Modelling Ammonium Transporters in Arbuscular Mycorrhiza Symbiosis

  • Mario Coppo
  • Ferruccio Damiani
  • Maurizio Drocco
  • Elena Grassi
  • Mike Guether
  • Angelo Troina
Part of the Lecture Notes in Computer Science book series (LNCS, volume 6575)


The Stochastic Calculus of Wrapped Compartments (SCWC) is a recently proposed variant of the Stochastic Calculus of Looping Sequences (SCLS), a language for the representation and simulation of biological systems. In this work we apply SCWC to model a newly discovered ammonium transporter. This transporter is believed to play a fundamental role for plant mineral acquisition, which takes place in the arbuscular mycorrhiza, the most wide-spread plant-fungus symbiosis on earth. Investigating this kind of symbiosis is considered one of the most promising ways to develop methods to nurture plants in more natural manners, avoiding the complex chemical productions used nowadays to produce artificial fertilizers. In our experiments the passage of NH 3 / NH 4  +  from the fungus to the plant has been dissected in known and hypothetical mechanisms; with the model so far we have been able to simulate the behavior of the system under different conditions. Our simulations confirmed some of the latest experimental results about the LjAMT2;2 transporter. Moreover, by comparing the behaviour of LjAMT2;2 with the behaviour of another ammonium transporter which exists in plants, viz. LjAMT1;1, our simulations support an hypothesis about why LjAMT2;2 is so selectively expressed in arbusculated cells.


Arbuscular Mycorrhizal Fungus Arbuscular Mycorrhiza Stochastic Calculus Open Term Ammonium Transporter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Abate, A., Bai, Y., Sznajder, N., Talcott, C., Tiwari, A.: Quantitative and probabilistic modeling in Pathway Logic. In: IEEE 7th International Symposium on Bioinformatics and Bioengineering. IEEE, Los Alamitos (2007)Google Scholar
  2. 2.
    Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., Walter, P.: Molecular Biology of the Cell. Garland Science (2007)Google Scholar
  3. 3.
    Aldinucci, M., Coppo, M., Damiani, F., Drocco, M., Giovannetti, E., Grassi, E., Troina, A.: SCWC-bio-simulator. Dipartimento di Informatica, Università di Torino (2010),
  4. 4.
    Alur, R., Belta, C., Ivancic, F.: Hybrid modeling and simulation of biomolecular networks. In: Di Benedetto, M.D., Sangiovanni-Vincentelli, A.L. (eds.) HSCC 2001. LNCS, vol. 2034, pp. 19–32. Springer, Heidelberg (2001)CrossRefGoogle Scholar
  5. 5.
    Aman, B., Dezani-Ciancaglini, M., Troina, A.: Type disciplines for analysing biologically relevant properties. Electr. Notes Theor. Comput. Sci. 227, 97–111 (2009)CrossRefzbMATHGoogle Scholar
  6. 6.
    Balestrini, R., Gomez-Ariza, J., Lanfranco, L., Bonfante, P.: Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol. Plant Microbe Interact. 20, 1055–1062 (2007)CrossRefGoogle Scholar
  7. 7.
    Barbuti, R., Maggiolo-Schettini, A., Milazzo, P., Tiberi, P., Troina, A.: Stochastic calculus of looping sequences for the modelling and simulation of cellular pathways. In: Priami, C. (ed.) Transactions on Computational Systems Biology IX. LNCS (LNBI), vol. 5121, pp. 86–113. Springer, Heidelberg (2008)CrossRefGoogle Scholar
  8. 8.
    Barbuti, R., Maggiolo-Schettini, A., Milazzo, P., Troina, A.: Bisimulation congruences in the calculus of looping sequences. In: Barkaoui, K., Cavalcanti, A., Cerone, A. (eds.) ICTAC 2006. LNCS, vol. 4281, pp. 93–107. Springer, Heidelberg (2006)CrossRefGoogle Scholar
  9. 9.
    Barbuti, R., Maggiolo-Schettini, A., Milazzo, P., Troina, A.: A calculus of looping sequences for modelling microbiological systems. Fundam. Inform. 72(1-3), 21–35 (2006)MathSciNetzbMATHGoogle Scholar
  10. 10.
    Cardelli, L.: Brane calculi. In: Danos, V., Schachter, V. (eds.) CMSB 2004. LNCS (LNBI), vol. 3082, pp. 257–278. Springer, Heidelberg (2005)CrossRefGoogle Scholar
  11. 11.
    Chalot, M., Blaudez, D., Brun, A.: Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends in Plant Science 11, 263–266 (2005)CrossRefGoogle Scholar
  12. 12.
    Coppo, M., Damiani, F., Drocco, M., Grassi, E., Troina, A.: Stochastic Calculus of Wrapped Compatnents. In: QAPL 2010. EPTCS, vol. 28, pp. 82–98 (2010)Google Scholar
  13. 13.
    Danos, V., Laneve, C.: Formal molecular biology. Theor. Comput. Sci. 325(1), 69–110 (2004)MathSciNetCrossRefzbMATHGoogle Scholar
  14. 14.
    Dezani-Ciancaglini, M., Giannini, P., Troina, A.: A type system for required/excluded elements in CLS. In: DCM 2009. EPTCS, vol. 9, pp. 38–48 (2009)Google Scholar
  15. 15.
    Gillespie, D.: Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340–2361 (1977)CrossRefGoogle Scholar
  16. 16.
    Gonen, T., Walz, T.: The structure of aquaporins. Q. Rev. Biophys. 39, 361–396 (2006)CrossRefGoogle Scholar
  17. 17.
    Gout, E., Bligny, R., Douce, R.: Regulation of intracellular pH values in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. J. Biol. Chem. 267, 13903–13909 (1992)Google Scholar
  18. 18.
    Govindarajulu, M., Pfeffer, P.E., Jin, H., Abubaker, J., Douds, D.D., Allen, J.W., Bucking, H., Lammers, P.J., Shachar-Hill, Y.: Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823 (2005)CrossRefGoogle Scholar
  19. 19.
    Guether, M., Balestrini, R., Hannah, M.A., Udvardi, M.K., Bonfante, P.: Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol. 182, 200–212 (2009)CrossRefGoogle Scholar
  20. 20.
    Guether, M., Neuhauser, B., Balestrini, R., Dynowski, M., Ludewig, U., Bonfante, P.: A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiology 150, 73–83 (2009)CrossRefGoogle Scholar
  21. 21.
    Guttenberger, M.: Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211, 299–304 (2000)CrossRefGoogle Scholar
  22. 22.
    Harrison, M.J., Dewbre, G.R., Liu, J.: A phosphate transporter from medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell. 14, 2413–2429 (2002)CrossRefGoogle Scholar
  23. 23.
    Hause, B., Fester, T.: Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221, 184–196 (2005)CrossRefGoogle Scholar
  24. 24.
    Hohnjec, N., Perlick, A.M., Puhler, A., Kuster, H.: The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol. Plant Microbe Interact. 16, 903–915 (2003)CrossRefGoogle Scholar
  25. 25.
    Holm, L.M., Jahn, T.P., Moller, A.L., Schjoerring, J.K., Ferri, D., Klaerke, D.A., Zeuthen, T.: NH3 and NH4  +  permeability in aquaporin-expressing xenopus oocytes. Pflugers Arch. 450, 415–428 (2005)CrossRefGoogle Scholar
  26. 26.
    Jahn, T.P., Moller, A.L., Zeuthen, T., Holm, L.M., Klaerke, D.A., Mohsin, B., Kuhlbrandt, W., Schjoerring, J.K.: Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett. 574, 31–36 (2004)CrossRefGoogle Scholar
  27. 27.
    Javot, H., Pumplin, N., Harrison, M.J.: Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell and Environment 30, 310–322 (2007)CrossRefGoogle Scholar
  28. 28.
    Knowles, J.R.: Enzyme-catalyzed phosphoryl transfer reactions. Annu. Rev. Biochem. 49, 877–919 (1980)CrossRefGoogle Scholar
  29. 29.
    Martin, F., Gianinazzi-Pearson, V., Hijri, M., Lammers, P., Requena, N., Sanders, I.R., Shachar-Hill, Y., Shapiro, H., Tuskan, G.A., Young, J.P.W.: The long hard road to a completed Glomus intraradices genome. New Phytologist 180 (2008)Google Scholar
  30. 30.
    Matsuno, H., Doi, A., Nagasaki, M., Miyano, S.: Hybrid Petri net representation of gene regulatory network. In: Prooceedings of Pacific Symposium on Biocomputing, pp. 341–352. World Scientific Press, Singapore (2000)Google Scholar
  31. 31.
    Milazzo, P.: Qualitative and quantitative formal modelling of biological systems. PhD thesis, University of Pisa (2007)Google Scholar
  32. 32.
    Mills, J.C., Roth, K.A., Cagan, R.L., Gordon, J.I.: DNA microarrays and beyond: completing the journey from tissue to cell. Nat. Cell Biol. 3(8), 943 (2001)CrossRefGoogle Scholar
  33. 33.
    Niemietz, C.M., Tyerman, S.D.: Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett. 465, 110–114 (2000)CrossRefGoogle Scholar
  34. 34.
    Parniske, M.: Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775 (2008)CrossRefGoogle Scholar
  35. 35.
    Priami, C.: Stochastic pi-calculus. Comput. J. 38(7), 578–589 (1995)CrossRefGoogle Scholar
  36. 36.
    Priami, C., Regev, A., Shapiro, E.Y., Silverman, W.: Application of a stochastic name-passing calculus to representation and simulation of molecular processes. Inf. Process. Lett. 80(1), 25–31 (2001)MathSciNetCrossRefzbMATHGoogle Scholar
  37. 37.
    Pǎun, G.: Membrane computing. An introduction. Springer, Heidelberg (2002)CrossRefzbMATHGoogle Scholar
  38. 38.
    Regev, A., Shapiro, E.: Cells as computation. Nature 419, 343 (2002)CrossRefGoogle Scholar
  39. 39.
    Salvemini, F., Marini, A.M., Riccio, A., Patriarca, E.J., Chiurazzi, M.: Functional characterization of an ammonium transporter gene from lotus japonicus. Gene 270, 237–243 (2001)CrossRefGoogle Scholar
  40. 40.
    Schaarschmidt, S., Roitsch, T., Hause, B.: Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (lycopersicon esculentum) roots. J. Exp. Bot. 57, 4015–4023 (2006)CrossRefGoogle Scholar
  41. 41.
    Schena, M., Heller, R.A., Theriault, T.P., Konrad, K., Lachenmeier, E., Davis, R.W.: Microarrays: biotechnology’s discovery platform for functional genomics. Trends Biotechnol. 17(6), 217–218 (1999)CrossRefGoogle Scholar
  42. 42.
    Shacharhill, Y., Pfeffer, P.E., Douds, D., Osman, S.F., Doner, L.W., Ratcliffe, R.G.: Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiology 108, 7–15 (1995)CrossRefGoogle Scholar
  43. 43.
    Singer, S.J., Nicolson, G.L.: The fluid mosaic model of the structure of cell membranes. Science 175, 720–731 (1972)CrossRefGoogle Scholar
  44. 44.
    Solaiman, M.D.Z., Saito, M.: Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytologist. 136, 533–538 (1997)CrossRefGoogle Scholar
  45. 45.
    Tyerman, S.D., Niemietz, C.M., Bramley, H.: Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ. 25, 173–194 (2002)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Mario Coppo
    • 1
  • Ferruccio Damiani
    • 1
  • Maurizio Drocco
    • 1
  • Elena Grassi
    • 1
    • 2
  • Mike Guether
    • 3
  • Angelo Troina
    • 1
  1. 1.Dipartimento di InformaticaUniversità di TorinoItaly
  2. 2.Molecular Biotechnology Center, Dipartimento di GeneticaBiologia e Biochimica, Università di TorinoItaly
  3. 3.Dipartimento di Biologia VegetaleUniversità di TorinoItaly

Personalised recommendations