Future Environmental Conditions will Limit Yield in N2 Fixing Alfalfa

  • Gorka EriceEmail author
  • Alvaro Sanz-Sáez
  • Iker Aranjuelo
  • Juan José Irigoyen
  • Manuel Sánchez-Díaz


Drought is recognised as the major environmental factor that constrains productivity and stability of plants. Crop yield under future climatic conditions has increased the interest in “water stress physiology”. Plant development under limited water availability together with increasing atmospheric CO2 concentration is of primary interest to ensure crop production under the projected climate scenarios. The expected reduction in precipitation and rising evapotranspiration rates will limit plant growth either by restricting stomatal conductance and photosynthesis or by restricting leaf expansion. Furthermore, alfalfa is a legume that establishes a symbiotic relationship with N2-fixing bacteria and hence drought may indirectly compromise plant production via alterations in nodule performance. The effects of water stress on nodules include not only reduction in nodule mass but decreases in nodule functioning. Furthermore, previous studies have confirmed that the performance of nodules is conditioned by their active interaction with other organs like leaves and roots. After long-term exposure to elevated CO2, photosynthetic downregulation may limit leaf N demand and hence, nodule activity. Moreover, as observed for leaves, nodule responses to water deficit may be altered by the way that drought limitation is imposed. When water shortage is imposed by controlling irrigation levels, plants acclimatise their water status and growth and therefore nodule activity is usually unaffected. In contrast, after progressive drought treatment by withholding water, nodules show significant decreases in nitrogenase activity.


Relative Water Content Specific Leaf Area Total Soluble Protein Leaf Relative Water Content Leaf Area Ratio 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by Ministerio de Economía y Competitividad (MINECO BFU2011-26989), Fundación Universitaria de Navarra (PIUNA-2008) and Fundación Caja Navarra. Gorka Erice was the recipient of a research ANABASi+D contract from Gobierno de Navarra. The assistance of Amadeo Urdiain and Mónica Oyarzun is also appreciated.


  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedCrossRefGoogle Scholar
  2. Antolín MC, Yoller J, Sánchez-Díaz M (1995) Effects of temporary drought on nitrate-fed and nitrogen-fixing alfalfa plants. Plant Sci 107:159–165CrossRefGoogle Scholar
  3. Aranjuelo I, Pérez P, Hernández L, Irigoyen JJ, Zita G, Martínez-Carrasco R, Sánchez-Díaz M (2005) The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic down regulation. Physiol Plantarum 123:348–358CrossRefGoogle Scholar
  4. Aranjuelo I, Irigoyen I, Perez P, Martínez-Carrasco R, Sánchez-Díaz M (2006) Response of nodulated alfalfa to water supply, temperature and elevated CO2: productivity and water relations. Environ Exp Botany 55:130–141CrossRefGoogle Scholar
  5. Aranjuelo I, Irigoyen JJ, Sánchez-Díaz M (2007) Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. Environ Exp Botany 59:99–108CrossRefGoogle Scholar
  6. 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. Funct Plant Biol 35:306–317CrossRefGoogle Scholar
  7. Aranjuelo I, Irigoyen JJ, Sánchez-Díaz M, Nogués S (2009) Elevated CO2 and water-availability effect on gas exchange and nodule development in N2-fixing alfalfa plants. Environ Exp Botany 65:18–26CrossRefGoogle Scholar
  8. Aranjuelo I, Molero G, Erice G, Avice J-C, Nogués S (2011) Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). J Exp Bot 62:111–123PubMedCrossRefGoogle Scholar
  9. Araus JL, Slafer GA, Reynolds MP, Royo C (2002) Plant breeding and water relation in C3 cereals: what to breed for? Ann Bot 89:925–940PubMedCrossRefGoogle Scholar
  10. Arnau G, Monneveux P, This D, Alegre L (1997) Photosynthesis of six barley genotypes as affected by water stress. Photosynthetica 34:67–76CrossRefGoogle Scholar
  11. Arnone JA II, Gordon JC (1990) Effect of nodulation, nitrogen fixation and CO2 enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytol 116:55–66CrossRefGoogle Scholar
  12. Arrese-Igor C, González EM, Gordon AJ, Minchin FR, Gálvez L, Royuela M, Cabrerizo PM, Aparicio-Tejo PM (1999) Sucrose synthase and nodule nitrogen fixation under drought and other environmental stresses. Symbiosis 27:1–24Google Scholar
  13. Avice J-C, Le Dily F, Goulas E, Noquet C, Meuriot F, Volenec JJ, Cunningham SM, Sors TG, Dhont C, Castonguay Y, Nadeau P, Bélanger G, Chalifour FP, Ourry A (2003) Vegetative storage proteins in overwintering storage organs of forage legumes: roles and regulation. Can J Bot 81:1198–1212CrossRefGoogle Scholar
  14. Bewley JD (2002) Root storage proteins, with particular reference to taproots. Can J Botany 80:321–329CrossRefGoogle Scholar
  15. Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annu Rev Plant Physiol Plant Mol Biol 44:309–332CrossRefGoogle Scholar
  16. Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165:397–406CrossRefGoogle Scholar
  17. Bushby HVA (1982) Ecology. In: Broughton WJ (ed) Nitrogen fixation: volume 2 Rhizobium. Claredon Press, Oxford, pp 35–75Google Scholar
  18. Cabrerizo PM, Gonzalez 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. Physiol Plantarum 113:33–40CrossRefGoogle Scholar
  19. Castellanos JZ, Pena-Cabriales JJ, Costa-Gallegos JAA (1996) 15N-determined dinitrogen fixation capacity of common bean (Phaseolus vulgaris L.) cultivars under water stress. J Agr Sci 126:327–333CrossRefGoogle Scholar
  20. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  21. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedCrossRefGoogle Scholar
  22. Curtis J, Shearer G, Khol DH (2004) Bacteroid proline catabolism affects N2 fixation rate of drought-stressed soybeans. Plant Physiol 136:3313–3318PubMedCrossRefGoogle Scholar
  23. Dart PJ, Mercer FV (1965) The effect of growth temperature, level of ammonium nitrate and light intensity on the growth and nodulation of cowpea (Vigna sinensis Endl. ex. Hassk.). Austr J Agr Res 16:321–345CrossRefGoogle Scholar
  24. Davey PA, Parsons AJ, Atkinson L, Wadge K, Long SP (1999) Does photosynthetic acclimation to elevated CO2 increase photosynthetic nitrogen use efficiency? A study of three native UK grassland species in open-top chambers. Funct Ecol 13:21–28CrossRefGoogle Scholar
  25. De Vries GE, In′tVeld P, Kijne JW (1980) Production of organic acids in Pisum sativum, root nodules as a result of oxygen stress. Plant Sci 20:115–123Google Scholar
  26. Dixon ROD, Wheeler CT (1983) Biochemical, physiological and environmental aspects of symbiotic nitrogen fixation. In: Gordon JC, Wheeler CT (eds) Biological nitrogen fixation in forest ecosystems: foundations and applications. Nijhoff/junk Publishers, The Hague, pp 107–171CrossRefGoogle Scholar
  27. Drake BG, Leadley PW (1991) Canopy photosynthesis of crops and native plants communities exposed to long-term elevated CO2. Plant Cell Environ 14:853–860CrossRefGoogle Scholar
  28. Drake BG, González-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Mol Biol 48:609–639CrossRefGoogle Scholar
  29. Erice G, Irigoyen JJ, Pérez P, Martínez-Carrasco R, Sánchez-Díaz M (2006a) Effect of elevated CO2, temperature and drought on dry matter partitioning and photosynthesis before and after cutting of nodulated alfalfa. Plant Sci 170:1059–1067CrossRefGoogle Scholar
  30. Erice G, Irigoyen JJ, Pérez P, Martínez-Carrasco R, Sánchez-Díaz M (2006b) Effect of elevated CO2, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle. Physiol Plantarum 126:458–468CrossRefGoogle Scholar
  31. Erice G, Irigoyen JJ, Sánchez-Díaz M, Avice JC, Ourry A (2007) Effect of drought, elevated CO2 and temperature on accumulation of N and vegetative storage proteins (VSP) in taproot of nodulated alfalfa before and after cutting. Plant Sci 172:903–912CrossRefGoogle Scholar
  32. Erice G, Louahlia S, Irigoyen JJ, Sánchez-Díaz M, Avice J-C (2010) Biomass partitioning, morphology and water status of four alfalfa genotypes submitted to progressive drought and subsequent recovery. J Plant Physiol 167:114–120PubMedCrossRefGoogle Scholar
  33. Erice G, Louahlia S, Irigoyen JJ, Sánchez-Díaz M, Thami Alami I, Avice J-C (2011) Water use efficiency, transpiration and net CO2 exchange of four alfalfa genotypes submitted to progressive drought and subsequent recovery. Environ Exp Bot 72:123–130CrossRefGoogle Scholar
  34. FAO (2006) FAOSTAT. Food and Agriculture Organization of the United NationsGoogle Scholar
  35. Farrar JF, Williams ML (1991) The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant Cell Environ 14:819–830CrossRefGoogle Scholar
  36. Finn GA, Brun WA (1980) Water stress effects on CO2 assimilation, photosynthate partitioning, stomatal resistance, and nodule activity in soybean. Crop Sci 20:431–434CrossRefGoogle Scholar
  37. Frings JFJ (1976) The rhizobium-pea symbiosis as affected by high temperatures. Ph.D. Thesis. Wageningen Agricultural University, NetherlandsGoogle Scholar
  38. Goicoechea N, Merino S, Sánchez-Díaz M (2004) Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides L. under water deficit. Physiol Plantarum 122:453–464CrossRefGoogle Scholar
  39. Goicoechea N, Merino S, Sánchez-Díaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. J Plant Physiol 162:27–35PubMedCrossRefGoogle Scholar
  40. González EM, Gálvez L, Royuela M, Aparicio-Tejo PM, Arrese-Igor C (2001) Insights into regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomie 21:607–613CrossRefGoogle Scholar
  41. Haase P, Pugnaire FI, Clarck SC, Incoll LD (2000) Photosynthetic rate and canopy development in the drought-deciduous shrub Anthyllis cytisoides L. J Arid Environ 46:79–91CrossRefGoogle Scholar
  42. Hardy RWF, Havelka UD (1976) Photosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybeans. In: Nutman PS (ed) Symbiotic nitrogen fixation. Cambridge University Press, Cambridge, pp 421–439Google Scholar
  43. Hartwig UA (1998) The regulation of symbiotic N2 fixation: a conceptual model of N feedback from ecosystem to the gene expression level. Perspect Plant Ecol Evol Syst 1:92–120CrossRefGoogle Scholar
  44. Hernandez-Armenta R, Wien HC, Eaglesham ARJ (1989) Maximum temperature for nitrogen fixation in common bean. Crop Sci 29:1260–1265CrossRefGoogle Scholar
  45. Heytler PG, Reddy GS, Hardy RWF (1985) In vivo energetics of symbiotic nitrogen fixation in soybeans. In: Ludden PL, Berris JE (eds) Nitrogen fixation and CO2 metabolism. Elsevier, New York, pp 283–292Google Scholar
  46. Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102CrossRefGoogle Scholar
  47. IPCC (2007) Climate Change 2007: impacts, adaptation and vulnerability. Working Group II Contribution to the Intergovernmental Panel on Climate Change. Fourth Assessment Report. Summary for Policymakers. BrusselsGoogle Scholar
  48. Jifon JL, Wolfe DW (2002) Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. Global Change Biol 8:1018–1027CrossRefGoogle Scholar
  49. Jones FR, Tisdale WB (1921) Effect of soil temperature upon the development of nodules on the roots of certain legumes. J Agr Res 22:17–37Google Scholar
  50. Jordan DB, Ögren WL (1984) The CO2/O2 specificity of ribulose 1, 5 bisphosphate carboxylase/oxygenase. Planta 161:308–313CrossRefGoogle Scholar
  51. King BJ, Layzell DB, Canvin DT (1986) The role of dark carbon dioxide fixation in root nodules of soybean. Plant Physiol 81:200–205PubMedCrossRefGoogle Scholar
  52. Kirkby EA (1981) Plant growth in relation to nitrogen supply. In: Clark FE, Rosswall T (eds) Terrestrial nitrogen cycles: processes, ecosystem strategies and management impacts, vol 33., ScopeEcological Bulletins, Stockholm, pp 249–267Google Scholar
  53. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, LondonGoogle Scholar
  54. Ladrera R, Marino D, Larrainzar E, González EM, Arrese-Igor C (2007) Reduced carbon availability to bacteroides and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol 145:539–546PubMedCrossRefGoogle Scholar
  55. Larcher W (2000) Temperature stress and survival ability of Mediterranean schlerophyll plants. Plant Biosyst 134:279–295CrossRefGoogle Scholar
  56. Larcher W (2003) Physiological Plant Ecology. Springer, BerlinGoogle Scholar
  57. Larrainzar E, Wienkoop S, Scherling C, Kempa S, Ladrera R, Arrese-Igor C, Weckwerth W, Gonzalez EM (2009) Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Molecular Plant Microbe In 22:1565–1576CrossRefGoogle Scholar
  58. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294PubMedCrossRefGoogle Scholar
  59. Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:543–549PubMedCrossRefGoogle Scholar
  60. Llusià J, Peñuelas J (2000) Seasonal patterns of terpene content and emission from seven Mediterranean woody species in field conditions. Am J Bot 87:133–140PubMedCrossRefGoogle Scholar
  61. Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentration: has its importance been underestimated? Plant Cell Environ 14:729–739CrossRefGoogle Scholar
  62. Long SP, Drake BG (1992) Photosynthetic CO2 assimilation and rising CO2 atmospheric CO2 concentrations. In: Baker NR, Thomas N (ed) Photosynthesis: crop photosynthesis: spatial and temporal determinations. Elsevier Science, Amsterdam, pp 69–107Google Scholar
  63. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  64. Lüscher A, Hartwig UA, Suter D, Nösberger J (2002) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Global Change Biol 6:655–662CrossRefGoogle Scholar
  65. Marcelis LFM, Heuvelink E, Goudriaan J (1998) Modelling biomass production and yield of horticultural crops: a review. Scientia Hort 74:83–111CrossRefGoogle Scholar
  66. Medrano H, Escalona JM, Bota J, Gulias J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89:895–905PubMedCrossRefGoogle Scholar
  67. Meyer DR, Anderson AJ (1959) Temperature and symbiotic nitrogen fixation. Nature 183:161CrossRefGoogle Scholar
  68. Michaud R, Lehmen WF, Rumbaugh MD (1988) World distribution and historical development. In: Hanson AA, Barnes DK, Hill RR (eds) Alfalfa and alfalfa improvement. American Society of Agronomy, Madison, pp 25–91Google Scholar
  69. Monneveux P, Belhassen E (1996) The diversity of drought adaptation in the wide. Plant Growth Regul 20:85–92CrossRefGoogle Scholar
  70. Mooney HA (1983) Carbon-gaining capacity and allocation patterns of Mediterranean climate plants. In: Kruger FJ, Mitchel DT, Jarvis JUM (eds) Mediterranean type ecosystems: the role of nutrients. Springer, Berlin, pp 103–119CrossRefGoogle Scholar
  71. Moore BE, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for acclimation to elevated CO2. Plant Cell Environment 22:567–582CrossRefGoogle Scholar
  72. Morgan JM (1983) Osmoregulation as a metabolism criterion for drought tolerance in wheat. Austr J Agr Res 34:607–614CrossRefGoogle Scholar
  73. Morgan JM, Condon AG (1986) Water use, grain yield and osmoregulation in wheat. Austr J Plant Physiol 13:523–532CrossRefGoogle Scholar
  74. Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant Cell Environ 22:659–682CrossRefGoogle Scholar
  75. Norby RJ (1987) Nodulation and nitrogenase activity in nitrogen-fixing woody plants stimulated by CO2 enrichment of the atmosphere. Physiol Plantarum 71:77–82CrossRefGoogle Scholar
  76. Ogaya R, Peñuelas J (2003) Comparative field studies of Quercus ilex and Phillirea latifolia: photosynthetic response to experimental drought conditions. Environ Exp Botany 50:137–148CrossRefGoogle Scholar
  77. Osborne CP, LaRoche J, Garcia RL, Kimball BA, Wall GW, Pinter PJ Jr, LaMorte RL, Hendrey GR, Long SP (1998) Does leaf position within a canopy affect acclimation of photosynthesis to elevated CO2? 1. Analysis of a wheat crop under free-air CO2 enrichment. Plant Physiol 117:1037–1045PubMedCrossRefGoogle Scholar
  78. Pankhurst CE, Sprent JI (1976) Effects of temperature and oxygen tension on the nitrogenase and respiratory activities of turgid and water-stressed soybeans and French bean root nodules. J Exp Bot 27:1–9CrossRefGoogle Scholar
  79. Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83CrossRefGoogle Scholar
  80. Peñuelas J, Filella I, Llusià J, Piñol J (1998) Comparative field study of spring and summer leaf gas exchange and photobiology of the Mediterranean trees Quercus ilex and Phillyrea latifolia. J Exp Bot 49:229–238Google Scholar
  81. Piha MI, Munns DN (1987) Sensitivity of the common bean (Phaseolus vulgaris) symbiosis to high soil temperature. Plant Soil 98:183–194CrossRefGoogle Scholar
  82. Pinheiro C, Passarinho JA, Ricardo CP (2004) Effect of drought and rewatering on the metabolism of Lupinus albus organs. J Plant Physiol 161:1203–1210PubMedCrossRefGoogle Scholar
  83. Power PF, Zachariassen JF (1993) Relative nitrogen utilization by legume cover crop species at three soil temperatures. Agron J 85:134–140CrossRefGoogle Scholar
  84. Radovic J, Sokolovic D, Markovic J (2009) Alfalfa-most important perennial forage legume in animal husbandry. Biotech Anim Husbandry 25:465–475CrossRefGoogle Scholar
  85. 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 legume. Plant Cell Environ 29:1651–1658PubMedCrossRefGoogle Scholar
  86. Ryle GJA, Powell CE, Davidson IA (1992) Growth of white clover, dependent on N2 fixation, in elevated CO2 and temperature. Ann Bot 70:221–228Google Scholar
  87. Sábate S, Gracia CA, Sánchez A (2002) Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region. Forest Ecol Manag 162:23–37CrossRefGoogle Scholar
  88. Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynth Res 39:351–368CrossRefGoogle Scholar
  89. Sanz-Sáez A, Erice G, Aguirrolea J, Irigoyen JJ, Sánchez-Díaz M (2012) Alfalfa yield under elevated CO2 and temperature depends on the Sinorhizobium strain and growth season. Environ Exp Bot 77:267–273CrossRefGoogle Scholar
  90. Serraj R, Sinclair TR, Allen LH (1998) Soybean nodulation and N2 fixation response to drought under carbon dioxide enrichment. Plant Cell Environ 21:491–500CrossRefGoogle Scholar
  91. Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155Google Scholar
  92. Streeter JG (2003) Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ 26:1199–1204CrossRefGoogle Scholar
  93. Taylor HM, Klepper B (1978) The role of rooting characteristics in the supply of water to plants. Adv Agron 30:99–128CrossRefGoogle Scholar
  94. Thomas Robertson MJ, Fukai S, Peoples MB (2004) The effect of timing and severity of water deficit on growth, development, yield accumulation and nitrogen fixation of mungbean. Field Crop Res 86:67–80CrossRefGoogle Scholar
  95. Tretiach M, Bolognini G, Rondi A (1997) Photosynthetic activity of Quercus ilex at the extremes of a transect between Mediterranean and submediterranean vegetation (Trieste, NE, Italy). Flora 192:369–378Google Scholar
  96. Udvardi MK, Day DA (1997) Metabolic transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48:493–523PubMedCrossRefGoogle Scholar
  97. Valladares F, Pearcy RW (1997) Interactions between water stresses, sun-shade acclimation, heat tolerance and photo inhibition in the schlerophyll Heteromeles arbutifoliar. Plant Cell Environ 20:25–36CrossRefGoogle Scholar
  98. Webber AN, Nie G-Y, Long SP (1994) Acclimation of photosynthetic proteins to rising atmospheric CO2. Photosynth Res 39:401–412CrossRefGoogle Scholar
  99. West JB, HilleRisLambers J, Lee TD, Hobbies SE, Reich PE (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530PubMedCrossRefGoogle Scholar
  100. Wilson PW, Fred EB, Salmon MR (1933) Relation between carbon dioxide and elemental nitrogen assimilation in leguminous plants. Soil Sci 35:145–165CrossRefGoogle Scholar
  101. Wolfe DW, Gifford RM, Hilbert D, Luo Y (1998) Integration of photosynthetic acclimation to CO2 at the whole-plant level. Global Change Biol 4:879–893CrossRefGoogle Scholar
  102. Yin C, Duan B, Wang X, Li C (2004) Morphological and physiological responses of two contrasting poplar species to drought stress and exogenous abscisic acid application. Plant Sci 167:1091–1097CrossRefGoogle Scholar
  103. Zanetti S, Hartwig UA, Lüscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nösberger J (1996) Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiol 112:575–583PubMedGoogle Scholar
  104. Zerihun A, BassiriRad H (2000) Photosynthesis of Helianthus annuus does not acclimate to elevated CO2 regardless of N supply. Plant Physiol Biochem 38:897–903CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Gorka Erice
    • 1
    Email author
  • Alvaro Sanz-Sáez
    • 1
  • Iker Aranjuelo
    • 2
  • Juan José Irigoyen
    • 1
  • Manuel Sánchez-Díaz
    • 1
  1. 1.Departamento de Biología VegetalSección Biología Vegetal (Unidad Asociada al CSIC, EEAD, Zaragoza e ICVV, Logroño), Facultades de Ciencias y Farmacia, Universidad de NavarraPamplonaSpain
  2. 2.Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, Campus de ArrosadíaMutilva BajaSpain

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