Biologia plantarum 2016, 60:563-571 | DOI: 10.1007/s10535-016-0627-1

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

B. T. Zhao1,*, X. F. Zhu2, J. H. Jung3, Y. H. Xuan2,*
1 College of Life Sciences, Shandong Normal University, Jinan, Shandong, P.R. China
2 College of Plant Protection, Shenyang Agricultural University, Shenyang, Liaoning, P.R. China
3 Department of Biotech R&D, Amicogen Inc., Jinju, South Korea

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.

Keywords: brassinosteroid signaling transcription factor; glutamate synthase; glutamine synthetase; mutant
Subjects: brassinosteroids; ammonium uptake; ammonium transporter; nitrogen metabolism; transcription factor; glutamate synthase; glutamine synthase; chlorophyll; gene expression
Species: Arabidopsis thaliana

Received: March 17, 2015; Revised: October 27, 2015; Accepted: November 11, 2015; Published: September 1, 2016Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Zhao, B.T., Zhu, X.F., Jung, J.H., & Xuan, Y.H. (2016). Effect of brassinosteroids on ammonium uptake via regulation of ammonium transporter and N-metabolism genes in Arabidopsis. Biologia plantarum60(3), 563-571. doi: 10.1007/s10535-016-0627-1.
Download citation

Supplementary files

Download filebpl-201603-0019_S1.pdf

File size: 3.06 MB

References

  1. 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.
  2. Britto, D.T., Kronzucker, H.J.: NH4+ toxicity in higher plants: a critical review. - J. Plant Physiol. 159: 567-584, 2002. Go to original source...
  3. 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. Go to original source...
  4. 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. Go to original source...
  5. 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. Go to original source...
  6. Kim, T.W., Wang, Z.Y.: Brassinosteroid signal transduction from receptor kinases to transcription factors. - Annu. Rev Plant Biol. 61: 681-704, 2010. Go to original source...
  7. 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. Go to original source...
  8. Li, B., Li, Q., Su, Y., Chen, H., Xiong, 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. Go to original source...
  9. Li, B., Li, Q., Xiong, 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. Go to original source...
  10. 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. Go to original source...
  11. Li, J., Chory, J.: A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. - Cell 90: 929-938, 1997. Go to original source...
  12. 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. Go to original source...
  13. Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Methods. Enzymol. 148: 350-382, 1987. Go to original source...
  14. 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. Go to original source...
  15. 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. Go to original source...
  16. Nam, K.H., Li, J.: BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. - Cell 110: 203-212, 2002. Go to original source...
  17. 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.
  18. 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. Go to original source...
  19. 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. Go to original source...
  20. 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. Go to original source...
  21. 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. Go to original source...
  22. Sohlenkamp, C., Shelden, M., Howitt, S., Udvardi, M.: Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. - FEBS. Lett. 467: 273-278, 2000. Go to original source...
  23. 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. Go to original source...
  24. 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. Go to original source...
  25. Yang, C.J., Zhang, C., Lu, Y.N., Jin, J.Q., Wang, X.L.: The mechanisms of brassinosteroids' action: from signal transduction to plant development. - Mol. Plant 4: 588-600, 2011. Go to original source...
  26. 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. Go to original source...
  27. 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. Go to original source...
  28. 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. Go to original source...