, Mary B, Voisin A-S, de Faccio Carvalho PC, Gastal F (2015) The amounts and dynamics of nitrogen transfer to grasses differ in alfalfa and white clover-based grass-legume mixtures as a result of rooting strategies and rhizodeposit quality. Plant Soil 389:289–305
Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739
Mariotte P, Cresswell T, Johansen MP, Harrison JJ, Keitel C, Dijkstra FA (2020) Plant uptake of nitrogen and phosphorus among grassland species affected by drought along a soil available phosphorus gradient. Plant Soil:1–12
Mehnaz K, Dijkstra F (2016) Denitrification and associated N2O emissions are limited by phosphorus availability in a grassland soil. Geoderma 284:34–41
Mehnaz K, Keitel C, Dijkstra FA (2019) Phosphorus availability and plants alter soil nitrogen retention and loss. Sci Tot Environ 671:786–794
Meisser M, Vitra A, Deléglise C, Dubois S, Probo M, Mosimann E, Buttler A, Mariotte P (2019) Nutrient limitations induced by drought affect forage N and P differently in two permanent grasslands. Agric Ecosyst Environ 280:85–94
Mia S, Singh B, Dijkstra FA (2017) Aged biochar affects gross nitrogen mineralization and recovery: a 15N study in two contrasting soils. GCB Bioenergy 9:1196–1206
Mia S, Dijkstra FA, Singh B (2018) Enhanced biological nitrogen fixation and competitive advantage of legumes in mixed pastures diminish with biochar aging. Plant Soil 424:639–651
Minucci JM, Miniat CF, Teskey RO, Wurzburger N (2017) Tolerance or avoidance: drought frequency determines the response of an N2-fixing tree. New Phytol 215:434–442
Moinet GYK, Midwood AJ, Hunt JE, Rumpel C, Millard P, Chabbi A (2019) Grassland management influences the response of soil respiration to drought. Agronomy 9:124
Mouradi M, Farissi M, Bouizgaren A, Makoudi B, Kabbadj A, Very A-A, Sentenac H, Qaddourya A, Ghoulam C (2016) Effects of water deficit on growth, nodulation and physiological and biochemical processes in Medicago sativa-rhizobia symbiotic association. Arid Land Res Manage 30:193–208
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
Nyfeler D, Huguenin-Elie O, Suter M, Frossard E, Lüscher A (2011) Grass–legume mixtures can yield more nitrogen than legume pure stands due to mutual stimulation of nitrogen uptake from symbiotic and non-symbiotic sources. Agric Ecosyst Environ 140:155–163
Palmborg C, Scherer-Lorenzen M, Jumpponen A, Carlsson G, Huss-Danell K, Högberg P (2005) Inorganic soil nitrogen under grassland plant communities of different species composition and diversity. Oikos 110:271–282
Parvin S, Uddin S, Tausz-Posch S, Armstrong R, Tausz M (2020) Carbon sink strength of nodules but not other organs modulates photosynthesis of faba bean (Vicia faba) grown under elevated CO2 and different water supply. New Phytol 227:132–145
Pataki D, Ehleringer J, Flanagan L, Yakir D, Bowling D, Still C, Buchmann N, Kaplan JO, Berry J (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Glob Biogeochem Cycles 17(1):1022
Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob Change Biol 24:1–12
Peñuelas J, Prieto P, Beier C, Cesaraccio C, De Angelis P, De Dato G, Emmett BA, Estiarte M, Garadnai J, Gorissen A, LÁNg EK, KrÖEl-Dulay G, Llorens L, Pellizzaro G, Riis-Nielsen T, Schmidt IK, Sirca C, Sowerby A, Spano D, Tietema A (2007) Response of plant species richness and primary productivity in shrublands along a north–south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Glob Change Biol 13:2563–2581
Peterson PR, Sheaffer CC, Hall MH (1992) Drought effects on perennial forage legume yield and quality. Agron J 84:774–779
Pirhofer-Walzl K, Rasmussen J, Høgh-Jensen H, Eriksen J, Søegaard K, Rasmussen J (2012) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil 350:71–84
Preece C, Peñuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–17
Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012) Carbon allocation in grassland communities under drought stress followed by 14C pulse labeling. Soil Biol Biochem 55:132–139
Sardans J, Rivas-Ubach A, Peñuelas J (2012) The C: N: P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspect Plant Ecol Evol Syst 14:33–47
Schmitt A, Pausch J, Kuzyakov Y (2013) Effect of clipping and shading on C allocation and fluxes in soil under ryegrass and alfalfa estimated by 14C labelling. Appl Soil Ecol 64:228–236
Schnyder H, Lattanzi F (2005) Partitioning respiration of C3-C4 mixed communities using the natural abundance 13C approach - testing assumptions in a controlled environment. Plant biology (Stuttgart, Germany) 7:592–600
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155
Shi M, Fisher JB, Brzostek ER, Phillips RP (2016) Carbon cost of plant nitrogen acquisition: global carbon cycle impact from an improved plant nitrogen cycle in the community land model. Glob Change Biol 22:1299–1314
Soussana J-F, Lemaire G (2014) Coupling carbon and nitrogen cycles for environmentally sustainable intensification of grasslands and crop-livestock systems. Agric Ecosyst Environ 190:9–17
Suter M, Connolly J, Finn JA, Loges R, Kirwan L, Sebastià MT, Lüscher A (2015) Nitrogen yield advantage from grass–legume mixtures is robust over a wide range of legume proportions and environmental conditions. Glob Change Biol 21:2424–2438
Terrer C, Vicca S, Stocker BD, Hungate BA, Phillips RP, Reich PB, Finzi AC, Prentice IC (2018) Ecosystem responses to elevated CO2 governed by plant–soil interactions and the cost of nitrogen acquisition. New Phytol 217:507–522
Thornton PE, Lamarque JF, Rosenbloom NA, Mahowald NM (2007) Influence of carbon-nitrogen cycle coupling on land model response to CO2 fertilization and climate variability. Glob Biogeochem Cycles 21:GB4018
Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302
Tzanakakis V, Sturite I, Dörsch P (2017) Biological nitrogen fixation and transfer in a high latitude grass-clover grassland under different management practices. Plant Soil 421:107–122
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB (2002) Towards an ecological understanding of biological nitrogen fixation. The nitrogen cycle at regional to global scales. Springer
Wang X, Zhu B, Wang Y, Zheng X (2008) Field measures of the contribution of root respiration to soil respiration in an alder and cypress mixed plantation by two methods: trenching method and root biomass regression method. Eur J For Res 127:285–291
Wang Y, Hao Y, Cui XY, Zhao H, Xu C, Zhou X, Xu Z (2014) Responses of soil respiration and its components to drought stress. J Soils Sed 14:99–109
Wang R, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA (2021a) Carbon allocation to the rhizosphere is affected by drought and nitrogen addition. J Ecol 109:3699–3709
Wang R, Bicharanloo B, Shirvan MB, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA (2021b) A novel 13C pulse-labelling method to quantify the contribution of rhizodeposits to soil respiration in a grassland exposed to drought and nitrogen addition. New Phytol 230:857–866
Wegener F, Beyschlag W, Werner C (2010) The magnitude of diurnal variation in carbon isotopic composition of leaf dark respired CO2 correlates with the difference between δ13C of leaf and root material. Funct Plant Biol 37:849–858
Wei X, Reich PB, Hobbie SE (2019) Legumes regulate grassland soil N cycling and its response to variation in species diversity and N supply but not CO2. Glob Change Biol 25:2396–2409
Williams A, de Vries FT (2020) Plant root exudation under drought: implications for ecosystem functioning. New Phytol 225:1899–1905
Acknowledgements
We thank Dr. Sonam Tashi for isotopic analysis. This research was funded by the Australian Research Council (Grant no. DP190102262) and the National Natural Science Foundation of China (Grant no. 32001187).
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Chunlian Qiao and Feike A. Dijkstra designed the research and analysed data. Chunlian Qiao, Xiaoguang Wang and Milad Bagheri Shirvan established and performed the experiment. Chunlian Qiao, Claudia Keitel and Feike A. Dijkstra led the isotope measurements and data interpretation. All authors contributed to the writing of the manuscript.
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Qiao, C., Wang, X., Shirvan, M.B. et al. Drought and interspecific competition increase belowground carbon allocation for nitrogen acquisition in monocultures and mixtures of Trifolium repens and Lolium perenne. Plant Soil 481, 269–283 (2022). https://doi.org/10.1007/s11104-022-05636-6
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DOI: https://doi.org/10.1007/s11104-022-05636-6