Skip to main content

Nitrogen Metabolism in Acorus calamus L. Leaves Induced Changes in Response to Microcystin–LR at Environmentally Relevant Concentrations

Abstract

Acorus calamus L., a semiaquatic plant with a high capacity to remove nitrogen and phosphorus from polluted water, is a potential candidate plant for use in the restoration of eutrophic aquatic ecosystems. However, it is not clear how microcystins (MCs), commonly found in eutrophic water, influence plant growth since the effects of MCs are likely to be dose and species dependent. The present study aimed to investigate the regulation of nitrogen metabolism, a key metabolic process related to plant growth, in the leaves of A. calamus L. exposed to microcystin–leucine-arginine (MC–LR) (1.0–29.8 µg/L). Nitrate (NO3) uptake, assimilation and transformation was stimulated in the leaves of A. calamus L. when exposed to 1.0 µg/L MC–LR through the elevation of nitrate reductase (NR), glutamine synthetase (GS), glutamate synthase (GOGAT), glutamic-pyruvic transaminase (GPT), and glutamic-oxaloacetic transaminase (GOT) activity. Conversely, MC–LR inhibited nitrogen metabolism by decreasing NO3 uptake and the activities of enzymes related to nitrogen metabolism following exposure to MC–LR (9.9–29.8 µg/L) for 30 days, while, ammonium nitrogen (NH4+) content and glutamate dehydrogenase (GDH) activity increased significantly (p < 0.05, LSD test), when compared with the control group. Chronic exposure to MC–LR (9.9–29.8 µg/L) negatively influenced nitrogen metabolism in A. calamus L. leaves, which suggested that it may not be a suitable candidate species for use in the restoration of eutrophic aquatic ecosystems containing MC–LR at concentrations ≥ 9.9 µg/L.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Amrani A, Nasri H, Azzouz A, Kadi Y, Bouaïcha N (2014) Variation in cyanobacterial hepatotoxin (microcystin) content of water samples and two species of fishes collected from a shallow lake in Algeria. Arch Environ Contam Toxicol 66:379–389

    Article  CAS  Google Scholar 

  2. Azevedo CC, Azevedo J, Osório H, Vasconcelos V, Campos A (2014) Early physiological and biochemical responses of rice seedlings to low concentration of microcystin-LR. Ecotoxicology 23:107–121

    Article  CAS  Google Scholar 

  3. Bashri G, Singh M, Mishra RK, Kumar J, Singh VP, Prasad SM (2018) Kinetin regulates UV-B-induced damage to growth, photosystem II photochemistry, and nitrogen metabolism in tomato seedlings. J Plant Growth Regul 37:233–245

    Article  CAS  Google Scholar 

  4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  5. Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6(1):71–80

    Article  CAS  Google Scholar 

  6. Chen FL, Cullimore JV (1988) Two isoenzymes of NADH-dependent glutamate synthase in root nodules of Phaseolus vulgare L. purification, properties and activity changes during nodule development. Plant Physiol 88(4):1411–1417

    Article  CAS  Google Scholar 

  7. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Spon Press, London

    Book  Google Scholar 

  8. Fu J, Wang YF, Liu ZH, Li ZT, Yang KJ (2018) Trichoderma asperellum alleviates the effects of saline–alkaline stress on maize seedlings via the regulation of photosynthesis and nitrogen metabolism. Plant Growth Regul 85:363–374

    Article  CAS  Google Scholar 

  9. Hu XB, Zhang RF, Ye JY, Wu X, Zhang YX, Wu CL (2018) Monitoring and research of microcystins and environmental factors in a typical artificial freshwater aquaculture pond. Environ Sci Pollut Res 25:5921–5933

    Article  CAS  Google Scholar 

  10. Jawad MS, Syed AHB, Zeng J, Quan X, Essa A, Noor M, Zhang G (2017) Nitrogen (N) metabolism related enzyme activities, cell ultrastructure and nutrient contents as affected by N level and barley genotype. J Integr Agric 16(1):190–198

    Article  Google Scholar 

  11. Lahrouni M, Oufdou K, Khalloufi FE, Benidire L, Albert S, Göttfert M, Caviedes MA, Rodriguez-Llorente ID, Oudra B, Pajuelo E (2016) Microcystin-tolerant rhizobium protects plants and improves nitrogen assimilation in Vicia faba irrigated with microcystin-containing waters. Environ Sci Pollut Res 23:10037–10049

    Article  CAS  Google Scholar 

  12. Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53(370):773–787

    Article  CAS  Google Scholar 

  13. Liang CJ, Wang WM (2015) Response and recovery of rice (Oryza sativa) seedlings to irrigation with microcystin-contaminated water. Environ Earth Sci 73:4573–4580

    Article  CAS  Google Scholar 

  14. Major Y, Kifle D, Spoof L, Meriluoto J (2018) Cyanobacteria and microcystins in Koka reservoir (Ethiopia). Environ Sci Pollut Res 25:26861–26873

    Article  CAS  Google Scholar 

  15. Pantelić D, Svirčev Z, Simeunović J, Vidović M, Trajković I (2013) Cyanotoxins: characteristics, production and degradation routes in drinking water treatment with reference to the situation in Serbia. Chemosphere 91(4):421–441

    Article  CAS  Google Scholar 

  16. Parween T, Jan S, Mahmooduzzafar, Fatma T (2011) Alteration in nitrogen metabolism and plant growth during different developmental stages of green gram (Vigna radiata L.) in response to chlorpyrifos. Acta Physiol Plant 33:2321–2328

    Article  CAS  Google Scholar 

  17. Peng WT, Zhou L, Duan WB, Li YX, Pan YZ, Zeng DG (2012) Efficiency of nitrogen and phosphorus removal from sewage by various combinations of wetland plants. Acta Sci Circum 32(3):612–617 (in Chinese)

    CAS  Google Scholar 

  18. Pereira S, Saker ML, Vale M, Vasconcelos VM (2009) Comparison of sensitivity of grasses (Lolium perenne L. and Festuca rubra L.) and lettuce (Lactuca sativa L.) exposed to water contaminated with microcystins. Bull Environ Contam Toxicol 83:81–84

    Article  CAS  Google Scholar 

  19. Pflugmacher S, Jung K, Lundvall L, Neumann S, Peuthert A (2006) Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress. Environ Toxicol Chem 25(9):2381–2387

    Article  CAS  Google Scholar 

  20. Rojo C, Segura M, Cortés F, Rodrigo MA (2013) Allelopathic effects of microcystin-LR on the germination, growth and metabolism of five charophyte species and a submerged angiosperm. Aquat Toxicol 144–145C:1–10

    Article  CAS  Google Scholar 

  21. Shanghai Institute of Plant Physiology, Chinese Academy of Sciences (1999) Experimental guide of modern plant physiology. Science Press, Beijing

    Google Scholar 

  22. Wang NY, Wang C (2018) Effects of microcystin-LR on the tissue growth and physiological responses of the aquatic plant Iris pseudacorus L. Aquat Toxicol 200:197–205

    Article  CAS  Google Scholar 

  23. Zhang HF, Zhao YX, Yin H, Wang YY, Li HX, Wang ZS, Geng YB, Liang WY, Wang HJ (2018a) Effect of aquatic macrophyte growth on landscape water quality improvement. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-018-2421-4

    Article  Google Scholar 

  24. Zhang L, Liu JT, Zhang DW, Luo LG, Liao QG, Yuan LJ, Wu NC (2018b) Seasonal and spatial variations of microcystins in Poyang Lake, the largest freshwater lake in China. Environ Sci Pollut Res 25:6300–6307

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (51309197 and 51878582) and the Natural Science Foundation of Fujian Province of China (2017J01491).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Guoyuan Chen.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, G., Li, Q., Bai, M. et al. Nitrogen Metabolism in Acorus calamus L. Leaves Induced Changes in Response to Microcystin–LR at Environmentally Relevant Concentrations. Bull Environ Contam Toxicol 103, 280–285 (2019). https://doi.org/10.1007/s00128-019-02597-y

Download citation

Keywords

  • Microcystin-leucine-arginine
  • Environmentally relevant concentrations
  • Acorus calamus Linnaeus
  • Nitrogen metabolism