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Does Elevated CO2 Provide Real Benefits for N2-Fixing Leguminous Symbioses?

  • Saad SuliemanEmail author
  • Nguyen Phuong Thao
  • Lam-Son Phan TranEmail author
Chapter

Abstract

Feeding the growing world population will be a significant challenge for agricultural development in the twenty-first century. Simultaneously, global climate change will provide an additional challenge by significantly modifying the potential capability of the cultivated plants, particularly for those favoring symbiotic association with soil bacteria. Hence, the whole-plant nutritional metabolism is expected to reprogram basically to meet these climatic variables that collectively become a major concern for future agriculture. In the frame of the current and projected climate scenarios, this chapter attempts to address whether symbiotic legumes would benefit greatly from the current and projected higher levels of carbon dioxide (CO2) in the atmosphere—sometimes called the CO2 fertilization effect. On the basis of the results obtained by several researchers, nodulated legumes are projected to have a stronger response to elevated CO2 whose level is continuously rising. In sharp contrast, another group of researchers has questioned such beneficial responses by symbiotic legumes. Apparently, the experimental findings dealing with the effects of elevated CO2 on legume growth and function have revealed significant discrepancies and variability. In this chapter, we briefly outline the nature of global climate change in terms of rising atmospheric CO2 and then discuss the potential biotechnological targets for improving N2-fixing symbioses in a world of increasing CO2 level. Current interest in understanding legume responses to changing global climate makes this overview timely.

Keywords

Climate change C/N metabolism Elevated CO2 N2 fixation Legumes Symbiosis Nodules Productivity 

Notes

Acknowledgements

The authors are grateful to the Japan Society for the Promotion of Science (JSPS) for financial support for this work and for awarding a postdoc fellowship to Saad Sulieman.

References

  1. Ainsworth EA, Rogers A, Nelson R et al (2004) Testing the “source-sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agric Forest Meteorol 122:85–94Google Scholar
  2. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising (CO2): Mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedGoogle Scholar
  3. Ainsworth EA, Ort DR (2010) How do we improve crop production in a warming world? Plant Physiol 154(2):526–530PubMedCentralPubMedGoogle Scholar
  4. Almeida JPF, Hartwig UA, Frehner M et al (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51:1289–1297PubMedGoogle Scholar
  5. Aranjuelo I, Irigoyen JJ, Perez P et al (2005) The use of temperature gradient tunnels for studying the combined effect of CO2, temperature and water availability in N2 fixing alfalfa plants. Ann Appl Biol 146:51–60Google Scholar
  6. Aranjuelo I, Irigoyen JJ, Perez P et al (2006) Response of nodulated alfalfa to water supply, temperature and elevated CO2: productivity and water relations. Environ Exp Bot 55:130–141Google Scholar
  7. Aranjuelo I, Irigoyen JJ, Sánchez-Díaz M et al (2008) Carbon partitioning in N2 fixing Medicago sativa plants exposed to different CO2 and temperature conditions. Funct Plant Biol 35(4):306–317Google Scholar
  8. Aranjuelo I, Cabrerizo PM, Arrese-Igor C et al (2013) Pea plant responsiveness under elevated [CO2] is conditioned by the N source (N2 fixation versus NO3 fertilization). Environ Exp Bot 95:34–40Google Scholar
  9. Aranjuelo I, Cabrerizo PM, Aparicio-Tejo PM et al (2014) Unravelling the mechanisms that improve photosynthetic performance of N2-fixing pea plants exposed to elevated [CO2]. Environ Exp Bot 99:167–174Google Scholar
  10. Araújo SS, Beebe S, Crespi M et al (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280Google Scholar
  11. Arrese-Igor C, Gonzalez EM, Gordon AJ et al (1999) Sucrose synthase and nodule nitrogen fixation under drought and other environmental stresses. Symbiosis 27:189–212Google Scholar
  12. Baslam M, Antolín MC, Gogorcena Y et al (2014) Changes in alfalfa forage quality and stem carbohydrates induced by arbuscular mycorrhizal fungi and elevated atmospheric CO2. Ann Appl Biol 164:190–199Google Scholar
  13. Bertrand A, Prévost D, Bigras FJ et al (2007a) Elevated atmospheric CO2 and strain of Rhizobium alter freezing tolerance and cold-induced molecular changes in alfalfa (Medicago sativa). Ann Bot 99:275–284PubMedCentralPubMedGoogle Scholar
  14. Bertrand A, Prévost D, Bigras FJ et al (2007b) Alfalfa response to elevated atmospheric CO2 varies with the symbiotic rhizobial strain. Plant Soil 301:173–187Google Scholar
  15. Bertrand A, Prévost D, Juge C et al (2011) Impact of elevated CO2 on carbohydrate and ureide concentrations in soybean inoculated with different strains of Bradyrhizobium japonicum. Botany 89:481–490Google Scholar
  16. Cabeza RA, Lingner A, Liese R et al (2014) The activity of nodules of the supernodulating mutant Mtsunn is not limited by photosynthesis under optimal growth conditions. Int J Mol Sci 15:6031–6045PubMedCentralPubMedGoogle Scholar
  17. Cabrerizo PM, González EM, Aparicio-Tejo PM et al (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 Plant 113(1):33–40Google Scholar
  18. Cen YP, Layzell DB (2004) Does oxygen limit nitrogenase activity in soybean exposed to elevated CO2? Plant Cell Environ 27:1229–1238Google Scholar
  19. Cernusak LA, Winter K, Martínez C et al (2011) Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiol 157(1):372–385PubMedCentralPubMedGoogle Scholar
  20. Charpentier M, Oldroyd G (2010) How close are we to nitrogen-fixing cereals? Curr Opin Plant Biol 13:556–564PubMedGoogle Scholar
  21. Daepp M, Suter D, Almeida JPF et al (2000) Yield response of Lolium perenne swards to free air CO2 enrichment increased over six years in a high N input system on fertile soil. Global Change Biol 6(7):805–816Google Scholar
  22. Dakora FD, Drake BG (2000) Elevated CO2 stimulates associative N2 fixation in a C3 plant of the Chesapeake Bay wetland. Plant Cell Environ 23(9):943–953Google Scholar
  23. Deiglmayr K, Philippot L, Hartwig UA et al (2004) Structure and activity of the nitrate-reducing community in the rhizosphere of Lolium perenne and Trifolium repens under long-term elevated atmospheric pCO2. FEMS Microbiol Ecol 49:445–454PubMedGoogle Scholar
  24. Ellsworth DS, Reich PB, Naumburg ES et al (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 Biol 10(12):2121–2138Google Scholar
  25. Erice G, Irigoyen JJ, Sánchez-Díaz M et al (2007a) 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 172:903–912Google Scholar
  26. Erice G, Aranjuelo I, Irigoyen JJ et al (2007b) Effect of elevated CO2, temperature and limited water supply on antioxidant status during regrowth of nodulated alfalfa. Physiol Plant 130:33–45Google Scholar
  27. Erice G, Sanz-Sáez A, Aranjuelo I et al (2011) Photosynthesis, N2 fixation and taproot reserves during the cutting regrowth cycle of alfalfa under elevated CO2 and temperature. J Plant Physiol 168:2007–2014PubMedGoogle Scholar
  28. Feng Z, Dyckmans J, Flessa H (2004) Effects of elevated carbon dioxide concentration on growth and N2 fixation of young Robinia pseudoacacia. Tree Physiol 24:323–330PubMedGoogle Scholar
  29. Fischinger SA, Drevon JJ, Claassen N et al (2006) Nitrogen from senescing lower leaves of common bean is re-translocated to nodules and might be involved in a N-feedback regulation of nitrogen fixation. J Plant Physiol 163:987–995PubMedGoogle Scholar
  30. Fischinger SA, Schulze J (2010) The importance of nodule CO2 fixation for the efficiency of symbiotic nitrogen fixation in pea at vegetative growth and during pod formation. J Exp Bot 61(9):2281–2291PubMedCentralPubMedGoogle Scholar
  31. Fischinger SA, Hristozkova M, Mainassara Z et al (2010) Elevated CO2 concentration around alfalfa nodules increases N2 fixation. J Exp Bot 61:121–130PubMedCentralPubMedGoogle Scholar
  32. Fotelli MN, Tsikou D, Kolliopoulou A et al (2011) Nodulation enhances dark CO2 fixation and recycling in the model legume Lotus japonicus. J Exp Bot 62(8):2959–2971PubMedGoogle Scholar
  33. Freeman C, Kim S-Y, Lee S-H et al (2004) Effects of elevated atmospheric CO2 concentrations on soil microorganisms. J Microbiol 42:267–277PubMedGoogle Scholar
  34. Garg NJ (2007) Relationship between nitrogen fixation and carbon metabolism in legumes: a review. Agric Rev 28(2):127–134Google Scholar
  35. Goicoechea N, Baslam M, Erice G et al (2014) Increased photosynthetic acclimation in alfalfa associated with arbuscular mycorrhizal fungi (AMF) and cultivated in greenhouse under elevated CO2. J Plant Physiol 171:1774–1781PubMedGoogle Scholar
  36. Gray SB, Strellner RS, Puthuval KK et al (2013) Minirhizotron imaging reveals that nodulation of field-grown soybean is enhanced by free-air CO2 enrichment only when combined with drought stress. Funct Plant Biol 40:137–147Google Scholar
  37. Guo H, Sun Y, Li Y et al (2013a) Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Global Change Biol 19:3210–3223Google Scholar
  38. Guo H, Sun Y, Li Y et al (2013b) Elevated CO2 modifies N acquisition of Medicago truncatula by enhancing N fixation and reducing nitrate uptake from soil. PLoS One 8:e81373PubMedCentralPubMedGoogle Scholar
  39. Guo H, Sun Y, Li Y et al (2014) Elevated CO2 alters the feeding behaviour of the pea aphid by modifying the physical and chemical resistance of Medicago truncatula. Plant Cell Environ 37:2158–2168PubMedGoogle Scholar
  40. Haase S, Neumann G, Kania A et al (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221Google Scholar
  41. Hartwig UA, Trommler J (2001) Increase in the concentrations of amino acids in the vascular tissue of white clover and white lupin after defoliation: an indication of a N feedback regulation of symbiotic N2 fixation. Agronomie 21:615–620Google Scholar
  42. He Z, Xiong J, Kent AD et al (2014) Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. ISME J 8(3):714–726PubMedCentralPubMedGoogle Scholar
  43. Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511Google Scholar
  44. Imtiaz M, Malhotra RS, Yadav SS (2011) Genetic adjustment to changing climates: chickpea. In: Yadav SS, Redden RJ, Hatfield JL, Lotze-Campen H, Hall AE (eds) Crop adaptation to climate change, 1st edn. Blackwell/Wiley, Hoboken, NJ, pp 251–268Google Scholar
  45. IPCC (2007) Summary for policymakers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press, pp 1–18Google Scholar
  46. Irigoyen JJ, Goicoechea N, Antolín MC et al (2014) Growth, photosynthetic acclimation and yield quality in legumes under climate change simulations: an updated survey. Plant Sci 226:22–29PubMedGoogle Scholar
  47. Johnson SN, Ryalls JMW, Karley AJ (2014) Global climate change and crop resistance to aphids: contrasting responses of lucerne genotypes to elevated atmospheric carbon dioxide. Ann Appl Biol 165:62–72Google Scholar
  48. Kanemoto K, Yamashita Y, Ozawa T et al (2009) Photosynthetic acclimation to elevated CO2 is dependent on N partitioning and transpiration in soybean. Plant Sci 177:398–403Google Scholar
  49. Kant S, Seneweera S, Rodin J et al (2012) Improving yield potential in crops under elevated CO2: integrating the photosynthetic and nitrogen utilization efficiencies. Front Plant Sci 3:162Google Scholar
  50. Karunakaran R, East AK, Poole PS (2013) Malonate catabolism does not drive N2 fixation in legume nodules. Appl Environ Microbiol 79(14):4496–4498PubMedCentralPubMedGoogle Scholar
  51. Kaschuk G, Kuyper TW, Leffelaar PA et al (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244Google Scholar
  52. Krausmann F, Gingrich S, Eisenmenger N et al (2009) Growth in global materials use, GDP and population during the 20th century. Ecol Econ 68:2696–2705Google Scholar
  53. Ladrera R, Marino D, Larrainzar E et al (2007) Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol 145:539–546PubMedCentralPubMedGoogle Scholar
  54. Lam SK, Chen D, Norton R et al (2012) Nitrogen dynamics in grain crop and legume pasture systems under elevated atmospheric carbon dioxide concentration: a meta-analysis. Global Change Biol 18:2853–2859Google Scholar
  55. Larrainzar E, Wienkoop S, Scherling C et al (2009) Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Mol Plant Microbe Interact 22:1565–1576PubMedGoogle Scholar
  56. Leakey ADB, Ainsworth EA, Bernacchi CJ et al (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876PubMedGoogle Scholar
  57. Leakey ADB, Bishop KA, Ainsworth EA (2012) A multi-biome gap in understanding of crop and ecosystem responses to elevated CO2. Curr Opin Plant Biol 15:228–236PubMedGoogle Scholar
  58. Libault M (2014) The carbon-nitrogen balance of the nodule and its regulation under elevated carbon dioxide concentration. BioMed Res Int 2014:7 p, Article ID 507946Google Scholar
  59. Lima JD, Sodek L (2003) N-stress alters aspartate and asparagine levels of xylem sap in soybean. Plant Sci 165:49–56Google Scholar
  60. Luo Y, Su B, Currie WS et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54(8):731–739Google Scholar
  61. Lüscher A, Hartwig UA, Suter D et al (2000) 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(6):655–662Google Scholar
  62. Marilley L, Hartwig UA, Aragno M (1999) Influence of an elevated atmospheric CO2 content on soil and rhizosphere bacterial communities beneath Lolium perenne and Trifolium repens under field conditions. Microb Ecol 38:39–49PubMedGoogle Scholar
  63. Milchunas DG, Mosier AR, Morgan JA et al (2005) Elevated CO2 and defoliation effects on a shortgrass steppe: forage quality versus quantity for ruminants. Agr Ecosyst Environ 111:166–184Google Scholar
  64. Minchin FR, Witty JF (2005) Respiratory/carbon costs of symbiotic nitrogen fixation in legumes. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem. Springer, Dordrecht, The Netherlands, pp 195–205Google Scholar
  65. Montealegre CM, Van Kessel C, Blumenthal JM et al (2000) Elevated atmospheric CO2 alters microbial population structure in a pasture ecosystem. Global Change Biol 6:475–482Google Scholar
  66. Nasser RR, Fuller MP, Jellings AJ (2008) Effect of elevated CO2 and nitrogen levels on lentil growth and nodulation. Agron Sustain Dev 28:175–180Google Scholar
  67. Nasr Esfahani M, Sulieman S, Schulze J et al (2014a) Approaches for enhancement of N2 fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions. Plant Biotechnol J 12:387–397Google Scholar
  68. Nasr Esfahani M, Sulieman S, Schulze J et al (2014b) Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls. Plant J 79:964–980PubMedGoogle Scholar
  69. Neo HH, Layzell DB (1997) Phloem glutamine and the regulation of O2 diffusion in legume nodules. Plant Physiol 113:259–267PubMedCentralPubMedGoogle Scholar
  70. Nösberger J, Long SP, Norby RJ et al (2006) Managed ecosystems and CO2: case studies, processes, and perspectives. Springer, BerlinGoogle Scholar
  71. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedGoogle Scholar
  72. Oldroyd GED, Dixon R (2014) Biotechnological solutions to the nitrogen problem. Curr Opin Biotechnol 26:19–24PubMedGoogle Scholar
  73. Parsons R, Stanforth A, Raven AJ et al (1993) Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Environ 16:125–136Google Scholar
  74. Prasad PVV, Allen LH Jr, Boote KJ (2005) Crop responses to elevated carbon dioxide and interaction with temperature: grain legumes. J Crop Improv 13:113–155Google Scholar
  75. Prévost D, Bertrand A, Juge C et al (2010) Elevated CO2 induces differences in nodulation of soybean depending on bradyrhizobial strain and method of inoculation. Plant Soil 331:115–127Google Scholar
  76. Pritchard SG (2011) Soil organisms and global climate change. Plant Pathol 60:82–99Google Scholar
  77. Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512Google Scholar
  78. Rogers A, Gibon Y, Stitt M et al (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658PubMedGoogle Scholar
  79. Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016PubMedCentralPubMedGoogle Scholar
  80. Rosenthal DM, Ruiz-Vera UM, Siebers MH et al (2014) Biochemical acclimation, stomatal limitation and precipitation patterns underlie decreases in photosynthetic stimulation of soybean (Glycine max) at elevated [CO2] and temperatures under fully open airfield conditions. Plant Sci 226:136–146PubMedGoogle Scholar
  81. Ryalls JMW, Riegler M, Ben D et al (2013) Effects of elevated temperature and CO2 on aboveground–belowground systems: a case study with plants, their mutualistic bacteria and root/shoot herbivores. Front Plant Sci 4:445Google Scholar
  82. Sanz-Sáez Á, Erice G, Aranjuelo I et al (2010) Photosynthetic down-regulation under elevated CO2 exposure can be prevented by nitrogen supply in nodulated alfalfa. J Plant Physiol 167:1558–1565PubMedGoogle Scholar
  83. Sanz-Sáez Á, Erice G, Aguirreolea J et al (2012) Alfalfa forage digestibility, quality and yield under future climate change scenarios vary with Sinorhizobium meliloti strain. J Plant Physiol 169:782–788Google Scholar
  84. Sanz-Sáez Á, Erice G, Aranjuelo I et al (2013) Photosynthetic and molecular markers of CO2-mediated photosynthetic downregulation in nodulated alfalfa. J Integr Plant Biol 55:721–734PubMedGoogle Scholar
  85. Schortemeyer M, Hartwig UA, Hendrey GR et al (1996) Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free-air carbon dioxide enrichment (FACE). Soil Biol Biochem 28:1717–1724Google Scholar
  86. Schramm RW (1992) Proposed role of malonate in legume nodules. Symbiosis 14:103–113Google Scholar
  87. Schubert S (2007) The apoplast of indeterminate legume nodules: compartment for transport of amino acids, amides and sugars? In: Sattelmacher B, Horst WJ (eds) The apoplast of higher plants: compartment of storage, transport and reactions. Springer, Dordrecht, The Netherlands, pp 445–454Google Scholar
  88. Schulze J, Tesfaye M, Litjens RHMG et al (2002) Malate plays a central role in plant nutrition. Plant Soil 247:133–139Google Scholar
  89. Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137Google Scholar
  90. Serraj R, Vadez V, Sinclair TR (2001) Feedback regulation of symbiotic N2 fixation under drought stress. Agronomie 21:621–626Google Scholar
  91. Serraj R (2003) Atmospheric CO2 increase benefits symbiotic N2 fixation by legumes under drought. Curr Sci 85(9):1341–1343Google Scholar
  92. Serraj R, Sinclair TR (2003) Evidence that carbon dioxide enrichment alleviates ureide-induced decline of nodule nitrogenase activity. Ann Bot 91:85–89PubMedCentralPubMedGoogle Scholar
  93. Soussana J-F, Lüscher A (2007) Temperate grasslands and global atmospheric change: a review. Grass Forage Sci 62:127–134Google Scholar
  94. Sugawara M, Sadowsky MJ (2013) Influence of elevated atmospheric carbon dioxide on transcriptional responses of Bradyrhizobium japonicum in the soybean rhizoplane. Microbes Environ 28(2):217–227PubMedCentralPubMedGoogle Scholar
  95. Sulieman S, Schulze J (2010a) The efficiency of nitrogen fixation of the model legume Medicago truncatula (Jemalong A17) is low compared to Medicago sativa. J Plant Physiol 167:683–692PubMedGoogle Scholar
  96. Sulieman S, Schulze J (2010b) Phloem-derived γ-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ 33:2162–2172PubMedGoogle Scholar
  97. Sulieman S, Fischinger SA, Gresshoff PM et al (2010) Asparagine as a major factor in the N-feedback regulation of N2 fixation in Medicago truncatula. Physiol Plant 140:21–31PubMedGoogle Scholar
  98. Sulieman S (2011) Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal Behav 6:32–36PubMedCentralPubMedGoogle Scholar
  99. Sulieman S, Tran LS (2013) Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes. Crit Rev Biotechnol 33:309–327PubMedGoogle Scholar
  100. Sulieman S, Schulze J, Tran LS (2013a) Comparative analysis of the symbiotic efficiency of Medicago truncatula and Medicago sativa under phosphorus deficiency. Int J Mol Sci 14:5198–5213PubMedCentralPubMedGoogle Scholar
  101. Sulieman S, Ha CV, Schulze J et al (2013b) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot 64:2701–2712PubMedCentralPubMedGoogle Scholar
  102. Sulieman S, Schulze J, Tran LS (2014) N-feedback regulation is synchronized with nodule carbon alteration in Medicago truncatula under excessive nitrate or low phosphorus conditions. J Plant Physiol 171:407–410PubMedGoogle Scholar
  103. Suter D, Frehner M, Fischer BU et al (2002) Elevated CO2 increases carbon allocation to the roots of Lolium perenne under free-air CO2 enrichment but not in a controlled environment. New Phytol 154(1):65–75Google Scholar
  104. Tausz M, Tausz-Posch S, Norton RM et al (2013) Understanding crop physiology to select breeding targets and improve crop management under increasing atmospheric CO2 concentrations. Environ Exp Bot 88:71–80Google Scholar
  105. Terpolilli JJ, Hood GA, Poole PS (2012) What determines the efficiency of N2-fixing Rhizobium-legume symbioses? Adv Microb Physiol 60:325–389PubMedGoogle Scholar
  106. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327(5967):818–822PubMedGoogle Scholar
  107. Thomas RB, Van Bloem SJ, Schlesinger WH (2006) Climate change and symbiotic nitrogen fixation in agroecosystems. In: Newton PCD, Carran A, Edwards GR, Niklaus PA (eds) Agroecosystems in a changing climate. CRC Press, Boca Raton, FL, pp 85–116Google Scholar
  108. Tsikou D, Stedel C, Kouri ED et al (2011) Characterization of two novel nodule-enhanced α-type carbonic anhydrases from Lotus japonicus. Biochim Biophys Acta 1814:496–504PubMedGoogle Scholar
  109. Tu C, Booker FL, Burkey KO et al (2009) Elevated atmospheric carbon dioxide and O3 differentially alter nitrogen acquisition in peanut. Crop Sci 49:1827–1836Google Scholar
  110. Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805PubMedGoogle Scholar
  111. UNPD United Nations Population Division (2010) World population projections to 2150. United Nations, New YorkGoogle Scholar
  112. Vadez V, Sinclair TR, Serraj R (2000) Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiol Plant 110:215–223Google Scholar
  113. Vadez V, Berger JD, Warkentin T et al (2012) Adaptation of grain legumes to climate change: a review. Agron Sust Developm 32:31–44Google Scholar
  114. Valentine AJ, Benedito VA, Kang Y (2011) Legume nitrogen fixation and soil abiotic stress: from physiology to genome and beyond. Annu Plant Rev 42:207–248Google Scholar
  115. Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation of exquisite adaptation. Annu Rev Plant Physiol Plant Mol Biol 42:373–392Google Scholar
  116. Watanabe T, Bowatte S, Newton PCD (2013) A reduced fraction of plant N derived from atmospheric N (%Ndfa) and reduced rhizobial nifH gene numbers indicate a lower capacity for nitrogen fixation in nodules of white clover exposed to long-term CO2 enrichment. Biogeosciences 10:8269–8281Google Scholar
  117. Weisbach C, Hartwig UA, Heim I et al (1996) Whole-nodule carbon metabolites are not involved in the regulation of the oxygen permeability and nitrogenase activity in white clover nodules. Plant Physiol 110:539–545PubMedCentralPubMedGoogle Scholar
  118. White J, Prell J, James EK et al (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614PubMedCentralPubMedGoogle Scholar
  119. Whitehead LF, Tyerman SD, Day DA (2001) Polyamines as potential regulators of nutrient exchange across the peribacteroid membrane in soybean root nodules. Aust J Plant Physiol 28:675–681Google Scholar
  120. Yamakawa T, Tanaka S, Ishizuka J (1997) Effect of CO2-free air treatment on nitrogen fixation of soybeans inoculated with Bradyrhizobium japonicum and Rhizobium fredii. Soil Sci Plant Nutr 43:819–826Google Scholar
  121. Yamakawa T, Ikeda T, Ishizuka J (2004) Effects of CO2 concentration in rhizosphere on nodulation and N2 fixation of soybean and cowpea. Soil Sci Plant Nutr 50:713–720Google Scholar
  122. Yurgel SN, Kahn ML (2004) Dicarboxylate transport by rhizobia. FEMS Microbiol Rev 28:489–501PubMedGoogle Scholar
  123. Zanetti S, Hartwig UA, Lüscher A et al (1996) Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiol 112:575–583PubMedCentralPubMedGoogle Scholar
  124. Zavala JA, Nabity PD, DeLucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97PubMedGoogle Scholar
  125. Zhang L, Wu D, Shi H et al (2011) Effects of elevated CO2 and N addition on growth and N2 fixation of a legume subshrub (Caragana microphylla Lam.) in temperate grassland in China. PLoS One 6(10):e26842PubMedCentralPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Agronomy, Faculty of AgricultureUniversity of KhartoumShambatSudan
  2. 2.School of BiotechnologyInternational University, Vietnam National University HCMCHo Chi MinhVietnam
  3. 3.Signaling Pathway Research UnitRIKEN Center for Sustainable Resource Science (CSRS)YokohamaJapan

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