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Net NH4 + and NO3 − fluxes, and expression of NH4 + and NO3 − transporter genes in roots of Populus simonii after acclimation to moderate salinity

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Net NH + 4 flux was higher in fine roots of P. simonii after NaCl treatment compared to the NO − 3 flux which was consistent with the expression levels of AMTs and NRTs.

Abstract

The characteristics of nitrogen uptake under salt stress would provide insights into the mechanisms of salt tolerance in plants. In the present study, net NH4 + and NO3 − fluxes were measured using the non-invasive micro-test technique, and transcript abundance of ammonium/nitrate transporter genes (AMTs/NRTs) were determined by real time PCR in the fine roots of Populus simonii after treatment for 21 days with 75 mM NaCl. The NH4 + and NO3 − fluxes showed heterogeneous spatial patterns along the root tip in nutrient solution. The maximum influx of NH4 + occurred near the root tip, while that of NO3 − was 15 mm from the root tip. The net NO3 − flux was inhibited by ca. 25 % with the provision of NH4 +. On average, the newly grown fine roots took up more NH4 + after the 75 mM NaCl treatment than did the control. Consistent with the NH4 + and NO3 − influxes, most AMTs were up-regulated in the salt-treated roots relative to the control, while most NRTs were down-regulated. Our study provides insights into nitrogen uptake and the AMT/NRT expression levels in the fine roots of P. simonii after acclimation to moderate salinity. This may be valuable for understanding nitrogen uptake mechanisms after adaptation to salinity.

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References

  • Alber A, Ehlting B, Ehlting J, Hawkins BJ, Rennenberg H (2012) Net NH4 + and NO3 − flux, and expression of NH4 + and NO3 − transporters in roots of Picea glauca. Trees 26:1403–1411

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Bai H, Euring D, Volmer K, Janz D, Polle A (2013) The nitrate transporter (NRT) gene family in poplar. PLoS One 8:e72126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiol 99:1294–1301

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 174:137–150

    Article  CAS  PubMed  Google Scholar 

  • Dluzniewska P, Gessler A, Dietrich H, Schnitzler JP, Teuber M, Rennenberg H (2007) Nitrogen uptake and metabolism in Populus × canescens as affected by salinity. New Phytol 173:279–293

    Article  CAS  PubMed  Google Scholar 

  • Ehlting B, Dluzniewska P, Dietrich H, Selle A, Teuber M, Hansch R, Nehls U, Polle A, Schnitzler JP, Rennenberg H, Gessler A (2007) Interaction of nitrogen nutrition and salinity in grey poplar (Populus tremula × alba). Plant Cell Environ 30:796–811

    Article  CAS  PubMed  Google Scholar 

  • Enstone DE, Peterson CA, Hallgren SW (2001) Anatomy of seedling tap roots of loblolly pine (Pinus taeda L.). Trees 15:98–111

    Article  Google Scholar 

  • Fang YY, Babourina O, Rengel Z, Yang XE, Pu PM (2007) Spatial distribution of ammonium and nitrate fluxes along roots of wetland plants. Plant Sci 173:240–246

    Article  CAS  Google Scholar 

  • Gasic K, Hernandez A, Korban S (2004) RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Biol Rep 22:437–438

    Article  CAS  Google Scholar 

  • Glass AD, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi M, Unkles SE (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  CAS  PubMed  Google Scholar 

  • Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J Exp Bot 62:2299–2308

    Article  CAS  PubMed  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Hawkins HJ, Lewis OAM (1993) Combination effect of NaCl salinity, nitrogen form and calcium concentration on the growth, ionic content and gaseous exchange properties of Triticum aestivum L. cv. Gamtoos. New Phytol 124:161–170

    Article  CAS  Google Scholar 

  • Hawkins BJ, Boukcim H, Plassard C (2008) A comparison of ammonium, nitrate and proton net fluxes along seedling roots of Douglas-fir and lodgepole pine grown and measured with different inorganic nitrogen sources. Plant Cell Environ 31:278–287

    Article  CAS  PubMed  Google Scholar 

  • Hawkins BJ, Robbins S, Porter RB (2014) Nitrogen uptake over entire root systems of tree seedlings. Tree Physiol 34:334–342

    Article  CAS  PubMed  Google Scholar 

  • Hessini K, Hamed K, Gandour M, Mejri M, Abdelly C, Cruz C (2013) Ammonium nutrition in the halophyte Spartina alterniflora under salt stress: evidence for a priming effect of ammonium? Plant Soil 370:163–173

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. In: Circular California agricultural experiment station 347

  • Irshad M, Honna T, Eneji A, Yamamoto S (2002) Wheat response to nitrogen source under saline conditions. J Plant Nutr 25:2603–2612

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass AD, Kirk GJ (1999) Nitrate-ammonium synergism in rice. A subcellular flux analysis. Plant Physiol 119:1041–1046

    CAS  Google Scholar 

  • Langer K, Levchenko V, Fromm J, Geiger D, Steinmeyer R, Lautner S, Ache P, Hedrich R (2004) The poplar K+ channel KPT1 is associated with K+ uptake during stomatal opening and bud development. Plant J 37:828–838

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Li B-H, Kronzucker HJ, Shi W-M (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Loqué D, von Wirén N (2004) Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 55:1293–1305

    Article  PubMed  Google Scholar 

  • Lucas WJ, Kochian LV (1986) Ion transport processes in corn roots: an approach utilizing microelectrode techniques. In: Gensler WG (ed) Advanced agricultural instrumentation: design and use. Martinus Nijhoff, Dordrecht, pp 402–425

    Chapter  Google Scholar 

  • Luo J, Qin J, He F, Li H, Liu T, Polle A, Peng C, Luo ZB (2013a) Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta 237:919–931

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Li H, Liu T, Polle A, Peng C, Luo ZB (2013b) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maetz J (1973) Na+/NH4 +, Na+/H+ exchanges and NH3 movement across the gill of Carassius auratus. J Exp Biol 58:255–275

    CAS  Google Scholar 

  • Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306

    Article  CAS  PubMed  Google Scholar 

  • Mitsuya S, Takeoka Y, Miyake H (2000) Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro. J Plant Physiol 157:661–667

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Newman I (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24:1–14

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB, Mittra B (2004) Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees 18:167–174

    Article  CAS  Google Scholar 

  • Peinemann N, Guggenberger G, Zech W (2005) Soil organic matter and its lignin component in surface horizons of salt-affected soils of the Argentinian Pampa. Catena 60:113–128

    Article  CAS  Google Scholar 

  • Plassard C, Guérin-Laguette A, Véry AA, Casarin V, Thibaud JB (2002) Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant Cell Environ 25:75–84

    Article  Google Scholar 

  • Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol 12:275–291

    Article  CAS  PubMed  Google Scholar 

  • Selle A, Willmann M, Grunze N, Gessler A, Weiss M, Nehls U (2005) The high-affinity poplar ammonium importer PttAMT1.2 and its role in ectomycorrhizal symbiosis. New Phytol 168:697–706

    Article  CAS  PubMed  Google Scholar 

  • Senadheera P, Singh RK, Maathuis FJ (2009) Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. J Exp Bot 60:2553–2563

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shabala S, Bose J (2012) Application of non-invasive microelectrode flux measurements in plant stress physiology. In: Volkov AG (ed) Plant Electrophysiology. Springer, New York, pp 91–126

    Chapter  Google Scholar 

  • Silveira JAG, Melo ARB, Viégas RA, Oliveira JTA (2001) Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot 46:171–179

    Article  CAS  Google Scholar 

  • Socci AM, Templer PH (2011) Temporal patterns of inorganic nitrogen uptake by mature sugar maple (Acer saccharum Marsh.) and red spruce (Picea rubens Sarg.) trees using two common approaches. Plant Ecol Divers 4:141–152

    Article  Google Scholar 

  • Sohlenkamp C, Wood CC, Roeb GW, Udvardi MK (2002) Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiol 130:1788–1796

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Speer M, Brune A, Kaiser WM (1994) Replacement of nitrate by ammonium as the nitrogen source increases the salt sensitivity of pea plants. I. Ion concentrations in roots and leaves. Plant Cell Environ 17:1215–1221

    Article  Google Scholar 

  • Subudhi PK, Baisakh N (2011) Spartina alterniflora Loisel., a halophyte grass model to dissect salt stress tolerance. In Vitro Cell Dev Biol Plant 47:441–457

    Article  CAS  Google Scholar 

  • Tang Z, Liu Y, Guo X, Zu Y (2011) The combined effects of salinity and nitrogen forms on Catharanthus roseus: the role of internal ammonium and free amino acids during salt stress. J Plant Nutr Soil Sci 174:135–144

    Article  CAS  Google Scholar 

  • Templer PH, Dawson TE (2004) Nitrogen uptake by four tree species of the Catskill Mountains, New York: implications for forest N dynamics. Plant Soil 262:251–261

    Article  CAS  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467

    Article  CAS  PubMed  Google Scholar 

  • Weisgerber H, Han Y (2001) Diversity and breeding potential of poplar species in China. Forest Chron 77:227–237

    Article  Google Scholar 

  • Willmann A, Thomfohrde S, Haensch R, Nehls U (2014) The poplar NRT2 gene family of high affinity nitrate importers: impact of nitrogen nutrition and ectomycorrhiza formation. Environ Exp Bot. doi:10.1016/j.envexpbot.2014.02.003

    Google Scholar 

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Author contribution statement

Conceived and designed the experiments: Chunxia Zhang, Zhong Zhao. Performed the experiments: Chunxia Zhang, Sen Meng, Yiming Li. Analyzed the data: Chunxia Zhang, Sen Meng. Wrote the paper: Chunxia Zhang, Zhong Zhao.

Acknowledgments

We are grateful to Li Su, Yulin Yuan and Xiaoyu Wei for technical help. We also thank Dr. Mingjun Li for helpful discussions. This research is supported by National Key Basic Research Program of China (973 Program, Grant No. 2012CB416902).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Key Laboratory of Environment and Ecology in Western China of Ministry of Education, College of Forestry, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Chunxia Zhang, Sen Meng, Yiming Li & Zhong Zhao

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  1. Chunxia Zhang
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  2. Sen Meng
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  3. Yiming Li
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  4. Zhong Zhao
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Corresponding authors

Correspondence to Chunxia Zhang or Zhong Zhao.

Additional information

Communicated by H. Rennenberg.

Electronic supplementary material

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468_2014_1088_MOESM1_ESM.tif

Heat map of selected AMT genes in different tissues of P. tremula and P. trichocarpa according to the database (http://popgenie.org/heatmap) (TIFF 4265 kb)

Dry weights of salt-treated plants and control plants (TIFF 2273 kb)

The morphology of root tips of control (left) and salt treatment (right) (TIFF 188 kb)

Nitrogen concentrations of salt-treated plants and control plants (TIFF 183 kb)

468_2014_1088_MOESM5_ESM.tif

Net NH4 + flux over 10 min at positions 0.3 mm and 0.6 mm from the root tips in P. simonii under NaCl stress (A) and in controls (B). The data indicate the mean ± SE (n = 7). The measuring solution contained 1 mM KCl and 0.1 mM CaCl2, pH 5.5, to which either 0.1 mM NH4Cl or 0.1 mM NH4NO3 was added for NH4 + flux measurements (TIFF 81 kb)

468_2014_1088_MOESM6_ESM.tif

Net NO3 − flux over 10 min at positions 15 mm from the root tips in P. simonii under NaCl stress (A) and in controls (B). The data indicate the mean ± SE (n=7). The measuring solution contained 1 mM KCl and 0.1 mM CaCl2, pH 5.5, to which either 0.1 mM KNO3 or 0.1 mM NH4NO3 was added for NO3 − flux measurements (TIFF 82 kb)

Primers of AMTs and NRTs used for qRT-PCR (DOCX 18 kb)

Changes of root morphology indexes after 21d treated with 75 mM NaCl in P. simonii (DOCX 17 kb)

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Zhang, C., Meng, S., Li, Y. et al. Net NH4 + and NO3 − fluxes, and expression of NH4 + and NO3 − transporter genes in roots of Populus simonii after acclimation to moderate salinity. Trees 28, 1813–1821 (2014). https://doi.org/10.1007/s00468-014-1088-9

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  • DOI: https://doi.org/10.1007/s00468-014-1088-9

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