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Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE (Open Access)

Elevated field atmospheric CO2 concentrations affect the characteristics of winter wheat (cv. Bologna) grains

Francesca Verrillo A , Franz-Werner Badeck B , Valeria Terzi B G , Fulvia Rizza B , Letizia Bernardo B , Antimo Di Maro C , Clara Fares D , Alessandro Zaldei E , Francesco Miglietta E , Anna Moschella F , Marcella Bracale A and Candida Vannini A
+ Author Affiliations
- Author Affiliations

A Dipartimento Biotecnologie e Scienze della Vita, Università degli Studi dell’Insubria, Via J.H. Dunant 3, 21100 Varese, Italy.

B CREA-GB, Research Centre for Genomics and Bioinformatics, Via San Protaso 302, Fiorenzuola d’Arda, 29017 Piacenza, Italy.

C Dipartimento di Scienze e Tecnologie Ambientali Biologiche e Farmaceutiche, Università degli Studi della Campania ‘Luigi Vanvitelli’, Via Vivaldi 43, 81100 Caserta, Italy.

D CREA-CI, Research Centre for Cereal and Industrial Crops, S.S 16 Km 675, 71121 Foggia, Italy.

E CNR-IBIMET, Istituto di Biometeorologia, Via G. Caproni, 8-50145 Firenze, Italy.

F CREA-CI, Research Centre for Cereal and Industrial Crops, Via di Corticella 133, 40128 Bologna, Italy.

G Corresponding author. Email: valeria.terzi@crea.gov.it

Crop and Pasture Science 68(8) 713-725 https://doi.org/10.1071/CP17156
Submitted: 19 April 2017  Accepted: 6 September 2017   Published: 11 October 2017

Journal Compilation © CSIRO 2017 Open Access CC BY-NC-ND

Abstract

The aim of this study was to investigate the impact of elevated concentration of carbon dioxide (CO2), as expected over coming decades, on yield and quality of winter bread wheat (Triticum aestivum L.). Plants (cv. Bologna) were grown by using the free-air CO2 enrichment (FACE) system at Fiorenzuola d’Arda under ambient (control) and elevated (570 ppm, e[CO2]) CO2 concentrations for two growing seasons. We addressed whether there would be a response of wheat grains to elevated CO2 concentration in terms of the contents of nitrogen (N), micro- and macronutrients, proteins and free amino acids. Under e[CO2], total wheat biomass and grain yield increased in both years of the study. Grain N percentage was reduced under e[CO2], but grain N yield (kg ha–1) was increased. Among macro- and micronutrients, a decrease in zinc concentration was observed. The proteome pattern was significantly different in grains grown at the two different CO2 levels, but the observed changes were highly dependent on interactions with prevailing environmental conditions. Finally, a negative trend was observed in the early germination rates of seeds from plants grown under e[CO2] compared with the controls. The results suggest that the expected increase in CO2 levels and their interactive effects with environmental variables may influence agronomic performance by increasing yield and negatively affecting quality.

Additional keywords: climate change, candidate core proteins, proteomics.


References

Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U, Bracale M, Citterio S (2007) Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environmental and Experimental Botany 59, 381–392.
Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlCnsw%3D%3D&md5=cb835eefe5eb96b25a479244dc71d712CAS |

Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.Crossref | GoogleScholarGoogle Scholar |

Altenbach S, Kothari K (2004) Transcript profiles of genes expressed in endosperm tissue are altered by high temperature during wheat grain development. Cereal Science 40, 115–126.
Transcript profiles of genes expressed in endosperm tissue are altered by high temperature during wheat grain development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslWms7Y%3D&md5=64207d069527341b393864cf47a38ae5CAS |

Arachchige PMS, Ang C-S, Nicolas ME, Panozzo J, Fitzgerald G, Hirotsu N, Seneweera S (2017) Wheat (Triticum aestivum L.) grain proteome response to elevated [CO2] varies between genotypes. Journal of Cereal Science 75, 151–157.
Wheat (Triticum aestivum L.) grain proteome response to elevated [CO2] varies between genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlvFWkt7Y%3D&md5=c97ba6de7f5381f9a9a307bebae8f248CAS |

Aranjuelo I, Sanz-Sáez Á, Jauregui I, Irigoyen JJ, Araus JL, Sánchez-Díaz M, Erice G (2013) Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2. Journal of Experimental Botany 64, 1879–1892.
Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslSltLc%3D&md5=4a7025323a6e9bceaaac4ae1ed10ebdaCAS |

Arp WJ, Van Mierlo JEM, Berendse F, Snijders W (1998) Interactions between elevated CO2 concentration, nitrogen and water: Effects on growth and water use of six perennial plant species. Plant, Cell & Environment 21, 1–11.
Interactions between elevated CO2 concentration, nitrogen and water: Effects on growth and water use of six perennial plant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlCgsLw%3D&md5=f8bd122ea45a2788b3009c4fef309419CAS |

Badeck F-W, Rizza F (2015) A combined field/laboratory method for assessment of frost tolerance with freezing tests and chlorophyll fluorescence. Agronomy 5, 71–88.
A combined field/laboratory method for assessment of frost tolerance with freezing tests and chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |

Bloom A, Burger M, Rubio-Asensio J, Cousins A (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 | 1:CAS:528:DC%2BC3cXlvVeltrc%3D&md5=e3a5ba206d9116cda80f5a37846e3d35CAS |

Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=ec1c81995b5f1a7887c0acb71f446495CAS |

Broberg MC, Högy P, Pleijel H (2017) CO2-induced changes in wheat grain composition: Meta-analysis and response functions. Agronomy 7, 32
CO2-induced changes in wheat grain composition: Meta-analysis and response functions.Crossref | GoogleScholarGoogle Scholar |

Bykova N, Hoehn B, Rampitsch C, Banks T, Stebbing J-A, Fan T, Knox R (2011) Redox-sensitive proteome and antioxidant strategies in wheat seed dormancy control. Proteomics 11, 865–882.
Redox-sensitive proteome and antioxidant strategies in wheat seed dormancy control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitFGkur4%3D&md5=461a19d758588557bcb00ebc9c138ad4CAS |

Cheeseman J (2006) Hydrogen peroxide concentrations in leaves under natural conditions. Journal of Experimental Botany 57, 2435–2444.
Hydrogen peroxide concentrations in leaves under natural conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2lsrY%3D&md5=74a0d08d60bb014de9e92891c5f71d2bCAS |

Chung R, Neumann G, Polya G (1997) Purification and characterization of basic proteins with in vitro antifungal activity from seeds of cotton, Gossypium hirsutum. Plant Science 127, 1–16.
Purification and characterization of basic proteins with in vitro antifungal activity from seeds of cotton, Gossypium hirsutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltFWjtrw%3D&md5=977f1ac22e0a542c963c2e62f5cbef75CAS |

Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissue. Global Change Biology 4, 43–54.
Elevated CO2 reduces the nitrogen concentration of plant tissue.Crossref | GoogleScholarGoogle Scholar |

DaMatta FM, Grandis A, Arenque BC, Buckeridge MS (2010) Impacts of climate changes on crop physiology and food quality. Food Research International 43, 1814–1823.
Impacts of climate changes on crop physiology and food quality.Crossref | GoogleScholarGoogle Scholar |

Donaldson P, Anderson T, Lane B, Davidson A, Simmonds D (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotinia sclerotiorum. Physiological and Molecular Plant Pathology 59, 297–307.
Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotinia sclerotiorum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1Gns74%3D&md5=8d8622c9758ccdc7ad1a88ddea1ea2c0CAS |

Donohue K (2009) Completing the cycle, maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society. B. Biological Science 364, 1059–1074.
Completing the cycle, maternal effects as the missing link in plant life histories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkslGgtrY%3D&md5=fcb0f449c838f5df4784f02978c53115CAS |

Dunwell J, Khuri S, Gane P (2000) Microbial relatives of the seed storage proteins of higher plants, conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiology and Molecular Biology Reviews 64, 153–179.
Microbial relatives of the seed storage proteins of higher plants, conservation of structure and diversification of function during evolution of the cupin superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFygsrw%3D&md5=d141b7e364be1610aab2b51c0aab0d12CAS |

Dupont F, Vensel W, Tanaka C, Hurkman W, Altenbach S (2011) Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry. Proteome Science 9, 10–14.
Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFKktrs%3D&md5=866ab281f9939faf863fe5a7ff7f5a4eCAS |

Erbs M, Manderscheid R, Jansen G, Seddig S, Pacholski A, Weigel H (2010) Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation. Agriculture, Ecosystems & Environment 136, 59–68.
Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGrsr8%3D&md5=2ea048189fbebf4e364634f233c520cdCAS |

Fares C, Menga V, Badeck F, Rizza F, Miglietta F, Zaldei A, Codianni P, Iannucci A, Cattivelli L (2016) Increasing atmospheric CO2 modifies durum wheat grain quality and pasta cooking quality. Journal of Cereal Science 69, 245–251.
Increasing atmospheric CO2 modifies durum wheat grain quality and pasta cooking quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlsF2huro%3D&md5=6fc4cfaa705a543d032bc56a8d81e61fCAS |

Fedorova M, Bollineni R, Hoffmann R (2014) Protein carbonylation as a major hallmark of oxidative damage, Update of analytical strategies. Mass Spectrometry Reviews 33, 79–97.
Protein carbonylation as a major hallmark of oxidative damage, Update of analytical strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFWnsLc%3D&md5=33b097579f86ef714ff86392e8dae613CAS |

Fernando N, Panozzo J, Tausz M, Norton R, Fitzgerald G, Seneweera S (2012a) 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 | 1:CAS:528:DC%2BC38XjtF2hurk%3D&md5=961d2275c006cead3b39ad95dada6f76CAS |

Fernando N, Panozzo J, Tausz M, Norton R, Fitzgerald G, Myers S, Walker C, Stangoulis J, Seneweera S (2012b) Wheat grain quality under increasing atmospheric CO2 concentrations in a semi-arid cropping system. Journal of Cereal Science 56, 684–690.
Wheat grain quality under increasing atmospheric CO2 concentrations in a semi-arid cropping system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yqu7zP&md5=013ba455562ea957bdc9240d1ecaae2dCAS |

Fernando N, Panozzo J, Tausz M, Norton R, Neumann N, Fitzgerald G, 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 | 1:CAS:528:DC%2BC2cXkslSqurs%3D&md5=ec218f01be0c351bc041251eefe8f73fCAS |

Fernando N, Panozzo J, Tausz M, Fitzgerald G, Khan A, Seneweera S (2015) Rising CO2 concentration altered wheat grain proteome and flour rheological characteristics. Food Chemistry 170, 448–454.
Rising CO2 concentration altered wheat grain proteome and flour rheological characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFynsbfJ&md5=6de6c7459e7f835735fe66258f24fce8CAS |

Fernando N, Hirotsu N, Panozzo J, Tausz M, Norton RM, Seneweera S (2017) Lower grain nitrogen content of wheat at elevated CO2 can be improved through post-anthesis NH4 + supplement. Journal of Cereal Science 74, 79–85.
Lower grain nitrogen content of wheat at elevated CO2 can be improved through post-anthesis NH4 + supplement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXislygsr4%3D&md5=e2dd05851e0ba715500102c6929b9819CAS |

Hampton JG, Boelt B, Rolston MP, Chastain TG (2013) Effects of elevated CO2 and temperature on seed quality. The Journal of Agricultural Science 151, 154–162.
Effects of elevated CO2 and temperature on seed quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvVaqsbY%3D&md5=ebb75b150416da8dd794a91cff08735bCAS |

Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. Journal of Cereal Science 48, 580–591.
Effects of elevated atmospheric CO2 on grain quality of wheat.Crossref | GoogleScholarGoogle Scholar |

Högy P, Wieser H, Köhler P, Schwadorf K, Breuer J, Franzaring J, Muntifering R, Fangmeier A (2009a) 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 |

Högy P, Zörb C, Langenkämper G (2009b) Atmospheric CO2 enrichment changes the wheat grain proteome. Journal of Cereal Science 50, 248–254.
Atmospheric CO2 enrichment changes the wheat grain proteome.Crossref | GoogleScholarGoogle Scholar |

Högy P, Wieser H, Köhler P, Schwadorf K, Breuer J, Erbs M, Weber S, Fangmeier A (2009c) Does elevated atmospheric CO2 allow for sufficient wheat grain quality in the future? Journal of Applied Botany and Food Quality 82, 114–121.

Högy P, Keck M, Niehaus K, Franzaring J, Fangmeier A (2010) Effects of atmospheric CO2 enrichment on biomass, yield and low molecular weight metabolites in wheat grain. Journal of Cereal Science 52, 215–220.
Effects of atmospheric CO2 enrichment on biomass, yield and low molecular weight metabolites in wheat grain.Crossref | GoogleScholarGoogle Scholar |

Huxman TE, Hamerlynck EP, Jordan DN, Salsman KJ, Smith SD (1998) The effects of parental CO2 environment on seed quality and subsequent seedling performance in Bromus rubens. Oecologia 114, 202–208.
The effects of parental CO2 environment on seed quality and subsequent seedling performance in Bromus rubens.Crossref | GoogleScholarGoogle Scholar |

IPCC (2013) ‘Climate Change 2013: The physical science basis.’ Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Eds TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley) (Cambridge University Press: Cambridge, UK)

Iriti M, Di Maro A, Bernasconi S, Burlini N, Simonetti P, Picchi V, Panigada C, Gerosa G, Parente A, Faoro F (2009) Nutritional traits of bean (Phaseolus vulgaris) seeds from plants chronically exposed to ozone pollution. Journal of Agricultural and Food Chemistry 57, 201–208.
Nutritional traits of bean (Phaseolus vulgaris) seeds from plants chronically exposed to ozone pollution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKmt7bK&md5=45e8b66a71624622a9484fe10acf690aCAS |

Kimball B, LaMorte R, Pinter P, Wall G, Hunsaker D, Adamsen F, Leavitt S, Thompson T, Matthias A, Brooks T (1999) Free-air CO2 enrichment and soil nitrogen effects on energy balance and evapotranspiration of wheat. Water Research 35, 1179–1190.
Free-air CO2 enrichment and soil nitrogen effects on energy balance and evapotranspiration of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVCitrs%3D&md5=eca9708b029de9131e440af257d6b0b6CAS |

Kimball K, Morris C, Pinter P, Wall G, Hunsaker D, Adamsen F, LaMorte R, Leavitt S, Thompson T, Matthias A, Brooks T (2001) Elevated CO2, drought and soil nitrogen effects on wheat grain quality. New Phytologist 150, 295–303.
Elevated CO2, drought and soil nitrogen effects on wheat grain quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVegsro%3D&md5=464327159c796c07dd4c9aec5c597007CAS |

Koziol A, Loit E, McNulty M, Loit A, McNulty M, MacFarlane A, Scott F, Altosaar I (2012) Seed storage proteins of the globulin family are cleaved post-translationally in wheat embryos. BMC Research Notes 5, 385–395.
Seed storage proteins of the globulin family are cleaved post-translationally in wheat embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKjsbfN&md5=b6f02e5ab3ff1746ad9fbf83bd5e60ceCAS |

Laino P, Shelton D, Finnie C, De Leonardis A, Mastrangelo A, Svensson B, Lafiandra D, Masci S (2010) Comparative proteome analysis of metabolic proteins from seeds of durum wheat (cv. Svevo) subjected to heat stress. Proteomics 10, 2359–2368.
Comparative proteome analysis of metabolic proteins from seeds of durum wheat (cv. Svevo) subjected to heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns1CrtLo%3D&md5=a85b666f1533931d81695c4d7c1f2138CAS |

Lane B (2002) Oxalate, germins, and higher-plant pathogens. IUBMB Life 53, 67–75.
Oxalate, germins, and higher-plant pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlGis7c%3D&md5=d24ff0f378bd8cdf7ae8cf17b3a9bfb2CAS |

Levine R, Williams J, Stadtman E, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology 233, 346–357.
Carbonyl assays for determination of oxidatively modified proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1GgtLw%3D&md5=b41099d863d81c3049eb7dcb4f425213CAS |

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 |

Macedo M, Andrade L, Moraes R, Xavier-Filho J (1993) Vicilin variants and the resistance of cowpea (Vigna unguiculata) seeds to the cowpea weevil (Callosobruchus maculatus). Comparative Biochemistry and Physiology 105, 89–94.

Marcus J, Green J, Goulter K, Manners J (1999) A family of antimicrobial peptides is produced by processing of a 7S globulin protein in Macadamia integrifolia kernels. The Plant Journal 19, 699–710.
A family of antimicrobial peptides is produced by processing of a 7S globulin protein in Macadamia integrifolia kernels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFOnsbo%3D&md5=1125ce8aa78960d82a8c737e4ed8593cCAS |

Marsoni M, Bracale M, Espen L, Prinsi B, Negri S, Vannini C (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Reports 27, 347–356.
Proteomic analysis of somatic embryogenesis in Vitis vinifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosFWjsQ%3D%3D&md5=07ef9e640b02f8fdc569603075b13165CAS |

Moore S, Stein W (1963) Chromatographic determination of amino acids by the use of automatic recording equipment. Methods in Enzymology 6, 819–831.
Chromatographic determination of amino acids by the use of automatic recording equipment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKrs7Y%3D&md5=9cf8a4b09e876153c3259a442dce2624CAS |

Myers S, Zanobetti A, Kloog I, Huybers P, Leakey A, Bloom A, Carlisle E, Dietterich L, Fitzgerald G, Hasegawa T, Holbrook M, Nelson R, Ottman M, Raboy V, Sakai H, Sartor K, 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 | 1:CAS:528:DC%2BC2cXhtFygsrfE&md5=ff4c00f8bfc15c0e62e72dac0205f622CAS |

Naudts K, Van den Berge J, Farfan E, Rose P, AbdElgawad H, Ceulemans R, Janssens IA, Asard H, Nijs I (2014) Future climate alleviates stress impact on grassland productivity through altered antioxidant capacity. Environmental and Experimental Botany 99, 150–158.
Future climate alleviates stress impact on grassland productivity through altered antioxidant capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislGqsr0%3D&md5=1463a57da28e05f490e01084dc72b113CAS |

Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist 162, 253–280.
Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions?Crossref | GoogleScholarGoogle Scholar |

Nuttall JG, O’Leary GJ, Panozzo JF, Walkea CK, Barlow KM, Fitzgerald GJ (2017) Models of grain quality in wheat—A review. Field Crops Research 202, 136–145.
Models of grain quality in wheat—A review.Crossref | GoogleScholarGoogle Scholar |

O’Leary GJ, Christy B, Nuttall J, Huth N, Cammarano D, Stöckle C, Basso B, Shcherbak I, Fitzgerald G, Luo Q, Farre-Codina I, Palta J, Asseng S (2015) Response of wheat growth, grain yield and water use to elevated CO2 under a Free-Air CO2 Enrichment (FACE) experiment and modelling in a semi-arid environment. Global Change Biology 21, 2670–2686.
Response of wheat growth, grain yield and water use to elevated CO2 under a Free-Air CO2 Enrichment (FACE) experiment and modelling in a semi-arid environment.Crossref | GoogleScholarGoogle Scholar |

Panozzo J, Walker CK, Partington DL, Neumann NC, Tausz M, Seneweera S, Fitzgerald GL (2014) Elevated carbon dioxide changes grain protein concentration and composition and compromises baking quality. A FACE study. Journal of Cereal Science 60, 461–470.
Elevated carbon dioxide changes grain protein concentration and composition and compromises baking quality. A FACE study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslyksrbO&md5=01ede2c0ef051eb6772f05cec259e194CAS |

Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J (2011) Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant & Cell Physiology 52, 490–508.
Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivVOnsLY%3D&md5=c97903a0dfb3f22132d690af131223ccCAS |

Persson J, Gardeström P, Näsholm T (2006) Uptake metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. Journal of Experimental Botany 57, 2651–2659.
Uptake metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2mtL4%3D&md5=ac4f6a1c27b3c0d8100c2a5b850cf43eCAS |

Pompa M, Giuliani M, Palermo C, Agriesti F, Centonze D, Flagella Z (2013) Comparative analysis of gluten proteins in three durum wheat cultivars by a proteomic approach. Journal of Agricultural and Food Chemistry 61, 2606–2617.
Comparative analysis of gluten proteins in three durum wheat cultivars by a proteomic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Sltb8%3D&md5=d79c09d6104be7483a6f24e4d50ff3a1CAS |

Qiu Q, Huber J, Booker F, Jain V, Leakey A, Fiscus E, Yau P, Ort D, Huber S (2008) Increased protein carbonylation in leaves of Arabidopsis and soybean in response to elevated [CO2]. Photosynthesis Research 97, 155–166.
Increased protein carbonylation in leaves of Arabidopsis and soybean in response to elevated [CO2].Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovF2iu70%3D&md5=59d4b291dabb1296ec6b70609138641aCAS |

Sancho A, Gillabert M, Tapp H, Shewry P, Skegg P, Mills E (2008) Effect of environmental stress during grain filling on the soluble proteome of wheat (Triticum aestivum) dough liquor. Journal of Agricultural and Food Chemistry 56, 5386–5393.
Effect of environmental stress during grain filling on the soluble proteome of wheat (Triticum aestivum) dough liquor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Cltr0%3D&md5=f1a3137715bf9ba6b592e7ef72f7189eCAS |

Singh J, Blundell M, Tanner H, Skerritt J (2001) Albumin and globulin proteins of wheat flour, immunological and N-terminal sequence characterization. Journal of Cereal Science 34, 85–103.
Albumin and globulin proteins of wheat flour, immunological and N-terminal sequence characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFOqtL4%3D&md5=012d44602da0a6001c033b4cc65b76d4CAS |

Taub D, Wang X (2008) Why are nitrogen concentrations in plant tissue lower under CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology 50, 1365–1374.
Why are nitrogen concentrations in plant tissue lower under CO2? A critical examination of the hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltb7M&md5=a68a94e0ee920bf2b713c94d9fd33908CAS |

Tausz M, Tausz-Posch S, Norton G, Fitzgerald J, Nicolas M, Seneweera S (2013) Understanding crop physiology to select breeding targets and improve crop management under increasing atmospheric CO2 concentrations. Environmental and Experimental Botany 88, 71–80.
Understanding crop physiology to select breeding targets and improve crop management under increasing atmospheric CO2 concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslWkur4%3D&md5=d7fe4dd48b2c485a847e700ba8142791CAS |

Thürig B, Körner C, Stöcklin J (2003) Seed production and seed quality in a calcareous grassland in elevated CO2. Global Change Biology 9, 873–884.
Seed production and seed quality in a calcareous grassland in elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Wang W, Vignani R, Scali M, Cresti M (2006) Universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27, 2782–2786.
Universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnslCnt7w%3D&md5=2f1be81a830f53f0b1d497f83ce74a2bCAS |

Wieser H, Manderscheid R, Erbs M, Weigel H (2008) Effects of elevated atmospheric CO2 concentrations on the quantitative protein composition of wheat grain. Agriculture and Food Chemistry 56, 6531–6535.
Effects of elevated atmospheric CO2 concentrations on the quantitative protein composition of wheat grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotFGqtb8%3D&md5=d37c2f0b9a4b8b6d4b22b879898b1374CAS |

Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Frontiers in Plant Science 6, 534
Physiological implications of arginine metabolism in plants.Crossref | GoogleScholarGoogle Scholar |

Yamada K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I (1999) Multiple functional proteins are produced by cleaving Asn–Gln bonds of a single precursor by vacuolar processing enzyme. The Journal of Biological Chemistry 274, 2563–2570.
Multiple functional proteins are produced by cleaving Asn–Gln bonds of a single precursor by vacuolar processing enzyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXovVKjsQ%3D%3D&md5=c03d122ffdc2b7ce272731b3d0096cbeCAS |

Zheng ZL (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signaling & Behavior 4, 584–591.
Carbon and nitrogen nutrient balance signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGmsbjF&md5=4ee3361c7cc479fd5eb879ad5b880fcdCAS |