Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO 2?

Journal of Experimental Botany

Volumn 62, Issue 11, 2011, Pages 3957-3969

  Aranjuelo, Iker ^a,b   Cabrera Bosquet, Lloren ^b   Morcuende, Rosa ^d   Avice, Jean Christophe ^c   Nogués, Salvador ^b   Araus, José Luis ^b,e   Martínez Carrasco, Rafael ^d   Pérez, Pilar ^d  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITÉ DE CAEN   (France)

^d INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^e INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

Author keywords

C management; elevated CO 2; photosynthetic acclimation; proteomic characterization; Rubisco; stable isotopes

Indexed keywords

AMINO ACID; CARBON; CARBON DIOXIDE; NITROGEN; PHOSPHOGLYCERATE MUTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RCA PROTEIN, PLANT; RIBULOSEBISPHOSPHATE CARBOXYLASE; STARCH; VEGETABLE PROTEIN;

ACCLIMATIZATION; ARTICLE; BIOMASS; CELL RESPIRATION; CEREAL; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PLANT LEAF; WHEAT;

ACCLIMATIZATION; AMINO ACIDS; BIOMASS; CARBON; CARBON DIOXIDE; CARBON ISOTOPES; CELL RESPIRATION; CEREALS; GENE EXPRESSION REGULATION, PLANT; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; NITROGEN; PHOSPHOGLYCERATE MUTASE; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; RIBULOSE-BISPHOSPHATE CARBOXYLASE; STARCH; TRITICUM;

TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 79960534181     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err095     Document Type: Article

References (79)

1. Ainsworth EA, Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351-372. (Pubitemid 40177950)
2. Ainsworth EA, Rogers A. 2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell and Environment 30, 258-270. (Pubitemid 46184429)
3. 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. (Pubitemid 38362134)
4. Alonso A, Pérez P, Martínez-Carrasco R. 2009. Growth in elevated CO2 enhances temperature response of photosynthesis in wheat. Physiologia Plantarum 135, 109-120.
5. Amthor JS. 2001. Effects of atmospheric CO2 concentration on wheat yield: review or results from experiments using various approaches to control CO2 concentration. Field Crop Research 73, 1-34. (Pubitemid 32961600)
6. Aranjuelo I, Cabrera-Bosquet LL Mottaleb SA, Araus JL, Nogués S. 2009a. 13C/12C isotope labeling to study carbon partitioning and dark respiration in cereals subjected to water stress. Rapid Communication in Mass Spectrometry 23, 2819-2828.
7. Aranjuelo I, Irigoyen JJ, Pérez P, Martínez-Carrasco R, Sánchez-Díaz M. 2005a. The use of temperature gradient greenhouses for studying the combined effect of CO2, temperature and water availability in N2 fixing alfalfa plants. Annals of Applied Biology 146, 51-60. (Pubitemid 40218319)
8. Aranjuelo I, Irigoyen JJ, Sánchez-Díaz M, Nogués S. 2008. Carbon partitioning in N2 fixing Medicago sativa plants exposed to different CO2 and temperature conditions. Functional Plant Biology 35, 306-317. (Pubitemid 351785617)
9. Aranjuelo I, Molero G, Erice G, Avice JC, Nogués S. 2011. Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). Journal of Experimental Botany 62, 111-123.
10. Aranjuelo I, Pardo T, Biel C, SavéR, Azcón-Bieto J, Nogués S. 2009b. Leaf carbon management in slow-growing plants exposed to elevated CO2. Global Change Biology 15, 97-109.
11. Aranjuelo I, Zita G, Hernandez L, Pérez P, Martínez- Carrasco R, Sánchez-Díaz M. 2005b. Response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. Physiologia Plantarum 123, 348-358. (Pubitemid 40398692)
12. Araus JL, Brown HR, Febrero A, Bort J, Serret MD. 1993. Ear photosynthesis, carbon isotope discrimination and the contribution of respiratory CO2 to differences in grain mass in durum wheat. Plant, Cell and Environment 16, 383-392.
13. Batz O, Scheibe R, Neuhaus EH. 1992. Transport processes and corresponding changes in metabolite levels in relation to starch synthesis in barley (Hordeum vulgare L.) etioplasts. Plant Physiology 100, 184-190.
14. Bevan M, Bancroft I, Bent E, et al. 1998. Analysis of 19 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391, 485-488. (Pubitemid 28086548)
15. Bort J, Brown HR, Araus JL. 1996. Refixation of respiratory CO2 in the ears of C3 cereals. Journal of Experimental Botany 47, 1567-1575. (Pubitemid 27040042)
16. Bradford MM. 1976. A rapid method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Annals of Biochemistry 72, 248-254.
17. Desclos M, Etienne P, Coquet L, Cosette P, Bonnefoy J, Segura R, Reze S, Ourry A, Avice JC. 2009. A combined 15N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated to N remobilisation during leaf senescence induced by nitrate limitation or starvation. Proteomics 9, 3580-3608.
18. Davey PA, Hunt S, Hymus GJ, DeLucia EH, Drake BG, Karnosky DF, Long SP. 2004. Respiratory oxygen uptake is not decreased by an instantaneous elevation of [CO2], but is increased with long-term growth in the field at elevated [CO2]. Plant Physiology 134, 1-8.
19. Davey PA, Olcer H, Zakhleniuk O, Bernacchi CJ, Calfapietra C, Long SP, Raines CA. 2006. Can fast-growing plantation trees escape biochemical downregulation of photosynthesis when grown throughout their complete production cycle in the open air under elevated carbon dioxide? Plant, Cell and Environment 29, 1235-1244. (Pubitemid 43855741)
20. Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD. 2004. Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology 10, 2121-2138. (Pubitemid 40015011)
21. Emes MJ, Bowsher CG, Hedley C, Burrell MM, Scrase-Field ESF, Tetlow IJ. 2003. Starch synthesis and carbon partitioning in developing endosperm. Journal of Experimental Botany 54, 569-575. (Pubitemid 36122052)
22. Evans JR, Kaldenhoff R, Genty B, Terashima I. 2009. Resistances along the CO2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235-2248.
23. Evans LT, Dunstone RL, Rawson HM, Williams RF. 1970. Phloem of wheat stem in relation to requirements for assimilate by ear. Australian Journal of Biological Sciences 23, 743-752.
24. Evans LT, Wardlaw IF, Fischer RA. 1975. Wheat. In: Evans LT, ed. Crop physiology: some case histories. Cambridge, UK: Cambridge University Press, 101-150.
25. Fangmeier A, Chrost B, Hogy P, Krupiskam K. 2000. CO2 enrichment enhances flag senescence in barley due to greater grain nitrogen sink capacity. Environmental and Experimental Botany 44, 151-164.
26. Farquhar GD, von Caemmerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78-90.
27. Farquhar GD, Hubick KT, Condon AG, Richards RA. 1989. Carbon isotope fractionation and water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA, eds. Stable isotopes in ecological research. Ecological Studies vol. 68. Berlin: Springer, 21-40.
28. Flexas J, Díaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M. 2007. Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell and Environment 30, 1284-1298. (Pubitemid 47312337)
29. Flexas J, Ribas-Carbo M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R. 2006. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. The Plant Journal 48, 427-439. (Pubitemid 44571148)
30. Gebbing T, Schnyder H. 1999. Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat. Plant Physiology 121, 871-878.
31. Gillon JS, Yakir D. 2000. Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves. Plant Physiology 123, 201-213. (Pubitemid 30322829)
32. Gutiérrez D, Gutiérrez E, Pérez P, Morcuende R, Verdejo AL, Martínez-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.
33. Hare PE. 1977. Subnanomole-range amino acid analyses. Methods in Enzymology 47, 3-18.
34. Högy P, Zörb C, Langenkämper G, Betsche T, Fangmeier A. 2009. Atmospheric CO2 enrichment changes the wheat grain proteome. Journal of Cereal Science 50, 248-254.
35. Jebanathirajah JA, Coleman JR. 1998. Association of carbonic anhidrase with a Calvin cycle enzyme complex in Nicotiana tabacum. Planta 204, 177-182. (Pubitemid 28104665)
36. Jifon JL, Wolfe DW. 2002. Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. Global Change Biology 8, 1018-1027.
37. Kodama N, Ferrio JP, Brüggemann Gessler A. 2010. Short-term dynamics of the carbon isotope composition of CO2 emitted from a wheat agroecosystem-physiological and environmental controls. Plant Biology 31, 115-125.
38. Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G. 2005. Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309, 1360-1362.
39. Leakey ADB, Xu F, Gillespie KM, McGrath JM, Ainsworth EA. 2009. Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proceedings of the National Academy of Sciences, USA 106, 3597-3602.
40. Lewis JD, Wang XZ, Griffin KL, Tissue DT. 2002. Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant, Cell and Environment 25, 359-368. (Pubitemid 34209329)
41. 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. (Pubitemid 38940945)
42. 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. (Pubitemid 40801894)
43. Moore BD, Cheng SH, Sims D, Seemann JR. 1999. The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant, Cell and Environment 22, 567-582. (Pubitemid 29298256)
44. Morcuende R, Kostadinova S, Pérez P, Martín del Molino IM, Martínez-Carrasco R. 2004. Nitrate is a negative signal for fructan synthesis, and the fructosyltranferase-inducing trehalose inhibits nitrogen and carbon assimilation in excised barley leaves. New Phytologist 161, 749-759. (Pubitemid 38193013)
45. Morcuende R, Krapp A, Hurry V, Stitt M. 1998. Sucrose feeding leads to increased rates of nitrate assimilation, increased rates of oxoglutarate synthesis, and increased rates of a wide spectrum of amino acids in tobacco leaves. Planta 26, 394-409. (Pubitemid 28422206)
46. Morcuende R, Pérez P, Martínez-Carrasco R, Martín del Molino I, Sánchez de la Puente L. 1996. Long-and short-term responses of leaf carbohydrate levels and photosynthesis to decreased sink demand in soybean. Plant, Cell and Environment 19, 976-982.
47. Morcuende R, Pérez P, Martínez-Carrasco R. 1997. Short-term feedback inhibition of photosynthesis in wheat leaves supplied with sucrose and glycerol at two temperatures. Photosynthetica 33, 179-188. (Pubitemid 27191170)
48. Nakano H, Makino A, Mae T. 1997. The effect of elevated partial pressures of CO2 on the relationship between photosynthetic capacity and N content in rice leaves. Plant Physiology 115, 191-198. (Pubitemid 28381841)
49. Nakhoul NL, Davis BA, Romero MF, Boron WF. 1998. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. American Journal of Physiology 274, 543-548.
50. Naumburg E, Housman DC, Huxman T, Charlet TN, Loik ME, Smith SD. 2004. Photosynthetic responses of Mojave Desert shrubs to free-air CO2 enrichment are greatest during wet years. Global Change Biology 8, 276-285. (Pubitemid 36290357)
51. Nogués S, Tcherkez G, Cornic G, Ghashghaie J. 2004. Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling. Plant Physiology 136, 3245-3254.
52. Nogués S, Aranjuelo I, Pardo T, Azcón-Bieto J. 2008. Assessing the stable-carbon isotopic composition of intercellular CO2 in a CAM plant at two CO2 levels. Rapid Communications in Mass Spectrometry 22, 1017-1022.
53. Nowak RS, Ellsworth DS, Smith SD. 2004. Functional responses to elevated atmospheric CO2-do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist 162, 253-280. (Pubitemid 38503697)
54. Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ. 2008. Rubisco regulation: a role for inhibitors. Journal of Experimental Botany 59, 1569-1580. (Pubitemid 351786588)
55. Pérez P, Morcuende R, Martín del Molino I, Martínez-Carrasco R. 2005. Diurnal changes of Rubisco in response to elevated CO2, temperature and nitrogen in wheat grown under temperature gradient tunnels. Environmental and Experimental Botany 53, 13-27.
56. Pérez P, Rabnecz G, Laufer Z, Gutiérrez D, Tuba Z, Martínez-Carrasco R. 2011. Restoration of photosystem II photochemistry and carbon assimilation and related changes in chlorophyll and protein contents during the rehydration of desiccated Xerophyta scabrida leaves. Journal of Experimental Botany 62, 895-905.
57. Pérez P, Zita G, Morcuende R, Martínez-Carrasco R. 2007. Elevated CO2 and temperature differentially affect photosynthesis and resource allocation in flag and penultimate leaves of wheat. Photosynthetica 45, 9-17.
58. Prentice IC, Farquhar GD, Fasham MJR, et al. 2001. The carbon cycle and atmospheric carbon dioxide. In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Xiaosu D, eds. Climate change 2001: the scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press, 183-239.
59. Rawson HM, Gifford RM, Condon BN. 1995. Temperature gradient chambers for research on global environment change. Part I. Portable chambers for research on short-stature vegetation. Plant, Cell and Environment 18, 1048-1054. (Pubitemid 26454434)
60. Richter A, Wanek W, Werner RA, et al. 2009. Preparation of starch and soluble sugars of plant material for the analyses of carbon isotope composition: a comparison of methods. Rapid Communications in Mass Spectrometry 23, 2476-2488.
61. Robinson SP, Portis AR. 1989. Adenosine triphosphate hydrolysis by purified Rubisco activase. Archives of Biochemistry and Biophysics 268, 93-99.
62. Rodríguez-López M, Baroja-Fernández E, Zandueta-Criado A, Pozueta-Romero J. 2000. Adenosine diphosphate glucose pyrophosphatase: a plastidial phosphodiesterase that prevents starch biosynthesis. Proceedings of the Natural Academy of Sciences, USA 97, 8705-8710.
63. Rogers A, Ellsworth DS. 2002. Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant, Cell and Environment 25, 851-858. (Pubitemid 34775983)
64. Sasaki H, Hirose T, Watanabe Y, Ohsugi R. 1998. Carbonic anhydrase activity and CO2-transfer resistance in Zn-deficient rice leaves. Plant Physiology 118, 929-934. (Pubitemid 128653018)
65. Scheible WR, González-Fontes A, Lauerer M, Müller-Rober B, Caboche M, Stitt M. 1997. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. The Plant Cell 9, 783-798. (Pubitemid 28104507)
66. Schnyder H. 1993. The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling - a review. New Phytologist 123, 233-245.
67. Schnyder H, Schäufele R, Lötscher M, Gebbing T. 2003. Disentangling CO2 fluxes: direct measurements of mesocosm-scale natural abundance 13CO2/12CO2 gas exchange, 13C discrimination, and labelling of CO2 exchange flux components in controlled environments. Plant, Cell and Environment 26, 1863-1874.
68. Singsaas EL, Ort DR, DeLucia EH. 2003. Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology. Plant, Cell and Environment 27, 41-50. (Pubitemid 38126807)
69. Stitt M. 1991. Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell and Environment 14, 741-762.
70. Stitt M, Krapp A. 1999. The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant, Cell and Environment 22, 583-621. (Pubitemid 29298257)
71. Tambussi EA, Bort J, Guiamet JJ, Nogués S, Araus JL. 2007. The photosynthetic role of ears in C3 cereals: metabolism, water use efficiency and contribution to grain yield. Critical Reviews in Plant Sciences 26, 1-16. (Pubitemid 46293460)
72. Terashima I, Ono K. 2002. Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant and Cell Physiology 43, 70-78. (Pubitemid 34152458)
73. 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. (Pubitemid 128653020)
74. Thomas RB, Strain BR. 1991. Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiology 96, 627-634. (Pubitemid 21914060)
75. Uddling J, Gelang-Alfredsson J, Karlsson PE, Selldén G, Pleijel H. 2008. Source-sink balance of wheat determines responsiveness of grain production to increased [CO2] and water supply. Agriculture, Ecosystems and Environment 127, 215-222.
76. von Felten S, Hättenschwiler S, Saurer M, Siegwolf R. 2007. Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees 21, 283-294. (Pubitemid 46714366)
77. Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresto M. 2003. Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24, 2369-2375. (Pubitemid 38089022)
78. Zhang DY, Chen GY, Chen J, Yong ZH, Zhy JG, Xu DQ. 2009. Photosynthetic acclimation to CO2 enrichment related to ribulose-1, 5-bisphosphate carboxylation limitation in wheat. Photosynthetica 47, 152-154.
79. Zhu C, Zhu J, Zeng Q, Liu G, Xie Z, Tang H, Cao J, Zhao X. 2009. Elevated CO2 accelerates flag senescence in wheat due to ear photosynthesis which causes greater ear nitrogen sink capacity and ear carbon sink limitation. Functional Plant Biology 36, 291-299.