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Ammonium Excess Promotes Proline Synthesis but Inhibits Glutathione Synthesis in Oilseed Rape (Brassica napus L.)

  • Hyunjae Lee (Department of Animal Science, College of Agriculture & Life Science, Chonnam National University) ;
  • Seon-Hye Baek (Department of Animal Science, College of Agriculture & Life Science, Chonnam National University) ;
  • Tae-Hwan Kim (Department of Animal Science, College of Agriculture & Life Science, Chonnam National University)
  • 투고 : 2023.06.21
  • 심사 : 2023.06.27
  • 발행 : 2023.06.30

초록

Ammonium (NH4+) serves as a nitrogen source, but its elevated levels can hinder plant growth and production. Excess NH4+ with α-ketoglutarate is assimilated into glutamate, a precursor of proline and glutathione (GSH). This study aimed to investigate the effects of excessive NH4+ on the regulation of proline and GSH synthesis. Detached leaves from oilseed rape (Brassica napus L.) were fed with 0, 50, 100, 500, and 1000 mM NH4Cl for 16 h. As the NH4+ concentrations increased, the leaves exhibited progressive wilting and yellowing. Furthermore, total carotenoid and chlorophyll concentrations declined in response to all NH4+ treatments, with the lowest levels observed in 1000 mM NH4+ treatment. Hydrogen peroxide (H2O2) concentration showed a minor increase at low NH4+ concentration (50 and 100 mM) treatments but a significant increase at high NH4+ (500 and 1000 mM), which was consistent with the localization of H2O2. Amino acid concentrations increased with increasing in NH4+ concentration, while the protein concentration displayed the opposite trend. Proline and cysteine concentrations exhibited a gradual increase in response to increasing NH4+ concentrations. However, GSH concentrations rose only in the 50 mM NH4+ treatment and decreased in the 500 and 1000 mM NH4+ treatments. These results indicate that excessive NH4+ is primarily assimilated into proline, while GSH synthesis is adversely affected.

키워드

과제정보

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2022R1I1A3072357).

참고문헌

  1. Back, S.H., Muchamad, M., Lee, B.R. and Kim, T.H. 2022. Effect of exogenous sulfur on hydrogen peroxide, ammonia and proline synthesis in white clover (Trifollium repens L.). Journal of the Korean Society of Grassland and Forage Science. 42(3):195-200. https://doi.org/10.5333/KGFS.2022.42.3.195
  2. Barth, C., Gouzd, A.A., Steele, H.P. and Imperio, R.M. 2010. A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. Journal of Experimental Botany. 61(2):379-394. https://doi.org/10.1093/jxb/erp310
  3. Carr, N.F., Boaretto, R.M. and Mattos Jr, D. 2020. Coffee seedlings growth under varied NO3-:NH4+ ratio: Consequences for nitrogen metabolism, amino acids profile, and regulation of plasma membrane H+-ATPase. Plant Physiology and Biochemistry. 154:11-20. https://doi.org/10.1016/j.plaphy.2020.04.042
  4. Castro-Rodriguez, V., Garcia-Gutierrez, A., Canales, J., Avila, C., Kirby, E.G. and Canovas, F.M. 2011. The glutamine synthetase gene family in Populus. BMC Plant Biology. 11:119.
  5. Coskun, D., Britto, D.T., Mingyuan, Li, Becker, A. and Kronzucker, H.J., 2013. Rapid ammonia gas transport accounts for futile transmembrane cycling under NH3/NH4+ toxicity in plant roots. Plant Physiology. 163(4):1859-1867. https://doi.org/10.1104/pp.113.225961
  6. Foyer, C.H. and Noctor, G. 2011.Ascorbate and glutathione: The heart of the redox hub. Plant Physiology. 155:2-18. https://doi.org/10.1104/pp.110.167569
  7. Ghosh, U.K., Islam, M.N., Siddiqui, M.N., Cao, X. and Khan, M.A.R. 2021. Proline, a multifaceted signaling molecule in plant responses to abiotic stress: Understanding the physiological mechanisms. Plant Biology. 24(2):227-239. https://doi.org/10.1111/plb.13363
  8. Hasanuzzaman, M., Nahar, K., Anee, T.I. and Fujita, M. 2017. Glutathione in plants: Biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants. 23(2):249-268. https://doi.org/10.1007/s12298-017-0422-2
  9. Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J. and Ahmad, A. 2012. Role of proline under changing environments. Plant Signaling & Behavior. 7(11):1456-1466. https://doi.org/10.4161/psb.21949
  10. Junglee, S., Urban, L., Sallanon, H. and Lopez-Lauri, F. 2014. Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. American Journal of Analytical Chemistry. 5:730-736. https://doi.org/10.4236/ajac.2014.511081
  11. Kim, D.H., Lee, B.R., Park, S.H. and Kim, T.H. 2022. Phosphorus significance in alleviating oxidative stress induced by drought in Kentucky Bluegrass (Poa pratensis L.). Journal of the Korean Society of Grassland and Forage Science. 42(2):114-119. https://doi.org/10.5333/KGFS.2022.42.2.114
  12. Kim, T.H., Lee, B.R., Jung, W.J., Kim, K.Y., Avice, J.C. and Ourry, A. 2004. De novo protein synthesis in relation to ammonia and proline accumulation in water stressed white clover. Functional Plant Biology. 31(8):847-855. https://doi.org/10.1071/FP04059
  13. La, V.H., Lee, B.R., Islam, M.T., Mamun, M.A., Park, S.H., Bae, D.W. and Kim, T.H. 2020. Characterization of glutamate-mediated hormonal regulatory pathway of the drought responses in relation to proline metabolism in Brassica napus L.. Plants. 9:512.
  14. La, V.H., Lee, B.R., Islam, M.T., Park, S.H., Jung, H.I., Bae, D.W. and Kim, T.H. 2019. Characterization of salicylic acid-mediated modulation of the drought stress responses: Reactive oxygen species, proline, and redox state in Brassica napus. Environmental and Experimental Botany. 157:1-10. https://doi.org/10.1016/j.envexpbot.2018.09.013
  15. Lee, B.R., Jin, Y.L., Avice, J.C., Cliquet, J.B., Ourry, A. and Kim, T.H. 2009. Increased proline loading to phloem and its effects on nitrogen uptake and assimilation in water-stressed white clover (Trifolium repens). New Phytologist. 182(3):654-663. https://doi.org/10.1111/j.1469-8137.2009.02795.x
  16. Lee, B.R., Muneer, S., Park, S.H., Zhang, Q. and Kim, T.H. 2013. Ammonium-induced proline and sucrose accumulation, and their significance in antioxidant activity and osmotic adjustment. Acta Physiologia Plantarum. 35:2655-2664. https://doi.org/10.1007/s11738-013-1297-7
  17. Lee, B.R., Park, S.H., La, V.H., Bae, D.W. and Kim, T.H. 2022. Drought-induced xylem sulfate activates the ABA-mediated regulation of sulfate assimilation and glutathione redox in Brassica napus leaves. Metabolites. 12:1190.
  18. Luo, J., Qin, J.J., He, F.F., Li, H., Liu, T.X., Polle, A., Peng, C.H. and Luo, Z.B. 2013. Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta. 237:919-931. https://doi.org/10.1007/s00425-012-1807-7
  19. Lutts, S., Majerus, V. and Kinet, J.M. 1999. NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiologia Plantarum 105:450-458. https://doi.org/10.1034/j.1399-3054.1999.105309.x
  20. McAllister, C.H., Beatty, P.H. and Good, A.G. 2012. Engineering nitrogen use efficient crop plants: The current status. Plant Biotechnology Journal. 10:1011-1025. https://doi.org/10.1111/j.1467-7652.2012.00700.x
  21. Shilpha, J., Song, J. and Jeong, B.R. 2023. Ammonium phytotoxicity and tolerance: An insight into ammonium nutrition to improve crop productivity. Agronomy. 13:1487.
  22. Skopelitis, D.S., Paranychianakis, N.V., Paschalidis, K.A., Pliakonis, E.D., Delis, I.D., Yakoumakis, D.I., Kouvarakis, A., Papadakis, A.K., Stephanou, E.G. and Roubelakis-Angelakis, K.A. 2006. Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell. 18:2767-2781. https://doi.org/10.1105/tpc.105.038323
  23. Wang, Y., Wang, D., Shi, P. and Omasa, K. 2014. Estimating rice chlorophyll content and leaf nitrogen concentration with a digital still color camera under natural light. Plant Methods. 10:36.
  24. Xian, L., Zhang, Y., Cao, Y., Wan, T., Gong, Y., Dai, C., Ochieng, W.A., Nasimiyu, A.T., Li, W. and Liu, F. 2020. Glutamate dehydrogenase plays an important role in ammonium detoxification by submerged macrophytes. Science of the Total Environment. 722:137859.
  25. Yang, C.W. and Kao, C.H. 2000. Ammonium in relation to proline accumulation in detached rice leaves. Plant Growth Regulation. 30:139-144. https://doi.org/10.1023/A:1006329919243
  26. Yang, S., Hao, D., Jin, M., Li, Y., Liu, Z., Huang, Y., Chen, T. and Su, Y. 2020. Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice. BMC Plant Biology. 20:143.