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RESEARCH ARTICLE

Harvest index combined with impaired N availability constrains the responsiveness of durum wheat to elevated CO2 concentration and terminal water stress

Gorka Erice A D , Alvaro Sanz-Sáez B E , Amadeo Urdiain A , Jose L. Araus B , Juan José Irigoyen A and Iker Aranjuelo C F
+ Author Affiliations
- Author Affiliations

A Departamento de Biología Vegetal, Sección Biología Vegetal, Facultades de Ciencias y Farmacia, Universidad de Navarra, c/ Irunlarrea 1, Pamplona, Navarra, Spain.

B Departament de Biologia Vegetal, Facultat de Biologia, Universidad de Barcelona, Av. Diagonal, 645 08028 Barcelona, Spain.

C Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, Avenuenida de Pamplona 123, E-31192, Mutilva Baja, Spain.

D Present address: Institute for Genomic Biology, University of Illinois, Urbana-Champaign, 1206 W. Gregory Drive, Urbana, IL 61801, USA.

E Present address: Departments of Plant Biology and Crop Science, University of Illinois, Urbana-Champaign, 1201 W. Gregory Drive, Urbana, IL 61801, USA.

F Corresponding author. Email: iker.aranjuelo@gmail.com

Functional Plant Biology 41(11) 1138-1147 https://doi.org/10.1071/FP14045
Submitted: 7 February 2014  Accepted: 1 August 2014   Published: 11 September 2014

Abstract

Despite its relevance, few studies to date have analysed the role of harvest index (HI) in the responsiveness of wheat (Triticum spp.) to elevated CO2 concentration ([CO2]) under limited water availability. The goal of the present work was to characterise the role of HI in the physiological responsiveness of durum wheat (Triticum durum Desf.) exposed to elevated [CO2] and terminal (i.e. during grain filling) water stress. For this purpose, the performance of wheat plants with high versus low HI (cvv. Sula and Blanqueta, respectively) was assessed under elevated [CO2] (700 μmol mol–1 vs 400 μmol mol–1 CO2) and terminal water stress (imposed after ear emergence) in CO2 greenhouses. Leaf carbohydrate build-up combined with limitations in CO2 diffusion (in droughted plants) limited the responsiveness to elevated [CO2] in both cultivars. Elevated [CO2] only increased wheat yield in fully watered Sula plants, where its larger HI prevented an elevated accumulation of total nonstructural carbohydrates. It is likely that the putative shortened grain filling period in plants exposed to water stress also limited the responsiveness of plants to elevated [CO2]. In summary, our study showed that even under optimal water availability conditions, only plants with a high HI responded to elevated [CO2] with increased plant growth, and that terminal drought constrained the responsiveness of wheat plants to elevated [CO2].

Additional keywords: acclimation, C : N ratio, drought, physiology, Triticum durum.


References

Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155, 64–69.
Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsLo%3D&md5=cf689ba6f8bfa8187892b4b12d3be7a6CAS | 20971857PubMed |

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 | 15720649PubMed |

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. Agricultural and Forest Meteorology 122, 85–94.
Testing the “source–sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max.Crossref | GoogleScholarGoogle Scholar |

Aranjuelo I, Irigoyen JJ, Perez P, Martinez-Carrasco R, Sanchez-Díaz M (2005a) The use of temperature gradient tunnels for studying the combined effect of CO2, temperature and water availability in N2 fixing alfalfa plants. Annals of Applied Biology 146, 51–60.
The use of temperature gradient tunnels for studying the combined effect of CO2, temperature and water availability in N2 fixing alfalfa plants.Crossref | GoogleScholarGoogle Scholar |

Aranjuelo I, Pérez P, Hernández L, Irigoyen JJ, Zita G, Martínez-Carrasco R, Sánchez-Díaz M (2005b) The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. Physiologia Plantarum 123, 348–358.
The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1yhtLk%3D&md5=fd12c96a800a43ff512a29277c25b191CAS |

Aranjuelo I, Irigoyen JJ, Perez P, Martinez-Carrasco R, Sanchez-Díaz M (2006) Response of nodulated alfalfa to water supply, temperature and elevated CO2: productivity and water relations. Environmental and Experimental Botany 55, 130–141.
Response of nodulated alfalfa to water supply, temperature and elevated CO2: productivity and water relations.Crossref | GoogleScholarGoogle Scholar |

Aranjuelo I, Pardo A, Biel C, Savé R, Azcón-Bieto J, Nogués S (2009) Leaf carbon management in slow-growing plants exposed to elevated CO2. Global Change Biology 15, 97–109.
Leaf carbon management in slow-growing plants exposed to elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Aranjuelo I, Cabrera-Bosquet L, Morcuende R, Avice JC, Nogués S, Araus JL, Martínez-Carrasco R, Pérez P (2011) Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? Journal of Experimental Botany 62, 3957–3969.
Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFCqurw%3D&md5=05129ef6c4d87d3586488cc31b2e3e3fCAS | 21511906PubMed |

Aranjuelo I, Sanz-Saez A, 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=74d4cd80c6e94407a74f702b7d7443d3CAS | 23564953PubMed |

Bowes G (1993) Facing the inevitable: Plants and increasing atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 44, 309–332.
Facing the inevitable: Plants and increasing atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFKisbs%3D&md5=63306b9bab21d220ca6369f4b866f4e6CAS |

Bunce JA (2000) Responses of stomatal conductance to light, humidity and temperature in winter wheat and barley grown at three concentrations of carbon dioxide in the field. Global Change Biology 6, 371–382.
Responses of stomatal conductance to light, humidity and temperature in winter wheat and barley grown at three concentrations of carbon dioxide in the field.Crossref | GoogleScholarGoogle 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. Physiologia Plantarum 113, 33–40.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsF2ju7s%3D&md5=53b603ef3dc5854852097fce4532aeaeCAS |

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, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533.
Europe-wide reduction in primary productivity caused by the heat and drought in 2003.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVajs7rL&md5=20f493881df55bce959d0b279629a345CAS | 16177786PubMed |

Dias de Oliveira E, Bramley H, Siddique KHM, Henty S, Berger J, Palta JA (2013) Can elevated CO2 combined with high temperature ameliorate the effect of terminal drought in wheat? Functional Plant Biology 40, 160–171.
Can elevated CO2 combined with high temperature ameliorate the effect of terminal drought in wheat?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Knurg%3D&md5=67b7f451f62c2b72eb6f4318cbd3cae5CAS |

Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. Journal of Cereal Science 38, 133–146.
Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1ertLw%3D&md5=c96c85d7d80a985ff9c0f7f27bf98dadCAS |

European Environmental Agency (2013) Environmental Indicator Report. (European Environmental Agency: Copenhagen). Available online at: http://www.eea.europa.eu/publications/environmental-indicator-report-2013 [Verified 7 August 2014]

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=b0753d90a732e686217d58be94f309baCAS | 24306196PubMed |

Fitzpatrick EA (1970) ‘The expectancy of deficient winter rainfall and the potential for severe drought in the southwest of Western Australia.’ Miscellaneous publication vol. 70/1. (The University of Western Australia, Institute of Agriculture, Agronomy Dept: Perth)

Foulkes MJ, Reynolds MP, Sylvester-Bradley R (2009) Genetic improvement of grain crops: yield potential. In ‘Crop physiology: applications for genetic improvement and agronomy’. (Eds. VO Sadras, DF Calderini) pp. 355–385. (Academic Press: San Diego)

Gallé Á, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2009) Glutethione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit. Journal of Plant Physiology 166, 1878–1891.
Glutethione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit.Crossref | GoogleScholarGoogle Scholar | 19615785PubMed |

Galmés J, Aranjuelo I, Medrano H, Flexas H (2013) Variation in Rubisco content and activity under variable climatic factors. Photosynthesis Research 117, 73–90.
Variation in Rubisco content and activity under variable climatic factors.Crossref | GoogleScholarGoogle Scholar | 23748840PubMed |

Gebbing T, Schnyder H (1999) Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat. Plant Physiology 121, 871–878.
Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12ntLs%3D&md5=127807d645360d239496c716b8c9e8a1CAS | 10557235PubMed |

Gebbing T, Schnyder H, Kühbauch W (1998) Carbon mobilization in shoot parts and roots of wheat during grain filling: assessment by 13C/12C steady-state labelling, growth analysis and balance sheets of reserves. Plant, Cell & Environment 21, 301–313.
Carbon mobilization in shoot parts and roots of wheat during grain filling: assessment by 13C/12C steady-state labelling, growth analysis and balance sheets of reserves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVCjt74%3D&md5=4e9348d52772aff119ecf97419660891CAS |

González FG, Aldabe ML, Terrile II, Rondanini DP (2014) Grain weight response to different postflowering source : sink ratios in modern high-yielding Argentinean wheats differing in spike fruiting efficiency. Crop Science 54, 297–309.
Grain weight response to different postflowering source : sink ratios in modern high-yielding Argentinean wheats differing in spike fruiting efficiency.Crossref | GoogleScholarGoogle Scholar |

Gutiérrez D, Gutiérrez E, Pérez P, Morcuende R, Verdejo AL, Martinez-Carrasco R (2009) Acclimation to future atmospheric CO2 levels increases photochemical efficiency and mitigates photochemistry inhibition by warm temperatures in wheat under field chambers. Physiologia Plantarum 137, 86–100.
Acclimation to future atmospheric CO2 levels increases photochemical efficiency and mitigates photochemistry inhibition by warm temperatures in wheat under field chambers.Crossref | GoogleScholarGoogle Scholar | 19570134PubMed |

Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology 98, 1429–1436.
Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFagu7o%3D&md5=4cfc43014942dc0a87b3a4529d89d8cfCAS | 16668811PubMed |

Henkes S, Sonnewald U, Badur R, Flachmann R, Stitt M (2001) A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. The Plant Cell 13, 535–551.
A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1aktr0%3D&md5=bfe3b307c3ddbe7547c082805a110d24CAS | 11251095PubMed |

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 | 19778369PubMed |

Högy P, Zörb C, Langenkämper G, Betsche T, Fangmeier A (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, 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 |

Idso SB, Kimball BA (1992) Effects of atmospheric CO2 enrichment on photosynthesis, respiration, and growth of sour orange trees. Plant Physiology 99, 341–343.
Effects of atmospheric CO2 enrichment on photosynthesis, respiration, and growth of sour orange trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVCrsbg%3D&md5=b66418ba11962ba322f2a08765caadb1CAS | 16668873PubMed |

Kalina J, Ceulemans R (1997) Clonal differences in the response of dark and light reactions of photosynthesis to elevated atmospheric CO2 in poplar. Photosynthetica 33, 51–61.
Clonal differences in the response of dark and light reactions of photosynthesis to elevated atmospheric CO2 in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisFegsro%3D&md5=860ef995b39b4bc19ecb3649f02ac0dfCAS |

Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations : six lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
Elevated CO2 effects on plant carbon, nitrogen, and water relations : six lessons from FACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtLc%3D&md5=1d49c59efb9e3a5af3c02c27ae2d798aCAS |

Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiology 138, 451–460.
Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks12hs78%3D&md5=de21b1d6bd58ae386870934f0c87150dCAS | 15863701PubMed |

Li A, Hou Y-S, Wall GW, Trent A, Kimball BA, Pinter PJ (2000) Free-air CO2 enrichment and drought stress effects on grain filling rate and duration in spring wheat. Crop Science 40, 1263–1270.
Free-air CO2 enrichment and drought stress effects on grain filling rate and duration in spring wheat.Crossref | GoogleScholarGoogle Scholar |

Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54, 2393–2401.
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVert7s%3D&md5=6c5081f98567fc2577e931b8af85b52dCAS | 14512377PubMed |

Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology 55, 591–628.
Rising atmospheric carbon dioxide: plants FACE the future.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisb8%3D&md5=53f75084d90d0cda55b5f54bf3a4afb6CAS | 15377233PubMed |

Manderscheid R, Weigel HJ (1995) Do increasing atmospheric CO2 concentrations contribute to yield increases of German crops? Journal Agronomy & Crop Science 175, 73–82.
Do increasing atmospheric CO2 concentrations contribute to yield increases of German crops?Crossref | GoogleScholarGoogle Scholar |

Martínez-Carrasco R, Pérez P, Morcuende R (2005) Interactive effects of elevated CO2, temperature and nitrogen on photosynthesis of wheat grown under temperature gradient tunnels. Environmental and Experimental Botany 54, 49–59.
Interactive effects of elevated CO2, temperature and nitrogen on photosynthesis of wheat grown under temperature gradient tunnels.Crossref | GoogleScholarGoogle Scholar |

Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biology 10, 23–36.
Leaf nitrogen remobilisation for plant development and grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslajs70%3D&md5=7a449015f962dbe7f088b526bfe89bfbCAS | 18721309PubMed |

Mitchell RAC, Mitchell VJ, Lawlor DW (2001) Response of wheat canopy CO2 and water gas-exchange to soil water content under ambient and elevated CO2. Global Change Biology 7, 599–611.
Response of wheat canopy CO2 and water gas-exchange to soil water content under ambient and elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Oury F, Godin C, Mailliard A, Chassin A, Gardet O, Giraud A, Heumez E, Morlais J-Y, Rolland B, Rousset M, Trottet M, Charmet G (2012) A study of genetic progress due to selection reveals a negative effect of climate change on bread wheat yield in France. European Journal of Agronomy 40, 28–38.
A study of genetic progress due to selection reveals a negative effect of climate change on bread wheat yield in France.Crossref | GoogleScholarGoogle Scholar |

Passioura JB (1983) Roots and drought resistance. Agricultural Water Management 7, 265–280.
Roots and drought resistance.Crossref | GoogleScholarGoogle Scholar |

Pérez P, Alonso A, Zita G, Morcuende R, Martínez-Carrasco R (2011) Down-regulation of Rubisco activity under combined increases of CO2 and temperature minimized by changes in Rubisco kcat in wheat. Plant Growth Regulation 65, 439–447.
Down-regulation of Rubisco activity under combined increases of CO2 and temperature minimized by changes in Rubisco kcat in wheat.Crossref | GoogleScholarGoogle Scholar |

Pons TL, Flexas J, Von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. Journal of Experimental Botany 60, 2217–2234.
Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitbk%3D&md5=a3c670be065e3fbe4d1870003c744606CAS | 19357431PubMed |

Qiao Y, Zhang H, Dong B, Shi C, Li Y, Zhai H, Liu M (2010) Effects of elevated CO2 concentration on growth and water use efficiency of winter wheat under two soil water regimes. Agricultural Water Management 97, 1742–1748.
Effects of elevated CO2 concentration on growth and water use efficiency of winter wheat under two soil water regimes.Crossref | GoogleScholarGoogle Scholar |

Raines CA (2003) The Calvin cycle revisited. Photosynthesis Research 75, 1–10.
The Calvin cycle revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Kru7o%3D&md5=522e7a41d5d35eb541fa4a0a13c06741CAS | 16245089PubMed |

Rampino P, Mita G, Fasano P, Borrelli GM, Aprile A, Dalessandro G, De Bellis L, Perrotta C (2012) Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiology and Biochemistry 56, 72–78.
Novel durum wheat genes up-regulated in response to a combination of heat and drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVakurY%3D&md5=408753e4ca90ff668b94daeec696fb06CAS | 22609457PubMed |

Rawson HM, Gifford RM, Condon BN (1995) Temperature gradient chambers for research on global environment change. I. Portable chambers for research on short-stature vegetation. Plant, Cell & Environment 18, 1048–1054.
Temperature gradient chambers for research on global environment change. I. Portable chambers for research on short-stature vegetation.Crossref | GoogleScholarGoogle Scholar |

Savin R, Prystupa P, Araus JL (2006) Hordein composition as affected by post-anthesis source–sink ratio under different nitrogen availabilities. Journal of Cereal Science 44, 113–116.
Hordein composition as affected by post-anthesis source–sink ratio under different nitrogen availabilities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlKgu7g%3D&md5=e5f4078d151bd15ce7df577c5b4a1472CAS |

Schütz M, Fangmeier A (2001) Growth and yield responses of spring wheat (Triticum aestivum L. cv. Minaret) to elevated CO2 and water limitation. Environmental Pollution 114, 187–194.
Growth and yield responses of spring wheat (Triticum aestivum L. cv. Minaret) to elevated CO2 and water limitation.Crossref | GoogleScholarGoogle Scholar | 11504341PubMed |

Serrago RA, Alzueta I, Savin R, Slafer GA (2013) Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments. Field Crops Research 150, 42–51.
Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments.Crossref | GoogleScholarGoogle Scholar |

Slafer GA, Savin R (1994) Source–sink relationships and grain mass at different positions within the spike in wheat. Field Crops Research 37, 39–49.
Source–sink relationships and grain mass at different positions within the spike in wheat.Crossref | GoogleScholarGoogle Scholar |

Tamoi M, Nagaoka M, Miyagawa Y, Shigeoka S (2006) Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant & Cell Physiology 47, 380–390.
Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVCltb4%3D&md5=f63a8b78592fee360efcf35589ba6a83CAS |

Theobald JC, Mitchell RAC, Parry MAJ, Lawlor DW (1998) Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase/oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiology 118, 945–955.
Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase/oxygenase in leaves of spring wheat grown under elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFektLo%3D&md5=6ef9d9e7d9152a68fb50ef71ca45cc92CAS | 9808739PubMed |

Uematsu K, Suzuki N, Iwamae T, Inui M, Yukawa H (2012) Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. Journal of Experimental Botany 63, 3001–3009.
Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1emu7w%3D&md5=ecce53b8c541ac7695262466124a05bfCAS | 22323273PubMed |

Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2001) Wheat: water deficit-induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling. Agronomy Journal 93, 196–206.
Wheat: water deficit-induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitl2lsrw%3D&md5=d6df9d23848d3720795c631cbfbef559CAS |

Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst (London) 80, 209–214.
The determination of amino-acids with ninhydrin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXjsFClug%3D%3D&md5=4be6e18c65eac884a279cca9ea2eb6d0CAS |

Zhang D-Y, Chen G-Y, Chen J, Yong Z-H, Zhu J-G, Xu D-Q (2009) Photosynthetic acclimation to CO2 enrichment related to ribulose-1,5-bisphosphate carboxylation limitation in wheat. Photosynthetica 47, 152–154.
Photosynthetic acclimation to CO2 enrichment related to ribulose-1,5-bisphosphate carboxylation limitation in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVaquro%3D&md5=136ba705fc4e88a7e7dd16923749a99cCAS |

Zhang X, Cai J, Wollenweber B, Liu F, Dai T, Cao W, Jiang D (2013) Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat. Journal of Cereal Science 57, 134–140.
Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVWisrnE&md5=8f4a1448b61b5ae51422cbebf3c89193CAS |

Zhu X-G, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiology 145, 513–526.
Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLrF&md5=c9e052734931a0b7fc0158f5153bde9eCAS | 17720759PubMed |

Zhu C, Ziska L, Zhu J, Zeng Q, Xie Z, Tang H, Jia X, Hasegawa T (2012) The temporal and species dynamics of photosynthetic acclimation in flag leaves of rice (Oryza sativa) and wheat (Triticum aestivum) under elevated carbon dioxide. Physiologia Plantarum 145, 395–405.
The temporal and species dynamics of photosynthetic acclimation in flag leaves of rice (Oryza sativa) and wheat (Triticum aestivum) under elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOqsb7M&md5=9a902b1e4527b5c9da6ad8ae2d66ecb8CAS | 22268610PubMed |