Mycorrhiza

, Volume 27, Issue 7, pp 695–708 | Cite as

Phylogenetic, structural, and functional characterization of AMT3;1, an ammonium transporter induced by mycorrhization among model grasses

  • Sally Koegel
  • Delphine Mieulet
  • Sefer Baday
  • Odile Chatagnier
  • Moritz F. Lehmann
  • Andres Wiemken
  • Thomas Boller
  • Daniel Wipf
  • Simon Bernèche
  • Emmanuel Guiderdoni
  • Pierre-Emmanuel Courty
Original Article

Abstract

In the arbuscular mycorrhizal (AM) symbiosis, plants satisfy part of their nitrogen (N) requirement through the AM pathway. In sorghum, the ammonium transporters (AMT) AMT3;1, and to a lesser extent AMT4, are induced in cells containing developing arbuscules. Here, we have characterized orthologs of AMT3;1 and AMT4 in four other grasses in addition to sorghum. AMT3;1 and AMT4 orthologous genes are induced in AM roots, suggesting that in the common ancestor of these five plant species, both AMT3;1 and AMT4 were already present and upregulated upon AM colonization. An artificial microRNA approach was successfully used to downregulate either AMT3;1 or AMT4 in rice. Mycorrhizal root colonization and hyphal length density of knockdown plants were not affected at that time, indicating that the manipulation did not modify the establishment of the AM symbiosis and the interaction between both partners. However, expression of the fungal phosphate transporter FmPT was significantly reduced in knockdown plants, indicating a reduction of the nutrient fluxes from the AM fungus to the plant. The AMT3;1 knockdown plants (but not the AMT4 knockdown plants) were significantly less stimulated in growth by AM fungal colonization, and uptake of both 15N and 33P from the AM fungal network was reduced. This confirms that N and phosphorus nutrition through the mycorrhizal pathway are closely linked. But most importantly, it indicates that AMT3;1 is the prime plant transporter involved in the mycorrhizal ammonium transfer and that its function during uptake of N cannot be performed by AMT4.

Keywords

Arbuscular mycorrhizal symbiosis AM-inducible ammonium transporter Cereal plants Yeast complementation Artificial microRNA N transfer 

Supplementary material

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ESM 1(PDF 6749 kb)
572_2017_786_MOESM2_ESM.pdf (566 kb)
ESM 2(PDF 566 kb)
572_2017_786_MOESM3_ESM.docx (149 kb)
ESM 3(DOCX 149 kb)

References

  1. Baday S, Wang S, Lamoureux G, Bernèche S (2013) Two distinct transport mechanisms in AmtB and RhCG proteins. Biophys J 104:285aCrossRefGoogle Scholar
  2. Baday S, Orabi EA, Wang S, Lamoureux G, Bernèche S (2015) Mechanism of NH4 + recruitment and NH3 transport in Rh proteins. Structure 23:1550–1557CrossRefPubMedGoogle Scholar
  3. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691CrossRefPubMedPubMedCentralGoogle Scholar
  4. Boeckstaens ML, André B, Marini AM (2008) Distinct transport mechanisms in yeast ammonium transport/sensor proteins of the Mep/Amt/Rh family and impact on filamentation. J Biol Chem 283:21362–21370CrossRefPubMedGoogle Scholar
  5. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T (2009) Protein structure homology modelling using SWISS-MODEL workspace. Nat Protoc 4:1–13CrossRefPubMedGoogle Scholar
  6. Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, Bank MVD, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47:488–505CrossRefPubMedGoogle Scholar
  7. Breuillin-Sessoms F, Floss DS, Gomez SK et al (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter 4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 27:1352–1366CrossRefPubMedPubMedCentralGoogle Scholar
  8. Calabrese S, Perez-Tienda J, Ellerbeck M et al (2016) GiAMT3—a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Front Plant Sci 7:679CrossRefPubMedPubMedCentralGoogle Scholar
  9. Casieri L, Ait Lahmidi N, Doiddy J et al (2013) Biotrophic transportome in mutualistic plant-fungal interactions. Mycorrhiza 23:597–625CrossRefPubMedGoogle Scholar
  10. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182:736–750CrossRefPubMedGoogle Scholar
  11. Courty PE, Smith P, Koegel S, Redecker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit Rev Plant Sci 34:4–16CrossRefGoogle Scholar
  12. Couturier J, Montanini B, Martin F, Brun A, Blaudez D, Chalot M (2007) The expanded family of ammonium transporters in the perennial poplar plant. New Phytol 174:137–150CrossRefPubMedGoogle Scholar
  13. Cusack BP, Wolfe KH (2007) When gene marriages don’t work out: divorce by subfunctionalization. Trends Genet 23:270–272CrossRefPubMedGoogle Scholar
  14. Delaux PM, Séjalon-Delmas N, Bécard G, Ané JM (2013) Evolution of the plant-microbe “toolkit”. Trends Plant Sci 18:298–304CrossRefPubMedGoogle Scholar
  15. Dohmen RJ, Strasser AWM, Höner CB, Hollenberg CP (1991) An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera. Yeast 7:691–692CrossRefPubMedGoogle Scholar
  16. Fong RN, Kim KS, Yoshihara C, Inwood WB, Kustu S (2007) The W148L substitution in the Escherichia coli ammonium channel AmtB increases flux and indicates that the substrate is an ion. Proc Natl Acad Sci U S A 104:18706–18711CrossRefPubMedPubMedCentralGoogle Scholar
  17. Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol 124:221–230Google Scholar
  18. Gamborg OL, Wetter LR (1975) Plant tissue culture methods. Natrional Research Concil of Canada, SaskatoonGoogle Scholar
  19. Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–947CrossRefPubMedPubMedCentralGoogle Scholar
  20. Glémin S, Bataillon T (2009) A comparative view of the evolution of grasses under domestication. New Phytol 183:273–290CrossRefPubMedGoogle Scholar
  21. Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823CrossRefPubMedGoogle Scholar
  22. Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83CrossRefPubMedPubMedCentralGoogle Scholar
  23. Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429CrossRefPubMedPubMedCentralGoogle Scholar
  24. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091CrossRefGoogle Scholar
  25. Initiative TIB (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768CrossRefGoogle Scholar
  26. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380CrossRefGoogle Scholar
  27. Javelle A, Lupo D, Ripoche P, Fulford T, Merrick M, Winkler FK (2008) Substrate binding, deprotonation, and selectivity at the periplasmic entrance of the Escherichia coli ammonia channel AmtB. Proc Natl Acad Sci U S A 105:5040–5045CrossRefPubMedPubMedCentralGoogle Scholar
  28. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725CrossRefPubMedPubMedCentralGoogle Scholar
  29. Khademi S, O'Connell J, Remis J, Robles-Colmenares Y, Miercke LJW, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 a. Science 305:1587–1594CrossRefPubMedGoogle Scholar
  30. Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415CrossRefPubMedGoogle Scholar
  31. Koegel S, Ait Lahmidi N, Arnould C 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 198:853–865CrossRefPubMedGoogle Scholar
  32. Koegel S, Boller T, Lehmann MT, Wiemken A, Courty PE (2013b) Rapid nitrogen transfer in the Sorghum bicolor-Glomus mosseae arbuscular mycorrhizal symbiosis. Plant Signal Behav 8:e25229CrossRefPubMedPubMedCentralGoogle Scholar
  33. Koegel S, Brulé D, Wiemken A, Boller T, Courty PE (2015) The effect of different nitrogen sources on the symbiotic interaction between Sorghum bicolor and Glomus intraradices: Expression of plant and fungal genes involved in nitrogen assimilation. Soil Biol Biochem 86:159–163Google Scholar
  34. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207CrossRefPubMedGoogle Scholar
  35. López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N (2006) GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110CrossRefPubMedGoogle Scholar
  36. Ludewig U, Neuhäusser B, Dynowski M (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581:2301–2308CrossRefPubMedGoogle Scholar
  37. Mäder P, Vierheilig H, Streitwolf-Engel R, Boller T, Frey B, Christie P, Wiemken A (2000) Transport of N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146:155–161Google Scholar
  38. Marini AM, Soussi-Boudekou S, Vissers S, Andre B (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17:4282–4293CrossRefPubMedPubMedCentralGoogle Scholar
  39. Matsumoto T (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  40. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  41. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  42. Nagy R, Karandashov V, Chague W et al (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250CrossRefPubMedGoogle Scholar
  43. Ninnemann O, Jauniaux JC, Frommer WB (1994) Identification of a high-affinity NH4 + transporter from plants. EMBO J 13:3464–3471PubMedPubMedCentralGoogle Scholar
  44. Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583CrossRefPubMedGoogle Scholar
  45. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat Rev Microbiol 6:763–775CrossRefPubMedGoogle Scholar
  46. Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556CrossRefPubMedGoogle Scholar
  47. Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055CrossRefPubMedGoogle Scholar
  48. Perez-Tienda J, Corea A, Azcon-Aguilar C, Ferrol N (2014) Transcriptional regulation of host NH4 + transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiol Biochem 75:1–8CrossRefPubMedGoogle Scholar
  49. Prasad V, Strömberg CAE, Alimohammadian H, Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310:1177–1180CrossRefPubMedGoogle Scholar
  50. Ruzicka D, Hausmann N, Barrios-Masias F, Jackson L, Schachtman D (2012) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 350:145–162CrossRefGoogle Scholar
  51. Sallaud C, Meynard D, Van Boxtel J et al (2003) Highly efficient production and characterization of T-DNA plants for rice (Oryza sativa L.) functional genomics. Theor Appl Genet 106:1396–1408CrossRefPubMedGoogle Scholar
  52. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  53. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133CrossRefPubMedPubMedCentralGoogle Scholar
  54. Siewe RM, Weil B, Burkovski A, Eikmanns BJ, Eikmanns M, Krämer R (1996) Functional and genetic characterization of the (methyl)ammonium uptake carrier of Corynebacterium glutamicum. J Biol Chem 271:5398–5403CrossRefPubMedGoogle Scholar
  55. Suenaga A, Moriya K, Sonoda Y, Ikeda A, von Wiren N, Hayakawa T, Yamaguchi J, Yamaya T (2003) Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiol 44:206–211CrossRefPubMedGoogle Scholar
  56. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  57. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254CrossRefGoogle Scholar
  58. Thomas GH, Mullins JGL, Merrick M (2000) Membrane topology of the Mep/Amt family of ammonium transporters. Mol Microbiol 37:331–344CrossRefPubMedGoogle Scholar
  59. Tian CJ, Kasiborski B, Koul R, Lammers PJ, Bucking H, 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 153:1175–1187CrossRefPubMedPubMedCentralGoogle Scholar
  60. Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol 205:1632–1645CrossRefPubMedGoogle Scholar
  61. Wang B, Yeun LH, Xue JY, Liu Y, Ané JM, Qiu YL (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525CrossRefPubMedGoogle Scholar
  62. Wang S, Orabi EA, Baday S, Bernèche S, Lamoureux G (2012) Ammonium transporters achieve charge transfer by fragmenting their substrate. J Am Chem Soc 134:10419–10427CrossRefPubMedGoogle Scholar
  63. Wang S, Orabi EA, Baday S, Bernèche S, Lamoureux G (2013) Computational investigation of charge transfer mechanisms in ammonium transporters. Biophys J 104:285aCrossRefGoogle Scholar
  64. Warthmann N, Chen H, Ossowski S, Weigel D, Hervé P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3:e1829CrossRefPubMedPubMedCentralGoogle Scholar
  65. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wipf D, Benjdia M, Rikirsch E, Zimmermann S, Tegeder M, Frommer WB (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 46:177–181CrossRefPubMedGoogle Scholar
  67. Yang SY, Gronlund M, Jakobsen I, al. (2012) Non-redundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zhang G, Liu X, Quan Z et al (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30:549–554CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Sally Koegel
    • 1
  • Delphine Mieulet
    • 2
  • Sefer Baday
    • 3
    • 4
  • Odile Chatagnier
    • 5
  • Moritz F. Lehmann
    • 6
  • Andres Wiemken
    • 1
  • Thomas Boller
    • 1
  • Daniel Wipf
    • 5
  • Simon Bernèche
    • 3
  • Emmanuel Guiderdoni
    • 2
  • Pierre-Emmanuel Courty
    • 1
    • 5
  1. 1.Department of Environmental Sciences, Botany, Zurich-Basel Plant Science CenterUniversity of BaselBaselSwitzerland
  2. 2.CIRAD, UMR AGAPMontpellier Cedex 5France
  3. 3.SIB Swiss Institute of Bioinformatics and BiozentrumUniversity of BaselBaselSwitzerland
  4. 4.Applied Informatics Department, Informatics InstituteIstanbul Technical UniversityIstanbulTurkey
  5. 5.Agroécologie, AgroSupDijon, CNRS, INRAUniversité de Bourgogne Franche-ComtéDijonFrance
  6. 6.Department of Environmental Sciences, Aquatic and Stable Isotope BiogeochemistryUniversity of BaselBaselSwitzerland

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