Grain mineral quality of dryland legumes as affected by elevated CO2 and drought: a FACE study on lentil (Lens culinaris) and faba bean (Vicia faba)
Shahnaj Parvin A B J , Shihab Uddin B C D , Sabine Tausz-Posch D F I , Roger Armstrong E G , Glenn Fitzgerald D E and Michael Tausz H IA School of Ecosystem and Forest Sciences, The University of Melbourne, Creswick, Vic. 3363, Australia.
B Department of Agronomy, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh.
C NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, PMB Pine Gully Road, Wagga Wagga, NSW 2650, Australia.
D Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Creswick, Vic. 3363, Australia.
E Department of Economic Development, Jobs, Transport and Resources, Horsham, Vic. 3400, Australia.
F School of Biosciences, University of Birmingham, Edgbaston B15 2TT, UK.
G Department of Animal, Plant and Soil Sciences, La Trobe University, Bundoora, Vic. 3086, Australia.
H Birmingham Institute of Forest Research, University of Birmingham, Edgbaston B15 2TT, UK.
I Department of Agriculture, Science and Environment, School of Health and Applied Sciences, CQUniversity Australia, Rockhampton, QLD, Australia.
J Corresponding author. Email: sparvin@student.unimelb.edu.au
Crop and Pasture Science 70(3) 244-253 https://doi.org/10.1071/CP18421
Submitted: 11 September 2018 Accepted: 5 February 2019 Published: 14 March 2019
Abstract
Stimulation of grain yield under elevated [CO2] grown plants is often associated with the deterioration of grain quality. This effect may be further complicated by the frequent occurrence of drought, as predicted in most of the climate change scenarios. Lentil (Lens culinaris Medik.) and faba bean (Vicia faba L.) were grown in the Australian Grains Free Air CO2 Enrichment facility under either ambient CO2 concentration ([CO2], ~400 µmol mol–1) or elevated [CO2] (e[CO2], ~550 µmol mol–1), and with two contrasting watering regimes (for faba bean) or over two consecutive seasons contrasting in rainfall (for lentil), to investigate the interactive effect of e[CO2] and drought on concentrations of selected grain minerals (Fe, Zn, Ca, Mg, P, K, S, Cu, Mn, Na). Grain mineral concentration (Fe, Zn, Ca, K, S, Cu) increased and grain mineral yield (i.e. g mineral per plot surface area) decreased in dry growing environments, and vice versa in wet growing environments. Elevated [CO2] decreased Fe, Zn, P and S concentrations in both crops; however, the relative decrease was greater under dry (20–25%) than wet (4–10%) growing conditions. Principal component analysis showed that greater grain yield stimulation under e[CO2] was associated with a reduction in Fe and Zn concentrations, indicating a yield dilution effect, but this was not consistently observed for other minerals. Even if energy intake is kept constant to adjust for lower yields, decreased legume micronutrients densities under e[CO2] may have negative consequences for human nutrition, especially under drier conditions and in areas with less access to food.
Additional keywords: climate change, dry environments, grain legumes, nutritional quality.
References
Baslam M, Antolín MC, Gogorcena Y, Muñoz F, Goicoechea N (2014) Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2. Annals of Applied Biology 164, 190–199.| Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar |
Bourgault M, Brand J, Tausz M, Fitzgerals 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 Crops Research 196, 1–9.
| Yield, growth and grain nitrogen response to elevated CO2 of five field pea (Pisum sativum L.) cultivars in a low rainfall environment.Crossref | GoogleScholarGoogle Scholar |
Bourgault M, Brand J, Tausz-Posch S, Armstrong RD, O’Leary GL, Fitzgerald GJ, Tausz M (2017) Yield, growth and grain nitrogen response to elevated CO2 in six lentil (Lens culinaris) cultivars grown under Free Air CO2 Enrichment (FACE) in a semi-arid environment. European Journal of Agronomy 87, 50–58.
| Yield, growth and grain nitrogen response to elevated CO2 in six lentil (Lens culinaris) cultivars grown under Free Air CO2 Enrichment (FACE) in a semi-arid environment.Crossref | GoogleScholarGoogle Scholar |
Bourgault M, Löw M, Tausz-Posch S, Nuttall JG, Delahunty AJ, Brand J, Panozzo JF, McDonald L, O’Leary GJ, Armstrong RD, Fitzgerald GJ, Tausz M (2018) Effect of a heat wave on lentil grown under free-air CO2 enrichment (FACE) in a semi-arid environment. Crop Science 58, 803–812.
| Effect of a heat wave on lentil grown under free-air CO2 enrichment (FACE) in a semi-arid environment.Crossref | GoogleScholarGoogle 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 and Soil 391, 367–382.
Delahunty A, Nuttall J, Nicolas M, Brand J (2018) Response of lentil to high temperature under variable water supply and carbon dioxide enrichment. Crop & Pasture Science 69, 1103–1112.
| Response of lentil to high temperature under variable water supply and carbon dioxide enrichment.Crossref | GoogleScholarGoogle Scholar |
Denton MD, Phillips LA, Peoples MB, Pearce DJ, Swan AD, Mele PM, Brockwell J (2017) Legume inoculant application methods: effects on nodulation patterns, nitrogen fixation, crop growth and yield in narrow-leaf lupin and faba bean. Plant and Soil 419, 25–39.
| Legume inoculant application methods: effects on nodulation patterns, nitrogen fixation, crop growth and yield in narrow-leaf lupin and faba bean.Crossref | GoogleScholarGoogle Scholar |
Erbs M, Manderscheid R, Huther L, Schenderlein A, Wieser H, Danicke S, Weigel HJ (2015) Free-air CO2 enrichment modifies maize quality only under drought stress. Agronomy for Sustainable Development 35, 203–212.
| Free-air CO2 enrichment modifies maize quality only under drought stress.Crossref | GoogleScholarGoogle Scholar |
Erskine W, Sarker A, Kumar S (2011) Crops that feed the world 3. Investing in lentil improvement toward a food secure world. Food Security 3, 127–139.
| Crops that feed the world 3. Investing in lentil improvement toward a food secure world.Crossref | GoogleScholarGoogle Scholar |
Etienne P, Diquelou S, Prudent M, Salon C, Maillard A, Ourry A (2018) Macro and micronutrient storage in plants and their remobilization when facing scarcity: The case of drought. Agriculture-Basel 8.
FAO (2016) FAOSTAT—food and agriculture data. Food and Agriculture Organization of the United Nations, Rome.
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2017) Drought stress in grain legumes during reproduction and grain filling. Journal of Agronomy & Crop Science 203, 81–102.
| Drought stress in grain legumes during reproduction and grain filling.Crossref | GoogleScholarGoogle 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. Global Change Biology 21, 3152–3168.
| Constraints to nitrogen acquisition of terrestrial plants under elevated CO2.Crossref | GoogleScholarGoogle Scholar |
Fernando N, Panozzo J, Tausz M, Norton R, Fitzgerald G, Seneweera S (2012) Rising atmospheric CO2 concentration affects mineral nutrient and protein concentration of wheat grain. Food Chemistry 133, 1307–1311.
| Rising atmospheric CO2 concentration affects mineral nutrient and protein concentration of wheat grain.Crossref | GoogleScholarGoogle Scholar |
Fernando N, Panozzo J, Tausz M, Norton RM, Neumann N, Fitzgerald GJ, Seneweera S (2014) Elevated CO2 alters grain quality of two bread wheat cultivars grown under different environmental conditions. Agriculture, Ecosystems & Environment 185, 24–33.
| Elevated CO2 alters grain quality of two bread wheat cultivars grown under different environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Gavito ME, Curtis PS, Mikkelsen TN, Jakobsen I (2001) Interactive effects of soil temperature, atmospheric carbon dioxide and soil N on root development, biomass and nutrient uptake of winter wheat during vegetative growth. Journal of Experimental Botany 52, 1913–1923.
| Interactive effects of soil temperature, atmospheric carbon dioxide and soil N on root development, biomass and nutrient uptake of winter wheat during vegetative growth.Crossref | GoogleScholarGoogle Scholar | 11520880PubMed |
Goicoechea N, Bettoni MM, Fuertes-Mendizabal T, Gonzalez-Murua C, Aranjuelo I (2016) Durum wheat quality traits affected by mycorrhizal inoculation, water availability and atmospheric CO2 concentration. Crop & Pasture Science 67, 147–155.
| Durum wheat quality traits affected by mycorrhizal inoculation, water availability and atmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar |
Gray SB, Strellner RS, Puthuval KK, Ng C, Shulman RE, Siebers MH, Rogers A, Leakey ADB (2013) Minirhizotron imaging reveals that nodulation of field grown soybean is enhanced by free air CO2 enrichment only when combined with drought stress. Functional Plant Biology 40, 137–147.
| Minirhizotron imaging reveals that nodulation of field grown soybean is enhanced by free air CO2 enrichment only when combined with drought stress.Crossref | GoogleScholarGoogle 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. Nature Plants 2, art no. 16132
| Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean.Crossref | GoogleScholarGoogle Scholar | 27595230PubMed |
Guzmán C, Autrique JE, Mondal S, Singh RP, Govindan V, Morales-Dorantes A, Posadas , Romano G, Crossa J, Ammar K, Peña RJ (2016) Response to drought and heat stress on wheat quality, with special emphasis on bread-making quality, in durum wheat. Field Crops Research 186, 157–165.
| Response to drought and heat stress on wheat quality, with special emphasis on bread-making quality, in durum wheat.Crossref | GoogleScholarGoogle Scholar |
Heinemann AB, Maia AD, Dourado Neto D, Ingram KT, Hoogenboom C (2006) Soybean (Glycine max (L.) Merr.) growth and development response to CO2 enrichment under different temperature regimes. European Journal of Agronomy 24, 52–61.
| Soybean (Glycine max (L.) Merr.) growth and development response to CO2 enrichment under different temperature regimes.Crossref | GoogleScholarGoogle Scholar |
Hepper CM (1975) Extracellular polysaccharides of soil bacteria. In ‘Soil microbiology: a critical review’. (Ed. N Walker) pp. 93–111. (Wiley: New York)
Högy P, Wieser H, Koehler P, Schwadorf K, Breuer J, Franzaring J, Muntifering R, Fangmeier A (2009) Effects of elevated CO2 on grain yield and quality of wheat: results from a 3-year free-air CO2 enrichment experiment. Plant Biology 11, 60–69.
| Effects of elevated CO2 on grain yield and quality of wheat: results from a 3-year free-air CO2 enrichment experiment.Crossref | GoogleScholarGoogle Scholar | 19778369PubMed |
Högy P, Brunnbauer M, Koehler P, Schwadorf K, Breuer J, Franzaring J, Zhunusbayeva D, Fangmeier A (2013) Grain quality characteristics of spring wheat (Triticum aestivum) as affected by free-air CO2 enrichment. Environmental and Experimental Botany 88, 11–18.
| Grain quality characteristics of spring wheat (Triticum aestivum) as affected by free-air CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |
Houshmandfar A, Fitzgerald GJ, O’Leary G, Tausz-Posch S, Fletcher A, Tausz M (2018) The relationship between transpiration and nutrient uptake in wheat changes under elevated atmospheric CO2. Physiologia Plantarum 163, 516–529.
| The relationship between transpiration and nutrient uptake in wheat changes under elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 29205382PubMed |
Hu YC, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science 168, 541–549.
| Drought and salinity: a comparison of their effects on mineral nutrition of plants.Crossref | GoogleScholarGoogle 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. (Eds Core Writing Team, RK Pachauri, LA Meyer) (IPCC: Geneva)
Isbell RF (2002) ‘The Australian Soil Classification.’ (CSIRO Publishing: Melbourne)
Kumssa DB, Joy EJM, Ander EL, Watts MJ, Young SD, Walker S, Broadley MR (2015) Dietary calcium and zinc deficiency risks are decreasing but remain prevalent. Scientific Reports 5, 10974
| Dietary calcium and zinc deficiency risks are decreasing but remain prevalent.Crossref | GoogleScholarGoogle Scholar | 26098577PubMed |
Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends in Ecology & Evolution 17, 457–461.
| Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry?Crossref | GoogleScholarGoogle Scholar |
Loladze I (2014) Hidden shift of the ionome of plants exposed to elevated CO2 depletes minerals at the base of human nutrition. eLife 3,
Mahrookashani A, Siebert S, Huging H, Ewert F (2017) Independent and combined effects of high temperature and drought stress around anthesis on wheat. Journal of Agronomy & Crop Science 203, 453–463.
| Independent and combined effects of high temperature and drought stress around anthesis on wheat.Crossref | GoogleScholarGoogle Scholar |
Maillard A, Etienne P, Diquélou S, Trouverie J, Billard V, Yvin J-C, Ourry A (2016) Nutrient deficiencies modify the ionomic composition of plant tissues: a focus on cross-talk between molybdenum and other nutrients in Brassica napus. Journal of Experimental Botany 67, 5631–5641.
| Nutrient deficiencies modify the ionomic composition of plant tissues: a focus on cross-talk between molybdenum and other nutrients in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 27625417PubMed |
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 & Environment 36, 697–705.
| Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO2 concentrations.Crossref | GoogleScholarGoogle Scholar |
Mollah M, Norton R, Huzzey J (2009) Australian grains free-air carbon dioxide enrichment (AGFACE) facility: design and performance. Crop & Pasture Science 60, 697–707.
| Australian grains free-air carbon dioxide enrichment (AGFACE) facility: design and performance.Crossref | GoogleScholarGoogle 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 Science 62, 883–891.
| Understand distribution of carbon dioxide to interpret crop growth data: Australian grains free-air carbon dioxide enrichment experiment.Crossref | GoogleScholarGoogle Scholar |
Multari S, Stewart D, Russell WR (2015) Potential of fava bean as future protein supply to partially replace meat intake in the human diet. Comprehensive Reviews in Food Science and Food Safety 14, 511–522.
| Potential of fava bean as future protein supply to partially replace meat intake in the human diet.Crossref | GoogleScholarGoogle Scholar |
Murphy KM, Reeves PG, Jones SS (2008) Relationship between yield and mineral nutrient concentrations in historical and modern spring wheat cultivars. Euphytica 163, 381–390.
| Relationship between yield and mineral nutrient concentrations in historical and modern spring wheat cultivars.Crossref | GoogleScholarGoogle Scholar |
Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey ADB, Bloom AJ, Carlisle E, Dietterich LH, Fitzgerald G, Hasegawa T, Holbrook NM, Nelson RL, Ottman MJ, Raboy V, Sakai H, Sartor KA, Schwartz J, Seneweera S, Tausz M, Usui Y (2014) Increasing CO2 threatens human nutrition. Nature 510, 139–142.
| Increasing CO2 threatens human nutrition.Crossref | GoogleScholarGoogle Scholar | 24805231PubMed |
Myers SS, Wessells KR, Kloog I, Zanobetti A, Schwartz J (2015) Effect of increased concentrations of atmospheric carbon dioxide on the global threat of zinc deficiency: a modelling study. The Lancet. Global Health 3, e639–e645.
| Effect of increased concentrations of atmospheric carbon dioxide on the global threat of zinc deficiency: a modelling study.Crossref | GoogleScholarGoogle Scholar | 26189102PubMed |
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-year free-air CO2 enrichment study on lentil (Lens culinaris MEDIK.) in a water limited agroecosystem. Plant, Cell & Environment 41, 2418–2434.
| Water availability moderates N2 fixation benefit from elevated [CO2]: a 2-year free-air CO2 enrichment study on lentil (Lens culinaris MEDIK.) in a water limited agroecosystem.Crossref | GoogleScholarGoogle Scholar |
Pinheiro J, Bates D, DebRoy S, Sarkar D, and Team RC (2017) nlme: Linear and Nonlinear Mixed Effects Models. R package, version 3.1–131. The R Foundation, Vienna. Available at: https://CRAN.R-project.org/package=nlme
Poorter H, VanBerkel Y, Baxter R, DenHertog J, Dijkstra P, Gifford RM, Griffin KL, Roumet C, Roy J, Wong SC (1997) The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant, Cell & Environment 20, 472–482.
| The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species.Crossref | GoogleScholarGoogle 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 Research 49, 389–407.
| Modelling and prediction of soil water contents at field capacity and permanent wilting point of dryland cropping soils.Crossref | GoogleScholarGoogle 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 & Environment 29, 1651–1658.
| Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Vera UM, Siebers M, Gray SB, Drag DW, Rosenthal DM, Kimball BA, Ort DR, Bernacchi CJ (2013) Global warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the Midwestern United States. Plant Physiology 162, 410–423.
| Global warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the Midwestern United States.Crossref | GoogleScholarGoogle Scholar | 23512883PubMed |
Sehgal A, Sita K, Kumar J, Kumar S, Singh S, Siddique KHM, Nayyar H (2017) Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity. Frontiers of Plant Science 8, 1776
| Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity.Crossref | GoogleScholarGoogle Scholar |
Smith MR, Myers SS (2018) Impact of anthropogenic CO2 emissions on global human nutrition. Nature Climate Change 8, 834–839.
| Impact of anthropogenic CO2 emissions on global human nutrition.Crossref | GoogleScholarGoogle Scholar |
Stefaniak T, McPhee K (2015) Lentil. In ‘Grain legumes. Handbook of plant breeding’. Vol. 10. (Ed. A De Ron) (Springer-Verlag: New York)
Vurukonda SSKP, Vardharajula S, Shrivastava M, Ali SkZ (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research 184, 13–24.
| Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria.Crossref | GoogleScholarGoogle Scholar |
Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric-acid digestion and multielement analysis of plant-material by inductively coupled plasma spectrometry. Communications in Soil Science and Plant Analysis 18, 131–146.
| Nitric-acid digestion and multielement analysis of plant-material by inductively coupled plasma spectrometry.Crossref | GoogleScholarGoogle Scholar |