Nitrogen transfer in the arbuscular mycorrhizal symbiosis

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Abstract

Most land plants are symbiotic with arbuscular mycorrhizal fungi (AMF), which take up mineral nutrients from the soil and exchange them with plants for photosynthetically fixed carbon. This exchange is a significant factor in global nutrient cycles1 as well as in the ecology2, evolution3 and physiology4 of plants. Despite its importance as a nutrient, very little is known about how AMF take up nitrogen and transfer it to their host plants5. Here we report the results of stable isotope labelling experiments showing that inorganic nitrogen taken up by the fungus outside the roots is incorporated into amino acids, translocated from the extraradical to the intraradical mycelium as arginine, but transferred to the plant without carbon. Consistent with this mechanism, the genes of primary nitrogen assimilation are preferentially expressed in the extraradical tissues, whereas genes associated with arginine breakdown are more highly expressed in the intraradical mycelium. Strong changes in the expression of these genes in response to nitrogen availability and form also support the operation of this novel metabolic pathway in the arbuscular mycorrhizal symbiosis.

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Figure 1: Labelling of amino acids after supplying labelled nitrate or acetate to the extraradical mycelium.
Figure 2: Labelled arginine after addition of 2 mM 13 C U6 arginine to the ERM compartment for 6 weeks.
Figure 3: Model of nitrogen movement in the arbuscular mycorrhizal symbiosis.
Figure 4: Expression of primary nitrogen metabolic genes.

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Acknowledgements

We thank A. Abdul-Wakeel and D. Schwartz for their technical assistance, and acknowledge the financial support of this project from USDA-NRICGP.Author Contributions Experimental work was carried out by J.A., J.W.A., H.B., D.D.D., M.G., H.J. and PEP; experimental design was by H.B., M.G., P.J.L., P.E.P. and Y.S.-H.; data analysis was carried out by M.G., H.J., P.J.L., P.E.P. and Y.S.-H.; and project planning was by Y.S.-H.

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Correspondence to Philip E. Pfeffer or Peter J. Lammers.

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Competing interests

Accession numbers (GenBank) for gene sequences used to design the TaqMan assays are as follows: GS (DQ063587), GDH (AY745984), UAP (CV186300), OAT (BI452207) and S4 RP (BI452093). Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Govindarajulu, M., Pfeffer, P., Jin, H. et al. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823 (2005) doi:10.1038/nature03610

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