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Effect of brassinosteroids on ammonium uptake via regulation of ammonium transporter and N-metabolism genes in Arabidopsis

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Biologia Plantarum

Abstract

Several studies have been performed to elucidate the role of brassinosteroids (BRs) in plant growth and development. However, information on the role of BR signaling in nutrient uptake is limited. This study explores the relationship between BRs and ammonium transporter 1 (AMT1) expression in Arabidopsis roots. We found that BR treatment reduced the expression of AMT1 genes and that a BR receptor BRI1 mutant bri1-5 reversed its BR-repressed expression. Furthermore, the BR signaling transcription factor, BES1, regulates AMT1 expression in roots. NH4 +-mediated repression of AMT1;1, AMT1;2, and AMT1;3 was suppressed in a gain-of-function BES1 mutant (bes1-D). This mutant was more sensitive to methyl-ammonium and contained a higher ammonium content compared to wild-type plants. However, BES1 failed to bind E-box elements present in the promoter region of the AMT1 genes. Furthermore, NH4 +-mediated glutamine synthetase (GS) and glutamine oxoglutarate aminotransferase (GOGAT) gene expressions were partially inhibited, and GS activity was slightly lower in the bes1-D mutant relative to that observed in wild-type En2 roots. NH4 +-mediated AMT1 suppressions are known to be caused by N-metabolites rather than NH4 + itself, and glutamine application inhibited AMT1 expression in both En2 and bes1-D indicating that BES1 activation inhibited NH4 +-mediated GS/GOGAT induction, which might in turn inhibit AMT1 repression. In conclusion, the present study demonstrates that BR regulated nitrogen uptake and assimilation via the BR signaling pathway.

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Abbreviations

AMT:

ammonium transporter

BES:

brassinosteroid signaling transcription factor

BL:

brassinolide

BR:

brassinosteroid

ChIP:

chromatin immunoprecipitation

Col-0, En2, and WS2:

wild-types

GFP:

green fluorescent protein

GOGAT:

glutamate synthase

GS:

glutamine synthetase

MeA:

methylammonium

qko:

quadruple mutant

qPCR:

quantitative PCR

References

  • Bloom, A.J.: Nitrogen as a limiting factor: crop acquisition of ammonium and nitrate. - In: Jackson, L.E. (ed.): Ecology in Agriculture. Pp. 145–172, Academic Press, San Diego 1997.

    Chapter  Google Scholar 

  • Britto, D.T., Kronzucker, H.J.: NH4+ toxicity in higher plants: a critical review. — J. Plant Physiol. 159: 567–584, 2002.

    Article  CAS  Google Scholar 

  • Cao, Y., Glass, A.D., Crawford, N.M.: Ammonium inhibition of Arabidopsis root growth can be reversed by potassium and by auxin resistance mutations aux1, axr1, and axr2. — Plant. Physiol. 102: 983–989, 1993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y., Yoshida, S.: Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. — Plant. Physiol. 134: 1555–1573, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Je, B.I., Piao, H.L., Park, S.J., Park, S.H., Kim, C.M., Xuan, Y.H., Park, S.H., Huang, J., Do, C.Y., An, G., Wong, H.L., Fujioka, S., Kim, M.C., Shimamoto, K., Han, C.D.: RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. — Plant Cell 22: 1777–1791, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, T.W., Wang, Z.Y.: Brassinosteroid signal transduction from receptor kinases to transcription factors. — Annu. Rev Plant Biol. 61: 681–704, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Konishi, N., Ishiyama, K., Matsuoka, K., Maru, I., Hayakawa, T., Yamaya, T., Kojima, S.: NADH-dependent glutamate synthase plays a crucial role in assimilating ammonium in the Arabidopsis root. — Physiol. Plant. 152: 138–151, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Li, B., Li, Q., Su, Y., Chen, H., **ong, L., Mi, G., Kronzucker, H.J., Shi, W.: Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis. — Plant. Cell Environ. 34: 933–946, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Li, B., Li, Q., **ong, L., Kronzucker, H.J., Kramer, U., Shi, W.: Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. — Plant. Physiol. 160: 2040–2051, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, G., Li, B., Dong, G., Feng, X., Kronzucker, H.J., Shi, W.: Ammonium-induced shoot ethylene production is associated with the inhibition of lateral root formation in Arabidopsis. — J. exp Bot. 64: 1413–1425, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Chory, J.: A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. — Cell 90: 929–938, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., Walker, J.C.: BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. — Cell 110: 213–222, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Methods. Enzymol. 148: 350–382, 1987.

    Article  CAS  Google Scholar 

  • Loque, D., Yuan, L., Kojima, S., Gojon, A., Wirth, J., Gazzarrini, S., Ishiyama, K., Takahashi, H., Von Wiren, N.: Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. — Plant J. 48: 522–534, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Mack, G.: Organ-specific changes in the activity and subunit composition of glutamine-synthetase isoforms of barley (Hordeum vulgare L.) after growth on different levels of NH4+. — Planta 196: 231–238, 1995.

    Article  Google Scholar 

  • Nam, K.H., Li, J.: BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. — Cell 110: 203–212, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Noctor, G., Foyer, C.H.: A re-evaluation of the ATP:NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? — J. exp Bot. 49: 1895–1908, 1998.

    CAS  Google Scholar 

  • Oh, E., Zhu, J.Y., Wang, Z.Y.: Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. — Nat. cell. Biol. 14: 802–809, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira, I.C., Brears, T., Knight, T.J., Clark, A., Coruzzi, G.M.: Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light, and photorespiration. — Plant. Physiol. 129: 1170–1180, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patterson, K., Cakmak, T., Cooper, A., Lager, I., Rasmusson, A.G., Escobar, M.A.: Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. — Plant Cell Environ. 33: 1486–1501, 2010.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rawat, S.R., Silim, S.N., Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.: Atamt1 gene expression and NH4+ uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. — Plant J. 19: 143–152, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Sohlenkamp, C., Shelden, M., Howitt, S., Udvardi, M.: Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. — FEBS. Lett. 467: 273–278, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Y., Fan, X.Y., Cao, D.M., Tang, W., He, K., Zhu, J.Y., He, J.X., Bai, M.Y., Zhu, S., Oh, E., Patil, S., Kim, T.W., Ji, H., Wong, W.H., Rhee, S.Y., Wang, Z.Y.: Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. — Dev. Cell. 19: 765–777, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., Chory, J.: Nuclear-localized BZR1 mediates brassino-steroid- induced growth and feedback suppression of brassinosteroid biosynthesis. — Dev. Cell 2: 505–513, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Yang, C.J., Zhang, C., Lu, Y.N., **, J.Q., Wang, X.L.: The mechanisms of brassinosteroids' action: from signal transduction to plant development. — Mol. Plant 4: 588–600, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., Chory, J.: BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. — Cell 109: 181–191, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., Guo, H., Anderson, S., Aluru, S., Liu, P., Rodermel, S., Yin, Y.: A brassinosteroid transcriptional network revealed by genome-wide identification of BES1 target genes in Arabidopsis thaliana. — Plant J. 65: 634–646, 2011.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to B. T. Zhao or Y. H. Xuan.

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Acknowledgement

The bri1-5, bes1-D and 35S:BES1:GFP seeds were obtained from Wang Laboratory of the Carnegie Institution for Science as a kind gift. The qko and qko+ATM1;1 seeds were obtained from Dr. Nicolaus Von Wirén’s group at Leibniz Institute for Plant Genetics and Crop Plant Research. This work was supported by grants from the Wenzhou City public welfare technology projects (N20150021) and the Shenyang Agricultural University.

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Zhao, B.T., Zhu, X.F., Jung, J.H. et al. Effect of brassinosteroids on ammonium uptake via regulation of ammonium transporter and N-metabolism genes in Arabidopsis . Biol Plant 60, 563–571 (2016). https://doi.org/10.1007/s10535-016-0627-1

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  • DOI: https://doi.org/10.1007/s10535-016-0627-1

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