Abstract
Wheat proteins provide around 20% of all human dietary protein, but their end-use qualities are determined by the form and quantity of nitrogen in the endosperm. In the developed world, there is a heavy reliance in grain production on nitrogen supplied from synthetic fertilisers, and this fertiliser can contribute up to 50% of the on-farm emissions of greenhouse gasses in agriculture. However, despite increasing rates of application of synthetic nitrogen to cereals, wheat grain protein levels, in developed nations, have been frequently failing to reach the premium grade required by the bread-making market. Here, for the first time, we report that biological nitrogen fixation from a new generation of hardseeded annual forage legumes, when grown in rotation with cereal crops, can replace fertiliser N without compromising grain protein. The forage legumes were grown in rotation with Triticum aestivum, and compared with rotations that included a fallow, or a cereal crop at three rainfed sites in Western Australia with differing soil types for 2–4 years. The wheat received low, medium and high rates of urea to indicate if forage legumes can provide sufficient nitrogen for sustainable wheat production. At all sites and years studied, we discovered that cereal grains produced following a year of forage legumes had significantly higher protein levels than when grown as part of a continuous cereal rotation. These results were achieved in combination with a reduction in on-farm emissions (by over 200 kg/ha of CO2) without compromising yield as indicated by emissions accounting. Including appropriate forage legumes in farming systems allows production of low emission intensity grain proteins in dryland farming.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The authors confirm that the data supporting the findings of this study are available within the article. Further raw data is available from the corresponding author, upon reasonable request.
Code availability
Not applicable.
References
Angus JF, Fischer RA (1991) Grain protein responses to nitrogen applied to wheat growing on a red earth. Aust J Agric Res 42(5):735–746 (https://www.publish.csiro.au/CP/AR9910735)
Angus JF, Kirkegaard JA, Hunt JR, Ryan MH, Ohlander L, Peoples MB (2015) Break crops and rotations for wheat. Crop Pasture Sci 66(6):523–552. https://doi.org/10.1071/CP14252
Barton L, Thamo T, Engelbrecht D, Biswas WK (2014) Does growing grain legumes or applying lime cost effectively lower greenhouse gas emissions from wheat production in a semi-arid climate? J Clean Prod 83:194–203. https://doi.org/10.1016/j.jclepro.2014.07.020
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. Computer program. https://doi.org/10.48550/arXiv.1406.5823
Bestow S (1992) Quest for quality operation quality wheat, vol 6. vol 92. Department of Primary Industries and Regional Development, Perth, Western Australia. Report 6/92
Bloom AJ (1997) Nitrogen as a Limiting Factor: Crop Acquisition of nitrate and ammonium. Ecology in agriculture. pp 145–72 Academic Press, San Diego, CA
Borlaug NE (1968) Wheat breeding and its impact on world food supply. In: CIMMYT (ed) Proc 3rd Int Wheat Geneti Symp, Canberra, Aust. Academic Science 3:1–36
Brankatschk G, Finkbeiner M (2017) Crop rotations and crop residues are relevant parameters for agricultural carbon footprints. Agron Sustain Dev 37(6):58. https://doi.org/10.1007/s13593-017-0464-4
Browne NA, Eckard RJ, Behrendt R, Kingwell RS (2011) A comparative analysis of on-farm greenhouse gas emissions from agricultural enterprises in south eastern Australia. Anim Feed Sci Technol 166–167:641–652. https://doi.org/10.1016/j.anifeedsci.2011.04.045
Camargo GGT, Ryan MR, Richard TL (2013) Energy use and greenhouse gas emissions from crop production using the farm energy analysis tool. BioSci 63(4):263–273. https://doi.org/10.1525/bio.2013.63.4.6
Cann DJ, Hunt JR, Malcolm B (2020) Long fallows can maintain whole-farm profit and reduce risk in semi-arid south-eastern Australia. Agric Syst 178:102721. https://doi.org/10.1016/j.agsy.2019.102721
Chalk PM (1997) Dynamics of biologically fixed N in legume-cereal rotations: a review. Aust J Agric Res 49(3):303–316. https://doi.org/10.1071/A97013
Chen D, Suter H, Islam A, Edis R, Freney JR, Walker CN (2008) Prospects of improving efficiency of fertiliser nitrogen in Australian agriculture: a review of enhanced efficiency fertilisers. Soil Res 46(4):289–301. https://doi.org/10.1071/SR07197
Crews TE, Peoples MB (2005) Can the synchrony of nitrogen supply and crop demand be improved in legume and fertilizer-based agroecosystems? A Review. Nutr Cycl Agroecosyst 72(2):101–120. https://doi.org/10.1007/s10705-004-6480-1
Day L, Augustin MA, Batey IL, Wrigley CW (2006) Wheat-gluten uses and industry needs. Trends Food Sci Technol 17(2):82–90. https://doi.org/10.1016/j.tifs.2005.10.003
Diacono M, Rubino P, Montemurro F (2013) Precision nitrogen management of wheat. A Review. Agron Sustain Dev 33(1):219–241. https://doi.org/10.1007/s13593-012-0111-z
Donald CM (1960) The impact of cheap nitrogen. J Aust Inst Agric Sci 26:319–338
Donald CM (1965) The progress of Australian agriculture and the role of pastures in environmental change. Aust J Sci 27(7):187–198
Edwards TJ, Howieson JG, Nutt BJ, Yates RJ, O’Hara GW, Van Wyk BE (2019) A ley-farming system for marginal lands based upon a self-regenerating perennial pasture legume. Agron Sustain Dev 39(13):1–19. https://doi.org/10.1007/s13593-019-0558-2
Ekonomou A, Eckard RJ (2022) A greenhouse accounting framework for crop production (G-GAF) based on the Australian National Greenhouse Gas Inventory methodology. Primary Industires Climate Challenges Centre. http://www.piccc.org.au/resources/Tools. Accessed 7 Mar 2023
Erenstein O, Jaleta M, Mottaleb KA, Sonder K, Donovan J, Braun H-J (2022) Global trends in wheat production, consumption and trade. In: Reynolds MP, Braun H-J (eds) Wheat improvement: food security in a changing climate. Springer International Publishing, Cham, pp 47–66. https://doi.org/10.1007/978-3-030-90673-3_4
Erisman JW, Galloway JN, Seitzinger S, Bleeker A, Dise NB, Petrescu AMR, Leach AM, de Vries W (2013) Consequences of human modification of the global nitrogen cycle. Philos Trans R Soc b: Biol Sci 368(1621):20130116. https://doi.org/10.1098/rstb.2013.0116
Fillery IRP (2001) The fate of biologically fixed nitrogen in legume-based dryland farming systems: a review. Aust J of Exp Agric 41(3):361–381. https://doi.org/10.1071/EA00126
Geng S, Tan J, Li L, Miao Y, Wang Y (2023) Legumes can increase the yield of subsequent wheat with or without grain harvesting compared to Gramineae crops: A meta-analysis. Eur J Agron 142:126643. https://doi.org/10.1016/j.eja.2022.126643
Harrison RJ, Howieson JG, Yates RJ, Nutt BJ (2021) Long-term storage of forage legumes greatly alters the hardseed breakdown pattern in situ. Grass Forage Sci 76:72–81. https://doi.org/10.1111/gfs.12490
Henchion M, Hayes M, Mullen AM, Fenelon M, Tiwari B (2017) Future protein supply and demand: strategies and factors influencing a sustainable equilibrium. Foods 6(7):53. https://doi.org/10.3390/foods6070053
Hochman Z, Gobbett DL, Horan H (2017) Climate trends account for stalled wheat yields in Australia since 1990. Global Change Biol 23(5):2071–2081. https://doi.org/10.1111/gcb.13604
Houlton BZ, Almaraz M, Aneja V, Austin AT, Bai E, Cassman KG, Compton JE, Davidson EA, Erisman JW, Galloway JN, Gu B, Yao G, Martinelli LA, Scow K, Schlesinger WH, Tomich TP, Wang C, Zhang X (2019) A world of cobenefits: solving the global nitrogen challenge. Earth’s Future 7(8):865–872. https://doi.org/10.1029/2019EF001222
Howieson JG, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem 36(8):1261–1273. https://doi.org/10.1016/j.soilbio.2004.04.008
Howieson JG, Loi A, Carr SJ (1995) Biserrula pelecinus L.-a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Aust J Agric Res 46(5):997–1009. https://doi.org/10.1071/AR9950997
Howieson JG, O’Hara GW, Carr SJ (2000) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Res 65(2):107–122. https://doi.org/10.1016/S0378-4290(99)00081-7
Howieson JG, Harrison RJ, Yates RJ, Hackney B, Loi A, Nutt BJ (2021) Hard seed breakdown patterns of unprocessed forage legume seed sown into dry soil in summer in southern Australia. Grass Forage Sci 76(1):82–92. https://doi.org/10.1111/gfs.12526
Hu X, Spilke J (2009) Comparison of various spatial models for the analysis of cultivar trials. N Z J Agric Res 52(3):277–287. https://doi.org/10.1080/00288230909510512
VSN International (2019) Genstat for Windows, Computer Program 19th ed. Hemel Hempstead, UK
Isbell RF (2016) The Second Edition of the Australian Soil Classification. CSIRO, Canberra
Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, J.R. Alves B, Morrison MJ (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review. Agron Sustain Dev 32(2):329–364. https://doi.org/10.1007/s13593-011-0056-7
Kirkegaard J, Christen O, Krupinsky J, Layzell D (2008) Break crop benefits in temperate wheat production. Field Crops Res 107(3):185–195. https://doi.org/10.1016/j.fcr.2008.02.010
Lassaletta L, Billen G, Garnier J, Bouwman L, Velazquez E, Mueller ND, Gerber JS (2016) Nitrogen use in the global food system: past trends and future trajectories of agronomic performance, pollution, trade, and dietary demand. Environ Res Lett 11(9):095007. https://doi.org/10.1088/1748-9326/11/9/095007
Lenth R (2019) emmeans: Estimated marginal means, aka least-squares means. R package version 1.4. 3.01. https://CRAN.R-project.org/package=emmeans
Loi A, Howieson JG, Nutt BJ, Carr SJ (2005) A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems. Aust J Exp Agric 45(3):289–299. https://doi.org/10.1071/EA03134
Loi A, Thomas DT, Yates RJ, Harrison RJ, D’Antuono M, Re GA, Norman HC, Howieson JG (2022) Cereal and oil seed crops response to organic nitrogen when grown in rotation with annual aerial-seeded pasture legumes. J Agric Sci 160(3–4):207–219. https://doi.org/10.1017/S0021859622000326
Lu C, Yu Z, Zhang J, Cao P, Tian H, Nevison C (2022) Century-long changes and drivers of soil nitrous oxide (N2O) emissions across the contiguous United States. Global Change Biol 28(7):2505–2524. https://doi.org/10.1111/gcb.16061
MacLaren C, Storkey J, Strauss J, Swanepoel P, Dehnen-Schmutz K (2019) Livestock in diverse cropping systems improve weed management and sustain yields whilst reducing inputs. J Appl Ecol 56(1):144–156. https://doi.org/10.1111/1365-2664.13239
MacLaren C, Mead A, van Balen D, Claessens L, Etana A, de Haan J, Haagsma W, Jäck O, Keller T, Labuschagne J (2022) Long-term evidence for ecological intensification as a pathway to sustainable agriculture. Nat Sustain 5(9):770–779. https://doi.org/10.1038/s41893-022-00911-x
McGuire AM, Bryant DC, Denison RF (1998) Wheat Yields, Nitrogen Uptake, and Soil Moisture Following Winter Legume Cover Crop vs. Fallow. Agron J 90(3):404–410. https://doi.org/10.2134/agronj1998.00021962009000030015x
Monjardino M, Loi A, Thomas DT, Revell CK, Flohr BM, Llewellyn RS, Norman HC (2022) Improved legume pastures increase economic value, resilience and sustainability of crop-livestock systems. Agric Syst 203:103519. https://doi.org/10.1016/j.agsy.2022.103519
Moore GA (2001) Soil guide: A handbook for understanding and managing agricultural soils, vol bulletin 4343. Western Australian Department of Agriculture, Perth, WA
Mulvaney RL, Khan SA, Ellsworth TR (2009) Synthetic Nitrogen Fertilizers Deplete Soil Nitrogen: A Global Dilemma for Sustainable Cereal Production. J Environ Qual 38(6):2295–2314. https://doi.org/10.2134/jeq2008.0527
Nichols PGH, Loi A, Nutt BJ, Evans PM, Craig AD, Pengelly BC, Dear BS, Lloyd DL, Revell CK, Nair RM, Ewing MA, Howieson JG, Auricht GA, Howie JH, Sandral GA, Carr SJ, de Koning CT, Hackney BF, Crocker GJ, Snowball R, Hughes SJ, Hall EJ, Foster KJ, Skinner PW, Barbetti MJ, You MP (2007) New annual and short-lived perennial pasture legumes for Australian agriculture—15 years of revolution. Field Crops Res 104(1–3):10–23. https://doi.org/10.1016/j.fcr.2007.03.016
Nichols P, Loi A, Nutt B, Snowball R, Revell C (2010) Domestication of New Mediterranean Annual Pasture Legumes. In: Huyghe C (ed) Sustainable use of Genetic Diversity in Forage and Turf Breeding. Springer Netherlands, Dordrecht, pp 137–141. https://doi.org/10.1007/978-90-481-8706-5_19
Notz I, Topp CFE, Schuler J, Alves S, Gallardo LA, Dauber J, Haase T, Hargreaves PR, Hennessy M, Iantcheva A, Jeanneret P, Kay S, Recknagel J, Rittler L, Vasiljević M, Watson CA, Reckling M (2023) Transition to legume-supported farming in Europe through redesigning cropping systems. Agron Sustain Dev 43(1):12. https://doi.org/10.1007/s13593-022-00861-w
Nutt BJ, Harrison RJ, McComb JA, Howieson JG (2021) The breeding system of Ornithopus sativus Brot. subsp. sativus. Grass Forage Sci 76(1):3–9. https://doi.org/10.1111/gfs.12521
Nutt BJ, Loi A, Hackney B, Yates RJ, D’Antuono M, Harrison RJ, Howieson JG (2021) “Summer sowing”: A successful innovation to increase the adoption of key species of annual forage legumes for agriculture in Mediterranean and temperate environments. Grass Forage Sci 76(1):93–104. https://doi.org/10.1111/gfs.12516
O’Donovan JT, Grant CA, Blackshaw RE, Harker KN, Johnson EN, Gan Y, Lafond GP, May WE, Turkington TK, Lupwayi NZ, Stevenson FC, McLaren DL, Khakbazan M, Smith EG (2014) Rotational Effects of Legumes and Non-Legumes on Hybrid Canola and Malting Barley. Agron J 106(6):1921–1932. https://doi.org/10.2134/agronj14.0236
Oliver J (1988) Why is protein so important? In: Conference Proceedings "The Impact of Change - The Need to Adapt." Riverina outlook conferences. The Regional Institute, Australia. www.regional.org.au/au/roc/1988
Petersen EH, Scanlan CA, Burton MP, Oliver YM, Murphy DV, Hoyle FC (2023) Agronomic factors are the dominant influence on nitrogen fertilizer strategies in dryland cropping systems. Agron Sustain Dev 43(1):14. https://doi.org/10.1007/s13593-023-00867-y
Pingali PL (2012) Green Revolution: Impacts, limits, and the path ahead. Proc Natl Acad Sci 109(31):12302–12308. https://doi.org/10.1073/pnas.0912953109
Plaza-Bonilla D, Arrúe JL, Cantero-Martínez C, Fanlo R, Iglesias A, Álvaro-Fuentes J (2015) Carbon management in dryland agricultural systems. A Review. Agron Sustain Dev 35(4):1319–1334. https://doi.org/10.1007/s13593-015-0326-x
Pronin D, Börner A, Weber H, Scherf KA (2020) Wheat (Triticum aestivum L.) Breeding from 1891 to 2010 Contributed to Increasing Yield and Glutenin Contents but Decreasing Protein and Gliadin Contents. J Agric Food Chem 68(46):13247–13256. https://doi.org/10.1021/acs.jafc.0c02815
Puckridge DW, French RJ (1983) The annual legume pasture in cereal—Ley farming systems of southern Australia: a review. Agric, Ecosyst Environ 9(3):229–267. https://doi.org/10.1016/0167-8809(83)90100-7
Rascio N, La Rocca N (2008) Biological Nitrogen Fixation. In: Jørgensen SE, Fath BD (eds) Encyclopedia of Ecology. Academic Press, Oxford, pp 412–419. https://doi.org/10.1016/B978-008045405-4.00273-1
Revell CK, Taylor GB, Cocks PS (1998) Long-term softening of surface and buried hard seeds of yellow serradella grown in a range of environments. Aust J Agric Res 49(4):673–686. https://doi.org/10.1071/A97117
Robertson MJ, Lawes RA, Bathgate A, Byrne F, White P, Sands R (2010) Determinants of the proportion of break crops on Western Australian broadacre farms. Crop Pasture Sci 61(3):203–213. https://doi.org/10.1071/CP09207
Robson AD (1990) The Role of Self-regenerating Pasture in Rotation with Cereals in Mediterranean Areas. In: Osman AE, Ibrahim MH, Jones MA (eds) The Role of Legumes in the Farming Systems of the Mediterranean Areas: Proceedings of a Workshop on the Role of Legumes in the Farming Systems of the Mediterranean Areas UNDP/ICARDA, Tunis, June 20–24, 1988. Springer Netherlands, Dordrecht, pp 217–236. https://doi.org/10.1007/978-94-009-1019-5_19
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecol 85(3):591–602. https://doi.org/10.1890/03-8002
Shewry P (2019) What Is Gluten-Why Is It Special? Front Nutr 6:101. https://doi.org/10.3389/fnut.2019.00101
Smit EH, Strauss JA, Swanepoel PA (2021) Utilisation of cover crops: implications for conservation agriculture systems in a mediterranean climate region of South Africa. Plant Soil 462(1):207–218. https://doi.org/10.1007/s11104-021-04864-6
Stagnari F, Maggio A, Galieni A, Pisante M (2017) Multiple benefits of legumes for agriculture sustainability: an overview. Chem Biol Technol Agric 4(1):2. https://doi.org/10.1186/s40538-016-0085-1
Stoddard F, Marshall D (1990) Variability in grain protein in Australian hexaploid wheats. Aust J Agric Res 41(2):277–288. https://doi.org/10.1071/AR9900277
Team RC (2019) R: A language and environment for statistical computing (Version 3.0. 2) [Computer software]. Vienna, Austria: R Foundation for Statistical Computing.
Turner D, Edis R, Chen D, Freney J, Denmead O (2012) Ammonia volatilization from nitrogen fertilizers applied to cereals in two cropping areas of southern Australia. Nutr Cycling Agroecosyst 93:113–126. https://doi.org/10.1007/s10705-012-9504-2
Uthayakumaran S, Gras PW, Stoddard FL, Bekes F (1999) Effect of Varying Protein Content and Glutenin-to-Gliadin Ratio on the Functional Properties of Wheat Dough. Cereal Chem 76(3):389–394. https://doi.org/10.1094/CCHEM.1999.76.3.389
Van Herwaarden AF, Farquhar GD, Angus JF, Richards RA, Howe GN (1998) “Haying-off”, the negative grain yield response of dryland wheat to nitrogen fertiliser. I. Biomass, grain yield, and water use. Aust J Agric Res 49(7):1067–1082. https://doi.org/10.1071/A97039
Wells L (2022) Australia’s big wheat year big on low protein: AGIC Asia. Grain Central Nascon Media Pty Ltd. https://www.graincentral.com/markets/australias-big-wheat-year-big-on-low-protein-agic-asia/#:~:text=AUSTRALIA%20is%20in%20the%20midst,%2Dthan%2Dideal%20quality%20profile. Accessed 15 Jun 2023
Westfall DG, Havlin JL, Hergert GW, Raun WR (1996) Nitrogen management in dryland cropping systems. J Prod Agric 9(2):192–199. https://doi.org/10.2134/jpa1996.0192
White PF, Treacher TT, Termanini A (1997) Nitrogen cycling in semi-arid Mediterranean zones: removal and return of nitrogen to pastures by grazing sheep. Aust J Agric Res 48(3):317–322. https://doi.org/10.1071/A96041
Wickham H (2011) ggplot2. WIREs Comput Stat 3(2):180–185
Wicks GA, Smika DE (1973) Chemical fallow in a winter wheat-fallow rotation. Weed Sci 21(2):97–102. https://doi.org/10.1017/S0043174500031829
Wu F, Butz WP (2004) The gene revolution: Genetically modified crops. In: The future of genetically modified crops. Lessons from the green revolution, 1 edn. Santa Monica, CA, USA: RAND Corporation, pp 39–64
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14(6):415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zhao J, Chen J, Beillouin D, Lambers H, Yang Y, Smith P, Zeng Z, Olesen JE, Zang H (2022) Global systematic review with meta-analysis reveals yield advantage of legume-based rotations and its drivers. Nat Commun 13(1):4926. https://doi.org/10.1038/s41467-022-32464-0
Acknowledgements
The authors acknowledge the various technicians especially Sam Richards and Benedict Arthur, grower groups and support staff that have contributed to this project. We also appreciate the input from host farmers Clinton Butler (Narembeen), Jeremy Wasley (Canna) and Philip Foss (Ardath). Finally, our thanks also go to Kimberly Maslin for her graphic design of Fig. 6.
Funding
The Dryland Legumes Pasture Systems project, which is funded by the Australian Government Department of Agriculture Water and the Environment as part of its Rural R&D for Profit program, the Grains Research and Development Corporation, Meat and Livestock Australia and Australian Wool Innovation (Project No. RnD4Profit-16-03-010).
Author information
Authors and Affiliations
Contributions
Robert J. Harrison: conceptualisation, methodology, investigation, resources, data curation, writing—original, writing—review and editing, formal analysis, visualization. John G. Howieson: writing—original, writing—review and editing, conceptualisation, funding acquisition. Tom J. Edwards: conceptualisation, investigation, data curation, writing—original, writing—review and editing. Emma J Steel: formal analysis, visualisation. Chris M Poole: investigation, resources Ron J. Yates: conceptualisation, writing—original, supervision, project administration, funding acquisition
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent for publication and participation
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Harrison, R.J., Howieson, J.G., Edwards, T.J. et al. Increasing wheat proteins sustainably by rotation with forage legumes. Agron. Sustain. Dev. 43, 56 (2023). https://doi.org/10.1007/s13593-023-00913-9
Accepted:
Published:
DOI: https://doi.org/10.1007/s13593-023-00913-9