The Importance of Organic Nitrogen Transport Processes for Plant Productivity and Nitrogen Use Efficiency

  • Mechthild Tegeder
  • Molly Perchlik


Amino acids and ureides are the main nitrogen transport forms in plants. This review discusses key transporters that control root nitrogen uptake, as well as root-to-shoot and leaf-to-seed partitioning of organic nitrogen. It further examines the importance of amino acid and ureide transporters for plant growth, seed production, and plant nitrogen use efficiency.


Amino acid and ureide transporters Crop improvement Nitrogen uptake and partitioning Nitrogen use efficiency Source metabolism Sink development Seed yield 



Amino Acid Permease


Ammonium Transporter


Cationic Amino acid Transporter


Degradation of urea (urea transporter)


Lysine-Histidine-type Transporter


Nitrate Transporter


Peptide Transporter


NRT1/PTR Family


Proline Transporter


Usually Multiple Acids Move In and out Transporter


Ureide Permease



M.T. acknowledges support from the US National Science Foundation (IOS-1457183) and the Agriculture and Food Research Initiative (AFRI) competitive award number 2017-67013-26158 from the USDA National Institute of Food and Agriculture.


  1. Allen SM, Guo M, Loussaert DF, Rupe M, Wang H, Pioneer Hi-Bred International, Inc., EI Dupont De Nemours & Company (2016) Enhanced nitrate uptake and nitrate translocation by over-expressing maize functional low-affinity nitrate transporters in transgenic maize. U.S. patent application 14/770,863Google Scholar
  2. Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant, Cell Environ 9:511–519Google Scholar
  3. Andrews M, Morton JD, Lieffering M, Bisset L (1992) The partitioning of nitrate assimilation between root and shoot of a range of temperate cereals and pasture grasses. Ann Bot 70:271–276CrossRefGoogle Scholar
  4. Aoki N, Scofield GN, Wang X-D, Patrick JW, Offler CE, Furbank RT (2004) Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Plant 219:176–184CrossRefGoogle Scholar
  5. Atkins CA, Smith PM (2007) Translocation in legumes: assimilates, nutrients, and signaling molecules. Plant Physiol 144:550–561PubMedPubMedCentralCrossRefGoogle Scholar
  6. Atkins CA, Pate JS, Sharkey PJ (1975) Asparagine metabolism—key to the nitrogen nutrition of developing legume seeds. Plant Physiol 56:807–812PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bailey KJ, Leegood RC (2016) Nitrogen recycling from the xylem in rice leaves: dependence upon metabolism and associated changes in xylem hydraulics. J Exp Bot 67:2901–2911PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bao A, Liang Z, Zhao Z, Cai H (2015) Overexpressing of OsAMT1-3, a high affinity ammonium transporter gene, modifies rice growth and carbon-nitrogen metabolic status. Int J Mol Sci 16:9037–9063PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant Microbe Interact 27:349–363PubMedCrossRefGoogle Scholar
  10. van Bel AJ (1984) Quantification of the xylem-to-phloem transfer of amino acids by use of inulin [14C] carboxylic acid as xylem transport marker. Plant Sci Let 35:81–85CrossRefGoogle Scholar
  11. van Bel AJ (1990) Xylem-phloem exchange via the rays: the undervalued route of transport. J Exp Bot 41:631–644CrossRefGoogle Scholar
  12. van Bel AJ (1993) Strategies of phloem loading. Annu Rev Plant Phys Plant Mol Biol 44:253–281CrossRefGoogle Scholar
  13. Bergersen FJ (1971) Biochemistry of symbiotic nitrogen fixation in legumes. Ann Rev Plant Physiol 22:121–140CrossRefGoogle Scholar
  14. Besnard J, Pratelli R, Zhao C, Sonawala U, Collakova E, Pilot G, Okumoto S (2016) UMAMIT14 is an amino acid exporter involved in phloem unloading in Arabidopsis roots. J Exp Bot 67:6385–6397PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bittsánszky A, Pilinszky K, Gyulai G, Komives T (2015) Overcoming ammonium toxicity. Plant Sci 231:184–190PubMedCrossRefGoogle Scholar
  16. Bohner A, Kojima S, Hajirezaei M, Melzer M, Wirén N (2015) Urea retranslocation from senescing Arabidopsis leaves is promoted by DUR3-mediated urea retrieval from leaf apoplast. Plant J 81:377–387PubMedPubMedCentralCrossRefGoogle Scholar
  17. Britto DT, Kronzucker HJ (2002) NH4+ toxicity in plants: a critical review. J Plant Physiol 159:567–584CrossRefGoogle Scholar
  18. Carter AM, Tegeder M (2016) Increasing nitrogen fixation and seed development in soybean requires complex adjustments of nodule nitrogen metabolism and partitioning processes. Curr Biol 26:2044–2051PubMedCrossRefGoogle Scholar
  19. Chen J, Fan X, Qian K, Zhang Y, Song M, Liu Y, Xu G, Fan X (2017) pOsNAR2.1:OsNAR2.1 expression enhances nitrogen uptake efficiency and grain yield in transgenic rice plants. Plant Biotechnol J 15:1273–1283PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chen J, Zhang Y, Tan Y, Zhang M, Zhu L, Xu G, Fan X (2016) Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter. Plant Biotechnol J 14:1705–1715PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211PubMedCrossRefGoogle Scholar
  22. Collier R, Tegeder M (2012) Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. Plant J 72:355–367PubMedCrossRefGoogle Scholar
  23. Commichau FM, Forchhammer K, Stülke J (2006) Regulatory links between carbon and nitrogen metabolism. Curr Opin Microbiol 9:167–172Google Scholar
  24. Delin S, Stenberg M (2014) Effect of nitrogen fertilization on nitrate leaching in relation to grain yield response on loamy sand in Sweden. Eur J Agron 52:291–296CrossRefGoogle Scholar
  25. Delrot S, Rochat C, Tegeder M, Frommer WB (2001) Amino acid transport. In: Lea P, Gaudry JFM (eds) Plant nitrogen. INRA-Springer, Paris, France, pp 215–235Google Scholar
  26. Dickson RE, Vogelmann TC, Larson PR (1985) Glutamine transfer from xylem to phloem and translocation to developing leaves of Populus deltoides. Plant Physiol 77:412–417PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dordas CA, Sioulas C (2008) Safflower yield, chlorophyll content, photosynthesis, and water use efficiency response to nitrogen fertilization under rainfed conditions. Indust Crops Prod 27:75–85CrossRefGoogle Scholar
  28. Drechsler N, Zheng Y, Bohner A, Nobmann B, von Wirén N, Kunze R, Rausch C (2015) Nitrate-dependent control of shoot K homeostasis by the nitrate transporter1/peptide transporter family member NPF7.3/NRT1.5 and the Stelar K+ outward rectifier SKOR in Arabidopsis. Plant Physiol 169:2832–2847PubMedPubMedCentralGoogle Scholar
  29. Dündar E, Bush DR (2009) BAT1, a bidirectional amino acid transporter in Arabidopsis. Planta 229:1047–1056PubMedCrossRefGoogle Scholar
  30. Ellis RJ (1979) The most abundant protein in the world. Trends Biochem Sci 4:241–244CrossRefGoogle Scholar
  31. Engels C, Munkle L, Marschner H (1992) Effect of root zone temperature and shoot demand on uptake and xylem transport of macronutrients in maize (Zea mays L.). J Exp Bot 43:537–547CrossRefGoogle Scholar
  32. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Assoc. Inc., Sunderland, UKGoogle Scholar
  33. Escudero A, Mediavilla S (2003) Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. J Ecol 91:880–889CrossRefGoogle Scholar
  34. Fan XR, Feng HM, Tan YW, Xu YL, Miao QS, Xu GH (2016a) A putative 6-transmembrane nitrate transporter OsNRT1.1b plays a key role in rice under low nitrogen. J Integr Plant Biol 58:590–599PubMedCrossRefGoogle Scholar
  35. Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016b) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci USA 113:7118–7123PubMedCrossRefGoogle Scholar
  36. Fan X, Naz M, Fan X, Xuan W, Miller AJ, Xu G (2017) Plant nitrate transporters: from gene function to application. J Exp Bot 68:2463–2475PubMedCrossRefGoogle Scholar
  37. Fang Z, Xia K, Yang X, Grotemeyer MS, Meier S, Rentsch D, Xu X, Zhang M (2013) Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnol J 11:446–458PubMedCrossRefGoogle Scholar
  38. Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696CrossRefGoogle Scholar
  39. Feng H, Li B, Zhi Y, Chen J, Li R, Xia X, Xu G, Fan X (2017) Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation. Plant Cell Rep 36:1287–1296PubMedCrossRefGoogle Scholar
  40. Ferrario-Méry S, Valadier MH, Godefroy N, Miallier D, Hirel B, Foyer CH, Suzuki A (2002) Diurnal changes in ammonia assimilation in transformed tobacco plants expressing ferredoxin-dependent glutamate synthase mRNA in the antisense orientation. Plant Sci 163:59–67CrossRefGoogle Scholar
  41. Fischer WN, André B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195CrossRefGoogle Scholar
  42. Gallardo K, Firnhaber C, Zuber H, Héricher D, Belghazi M, Henry C, Küster H, Thompson R (2007) A combined proteome and transcriptome analysis of developing Medicago truncatula seeds: evidence for metabolic specialization of maternal and filial tissues. Mol Cell Proteomics 6:2165–2179PubMedCrossRefGoogle Scholar
  43. Gambín BL, Borrás L (2010) Resource distribution and the trade-off between seed number and seed weight: a comparison across crop species. Ann Appl Biol 156:91–102CrossRefGoogle Scholar
  44. Ganeteg U, Ahmad I, Jämtgård S, Aguetoni-Cambui C, Inselsbacher E, Svennerstam H, Schmidt S, Näsholm T (2017) Amino acid transporter mutants of Arabidopsis provides evidence that a non-mycorrhizal plant acquires organic nitrogen from agricultural soil. Plant, Cell Environ 40:413–423CrossRefGoogle Scholar
  45. Geiger D, Giaquinta R, Sovonick S, Fellows R (1973) Solute distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol 52:585–589PubMedPubMedCentralCrossRefGoogle Scholar
  46. Girondé A, Etienne P, Trouverie J, Bouchereau A, Le Cahérec F, Leport L, Orsel M, Niogret MF, Nesi N, Carole D, Soulay F (2015) The contrasting N management of two oilseed rape genotypes reveals the mechanisms of proteolysis associated with leaf N remobilization and the respective contributions of leaves and stems to N storage and remobilization during seed filling. BMC Plant Biol 15:59PubMedPubMedCentralCrossRefGoogle Scholar
  47. Glass AD, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864PubMedCrossRefGoogle Scholar
  48. Gouia H, Ghorbal MH, Touraine B (1994) Effects of NaCl on flows of N and mineral ions and on NO3- reduction rate within whole plants of salt-sensitive bean and salt-tolerant cotton. Plant Physiol 105:1409–1418PubMedPubMedCentralCrossRefGoogle Scholar
  49. Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus JM, Rentsch D (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137:117–126PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gregorich EG, Monreal CM, Carter MR, Angers DA, Ellert B (1994) Towards a minimum data set to assess soil organic matter quality in agricultural soils. Can J Soil Sci 74:367–385CrossRefGoogle Scholar
  51. Guo F-Q, Wang R, Crawford NM (2002) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J Exp Bot 53:835–844PubMedCrossRefGoogle Scholar
  52. Guo S, Kaldenhoff R, Uehlein N, Sattelmacher B, Brueck H (2007) Relationship between water and nitrogen uptake in nitrate-and ammonium-supplied Phaseolus vulgaris L. plants. J Plant Nutr Soil Sci 170:73–80CrossRefGoogle Scholar
  53. Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138:83–89CrossRefGoogle Scholar
  54. Hammes UZ, Nielsen E, Honaas LA, Taylor CG, Schachtman DP (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J 48:414–426PubMedCrossRefGoogle Scholar
  55. Haynes RJ (2012) Uptake and assimilation of mineral nitrogen by plants. Mineral nitrogen in the plant-soil system. Elsevier Science, Orlando, Fl, USA, pp 303–378Google Scholar
  56. Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer W, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hu B, Wang W, Ou S, Tang J, Li H, Che R, Zhang Z, Chai X, Wang H, Wang Y, Liang C (2015) Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat Genet 47:834–878PubMedCrossRefGoogle Scholar
  58. Huang N-C, Liu K-H, Lo H-J, Tsay Y-F (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–1392PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hunt E, Gattolin S, Newbury HJ, Bale JS, Tseng HM, Barrett DA, Pritchard J (2010) A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J Exp Bot 61:55–64PubMedCrossRefGoogle Scholar
  60. Jahn TP, Møller AL, Zeuthen T, Holm LM, Klærke DA, Mohsin B, Kühlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36PubMedCrossRefGoogle Scholar
  61. Ju X, Liu X, Zhang F, Roelcke M (2004) Nitrogen fertilization, soil nitrate accumulation, and policy recommendations in several agricultural regions of China. Ambio 33:300–305PubMedCrossRefGoogle Scholar
  62. Khan S (1971) Nitrogen fractions in a gray wooded soil as influenced by long-term cropping systems and fertilizers. Can J Soil Sci 51:431–437CrossRefGoogle Scholar
  63. Kempers R, Ammerlaan A, van Bel AJ (1998) Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically phloem-loading species. Plant Physiol 116:271–278PubMedCentralCrossRefPubMedGoogle Scholar
  64. Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA, Beecher SD, Dodgen AC, Jensen KH, Holbrook NM (2016) Testing the Münch hypothesis of long distance phloem transport in plants. eLife 5:e15341Google Scholar
  65. Kojima S, Bohner A, Gassert B, Yuan L, Wirén NV (2007) AtDUR3 represents the major transporter for high-affinity urea transport across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 52:30–40PubMedCrossRefGoogle Scholar
  66. Kojima S, Bohner A, Von Wirén N (2006) Molecular mechanisms of urea transport in plants. J Membr Biol 212:83–91PubMedCrossRefGoogle Scholar
  67. Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Grotemeyer MS, Tegeder M, Rentsch D (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol 148:856–869PubMedPubMedCentralCrossRefGoogle Scholar
  68. Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. J Exp Bot 65:789–798PubMedCrossRefGoogle Scholar
  69. Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Current Opin Plant Biol 25:115–122CrossRefGoogle Scholar
  70. Kumar A, Kaiser BN, Siddiqi MY, Glass AD (2006) Functional characterisation of OsAMT1.1 overexpression lines of rice, Oryza sativa. Funct Plant Biol 33:339–346CrossRefGoogle Scholar
  71. Kumar K, Goh K (2002) Recovery of 15N-labelled fertilizer applied to winter wheat and perennial ryegrass crops and residual 15N recovery by succeeding wheat crops under different crop residue management practices. Nutr Cycl Agroecosys 62:123–130CrossRefGoogle Scholar
  72. Ladwig F, Stahl M, Ludewig U, Hirner AA, Hammes UZ, Stadler R, Harter K, Koch W (2012) Siliques are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol 158:1643–1655PubMedPubMedCentralCrossRefGoogle Scholar
  73. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev Plant Biol 47:569–593CrossRefGoogle Scholar
  74. Lassaletta L, Billen G, Grizzetti B, Garnier J, Leach AM, Galloway JN (2014) Food and feed trade as a driver in the global nitrogen cycle: 50–year trends. Biogeochemistry 118:225–241CrossRefGoogle Scholar
  75. Lea PJ, Azevedo RA (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Ann Appl Biol 149:243–247CrossRefGoogle Scholar
  76. Lee BR, Lee DG, Avice JC, Kim TH (2014) Characterization of vegetative storage protein (VSP) and low molecular proteins induced by water deficit in stolon of white clover. Biochem Biophys Res Commun 443:229–233PubMedCrossRefGoogle Scholar
  77. Lee Y-H, Foster J, Chen J, Voll L, Weber A, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50:305–316PubMedCrossRefGoogle Scholar
  78. Lehmann S, Gumy C, Blatter E, Boeffel S, Fricke W, Rentsch D (2011) In planta function of compatible solute transporters of the AtProT family. J Exp Bot 62:787–796PubMedCrossRefGoogle Scholar
  79. Lemaître T, Gaufichon L, Boutet-Mercey S, Christ A, Masclaux-Daubresse C (2008) Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant Cell Physiol 49:1056–1065PubMedCrossRefGoogle Scholar
  80. Léran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5–9PubMedCrossRefGoogle Scholar
  81. Lewis CE, Noctor G, Causton D, Foyer CH (2000) Regulation of assimilate partitioning in leaves. Funct Plant Biol 27:507–519CrossRefGoogle Scholar
  82. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Phys 143:425–433CrossRefGoogle Scholar
  83. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874PubMedPubMedCentralCrossRefGoogle Scholar
  84. Liu Y, Ahn J-E, Datta S, Salzman RA, Moon J, Huyghues-Despointes B, Pittendrigh B, Murdock LL, Koiwa H, Zhu-Salzman K (2005) Arabidopsis vegetative storage protein is an insect acid phosphatase. Plant Physiol 139:1545–1556PubMedPubMedCentralCrossRefGoogle Scholar
  85. Liu G, Ji Y, Bhuiyan NH, Pilot G, Selvaraj G, Zou J, Wei Y (2010) Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell 22:3845–3863PubMedPubMedCentralCrossRefGoogle Scholar
  86. Lohaus G, Winter H, Riens B, Heldt HW (1995) Further studies of the phloem loading process in leaves of barley and spinach. The comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes. Plant Biol 108:270–275Google Scholar
  87. Loqué D, Ludewig U, Yuan L, von Wirén N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680PubMedPubMedCentralCrossRefGoogle Scholar
  88. Loqué D, von Wirén N (2004) Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 55:1293–1305PubMedCrossRefGoogle Scholar
  89. Makino A, Osmond B (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 96:355–362PubMedPubMedCentralCrossRefGoogle Scholar
  90. Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129PubMedCrossRefGoogle Scholar
  91. Masclaux-Daubresse C, Chardon F (2011) Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. J Exp Bot 62:2131–2142PubMedPubMedCentralCrossRefGoogle Scholar
  92. Martre P, Porter JR, Jamieson PD, Triboï E (2003) Modeling grain nitrogen accumulation and protein composition to understand the sink/source regulations of nitrogen remobilization for wheat. Plant Physiol 133:1959–1967PubMedPubMedCentralCrossRefGoogle Scholar
  93. Mérigout P, Lelandais M, Bitton F, Renou JP, Briand X, Meyer C, Daniel-Vedele F (2008) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiol 147:1225–1238PubMedPubMedCentralCrossRefGoogle Scholar
  94. Miflin BJ, Lea PJ (1977) Amino acid metabolism. Annu Rev Plant Physio 28:299–329CrossRefGoogle Scholar
  95. Millard P (1988) The accumulation and storage of nitrogen by herbaceous plants. Plant, Cell Environ 11:1–8CrossRefGoogle Scholar
  96. Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306PubMedCrossRefGoogle Scholar
  97. Miret JA, Munné-Bosch S (2014) Plant amino acids derived vitamins: biosynthesis and function. Amino Acids 46:809–824PubMedCrossRefGoogle Scholar
  98. Moll R, Kamprath E, Jackson W (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564CrossRefGoogle Scholar
  99. Mueller ND, West PC, Gerber JS, MacDonald GK, Polasky S, Foley JA (2014) A tradeoff frontier for global nitrogen use and cereal production. Environ Res Lett 9:P054002CrossRefGoogle Scholar
  100. Müller B, Fastner A, Karmann J, Mansch V, Hoffmann T, Schwab W, Suter-Grotemeyer M, Rentsch D, Truernit E, Ladwig F, Bleckmann A (2015) Amino acid export in developing Arabidopsis seeds depends on UmamiT facilitators. Curr Biol 25:3126–3131PubMedCrossRefGoogle Scholar
  101. Muurinen S, Kleemola J, Peltonen-Sainio P (2007) Accumulation and translocation of nitrogen in spring cereal cultivars differing in nitrogen use efficiency. Agron J 99:441–449CrossRefGoogle Scholar
  102. Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29CrossRefGoogle Scholar
  103. Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48PubMedCrossRefGoogle Scholar
  104. Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996PubMedCrossRefGoogle Scholar
  105. Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454PubMedCrossRefGoogle Scholar
  106. Okamoto M, Vidmar JJ, Glass ADM (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44:304–317PubMedCrossRefGoogle Scholar
  107. Oparka KJ, Turgeon R (1999) Sieve elements and companion cells—traffic control centers of the phloem. Plant Cell 11:739–750PubMedPubMedCentralGoogle Scholar
  108. Pate JS (1980) Transport and partitioning of nitrogenous solutes. Ann Rev Plant Physio 31:313–340CrossRefGoogle Scholar
  109. Pate JS, Sharkey PJ, Lewis OAM (1975) Xylem to phloem transfer of solutes in fruiting shoots of legumes, studied by a phloem bleeding technique. Planta 122:11–26PubMedCrossRefGoogle Scholar
  110. Patrick JW (1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annu Rev Plant Biol 48:191–222CrossRefGoogle Scholar
  111. Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. P Natl Acad Sci USA 105:4524–4529CrossRefGoogle Scholar
  112. Pélissier H, Frerich A, Desimone M, Schumacher K, Tegeder M (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol 134:664–675PubMedPubMedCentralCrossRefGoogle Scholar
  113. Pélissier H, Tegeder M (2007) PvUPS1 plays a role in source-sink transport of allantoin in French bean (Phaseolus vulgaris). Funct Plant Biol 18:282–291CrossRefGoogle Scholar
  114. Peoples MB, Pate JS, Atkins CA, Murray DR (1985) Economy of water, carbon, and nitrogen in the developing cowpea fruit. Plant Physiol 77:142–147PubMedCrossRefGoogle Scholar
  115. Perchlik M, Foster J, Tegeder M (2014) Different and overlapping functions of Arabidopsis LHT6 and AAP1 transporters in root amino acid uptake. J Exp Bot 65:5193–5204PubMedPubMedCentralCrossRefGoogle Scholar
  116. Perchlik M, Tegeder M (2017) Improving plant nitrogen use efficiency through alteration of amino acid transport processes. Plant Physiol 175:235–247PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rainbird RM, Thorne JH, Hardy RW (1984) Role of amides, amino acids, and ureides in the nutrition of developing soybean seeds. Plant Physiol 74:329–334PubMedPubMedCentralCrossRefGoogle Scholar
  118. Ranathunge K, El-kereamy A, Gidda S, Bi YM, Rothstein SJ (2014) AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. J Exp Bot 65:965–979PubMedPubMedCentralCrossRefGoogle Scholar
  119. Raun W, Johnson G (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363CrossRefGoogle Scholar
  120. Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581:2281–2289PubMedCrossRefGoogle Scholar
  121. Rennie EA, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proc Natl Acad Sci USA 106:14162–14167PubMedCrossRefGoogle Scholar
  122. Rolletschek H, Hosein F, Miranda M, Heim U, Götz KP, Schlereth A, Borisjuk L, Saalbach I, Wobus U, Weber H (2005) Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol 137:1236–1249PubMedPubMedCentralCrossRefGoogle Scholar
  123. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18524–18529PubMedCrossRefGoogle Scholar
  124. Sanders A, Collier R, Trethewy A, Gould G, Sieker R, Tegeder M (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J 59:540–552PubMedCrossRefGoogle Scholar
  125. Santiago J, Tegeder M (2016) Connecting source with sink: the role of Arabidopsis AAP8 in phloem loading of amino acids. Plant Physiol 171:508–521PubMedPubMedCentralCrossRefGoogle Scholar
  126. Scharff AM, Egsgaard H, Hansen PE, Rosendahl L (2003) Exploring symbiotic nitrogen fixation and assimilation in pea root nodules by in vivo 15N nuclear magnetic resonance spectroscopy and liquid chromatography-mass spectrometry. Plant Physiol 131:367–378PubMedPubMedCentralCrossRefGoogle Scholar
  127. Schobert C, Komor E (1990) Transfer of amino acids and nitrate from the roots into the xylem of Ricinus communis seedlings. Planta 181:85–90PubMedCrossRefGoogle Scholar
  128. Schmidt R, Stransky H, Koch W (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226:805–813PubMedCrossRefGoogle Scholar
  129. Schneitz K, Hülskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749CrossRefGoogle Scholar
  130. Schubert KR (1986) Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Ann Rev Plant Physiol 37:539–574CrossRefGoogle Scholar
  131. Seiffert B, Zhou Z, Wallbraun M, Lohaus G, Möllers C (2004) Expression of a bacterial asparagine synthetase gene in oilseed rape (Brassica napus) and its effect on traits related to nitrogen efficiency. Physiol Plant 121:656–665CrossRefGoogle Scholar
  132. Senwo Z, Tabatabai M (1998) Amino acid composition of soil organic matter. Biol Fert Soils 26:235–242CrossRefGoogle Scholar
  133. Servaites JC, Schrader LE, Jung DM (1979) Energy-dependent loading of amino acids and sucrose into the phloem of soybean. Plant Physiol 64:546–550PubMedPubMedCentralCrossRefGoogle Scholar
  134. Slewinski TL, Meeley R, Braun DM (2009) Sucrose transporter1 functions in phloem loading in maize leaves. J Exp Bot 60:881–892PubMedPubMedCentralCrossRefGoogle Scholar
  135. Sonoda Y, Ikeda A, Saiki S, Wirén NV, Yamaya T, Yamaguchi J (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1;1–1;3) in rice. Plant Cell Physiol 44:726–734PubMedCrossRefGoogle Scholar
  136. Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712PubMedPubMedCentralCrossRefGoogle Scholar
  137. Stahl A, Friedt W, Wittkop B, Snowdon RJ (2016) Complementary diversity for nitrogen uptake and utilisation efficiency reveals broad potential for increased sustainability of oilseed rape production. Plant Soil 400:245–262CrossRefGoogle Scholar
  138. Stöhr C, Mäck G (2001) Diurnal changes in nitrogen assimilation of tobacco roots. J Exp Bot 52:1283–1289PubMedCrossRefGoogle Scholar
  139. Streeter J (1979) Allantoin and allantoic acid in tissues and stem exudate from filed grown soybean plants. Plant Physiol 63:478–480PubMedPubMedCentralCrossRefGoogle Scholar
  140. Svennerstam H, Ganeteg U, Bellini C, Näsholm T (2007) Comprehensive screening of Arabidopsis mutants suggests the Lysine Histidine Transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143:1853–1860PubMedPubMedCentralCrossRefGoogle Scholar
  141. Svennerstam H, Ganeteg U, Näsholm T (2008) Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. New Phytol 180:620–630PubMedCrossRefGoogle Scholar
  142. Svennerstam H, Jämtgård S, Ahmad I, Huss-Danell K, Näsholm T, Ganeteg U (2011) Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytol 191:459–467PubMedCrossRefGoogle Scholar
  143. Tajima S, Nomura M, Kouchi H (2004) Ureide biosynthesis in legume nodules. Front Biosci 9:1374–1381PubMedCrossRefGoogle Scholar
  144. Tan Q, Grennan AK, Pélissier HC, Rentsch D, Tegeder M (2008) Characterization and expression of French bean amino acid transporter PvAAP1. Plant Sci 174:348–356CrossRefGoogle Scholar
  145. Tan Q, Zhang L, Grant J, Cooper P, Tegeder M (2010) Increased phloem transport of S-methylmethionine positively affects sulfur and nitrogen metabolism and seed development in pea plants. Plant Physiol 154:1886–1896PubMedPubMedCentralCrossRefGoogle Scholar
  146. Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J Exp Bot 65:1865–1878PubMedCrossRefGoogle Scholar
  147. Tegeder M, Masclaux-Daubresse C (2017) Source and sink mechanisms of nitrogen transport and use. New Phytol. Scholar
  148. Tegeder M, Rentsch D (2010) Uptake and partitioning of amino acids and peptides. Mol Plant 3:997–1011PubMedCrossRefGoogle Scholar
  149. Tegeder M, Ward JM (2012) Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Sci 3:21PubMedPubMedCentralCrossRefGoogle Scholar
  150. Tegeder M, Tan Q, Grennan AK, Patrick JW (2007) Amino acid transporter expression and localisation studies in pea (Pisum sativum). Funct Plant Biol 34:1019–1028CrossRefGoogle Scholar
  151. Todd CD, Tipton PA, Blevins DG, Piedras P, Pineda M, Polacco JC (2006) Update on ureide degradation in legumes. J Exp Bot 57:5–12PubMedCrossRefGoogle Scholar
  152. Tsay YF, Fan SC, Chen HY; Academia Sinica (2011) Method for changing nitrogen utilization efficiency in plants. U.S. Patent Application 12/832,234Google Scholar
  153. Wang WH, Köhler B, Cao FQ, Liu GW, Gong YY, Sheng S, Song QC, Cheng XY, Garnett T, Okamoto M, Qin R (2012) Rice DUR3 mediates high-affinity urea transport and plays an effective role in improvement of urea acquisition and utilization when expressed in Arabidopsis. New Phytol 193:432–444PubMedCrossRefGoogle Scholar
  154. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95:15134–15139PubMedCrossRefGoogle Scholar
  155. Weber H, Borisjuk L, Heim U, Buchner P, Wobus U (1995) Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. Plant Cell 7:1835–1846PubMedPubMedCentralGoogle Scholar
  156. Weigelt K, Küster H, Radchuk R, Müller M, Weichert H, Fait A, Fernie AR, Saalbach I, Weber H (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J 55:909–926PubMedCrossRefGoogle Scholar
  157. Windt CW, Vergeldt FJ, de Jager PA, Van As H (2006) MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant, Cell Environ 29:1715–1729CrossRefGoogle Scholar
  158. Winter H, Lohaus G, Heldt HW (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996–1004PubMedPubMedCentralCrossRefGoogle Scholar
  159. Xu G, Fan X, Miller A (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182PubMedCrossRefGoogle Scholar
  160. Yan M, Fan X, Feng H, Miller AJ, Shen Q, Xu G (2011) Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant, Cell Environ 34:1360–1372CrossRefGoogle Scholar
  161. Yang L, Cao W, Thorup-Kristensen K, Bai J, Gao S, Chang D (2015) Effect of Orychophragmus violaceus incorporation on nitrogen uptake in succeeding maize. Plant Soil Environ 61:260–265CrossRefGoogle Scholar
  162. Zhang L, Tan Q, Lee R, Trethewy A, Lee Y, 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 22:3603–3620PubMedPubMedCentralCrossRefGoogle Scholar
  163. Zhang L, Garneau M, Majumdar R, Grant J, Tegeder M (2015) Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids. Plant J 81:134–146PubMedCrossRefGoogle Scholar
  164. Zhu S, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333CrossRefGoogle Scholar
  165. Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Ann Rev Plant Biol 57:805–836CrossRefGoogle Scholar
  166. Züst T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:15206PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesWashington State UniversityPullmanUSA

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