Advertisement

Legume Nitrogen Utilization Under Drought Stress

  • V. Castañeda
  • E. Gil-Quintana
  • A. Echeverria
  • EM. González
Chapter

Abstract

Legumes account for around 27% of the world’s primary crop production and can be classified based on their use and traits into grain and forage legumes. Legumes can establish symbiosis with N-fixing soil bacteria. As a result, a new organ is formed, the nodule, where the reduction of atmospheric N2 into ammonia is carried out catalyzed by the bacterial exclusive enzyme nitrogenase. The process, highly energy demanding, is known as symbiotic nitrogen fixation and provides all the N needs of the plant, thus avoiding the use of N fertilizers in the context of sustainable agriculture. However, legume crops are often grown under non-fixing conditions since legume nodulation is suppressed by high levels of soil nitrogen occurring in chemically fertilized agro-environment. In addition, legumes are very sensitive to environmental stresses, being drought one of the significant constraints affecting crop production. Due to their agricultural and economic importance, scientists have carried out basic and applied research on legumes to better understand responses to abiotic stresses and to further comprehend plant–microbe interactions. An integrated view of nitrogen utilization under drought stress will be presented with particular focus on legume crops.

Keywords

Amino acids Drought Legumes Nitrogen fixation Roots 

References

  1. Andrews M (1986) Nitrate and reduced-N concentrations in the xylem sap of Stellaria media, Xanthium strumarium and six legume species. Plant, Cell Environ 9:605–608Google Scholar
  2. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation—an alternative respiratory substrate for stressed plants. Trends Plant Sci 16:489–498PubMedGoogle Scholar
  3. Ariz I, Esteban R, García-Plazaola JI, Becerril JM, Aparicio-Tejo PM, Moran JF (2010) High irradiance induces photoprotective mechanisms and a positive effect on NH4+ stress in Pisum sativum L. J Plant Physiol 167:1038–1045CrossRefPubMedGoogle Scholar
  4. Atkins CA, Pate JS, Peoples MB, Joy KW (1983) Amino acid transport and metabolism in relation to the nitrogen economy of a legume leaf. Plant Physiol 71:841–848Google Scholar
  5. Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C (2014) Autophagy, plant senescence, and nutrient recycling. J Exp Bot 65:3799–3811CrossRefPubMedGoogle Scholar
  6. Bacanamwo M, Harper JE (1997) The feedback mechanism of nitrate inhibition of nitrogenase activity in soybean may involve asparagine and/or products of its metabolism. Physiol Plant 100:371–377CrossRefGoogle Scholar
  7. Baier MC, Barsch A, Kuester H, Hohnjec N (2007) Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol 145:1600–1618CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bajaj S, Targolli J, Liu LF, David Ho TH, Wu R (1999) Transgenic approaches to increase dehydration-stress tolerance in plants. Mol Breed 5:493–503CrossRefGoogle Scholar
  9. Boyer JS (1982) Plant productivity and environment. Science 218:443–448CrossRefPubMedGoogle Scholar
  10. Brown CM, Dilworth MJ (1975) Ammonia assimilation by rhizobium cultures and bacteroids. J General Microbiol 86:39–48CrossRefGoogle Scholar
  11. Coruzzi GM (2003) Primary N-assimilation into amino acids in Arabidopsis. Arabidopsis Book 2:e0010CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dai A (2011) Drought under global warming: a review. Wiley Interdiscip Rev Clim Change 2:45–65CrossRefGoogle Scholar
  13. Daryanto S, Wang L, Jacinthe PA, Yu X, Luo L, Cui K (2016) Global synthesis of drought effects on maize and wheat production. PLoS ONE 11:e0156362CrossRefPubMedPubMedCentralGoogle Scholar
  14. Del Castillo LD, Layzell DB (1995) Drought stress, permeability to O2 diffusion, and the respiratory kinetics of soybean root-nodules. Plant Physiol 107:1187–1194CrossRefPubMedPubMedCentralGoogle Scholar
  15. Del Castillo LD, Hunt S, Layzell DB (1994) The role of oxygen in the regulation of nitrogenase activity in drought-stressed soybean nodules. Plant Physiol 106:949–955CrossRefPubMedPubMedCentralGoogle Scholar
  16. Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Cruz C, Martins- Loução MA, Moran JF (2008) Nitrogen nutrition and antioxidant metabolism in ammonium-tolerant and -sensitive plants. Physiol Plant 132:359–369CrossRefPubMedGoogle Scholar
  17. Durand JL, Sheehy JE, Minchin FR (1987) Nitrogenase activity, photosynthesis and nodule water potential in soybean plants experiencing water-deprivation. J Exp Bot 38:311–321CrossRefGoogle Scholar
  18. Edgerton SA, MacCracken MC, Jacobson MZ, Ayala A, Whitman CE, Trexler MC (2008) Prospects for future climate change and the reasons for early action. J Air Waste Manage Assoc 58:1386–1400CrossRefGoogle Scholar
  19. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Sustain Agric. Springer, Netherlands, Dordrecht, pp 153–188CrossRefGoogle Scholar
  20. Foyer CH, Valadier M-H, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of Nitrogen and carbon metabolism in maize leaves. Plant Physiol 117:283–292CrossRefPubMedPubMedCentralGoogle Scholar
  21. Frechilla S, González EM, Royuela M, Minchin FR, Aparicio-Tejo PM, Arrese-Igor C (2000) Source of nitrogen nutrition (nitrogen fixation or nitrate assimilation) is a major factor involved in pea response to moderate water stress. J Plant Physiol 157:609–617CrossRefGoogle Scholar
  22. Fresneau C, Ghashghaie J, Cornic G (2007) Drought effect on nitrate reductase and sucrose-phosphate synthase activities in wheat (Triticum durum L.): role of leaf internal CO2. J Exp Bot 58:2983–2992CrossRefPubMedGoogle Scholar
  23. Funayama K, Kojima S, Tabuchi-Kobayashi M, Sawa Y, Nakayama Y, Hayakawa T, Yamaya T (2013) Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant Cell Physiol 54:934–943CrossRefPubMedGoogle Scholar
  24. Galvez L, Gonzalez EM, Arrese-Igor C (2005) Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 56:2551–2561CrossRefPubMedGoogle Scholar
  25. Gilbert ME, Medina V (2016) Drought adaptation mechanisms should guide experimental design. Trends Plant Sci 21:639–647CrossRefPubMedGoogle Scholar
  26. Gil-Quintana E, Larrainzar E, Arrese-Igor C, González EM (2013a) Is N-feedback involved in the inhibition of nitrogen fixation in drought-stressed Medicago truncatula? J Exp Bot 64:281–292CrossRefPubMedGoogle Scholar
  27. Gil-Quintana E, Larrainzar E, Seminario A, Diaz-Leal JL, Alamillo JM, Pineda M, Arrese-Igor C, Wienkoop S, Gonzalez EM (2013b) Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean. J Exp Bot 64:2171–2182CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gonzalez EM, Aparicio-Tejo PM, Gordon AJ, Minchin FR, Royuela M, Arrese-Igor C (1998) Water-deficit effects on carbon and nitrogen metabolism of pea nodules. J Exp Bot 49:1705–1714CrossRefGoogle Scholar
  29. Gonzalez EM, Gordon AJ, James C, Arrese-Igor C (1995) The role of sucrose synthase in the response of soybean nodules to drought. J Exp Bot 46:1515–1523CrossRefGoogle Scholar
  30. Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120:867–877CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gordon AJ, Minchin FR, Skot L, James CL (1997) Stress-induced declines in soybean N2 fixation are related to nodule sucrose synthase activity. Plant Physiol 114:937–946CrossRefPubMedPubMedCentralGoogle Scholar
  32. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gray SB, Brady SM (2016) Plant developmental responses to climate change. Develop Biol 419:64–77CrossRefPubMedGoogle Scholar
  34. Guan M, Møller IS, Schjoerring JK (2015) Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seed yield structure in Arabidopsis. J Exp Bot 66:203–212CrossRefPubMedGoogle Scholar
  35. Hachiya T, Ueda N, Kitagawa M, Hanke G, Suzuki A, Hase T, Sakakibara H (2016) Arabidopsis root-type ferredoxin:NADP(H) oxidoreductase 2 is involved in detoxification of nitrite in roots. Plant Cell Physiol 57:2440–2450CrossRefPubMedGoogle Scholar
  36. Hildebrandt TM, Nunes Nesi A, Araujo WL, Braun H-P (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579CrossRefPubMedGoogle Scholar
  37. Hsiao TC (1973) Plant responses to water stress. Ann Rev Plant Physiol Plant Mol Biol 24:519–570CrossRefGoogle Scholar
  38. Jack DL, Paulsen IT, Saier MH (2000) The amino acid/polyamine/organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microbiol 146:1797–1814CrossRefGoogle Scholar
  39. Jacobsen SE, Jensen CR, Liu F (2012) Improving crop production in the arid mediterranean climate. Field Crops Res 128:34–47CrossRefGoogle Scholar
  40. Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci 16:614–623CrossRefPubMedGoogle Scholar
  41. Jeschke WD, Hartung W (2000) Root–shoot interactions in mineral nutrition. Plant Soil 226:57–69CrossRefGoogle Scholar
  42. Jeuffroy MH, Ney B (1997) Crop physiology and productivity. Field Crop Res 53:3–16CrossRefGoogle Scholar
  43. Joshi V, Joung JG, Fei Z, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–947CrossRefPubMedGoogle Scholar
  44. King CA, Purcell LC (2005) Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137:1389–1396CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kohli A, Narciso JO, Miro B, Raorane M (2012) Root proteases: reinforced links between nitrogen uptake and mobilization and drought tolerance. Physiol Plant 145:165–179CrossRefPubMedGoogle Scholar
  46. Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semiarid environments. Adv Agron 72:107–138CrossRefGoogle Scholar
  47. Ladrera R, Marino D, Larrainzar E, Gonzalez EM, Arrese-Igor C (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 145:539–546CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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. Mol Plant-Microbe Interact 22:1565–1576CrossRefPubMedGoogle Scholar
  49. Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87CrossRefPubMedGoogle Scholar
  50. Lyon D, Castillejo MA, Mehmeti-Tershani V, Staudinger C, Kleemaier C, Wienkoop S (2016) Drought and recovery: independently regulated processes highlighting the importance of protein turnover dynamics and translational regulation in Medicago truncatula. Mol Cell Proteomics 15:6CrossRefGoogle Scholar
  51. Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, Gonzalez EM (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974CrossRefPubMedPubMedCentralGoogle Scholar
  52. Micheletto S, Rodriguez-Uribe L, Hernandez R, Richins RD, Curry J, O’Connell MA (2007) Comparative transcript profiling in roots of Phaseolus acutifolius and P. vulgaris under water deficit stress. Plant Sci 173:510–520CrossRefGoogle Scholar
  53. Miller AJ, Shen Q, Xu G (2008) Freeways in the plant: transporters for N, P and S and their regulation. Curr Opin Plant Biol 12:284–290CrossRefGoogle Scholar
  54. Mintz-Oron S, Meir S, Malitsky S, Ruppin E, Aharoni A, Shlomi T (2012) Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. Proc Nat l Acad Sci USA 109:339–344CrossRefGoogle Scholar
  55. Muller B, Pantin F, Genard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729CrossRefPubMedGoogle Scholar
  56. Murray JD, Cheng-Wu L, Chen Y, Miller AJ (2017) Nitrogen sensing in legumes. J Exp Bot 68:1919–1926PubMedGoogle Scholar
  57. Naya L, Ladrera R, Ramos J, Gonzalez EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 144:1104–1114CrossRefPubMedPubMedCentralGoogle Scholar
  58. Neo HH, Layzell DB (1997) Phloem glutamine and the regulation of O2 diffusion in legume nodules. Plant Physiol 113:259–267CrossRefPubMedPubMedCentralGoogle Scholar
  59. Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pate JS, Gunning BES, Briarty LG (1969) Ultrastructure and functioning of transport system of leguminous root nodule. Planta 85:11–34CrossRefPubMedGoogle Scholar
  61. Perez E, Thompson P (1996) Natural hazards: causes and effects. Lesson 7-drought. Prehosp Disaster Med 11:71–77CrossRefPubMedGoogle Scholar
  62. Postel SL (2000) Water and world population growth. Am Water Works Assoc J 92:131–138CrossRefGoogle Scholar
  63. Pratelli R, Pilot G (2014) Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot 65:5535–5556CrossRefPubMedGoogle Scholar
  64. Ramos MLG, Gordon AJ, Minchin FR, Sprent JI, Parsons R (1999) Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean (Phaseolus vulgaris L.). Ann Bot 83:57–63CrossRefGoogle Scholar
  65. Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446CrossRefPubMedPubMedCentralGoogle Scholar
  66. Santiago JP, Tegeder M (2016) Connecting source with sink: the role of Arabidopsis AAP8 in phloem loading of amino acids. Plant Physiol 171:508–521CrossRefPubMedPubMedCentralGoogle Scholar
  67. Scheurwater I, Koren M, Lambers H, Atkin OK (2002) The contribution of roots and shoots to whole plant nitrate reduction in fast- and slow-growing grass species. J Exp Bot 53:1635–1642CrossRefPubMedGoogle Scholar
  68. Serraj R, Vadez V, Sinclair TR (2001) Feedback regulation of symbiotic N2 fixation under drought stress. Agronomie 21:621–626CrossRefGoogle Scholar
  69. Serraj R, Vadez V, Denison RF, Sinclair TR (1999) Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol 119:289–296CrossRefPubMedPubMedCentralGoogle Scholar
  70. Shu FH, Shang H, Glassgold AE, Lee T, Baker J, Bizzarro M, Wittig N, Connelly J, Haack H (2007) Model projections of an imminent transition to a more arid climate. Science 316:1181–1475CrossRefGoogle Scholar
  71. Somerville C, Briscoe J (2001) Genetic engineering and water. Science 292:2217CrossRefPubMedGoogle Scholar
  72. Sprent JI (2001) Nodulation in legumes. R Bot Gardens, KewGoogle Scholar
  73. Sulieman S, Fischinger SA, Gresshoff PM, Schulze J (2010) Asparagine as a major factor in the N-feedback regulation of N2 fixation in Medicago truncatula. Physiol Plant 140:21–31CrossRefPubMedGoogle Scholar
  74. Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J Exp Bot 65:1865–1878CrossRefPubMedGoogle Scholar
  75. Trenberth KE, Dai A, van der Schrier G, Jones PD, Barichivich J, Briffa KR, Sheffield J (2013) Global warming and changes in drought. Nat Clim Change 4:17–22CrossRefGoogle Scholar
  76. Trepp GB, Plank DW, Gantt JS, Vance CP (1999a) NADH-glutamate synthase in alfalfa root nodules.Immunocytochemical localization. Plant Physiol 119:829–837CrossRefPubMedPubMedCentralGoogle Scholar
  77. Trepp GB, van de Mortel M, Yoshioka H, Miller SS, Samac DA, Gantt JS, Vance CP (1999b) NADH-glutamate synthase in alfalfa root nodules. Genetic regulation and cellular expression. Plant Physiol 119:817–828CrossRefPubMedPubMedCentralGoogle Scholar
  78. Vadez V, Sinclair TR (2000) Ureide degradation pathways in intact soybean leaves. J Exp Bot 51:1459–1465PubMedGoogle Scholar
  79. Vadez V, Sinclair T, Serraj R (2000) Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiol Plant 110:215–223CrossRefGoogle Scholar
  80. Vance CP, Gregerson RG, Robinson DL, Miller SS, Gantt JS (1994) Primary assimilation of nitrogen in alfalfa nodules—molecular features of the enzymes involved. Plant Sci 101:51–64CrossRefGoogle Scholar
  81. Walsh KB, Canny MJ, Layzell DB (1989a) Vascular transport and soybean nodule function.2. A role for phloem supply in product export. Plant, Cell Environ 12:713–723CrossRefGoogle Scholar
  82. Walsh KB, McCully ME, Canny MJ (1989b) Vascular transport and soybean nodule function—nodule xylem is a blind alley, not a throughway. Plant, Cell Environ 12:395–405CrossRefGoogle Scholar
  83. Wan Y, King R, Mitchell RAC, Hassani-Pak K, Hawkesford MJ (2017) Spatiotemporal expression patterns of wheat amino acid transporters reveal their putative roles in nitrogen transport and responses to abiotic stress. Sci Rep 7:5461CrossRefPubMedPubMedCentralGoogle Scholar
  84. Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310CrossRefPubMedPubMedCentralGoogle Scholar
  85. Worrall VS, Roughley RJ (1976) Effect of moisture stress on infection of Trifolium Subterraneum L. by RhizobiumTrifolii Dang. J Exp Bot 27:1233–1241CrossRefGoogle Scholar
  86. Zhang JY, Cruz DE, Carvalho MH, Torres-Jerez I, Kang Y, Allen SN, Huhman D, Tang Y, Murray J, Sumner LW, Udvardi MK (2014) Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant, Cell Environ 37:2553–2576CrossRefGoogle Scholar
  87. Zhang L, Tan Q, Lee R, Trethewy A, Lee YH, Tegeder M (2010) Altered xylem-phloem transfer of amino acids affects metabolism and leads to increased seed yield and oil content in Arabidopsis. Plant Cell 22:3603–3620CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zhao H, Ma H, Yu L, Wang X, Zhao J (2012) Genome-wide survey and expression analysis of amino acid transporter gene family in rice (Oryza sativa L.). PLoS ONE 7:e49210CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • V. Castañeda
    • 1
  • E. Gil-Quintana
    • 1
  • A. Echeverria
    • 1
  • EM. González
    • 1
  1. 1.Department of Environmental SciencesPublic University of NavarraPamplonaSpain

Personalised recommendations