Abstract
Leymus chinensis (Trin.) Tzvel is a rhizomatous grass species in the Eastern Eurasian steppe zone that is often limited by low soil nitrogen availability. Although a previous study showed that the rhizomes of L. chinensis have the capacity to take up nitrogen, the importance of such uptake for nitrogen nutrition is unclear. Moreover, little is known regarding the inorganic nitrogen uptake kinetics of roots and rhizomes in response to nitrogen status. Here, we first found that ammonium is preferred over nitrate and glycine for L. chinensis growth. Using the 15N-labelling method, we found that the rate of ion influx into roots was approximately five-fold higher than into rhizomes under the same nitrogen content, and the ion influxes into roots and rhizomes under 0.05 mM N were greater than in the presence of 3 mM N, especially in the form of NH4+. Using a non-invasive micro-test technique, we characterised the patterns of NH4+ and NO3– fluxes in the root mature zone, root tip, rhizome mature zone, and rhizome tip following incubation in the solution with different N compounds and different N concentrations. These results suggest a dynamic balance between the uptake, utilisation, and excretion of nitrogen in L. chinensis.
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Abbreviations
- AMTs:
-
ammonium transport proteins
- HATS:
-
high-affinity transport system
- LATS:
-
low-affinity transport system
- NMT:
-
non-invasive micro-test
- NUE:
-
nitrogen-use efficiency
References
Britto, D.T., Kronzucker, H.J.: NH4 + toxicity in higher plants: a critical review. — J. Plant Physiol. 159: 567–584, 2002.
Brooker, R.W., Callaghan, T.V., Jonasson, S.: Nitrogen uptake by rhizomes of the clonal sedge Carex bigelowii: a previously overlooked nutritional benefit of rhizomatous growth. — New Phytol. 142: 35–48, 1999.
Cabrera, E., Gonzalez-Montelongo, R., Giraldez, T., De la Rosa, D.A., Siverio, J.M.: Molecular components of nitrate and nitrite efflux in yeast. — Eukaryot. Cell 13: 267–278, 2014.
Chen, G., Guo, S., Kronzucker, H.J., Shi, W.: Nitrogen use efficiency (NUE) in rice links to NH4 + toxicity and futile NH4 + cycling in roots. — Plant Soil 369: 351–363, 2013a.
Chen, S., Huang, X., Yan, X., Liang, Y., Wang, Y., Li, X., Peng, X., Ma, X., Zhang, L., Cai, Y., Ma, T., Cheng, L., Qi, D., Zheng, H., Yang, X., Li, X., Liu, G.: Transcriptome analysis in sheepgrass (Leymus chinensis): a dominant perennial grass of the eurasian steppe. — PLoS ONE 8: e67974, 2013b.
Crawford, N.M., Glass, A.D.M.: Molecular and physiological aspects of nitrate uptake in plants. — Trends Plant Sci. 3: 1360–1385, 1998.
Elashry, A., Okumoto, S., Siddique, S., Koch, W., Kreil, D.P., Bohlmann, H.: The AAP gene family for amino acid permeases contributes to development of the cyst nematode Heterodera schachtii in roots of Arabidopsis. — Plant Physiol. Biochem. 70: 379–386, 2013.
Fang, Y.Y., Babourina, O., Rengel, Z., Yang, X.E., Pu, P.M.: Spatial distribution of ammonium and nitrate fluxes along roots of wetland plants. — Plant Sci. 173: 240–246, 2007.
Gao, Y., Wang, D., Ba, L., Bai, Y., Liu, B.: Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis. — Environ. exp. Bot. 63: 113–122, 2008.
Han, M., Okamoto, M., Beatty, P.H., Rothstein, S.J., Good, A.G.: The genetics of nitrogen use efficiency in crop plants. — Annu. Rev. Genet. 49: 269–289, 2015.
Henriksen, G.H., Raman, D.R., Walker, L.P., Spanswick, R.M.: Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes: II. patterns of uptake along the root axis and evaluation of the microelectrode flux estimation technique. — Plant Physiol. 99: 734–747, 1992.
Ho, C.H., Lin, S.H., Hu, H.C., Tsay, Y.F.: CHL1 functions as a nitrate sensor in plants. — Cell 138: 1184–1194, 2009.
Ju, X.-T., Xing, G.-X., Chen, X.-P., Zhang, S.-L., Zhang, L.-J., Liu, X.-J., Cui, Z.-L., Yin, B., Christie, P., Zhu, Z.-L., Zhang, F.-S.: Reducing environmental risk by improving N management in intensive Chinese agricultural systems. — Proc. nat. Acad. Sci. USA 106: 3041–3046, 2009.
Kang, L., Han, X., Zhang, Z., Sun, O.J.: Grassland ecosystems in China: review of current knowledge and research advancement. — Phil. Trans. roy. Soc. London B Biol. Sci. 362: 997–1008, 2007.
Kiba, T., Feria-Bourrellier, A.B., Lafouge, F., Lezhneva, L., Boutet-Mercey, S., Orsel, M., Brehaut, V., Miller, A., Daniel-Vedele, F., Sakakibara, H., Krapp, A.: The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-straved plants. — Plant Cell 24: 245–258, 2012.
Kingston-Smith, A.H., Bollard, A.L., Minchin, F.R.: The effect of nitrogen status on the regulation of plant-mediated proteolysis in ingested forage; an assessment using nonnodulating white clover. — Ann. appl. Biol. 149: 35–42, 2006.
Krapp, A., David, L.C., Chardin, C., Girin, T., Marmagne, A., Leprince, A.-S., Chaillou, S., Ferrario-Méry, S., Meyer, C., Daniel-Vedele, F.: Nitrate transport and signalling in Arabidopsis. — J. exp. Bot. 65: 789–798, 2014.
Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.M.: Conifer root discrimination against soil nitrate and the ecology of forest succession. — Nature 385: 59–61, 1997.
Lee, Y.H., Foster, J., Chen, J., Voll, L.M., Weber, A.P., Tegeder, M.: AAP1 transports uncharged amino acids into roots of Arabidopsis. — Plant J. 50: 305–319, 2007.
Li, Q., Li, B.H., Kronzucker, H.J., Shi, W.M.: Root growth inhibition by NH4 + in Arabidopsis is mediated by the root tip and is linked to NH4 + efflux and GMPase activity. — Plant Cell Environ. 33: 1529–1542, 2010.
Liu, H., Liu, H., Song, Y.: Absorption and translocation of nitrogen in rhizomes of Leymus chinensis. — Rapid Commun. Mass Spectrometry 25: 665–671, 2011.
Liu, K.H., Tsay, Y.F.: Switching between the two action modes ofthe dual-affinity nitrate transporter CHL1 by phosphorylation. — EMBO J. 22: 1005–1013, 2003.
Liu, X., Zhang, Y., Han, W., Tang, A., Shen, J., Cui, Z., Vitousek, P., Erisman, J.W., Goulding, K., Christie, P., Fangmeier, A., Zhang, F.: Enhanced nitrogen deposition over China. — Nature 494: 459–462, 2013.
Loqueé, D., Von Wireé, N.: Regulatory levels for the transport of ammonium in plant roots. — J. exp. Bot. 55: 1293–1305, 2004.
Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A.: Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. — Ann. Bot. 105: 1141–1157, 2010.
Meng, S., Zhang, C., Su, L., Li, Y., Zhao, Z.: Nitrogen uptake and metabolism of Populus simonii in response to PEGinduced drought stress. — Environ. exp. Bot. 123: 78–87, 2016.
Mengel, K., Hütsch, B., Kane, Y.: Nitrogen fertilizer application rates on cereal crops according to available mineral and organic soil nitrogen. — Eur. J. Agr. 24: 343–348, 2006.
Miller, A.J., Fan, X., Orsel, M., Smith, S.J., Wells, D.M.: Nitrate transport and signalling. — J. exp. Bot. 58: 2297–2306, 2007.
Näsholm, T., Ekblad, A., Nordin, A., Giesler, R., Högberg, M., Högberg, P.: Boreal forest plants take up organic nitrogen. — Nature 392: 914–916, 1998.
Nakamura, M., Nakamura, T., Tsuchiya, T.: Advantages of NH4 + on growth, nitrogen uptake and root respiration of Phragmites australis. — Plant Soil 331: 463–470, 2010.
Persson, J., Gardestrom, P., Nasholm, T.: Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. — J. exp. Bot. 57: 2651–2659, 2006.
Plassard, C., Guerin-Laguette, A., Very, A.A., Casarin, V., Thibaud, J.B.: Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. — Plant Cell Environ. 25: 75–84, 2002.
Rentsch, D., Schmidt, S., Tegeder, M.: Transporters for uptake and allocation of organic nitrogen compounds in plants. — FEBS Lett. 581: 2281–2289, 2007.
Schulten, H.R., Schnitzer, M.: The chemistry of soil organic nitrogen: a review. — Biol. Fertil. Soils 26: 1–15, 1997.
Sohlenkamp, C., Shelden, M., Howitt, S., Udvardi, M.: Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. — FEBS Lett. 467: 273–278, 2000.
Sun, J., Chen, S., Dai, S., Wang, R., Li, N., Shen, X., Zhou, X., Lu, C., Zheng, X., Hu, Z., Zhang, Z., Song, J., Xu, Y.: NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. — Plant Physiol. 149: 1141–1153, 2009.
Sun, Y., Wang, F., Wang, N., Dong, Y., Liu, Q., Zhao, L., Chen, H., Liu, W., Yin, H., Zhang, X., Yuan, Y., Li, H.: Transcriptome exploration in Leymus chinensis under saline-alkaline treatment using 454 pyrosequencing. — PLoS ONE 8: e53632, 2013.
Svennerstam, H., Ganeteg, U., Näsholm, T.: Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. — New Phytol. 180: 620–630, 2008.
Taylor, A.R., Bloom, A.J.: Ammonium, nitrate, and proton fluxes along the maize root. — Plant Cell Environ. 21: 1255–1263, 1998.
Walch-Liu, P., Neumann, G., Engels, C.: Response of shoot and root growth to supply of different nitrogen forms is not related to carbohydrate and nitrogen status of tobacco plants. — J. Plant Nutr. Soil Sci. 164: 97–103, 2001.
Wipf, D., Ludewig, U., Tegeder, M., Rentsch, D., Koch, W., Frommer, W.B.: Conservation of amino acid transporters in fungi, plants and animals. — Trends Biochem. Sci. 27: 139–147, 2002.
Yuan, L., Loque, D., Kojima, S., Rauch, S., Ishiyama, K., Inoue, E., Takahashi, H., Von Wiren, N.: The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. — Plant Cell 19: 2636–2652, 2007.
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Acknowledgements: This work was co-supported by the National Natural Science Foundation of China grant No. 31070250, the Program for New Century Excellent Talents in University NCET-08-005 and the Fundamental Research Funds for the Central Universities 2009SD-16.
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Li, S., Jiang, F., Han, Y. et al. Comparison of nitrogen uptake in the roots and rhizomes of Leymus chinensis. Biol Plant 62, 149–156 (2018). https://doi.org/10.1007/s10535-017-0748-1
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DOI: https://doi.org/10.1007/s10535-017-0748-1