Inorganic Nitrogen Uptake and Transport in Beneficial Plant Root-Microbe Interactions

Critical Reviews in Plant Sciences

Volumn 34, Issue , 2015, Pages 4-16

  Courty, Pierre Emmanuel ^a   Smith, Penelope ^b   Koegel, Sally ^a   Redecker, Dirk ^c   Wipf, Daniel ^c  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

arbuscular mycorrhiza; ectomycorrhiza; inorganic nitrogen; legume rhizobia symbiosis; transport

Indexed keywords

EID: 84908429186     PISSN: 07352689     EISSN: 15497836     Source Type: Journal    
DOI: 10.1080/07352689.2014.897897     Document Type: Article

References (153)

1. Abd-Alla, M.H., Koyro, H.W., Yan, F., Schubert, S., and Peiter, E. 2000. Functional structure of the indeterminate Vicia faba L. root nodule: implications for metabolite transport. Plant Physiol. 157: 335–343.
2. Aouadj, R., Es-Sgaouri, A., and Botton, B. 2000. A study of the stability and properties of nitrate reductase from the ectomycorrhizal fungus Pisolithus tinctorius. Cryptogam. Mycol. 21: 187–202.
3. Atkins, C.A., Smith, P., and Storer, P.J. 1997. Reexamination of the intracellular localization of de novo purine synthesis in cowpea nodules. Plant Physiol. 113: 127–135.
4. Bago, B., Pfeffer, P.E., Abubaker, J., Jun, J., Allen, J.W., Brouillette, J., Douds, D.D., Lammers, P.J., and Shachar-Hill, Y. 2003. Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol. 131:1496–1507.
5. Bailly, J., Debaud, J.C., Vegner, M.C., Plassard, C., Chalot, M., Marmeisse, R., and Fraissinet-Tachet, L. 2007. How does a symbiotic fungus modulate expression of its host-plant nitrite reductase? New Phytol. 175: 155–165.
6. Barber, S.A. 1995. Soil Nutrient Bioavailability: A Mechanistic Approach. 2nd edition. Wiley, New York.
7. Benedito, V.A., Li, H., Dai, X., Wandrey, M., He, J., Kaundal, R., Torres-Jerez, I., Gomez, S.K., Harrison, M.J., Tang, Y., Zhao, P.X., and Udvardi, M.K. 2010. Genomic inventory and transcriptional analysis of Medicago truncatula transporters. Plant Physiol. 152: 1716–1730.
8. Berger, H., Basheer, A., Böck, S., Reyes-Dominguez, Y., Dalik, T., Altmann, F., and Strauss, J. 2008. Dissecting individual steps of nitrogen transcription factor cooperation in the Aspergillus nidulans nitrate cluster. Mol. Microbiol. 69: 1385–1398.
9. 2-fixing bacteria. Planta 215: 424–429.
10. Bernreiter, A., Ramon, A., Fernandez-Martinez, J., Berger, H., Araujo-Bazon, L., Esperso, E.A., Pachlinger, R., Gailmetzer, A., Anderi, L., Scazzocchio, C., and Strauss, J. 2007. Nuclear export of the transcription factor NirA is a regulatory check-point for nitrate induction in Aspergillus nidulans. Mol. Cell. Biol. 27: 791–802.
11. Bishop, P.E., Guevara, J.G., Engelke, J.A., and Evans, H.J. 1976. Relation between glutamine synthetase and nitrogenase activities in the symbiotic association between Rhizobium japonicum and Glycine max. Plant Physiol. 57: 542–546.
12. Brown, C.M. and Dilworth, M.J. 1975. Ammonia assimilation by Rhizobium cultures and bacteroids. J. Gen. Microbiol. 86: 39–48.
13. Brown, S.M., Oparka, K.J., Sprent, J.I., and Walsh, K.B. 1995. Symplastic transport in soybean root nodules. Soil Biol. Biochem. 27: 387–399.
14. Burger, M., Jackson, L.E., Lundquist, E.J., Louie, D.T., Miller, R.L., Roiston, D.E., and Scow, K.M. 2005. Microbial responses and nitrous oxide emissions during wetting and drying of organically and conventionally managed soil under tomatoes. Biol. Fertil. Soils 42: 109–118.
15. Caddick, M.X., Peters, P., and Platt, A. 1994. Nitrogen regulation in fungi. Antonie van Leeuwenhoek 65: 169–177.
16. Collier, R. and Tegeder, M. 2012. Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. Plant J. 72: 355–367.
17. Crawford, N.M. and Glass, A.D. M. 1998. Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci. 3: 389–395.
18. Cardenas-Navarro, R., Adamowics, S., and Robin, P. 1998. Diurnal nitrate uptake in young tomato (Lycopersicon esculentum Mill.) plants: test of a feedback-based model. J. Exp. Bot. 49: 721–730.
19. Chalot, M., Blaudez, D., and Brun, A. 2006. Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci. 11: 263–266.
20. Chalot, M. and Plassard, C. 2011. Ectomycorrhiza and nitrogen provision to the host tree. In: Ecological Aspects of Nitrogen Metabolism in Plants, Polacco, J.C., and Todd, C.D., Eds. John Wiley & Sons Inc., Hoboken, NJ.
21. Clemmensen, K.E., Sorensen, P.L., Michelsen, A., Jonasson, S., and Ström, L. 2008. Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155: 771–783.
22. Couturier, J., Montanini, B., Martin, F., Brun, A., Blaudez, D., and Chalot, M. 2007. The expanded family of ammonium transporters in the perennial poplar plant. New Phytol. 174: 137–150.
23. Crawford, N.M. and Arst, H.N., Jr. 1993. The molecular genetics of nitrate assimilation in fungi and plants. Annu. Rev. Genet. 27: 115–146.
24. D’Apuzzo, E., Rogato, A., Simon-Rosin, U., El Alaoui, H., Barbulova, A., Betti, M., Dimou, M., Katinakis, P., Marquez, A., Marini, A.M., Udvardi, M.K., and Chiurazzi, M. 2004. Characterization of three functional high-affinity ammonium transporters in Lotus japonicus with differential transcriptional regulation spatial expression. Plant Physiol. 134: 1763–1774.
25. De Willigen, P. 1986. Supply of soil nitrogen to the plant during the growing season. In: Fundamental, Ecological and Agricultural Aspects of Nitrogen Metabolism in Higher Plants, pp. 417–432. Lambers, H., Neeteson, J.J., Stulen, I., Eds. Martinus Nijhoff, Dordrecht.
26. Dietz, S., von Bülow, J., Beitz, E., and Nehls, U. 2011. The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytol. 190: 927–940.
27. Fellbaum, C.R., Gachomo, E.W., Beesetty, Y., Choudhari, S., Strahan, G.D., Pfeffer, P.E., Kiers, E.T., and Buecking, H. 2012. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 109: 2666–2671.
28. Feng, H., Yan, M., Fan, X., Li, B., Shen, Q., Miller, A.J., and Xu, G. 2011. Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J. Exp. Bot. 62: 2319–2332.
29. Fernandez, E. and Galvan, E. 2008. Nitrate assimilation in Chlamydomonas. Eukaryot Cell 7: 555–559.
30. Forde, B.G. 2000. Nitrate transporters in plants: structure, function and regulation. Biochim. Biophys. Acta 1465: 219–235.
31. Forde, B.G. 2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol. 53: 203–224.
32. Foyer, C.H., Parry, M., and Noctor, G. 2003. Markers and signals associated with nitrogen assimilation in higher plants. J. Exp. Bot. 54: 585–593.
33. Fu, Y.H., Feng, B., Evans, S., and Marzluf, G.A. 1995. Sequence-specific DNA binding by NIT4, the pathway specific regulatory protein that mediates nitrate induction. Neurospora. Mol. Microbiol. 15: 935–942.
34. Fu, Y.H. and Marzluf, G.A. 1987. Characterization of nit-2, the major nitrogen regulatory gene of Neurospora crassa. Mol. Cell. Biol. 7: 1691–1696.
35. Gaude, N., Bortfeld, S., Duensing, N., Lohse, M., and Krajinski, F. 2011. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo a massive and specific reprogramming during arbuscular mycorrhizal development. Plant J. 69: 510–528.
36. Gazzarrini, S., Lejay, T., Gojon, A., Ninnemann, O., Frommer, W.B., and von Wiren, N. 1999. Three functional transporters for constitutive, diurnally regulated, and starvation- induced uptake of ammonium into Arabidopsis roots. Plant Cell 11: 937–947.
37. Glass, A.D. M. 2003. Nitrogen use efficiency of crop plants: Physiological constraints upon nitrogen absorption. Crit. Rev. Plant Sci. 22: 453–470.
38. − uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association. New Phytol. 154: 509–516.
39. +. Plant Cell Environ. 30: 1309–1319.
40. Godde, M. and Conrad, R. 2000. Influence of soil properties on the turn over of nitric oxide and nitrous oxide by nitrification and denitrification at constant temperature and moisture. Biol. Fertil. Soils 32: 120–128.
41. Gomez, S.K., Javot, H., Deewatthanawong, P., Torres-Jerez, I., Tang, Y.H., Blancaflor, E.B., Udvardi, M.K., and Harrison, M.J. 2009. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 9: 10.
42. Gorfer, M., Blumhoff, M., Klaubauf, S., Urban, A., Inselsbacher, E., Bandian, D., Mitter, B., Sessitsch, A., Wanek, W. and Strauss, J. 2011. Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. ISME J. 11: 1771–1783.
43. Gregory, P.J. 2006. Plant Roots: Growth, Activity and Interaction with Soils. Blackwell Publishing, Oxford.
44. Gessler, A., Schneider, S., Von Sengbusch, D., Weber, P., Hanemann, U., Huber, C., Rothe, A., Kreutzer, K., and Rennenberg, H. 1998. Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol. 138: 275–285.
45. Govindarajulu, M., Pfeffer, P.E., Jin, H.R., Abubaker, J., Douds, D.D., Allen, J.W., Bucking, H., Lammers, P.J., and Shachar-Hill, Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819–823.
46. Guescini, M., Pierloeni, R., Palma, F., Zeppa, S., Vallorani, L., Potenza, L., Sacconi, C., Giomaro, G., and Stocchi, V. 2003. Characterization of the Tuber borchii nitrate reductase gene and its role in ectomycorrhizae. Mol. Genet. Genomics 269: 807–816.
47. Guescini, M., Zeppa, S., Pierleoni, R., Sisti, D., Stocchi, L., and Stocchi, V. 2007. The expression profile of the Tuber borchii nitrite reductase suggests its positive contribution to the host plant nitrogen nutrition. Curr. Genet. 5: 31–41.
48. Guether, M., Neuhauser, B., Balestrini, R., Dynowski, M., Ludewig, U., and Bonfante, P. 2009. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150: 73–83.
49. Guidot, A., Verner, M.C., Debaud, J.C., and Marmeisse, R. 2005. Intraspecific variation in use of different organic nitrogen sources by the ectomycorrhizal fungus Hebeloma cylindrosporum. Mycorrhiza 15: 167–177.
50. Hacquart, S., Tisserand, E., Brun, A., Legué, V., Martin, F., and Kohler, A. 2013. Laser microdissection and microarray analysis of Tuber melanosporum ectomycorrhizas reveal functional heterogeneity between mantle and Hartig net compartments. Environ. Microbiol. 15: 1853–1869.
51. Hildebrandt, U., Schmelzer, E., and Bothe, H. 2002. Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol. Plant. 115: 125–136.
52. Hobbie, E.A. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 8: 563–569.
53. Hogekamp, C., Arndt, D., Pereira, P.A., Becker, J.D., Hohnjec, N., and Kuster, H. 2011. Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-Box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol. 157: 2023–2043.
54. Hohnjec, N., Vieweg, M.F., Pühler, A., Becker, A., and Küster, H. 2005. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137: 1283–1301.
55. Howitt, S.M., Udvardi, M.K., Day, D.A., and Gresshoff, P.M. 1986. Ammonia transport in free-living and symbiotic Rhizobium sp. ANU289. J. Gen. Microbiol. 132: 257–261.
56. Howitt, S.M., and Udvardi, M.K. 2000. Structure, function and regulation of ammonium transporters in plants. Biochim. Biophys. Acta BBA - Biomembranes 1465: 152–170.
57. Jackson, L.E., Burger, M., and Cavagnaro, T.R. 2008. Roots, nitrogen transformations, and ecosystem services. Annu. Rev. Plant Biol. 59: 341–363.
58. Jargeat, P., Gay, G., Debaud, J.C., and Marmeisse, R. 2000. Transcription of a nitrate reductase gene isolated from the symbiotic basidiomycete fungus Hebeloma cylindrosporum does not require induction by nitrate. Mol. Genet. Genomics 263: 948–956.
59. Jargeat, P., Rekangalt, D., Verner, M., Gay, G., Debaud, J., Marmeisse, R., and Fraissinet-Tachet, L. 2003. Characterisation and expression analysis of a nitrate transporter and nitrite reductase genes, two members of a gene cluster for nitrate assimilation from the symbiotic basidiomycete Hebeloma cylindrosporum. Curr. Genet. 43: 199–205.
60. Javelle, A., Rodriguez-Pastrana, B.R., Jacob, C., Botton, B., Brun, A., André, B., Marini, A.M., and Chalot, M. 2001. Molecular characterization of two ammonium transporters from the ectomycorrhizal fungus Hebeloma cylindrosporum. FEBS Lett. 505: 393–398.
61. Javelle, A., Morel, M., Rodríguez-Pastrana, B.R., Botton, B., André, B., Marini, A.M., Brun, A., and Chalot, M. 2003. Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium-metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum. Mol. Microbiol. 47: 411–430.
62. Jeong, J., Suh, S., Guan, C., Tsay, Y.F., Moran, N., Oh, C.J., An, C.S., Demchenko, K.N., Pawlowski, K., and Lee, Y. 2004. A nodule-specific dicarboxylate transporter from alder is a member of the peptide transporter family. Plant Physiol. 134: 969–978.
63. Jin, H., Pfeffer, P.E., Douds, D.D., Piotrowski, E., Lammers, P.J., and Shachar-Hill, Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 168: 687–696.
64. Khademi, S., O’Connell, J., III, Remis, J., Robles-Colmenares, Y., Miercke, L.J. W., and Stroud, R.M. 2004. Mechanism of Ammonia Transport by Amt/MEP/Rh: Structure of AmtB at 1.35 A. Science 305: 1587–1594.
65. Kobae, Y., Tamura, Y., Takai, S., Banba, M., and Hata, S. 2010. Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in Soybean. Plant Cell Physiol. 51: 1411–1415.
66. Koegel, S., Ait Lahmidi, N., Arnould, C., Chatagnier, O., Walder, F., Ineichen, K., Boller, T., Wipf, D., Wiemken, A., and Courty, P.E. 2013. The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol. 198: 853–865.
67. Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., Hoyerova, K., Tillard, P., Leon, S., Ljung, K., Zazimalova, E., Benkova, E., Nacry, P., and Gojon, A. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell. 18: 927–937.
68. Kudla, B., Caddick, M.X., Langdon, T., Marinez-Rossi, N.M., Bennett, C.F., Sibley, C.F., Davies, R.W., and Arst, H.N. Jr. 1990. The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 9: 1355–1364.
69. Lauter, F.R., Ninnemann, O., Bucher, M., Riesmeier, J.W., and Frommer, W.B. 1996. Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc. Natl. Acad. Sci. USA. 93: 8139–8144.
70. − uptake systems by N- and C-status of Arabidopsis plants. Plant J. 18: 509–519.
71. Lejay, L., Gansel, X., Cerezo, M., Tillard, P., Müller, C., Krapp, A., von Wirén, N., Daniel-Velede, F., and Gojon, A. 2003. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15: 2218–2232.
72. Léran, S., Varala, K., Boyer, J.C., Chiurazzi, M., Crawford, N., Daniel-Vedele, F., David, L., Dickstein, R., Fernandez, E., Forde, B., Gassmann, W., Geiger, D., Gojon, A., Gong, J.M., Halkier, B.A., Harris, J.M., Hedrich, R., Limami, A.M., Rentsch, D., Seo, M., Tsay, Y.F., Zhang, M., Coruzzi, G., and Lacombe, B. 2013. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Plant Cell, doi.org/10.1016/j.tplants.2013.08.008.
73. 2 fixation by bacteroids from soybean root nodules. Microbiology 148: 1959–1966.
74. Libault, M., Farmer, A., Joshi, T., Takahashi, K., Langley, R.J., Franklin, L.D., He, J., Xu, D., May, G., and Stacey, G. 2010. An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 63: 86–99.
75. Liu, K.H., Huang, C.Y., and Tsay, Y.F. 1999. CHL1 is a dual- affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11, 865–874.
76. Liu, K.H., and Tsay, Y.F. 2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22: 1005–1013.
77. Lodwig, E.M., Hosie, A.H., Bourdès, A., Findlay, K., Allaway, D., Karunakaran, R., Downie, J.A., and Poole, P.S. 2003. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature. 422: 722–726.
78. Lopez-Pedrosa, A., Gonzalez-Guerrero, M., Valderas, A., Azcon-Aguilar, C., and Ferrol, N. 2006. GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet. Biol. 43: 102–110.
79. Loque, D., and von Wiren, N. 2004. Regulatory levels for the transport of ammonium in plant roots. J. Exp. Bot. 55: 1293–1305.
80. Loque, D., Mora, S.I., Andrade, S.L. A., Pantoja, O., and Frommer, W.B. 2009. Pore mutations in ammonium transporter AMT1 with increased electrogenic ammonium transport activity. J. Biol. Chem. 284: 24988–24995.
81. Lucic, E., Fourrey, C., Kohler, A., Martin, F., Chalot, M., and Brun-Jacob, A. 2008. A gene repertoire for nitrogen transport in Laccaria bicolor. New Phytol. 180: 323–364.
82. + by the root hair plasma membrane ammonium transporter LeAMT1;1. J. Biol. Chem. 277: 13548–13555.
83. Mader, P., Vierheilig, H., Streitwolf-Engel, R., Boller, T., Frey, B., Christie, P., and Wiemken, A. 2000. Transport of N-15 from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol. 146: 155–161.
84. Marini, A.M., Vissers, S., Urrestarazu, B., and André, B. 1994. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 13: 3456–3463.
85. Marini, A.M., Soussi Boudekou, S., Vissers, S., and Andre, B. 1997. A family of ammonium transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 4282–4293.
86. Marschner, H. 1995. Mineral Nutrition of Higher Plants. 2nd edition. Academic Press, London
87. Marzluf, G.A. 1997. Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61: 17–32.
88. Masalkar, P., Wallace, I.S., Hwang, J.H., and Roberts, D.M. 2010. Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol. Chem. 285: 23880–23888.
89. Miller, A., and Cramer, M. 2004. Root nitrogen acquisition and assimilation. Plant Soil 274: 1–36.
90. Miller, A.J., Fan, X.R., Orsel, M., Smith, S.J., and Wells, D.M. 2007. Nitrate transport and signalling. J. Exp. Bot. 58: 2297–2306.
91. Montanini, B., Moretto, N., Soragni, E., Percudani, R., and Ottonello, S. 2002. A high-affinity ammonium transporter from the mycorrhizal ascomycete Tuber borchii. Fungal Genet. Biol. 36: 22–34.
92. Montanini, B., Viscomi, A.R., Bolchi, A., Martin, Y., Siverio, J.M., Balestrini, R., Bonfante, P., and Ottonello, S. 2006. Functional properties and differential mode of regulation of the nitrate transporter from a plant symbiotic ascomycete. Biochem J. 394: 125–134.
93. Montesinos, M.L., Muro-Pastor, A.M., Herrero, A., and Flores, E. 1998. Ammonium/Methylammonium Permeases of a Cyanobacterium: Identification and analysis of three nitrogen-regulated AMT genes in Synechocystis sp. PCC. J. Biol. Chem. 273: 31463–31470.
94. Nehls, U., and Hampp, R., 2000. Carbon allocation in ectomycorrhizas. Physiol. Mol. Plant Pathol. 57: 95–100.
95. Nehls, U., Grunze, N., Willmann, M., Reich, M., and Küster, H. 2007. Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochem. 86: 82–91.
96. +-N) on arbuscular mycorrhiza development and N transfer in a Glomus intraradices - cowpea symbiosis. Mycorrhiza 23: 107–117.
97. Niemietz, C.M. and Tyerman, S.D. 2000. Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett. 465: 110–114.
98. + transporter from plants. EMBO J. 13: 3464–3471.
99. Nygren, C.M. R., Eberhardt, U., Karlsson, M., Parret, J.L., Lindahl, B.D., and Taylor, A.F. S. 2008. Growth on nitrate and occurrence of nitrate reductase-encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi. New Phytol. 180: 875–889.
100. Orsel, M., Filleur, S., Fraisier, V., and Daniel-Vedele, F. 2002a. Nitrate transport in plants: which gene and which control? J. Exp. Bot. 53: 825–833.
101. Orsel, M., Krapp, A., and Daniel-Vedele, F. 2002b. Analysis of the NRT2 nitrate transporter family in Arabidopsis: structure and gene expression. Plant Physiol. 129: 886–896.
102. Orsel, M., Chopin, F., Leleu, O., Smith, S.J., Krapp A, Daniel-Vedele, F., and Miller, A.J. 2006. Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein–protein interaction. Plant Physiol. 142: 1304–1317.
103. Pearson, J.N., Finnemann, J., and Schjoerring, J.K. 2002. Regulation of the high-affinity ammonium transporter (BnAMT1;2) in the leaves of Brassica napus by nitrogen status. Plant Mol. Biol. 49: 483–490.
104. Peiter, E., Yan, F., and Schubert, S. 2004. Amino acid export from infected cells of Vicia faba root nodules: evidence for an apoplastic step in the infected zone. Physiol. Plant. 122: 107–114.
105. Pélissier, H. C., Frerich, A., Desimone, M., Schumacher, K., and Tegeder, M. 2004. PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol. 134: 664675.
106. Pérez-Tienda, J., Testillano, P.S., Balestrini, R., Fiorilli, V., Azcón-Aguilar, C., and Ferrol, N. 2011. GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet. Biol. 48: 1044–1055.
107. Plassard, C., Bonafos, B., and Touraine, B. 2000. Differential effects of mineral and organic N sources, and of ectomycorrhizal infection by Hebeloma cylindrosporum, on growth and N utilization in Pinus pinaster. Plant Cell Environ. 23: 1195–1205.
108. Plassard, C., Guérin-Laguet, E.A., Véry, A.A., Casarin, V., and Thibaud, J.B. 2002. Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant Cell Environ. 25: 1–10.
109. Prell, J., Bourdes, A., Kumar, S., Lodwig, E., Hosie, A., Kinghorn, S., White, J., and Poole, P. 2010 Role of symbiotic auxotrophy in the Rhizobium-legume symbioses. PLoS One 5: e13933.
110. Prell, J., White, J.P., Bourdes, A., Bunnewell, S., Bongaerts, R.J., and Poole, P.S. 2009. Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci U S A 106247712482.
111. Punt, P.J., Strauss, J., Smit, R., Kinghorn, J.R., van den Honderl, C.A. M. J. J., and Scazzocchio, C. 1995. The intergenic region between the divergently transcribed niiA and niaD genes of Aspergillus nidulans contains multiple NirA- binding sites which act bidirectionally. Mol. Cell. Biol. 10: 5688–5699.
112. Quesada, A., Hidalgo, J., and Fernandez, E. 1998. Three Nrt2 genes are differentially regulated in Chlamydomonas reinardtii. Mol. Gen. Genet. 258: 373–377.
113. Rangel-Castro, J.I., Danell, E., and Taylor, F. 2002. Use of different nitrogen sources by the edible ectomycorrhizal mushroom Cantharellus cibarius. Mycorrhiza 12: 131–137.
114. Read, D.J., and Perez-Moreno, J. 2003. Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol. 157: 475–492.
115. 2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiol. 128: 370–378.
116. Rogato, A., D’Apuzzo, E., Barbulova, A., Omrane, S., Stedel, C., Simon-Rosin, U., Katinakis, P., Flemetakis, M., Udvardi, M., and Chiurazzi, M. 2008. Tissue-specific down-regulation of LjAMT1;1 compromises nodule function and enhances nodulation in Lotus japonicus. Plant Mol Biol. 68: 585–595.
117. Ruzicka, D.R., Hausmann, N.T., Barrios-Masias, F.H., Jackson, L.E., and Schachtman, D.P. 2012. Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 350: 145–162.
118. Salehin, M., Huang, Y.S., Bagchi, R., Sherrier, D.J., and Dickstein, R. 2012. Allelic differences in Medicago truncatula NIP/LATD mutants correlate with their encoded proteins’ transport activities in planta. Plant Signal Behav. 8: e22813.
119. Salvemini, F., Marini, A.M., Riccio, A., Patriarca, E.J., and Chiurazzi, M. 2001. Functional characterization of an ammonium transporter gene from Lotus japonicus. Gene 270: 237–243.
120. Scazzocchio, C. 2000. The fungal GATA-factors. Curr. Opin. Microbiol. 3: 126–131.
121. Scheromm, P., Plassard, P., and Salsac, L. 1990. Regulation of nitrate reductase in the ectomycorrhizal basidiomycete Hebeloma cylindrosporum Romagn., cultured on nitrate or ammonium. New Phytol. 112: 441–447.
122. Selle, A., Willmann, M., Grunze, N., Gessler, A, Weiss, M., and Nehls, U. 2005. The high-affinity poplar ammonium importer PttAMT1.2 and its role in ectomycorrhizal symbiosis. New Phytol. 168: 697–706.
123. Severin, A.J., Woody, J.L., Bolon, Y.T., Joseph, B., Diers, B.W., Farmer, A.D., Muehlbauer, G.J., Nelson, R.T., Grant, D., Specht, J.E., Graham, M.A., Cannon, S.B., May, G.D., Vance, C.P., and Shoemaker, R.C. 2010. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10: 160.
124. Siewe, R.M., Weil, B., Burkovski, A., Eikmanns, B.J., Eikmanns, M., and Krämer, R. 1996. Functional and genetic characterization of the (methyl)ammonium uptake carrier of Corynebacterium glutamicum. J. Biol. Chem. 271: 5398–5403.
125. Simon-Rosin, U., Wood, C., and Udvardi, M.K. 2003. Molecular and cellular characterisation of LjAMT2;1, an ammonium transporter from the model legume Lotus japonicus. Plant Mol. Biol. 51: 99–108.
126. Smith, P.M., and Atkins, C.A. 2002. Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol. 128: 793–802.
127. Smith, S.E. and Smith, F.A. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62: 227–250
128. Smith, S.E., and Read, D.J. 2008. Mycorrhizal Symbiosis. Cambridge, UK: Academic Press.
129. Söderström, B., 2002. Challenges for mycorrhizal research into the new millennium. Plant Soil 244: 1–7.
130. Sonoda, Y., Ikeda, A., Saiki, S., von Wiren, N., Yamaya, T., and Yamaguchi, J. 2003. Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice. Plant Cell Physiol. 44: 726–734.
131. Streeter, J.G. 1992. Analysis of apoplastic solutes in the cortex of soybean nodules. Physiol. Plant. 84: 584–592.
132. Suenaga, A., Moriya, K., Sonoda, Y., Ikeda, A., von Wiren, N., Hayakawa, T., Yamaguchi, J., and Yamaya, T. 2003. Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiol. 44: 206–211.
133. Tanaka, Y. and Yano, K. 2005. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ. 28: 1247–1254.
134. Tinker, P.B. and Nye, P.H. 2000. Solute Movement in the Rhizosphere. Oxford University Press, New York.
135. Tsay, Y.F., Chiu, C.C., Tsai, C.B., Ho, C.H., and Hsu, P.K. 2007. Nitrate transporters and peptide transporters. FEBS Lett. 58: 2290–2300.
136. 2-fixing plants. Nature 378: 629–632.
137. Udvardi, M.K. and Day, D.A. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 493–523.
138. Udvardi, M. and Poole, P.S. 2013. Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64: 781805.
139. Van Dommelen, A., Keijers, V., Vanderleyden, J., and de Zamaroczy, M. 1998. (Methyl)ammonium transport in the nitrogen-fixing bacterium Azospirillum brasilense. J. Bact. 180: 2652–2659.
140. Vidmar, J.J., Zhuo, D., Siddiqi, M.Y., Schjoerring, J.K., Touraine, B., and Glass, A.D. M. 2000. Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol. 123: 307–318.
141. Vincill, E.D., Szczyglowski, K., and Roberts, D.M. 2005. GmN70 and LjN70. Anion transporters of the symbiosome membrane of nodules with a transport preference for nitrate. Plant Physiol. 137: 1435–1444.
142. von Wiren, N., Lauter, F.R., Ninnemann, O., Gillissen, B., Walch-Liu, P., Engels, C., Jost, W., and Frommer, W.B. 2000. Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J. 21: 167–175.
143. Wang, R., Liu, D., and Crawford, N.M. 1998. The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl. Acad. Sci. USA. 95: 15134–15139.
144. Wang, S., Orabi, E.A., Baday, S., Bernèche, S., and Lamoureux, G. 2012. Ammonium transporters achieve charge transfer by fragmenting their substrate. J. Am. Chem. Soc. 134: 10419–10427.
145. 2-fixing soybean nodule bacteroids. Proc. Natl. Acad. Sci. USA 95: 12038–12042.
146. Willmann, A., Weiss, M., and Nehls, U. 2007. Ectomycorrhiza-mediated repression of the high- affinity ammonium importer gene AmAMT2 in Amanita muscaria. Curr. Genet. 51: 71–78.
147. Wong, K.H., Hynes, M.J., and Davis, M.A. 2008. Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot. Cell 7: 917–925.
148. Wood, C.C., Porée, F., Dreyer, I., Koehler, G.J., and Udvardi, M.K. 2006. Mechanisms of ammonium transport, accumulation, and retention in oocytes and yeast cells expressing Arabidopsis AtAMT1;1. FEBS Lett. 580: 3931–3936.
149. Wright, D.P., Read, D.J., and Scholes, J.D. 1998. Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell. Environ. 21: 881–891.
150. Yamanaka, T. 1999. Utilization of inorganic nitrogen in pure cultures by saprotrophic and ectomycorrhizal fungi producing sporophores on urea-treated forest floor. Mycol. Res. 103: 811–816.
151. Yendrek, C.R., Lee, Y.C., Morris, V., Liang, Y., Pislariu, C.I., Burkart, G., Meckfessel, M.H., Salehin, M., Kessler, H., Wessler, H., Lloyd, M., Lutton, H., Teillet, A., Sherrier, D.J., Journet, E.P., Harris, J.M., and Dickstein, R. 2010. A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J. 62: 100–112.
152. Zheng, L., Kostrewa, D., Bernèche, S., Winkler, F.K., and Li, X.D. 2004. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc. Natl. Acad. Sci. USA. 101: 17090–17095.
153. Zrenner, R., Stitt, M., Sonnewald, U., and Boldt, R. 2006. Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57: 805–836.