GintAMT3-a low-affinity ammonium transporter of the arbuscular mycorrhizal rhizophagus irregularis

Frontiers in Plant Science

Volumn 7, Issue MAY2016, 2016, Pages

  Calabrese, Silvia ^a   Pérez Tienda, Jacob ^b   Ellerbeck, Matthias ^c   Arnould, Christine ^d   Chatagnier, Odile ^d   Boller, Thomas ^a   Schüßler, Arthur ^c   Brachmann, Andreas ^c   Wipf, Daniel ^d   Ferrol, Nuria ^b   Courty, Pierre Emmanuel ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b CSIC   (Spain)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

Ammonium transporter; Arbuscular mycorrhizal fungi; Extraradical mycelium; Intraradical mycelium; Low affinity transporter

Indexed keywords

EID: 84971433468     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00679     Document Type: Article

References (80)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
2. Bago, B., Pfeffer, P., and Shachar-Hill, Y. (2001). Could the urea cycle be translocating nitrogen in the arbuscular mycorrhizal symbiosis? New Phytol. 149, 4-8. doi: 10.1046/j.1469-8137.2001.00016.x
3. Bago, B., Vierheilig, H., Piché, Y., and Azcón-Aguilar, C. (1996). Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol. 133, 273-280. doi: 10.1111/j.1469-8137.1996.tb01894.x
4. Benkert, P., Biasini, M., and Schwede, T. (2011). Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27, 343-350. doi: 10.1093/bioinformatics/btq662
5. Breuninger, M., Trujillo, C. G., Serrano, E., Fischer, R., and Requena, N. (2004). Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet. Biol. 41, 542-552. doi: 10.1016/j.fgb.2004.01.003
6. Brundrett, M. C., Piché, Y., and Peterson, R. L. (1984). A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can. J. Bot. 62, 2128-2134. doi: 10.1139/b84-290
7. Cappellazzo, G., Lanfranco, L., Fitz, M., Wipf, D., and Bonfante, P. (2008). Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 147, 429-437. doi: 10.1104/pp.108.117820
8. Casieri, L., Ait Lahmidi, N., Doidy, J., Fourrey, C., Migeon, A., Bonneau, L., et al. (2013). Biotrophic transportome in mutualistic plant-fungal interactions. Mycorrhiza 23, 597-625. doi: 10.1007/s00572-013-0496-9
9. Chabot, S., Bel-Rhlid, R., Chenevert, R., and Piché, Y. (1992). Hyphal growth promotion in vitro of the VA mycorrhizal fungus, Gigaspora margarita Becker and Hall, by the activity of structurally specific flavonoid compounds under CO2-enriched conditions. New Phytol. 122, 461-467. doi: 10.1111/j.1469-8137.1992.tb00074.x
10. Chalot, M., Blaudez, D., and Brun, A. (2006). Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci. 11, 263-266. doi: 10.1016/j.tplants.2006.04.005
11. Courty, P.-E., Hoegger, P., Kilaru, S., Kohler, A., Buée, M., Garbaye, J., et al. (2009). Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol. 182, 736-750. doi: 10.1111/j.1469-8137.2009.02774.x
12. 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. doi: 10.1111/j.1469-8137.2007.01992.x
13. Cruz, C., Egsgaard, H., Trujillo, C., Ambus, P., Requena, N., Martins-Loução, M. A., et al. (2007). Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol. 144, 782-792. doi: 10.1104/pp.106.090522
14. Dohmen, R. J., Strasser, A. W. M., Höner, C. B., and Hollenberg, C. P. (1991). An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera. Yeast 7, 691-692. doi: 10.1002/yea.320070704
15. Ellerbeck, M., Schüßler, A., Brucker, D., Dafinger, C., Loos, F., and Brachmann, A. (2013). Characterization of three ammonium transporters of the Glomeromycotan fungus Geosiphon pyriformis. Eukaryot. Cell 12, 1554-1562. doi: 10.1128/EC.00139-13
16. Fortin, J. A., Bécard, G., Declerck, S., Dalpé, Y., St-Arnaud, M., Coughlan, A. P., et al. (2002). Arbuscular mycorrhiza on root-organ cultures. Can. J. Bot. 80, 1-20. doi: 10.1139/b01-139
17. Fried, M., Zsoldos, F., Vose, P. B., and Shatokhin, I. L. (1965). Characterizing the NO3 and NH4 uptake process of rice roots by use of 15N labeled NH4NO3. Physiol. Plant 18, 313-320. doi: 10.1111/j.1399-3054.1965.tb06894.x
18. Gamborg, O. L., and Wetter, L. (1975). Plant Tissue Culture Methods. National research council of Canada. Saskatoon: Prairie Regional Lab.
19. Gazzarrini, S., Lejay, L., Gojon, A., Ninnemann, O., Frommer, W. B., and von Wirén, N. (1999). Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11, 937-947. doi: 10.1105/tpc.11.5.937
20. Gomez, S. K., Javot, H., Deewatthanawong, P., Torres-Jerez, I., Tang, Y., Blancaflor, E., et al. (2009). Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 9:10. doi: 10.1186/1471-2229-9-10
21. Govindarajulu, M., Pfeffer, P. E., Jin, H., Abubaker, J., Douds, D. D., Allen, J. W., et al. (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819-823. doi: 10.1038/nature03610
22. Graham, J. (2000). Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. Curr. Adv. Mycorrhizae Res. 4, 111-126.
23. Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M. K., and Bonfante, P. (2009a). Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol. 182, 200-212. doi: 10.1111/j.1469-8137.2008.02725.x
24. Guether, M., Neuhäuser, B., Balestrini, R., Dynowski, M., Ludewig, U., and Bonfante, P. (2009b). A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150, 73-83. doi: 10.1104/pp.109.136390
25. Hawkins, H.-J., Johansen, A., and George, E. (2000). Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226, 275-285. doi: 10.1023/a:1026500810385
26. Helber, N., Wippel, K., Sauer, N., Schaarschmidt, S., Hause, B., and Requena, N. (2011). A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23, 3812-3823. doi: 10.1105/tpc.111.089813
27. Hodge, A., Helgason, T., and Fitter, A. H. (2010). Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol. 3, 267-273. doi: 10.1016/j.funeco.2010.02.002
28. Javelle, A., André, B., Marini, A.-M., and Chalot, M. (2003a). High-affinity ammonium transporters and nitrogen sensing in mycorrhizas. Trends Microbiol. 11, 53-55. doi: 10.1016/S0966-842X(02)00012-4
29. Javelle, A., Morel, M., Rodríguez-Pastrana, B.-R., Botton, B., André, B., Marini, A.-M., et al. (2003b). 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. doi: 10.1046/j.1365-2958.2003.03303.x
30. Javelle, A., Chalot, M., Söderström, B., and Botton, B. (1999). Ammonium and methylamine transport by the ectomycorrhizal fungus Paxillus involutus and ectomycorrhizas. FEMS Microbiol. Ecol. 30, 355-366. doi: 10.1111/j.1574-6941.1999.tb00663.x
31. Javelle, A., Rodrı ìguez-Pastrana, B.-R., Jacob, C., Botton, B., Brun, A., André, B., et al. (2001). Molecular characterization of two ammonium transporters from the ectomycorrhizal fungus Hebeloma cylindrosporum. FEBS Lett. 505, 393-398. doi: 10.1016/S0014-5793(01)02802-2
32. 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. doi: 10.1111/j.1469-8137.2005.01536.x
33. Johansen, A., Finlay, R. D., and Olsson, P. A. (1996). Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 133, 705-712. doi: 10.1111/j.1469-8137.1996.tb01939.x
34. Khademi, S., O’Connell, J., 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 Å. Science 305, 1587-1594. doi: 10.1126/science.1101952
35. 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. doi: 10.1093/pcp/pcq099
36. Koegel, S., Ait Lahmidi, N., Arnould, C., Chatagnier, O., Walder, F., Ineichen, K., et al. (2013a). 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. doi: 10.1111/nph.12199
37. Koegel, S., Boller, T., Lehmann, M. F., Wiemken, A., and Courty, P.-E. (2013b). Rapid nitrogen transfer in the Sorghum bicolor-Glomus mosseae arbuscular mycorrhizal symbiosis. Plant Signal. Behav. 8:e25229. doi: 10.4161/psb.25229
38. Lamoureux, G., Javelle, A., Baday, S., Wang, S., and Berneche, S. (2010). Transport mechanisms in the ammonium transporter family. Transfusion Clin. Biol. 17, 168-175. doi: 10.1016/j.tracli.2010.06.004
39. Leigh, J., Hodge, A., and Fitter, A. H. (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol. 181, 199-207. doi: 10.1111/j.1469-8137.2008.02630.x
40. López-Pedrosa, A., González-Guerrero, M., Valderas, A., Azcón-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. doi: 10.1016/j.fgb.2005.10.005
41. Loqué, D., Ludewig, U., Yuan, L., and von Wirén, N. (2005). Tonoplast intrinsic proteins AtTIP2; 1 and AtTIP2; 3 facilitate NH3 transport into the vacuole. Plant Physiol. 137, 671-680. doi: 10.1104/pp.104.051268
42. Lorenz, M. C., and Heitman, J. (1998). The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J. 17, 1236-1247. doi: 10.1093/emboj/17.5.1236
43. Lucic, E., Fourrey, C., Kohler, A., Martin, F., Chalot, M., and Brun-Jacob, A. (2008). A gene repertoire for nitrogen transporters in Laccaria bicolor. New Phytol. 180, 343-364. doi: 10.1111/j.1469-8137.2008.02580.x
44. Mäder, P., Vierheilig, H., Streitwolf-Engel, R., Boller, T., Frey, B., Christie, P., et al. (2000). Transport of 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol. 146, 155-161. doi: 10.1046/j.1469-8137.2000.00615.x
45. 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. doi: 10.1128/MCB.17.8.4282
46. Marini, A. M., Vissers, S., Urrestarazu, A., and Andre, B. (1994). Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 13, 3456-3463.
47. Martin, F. (1985). 15N-NMR studies of nitrogen assimilation and amino acid biosynthesis in the ectomycorrhizal fungus Cenococcum graniforme. FEBS Lett. 182, 350-354. doi: 10.1016/0014-5793(85)80331-8
48. Marzluf, G. A. (1996). Regulation of nitrogen metabolism in mycelial fungi. Biochem. Mol. Biol. 3, 357-368. doi: 10.1007/978-3-662-10367-8_16
49. Mayer, M., Schaaf, G., Mouro, I., Lopez, C., Colin, Y., Neumann, P., et al. (2006). Different transport mechanisms in plant and human AMT/Rh-type ammonium transporters (vol 127, pg 133, 2006). J. Gen. Physiol. 127, 353-353. doi: 10.1085/jgp.20050936920060216c
50. 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. doi: 10.1016/S1087-1845(02)00001-4
51. Ninnemann, O., Jauniaux, J. C., and Frommer, W. B. (1994). Identification of a high-affinity NH4+ transporter from plants. Embo J. 13, 3464-3471.
52. Oehl, F., Sieverding, E., Mäder, P., Dubois, D., Ineichen, K., Boller, T., et al. (2004). Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138, 574-583. doi: 10.1007/s00442-003-1458-2
53. Omasits, U., Ahrens, C. H., Müller, S., and Wollscheid, B. (2013). Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30, 884-886. doi: 10.1093/bioinformatics/btt607
54. Paterson, A. H., Bowers, J. E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., et al. (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556. doi: 10.1038/nature07723
55. Pearson, J., and Jakobsen, I. (1993). Symbiotic exchange of carbon and pho sphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol. 124, 481-488. doi: 10.1111/j.1469-8137.1993.tb03839.x
56. 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. doi: 10.1016/j.fgb.2011.08.003
57. Pérez-Tienda, J., Valderas, A., Camañes, G., García-Agustín, P., and Ferrol, N. (2012). Kinetics of NH4+ uptake by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mycorrhiza 22, 485-491. doi: 10.1007/s00572-012-0452-0
58. Pfeffer, P. E., Douds, D. D., Bécard, G., and Shachar-Hill, Y. (1999). Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120, 587-598. doi: 10.1104/pp.120.2.587
59. Schüßler, A., Schwarzott, D., and Walker, C. (2001). A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413-1421. doi: 10.1017/S0953756201005196
60. Shelden, M., Dong, B., de Bruxelles, G., Trevaskis, B., Whelan, J., Ryan, P., et al. (2001). Arabidopsis ammonium transporters, AtAMT1;1 and AtAMT1;2, have different biochemical properties and functional roles. Plant Soil 231, 151-160. doi: 10.1023/a:1010303813181
61. Smith, S. E., and Read, D. J. (2008). Mycorrhizal Symbiosis. London: Academic Press.
62. Sohlenkamp, C., Shelden, M., Howitt, S., and Udvardi, M. (2000). Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. FEBS Lett. 467, 273-278. doi: 10.1016/S0014-5793(00)01153-4
63. Soupene, E., He, L., Yan, D., and Kustu, S. (1998). Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc. Natl. Acad. Sci. U.S.A. 95, 7030-7034. doi: 10.1073/pnas.95.12.7030
64. Soupene, E., Lee, H., and Kustu, S. (2002). Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proc. Natl. Acad. Sci. U.S.A. 99, 3926-3931. doi: 10.1073/pnas.062043799
65. Soupene, E., Ramirez, R. M., and Kustu, S. (2001). Evidence that fungal MEP proteins mediate diffusion of the uncharged species NH3 across the cytoplasmic membrane. Mol. Cell. Biol. 21, 5733-5741. doi: 10.1128/mcb.21.17.5733-5741.2001
66. St-Arnaud, M., Hamel, C., Vimard, B., Caron, M., and Fortin, J. (1996). Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol. Res. 100, 328-332. doi: 10.1016/S0953-7562(96)80164-X
67. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
68. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
69. Tian, C., Kasiborski, B., Koul, R., Lammers, P. J., Bücking, H., and Shachar- Hill, Y. (2010). Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol. 153, 1175-1187. doi: 10.1104/pp.110.156430
70. Tisserant, E., Kohler, A., Dozolme-Seddas, P., Balestrini, R., Benabdellah, K., Colard, A., et al. (2012). The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol. 193, 755-769. doi: 10.1111/j.1469-8137.2011.03948.x
71. Toussaint, J.-P., St-Arnaud, M., and Charest, C. (2004). Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can. J. Microbiol. 50, 251-260. doi: 10.1139/w04-009
72. Ullrich, W. R., Larsson, M., Larsson, C.-M., Lesch, S., and Novacky, A. (1984). Ammonium uptake in Lemna gibba G1, related membrane potential changes, and inhibition of anion uptake. Physiol. Plant. 61, 369-376. doi: 10.1111/j.1399-3054.1984.tb06342.x
73. Vale, F., Volk, R., and Jackson, W. (1988). Simultaneous influx of ammonium and potassium into maize roots: kinetics and interactions. Planta 173, 424-431. doi: 10.1007/bf00401031
74. Van Dommelen, A., Keijers, V., Vanderleyden, J., and de Zamaroczy, M. (1998). (Methyl)ammonium transport in the nitrogen-fixing bacterium Azospirillum brasilense. J. Bacteriol. 180, 2652-2659.
75. Villegas, J., Williams, R. D., Nantais, L., Archambault, J., and Fortin, J. A. (1996). Effects of N source on pH and nutrient exchange of extramatrical mycelium in a mycorrhizal Ri T-DNA transformed root system. Mycorrhiza 6, 247-251. doi: 10.1007/s005720050132
76. von Wirén, N., Gazzarrini, S., Gojon, A., and Frommer, W. B. (2000). The molecular physiology of ammonium uptake and retrieval. Curr. Opin. Plant Biol. 3, 254-261. doi: 10.1016/S1369-5266(00)80074-6
77. Wang, M. Y., Glass, A., Shaff, J. E., and Kochian, L. V. (1994). Ammonium uptake by rice roots (III. Electrophysiology). Plant Physiol. 104, 899-906. doi: 10.1104/pp.104.3.899
78. Wang, M. Y., Siddiqi, M. Y., Ruth, T. J., and Glass, A. (1993). Ammonium uptake by rice roots (II. Kinetics of 13NH4+ Influx across the Plasmalemma). Plant Physiol. 103, 1259-1267. doi: 10.1104/pp.103.4.1259
79. 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. doi: 10.1007/s00294-006-0106-x
80. Wipf, D., Benjdia, M., Rikirsch, E., Zimmermann, S., Tegeder, M., and Frommer, W. B. (2003). An expression cDNA library for suppression cloning in yeast mutants, complementation of a yeast his4 mutant, and EST analysis from the symbiotic basidiomycete Hebeloma cylindrosporum. Genome 46, 177-181. doi: 10.1139/g02-121