Abstract
The interactions between ammonium fertilization, cyanide (KCN) assimilation and proline accumulation in rice seedlings (Oryza sativa L. cv. XZX 45) were investigated during the current investigation. Results indicated that rice seedlings possess effective assimilation potential for exogenous CN− after 2-d exposure, where increases in the assimilation rates of CN− were negatively correlated with ammonium fertilization. During ammonium starvation, negligible change in proline content was detected in both rice tissue samples subjected to CN− exposure, suggesting that the degradation products of CN− by rice seedlings might not serve as nitrogen donors for proline synthesis. In the absence of exogenous CN−, proline accumulation in shoots was evident with enhancing ammonium fertilization, whereas marginal changes of proline content were observed in roots. Results also indicated that the addition of exogenous CN− significantly decreased proline content in shoots of rice seedlings fed with ammonium at the concentrations of 19.75–59.25 mg N/L. In conclusion, both the supplied ammonium and CN− were quickly assimilated into other nitrogen-containing compounds in rice seedlings through a nitrogen nutrient pathway; the contribution of nitrogen from ammonium assimilation into proline synthesis was evident in shoots after 2-d exposure, but it was repressed by exogenous CN−.
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References
Atanasova E (2008) Effect of nitrogen sources on the nitrogenous forms and accumulation of amino acid in head cabbage. Plant Soil Environ 54:66–71
Ben Rejeb K, Adbelly C, Savoure A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284
Cai HM, Xiao JH, Zhang QF, Lian XM (2010) Co-suppressed glutamine synthetase2 gene modifies nitrogen metabolism and plant growth in rice. Chin Sci Bull 55:876–886
Chen CT, Chen L, Chuan CL, Kao CH (2001) Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci 160:283–290
Chen CT, Chen TH, Lo KF, Chiu CY (2004) Effect of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111
Ebbs SD, Bushey J, Poston S, Kosma D, Samiotakis M, Dzombak D (2003) Transport and metabolism of free cyanide and iron cyanide complexes by willow. Plant Cell Environ 26:1467–1478
Gordon SA, Fleck A, Bell J (1978) Optimal conditions for the estimation of ammonium by the Berthelot reaction. Ann Clin Biochem 15:270–275
Guan M, Moller IS, Schjoerring JK (2015) Two cytosolic glutamine synthetase isoforms play specific roles for seed germination and seed yield structure in Arabidopsis. J Exp Bot 66:203–212
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102
Hare PD, Cress WA, Van Staden J (1999) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
Hirel B, Martin A, Terce-Laforgue T, Gonzalez-Moro MB, Estavillo JM (2005) Physiology of maize I: a comprehensive and integrated view of nitrogen metabolism in a C4 plant. Physiol Plant 124:167–177
Islam MM, Hoque MA, Okuma E, Nasrin M, Banu A, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597
Kumar AK, Prasad MNV, Achary VMM, Panda BB (2013) Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environ Sci Pollut Res 20:4551–4561
Larsen M, Ucisik A, Trapp S (2005) Uptake, metabolism, accumulation and toxicity of cyanide in willow trees. Environ Sci Technol 39:2135–2142
Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG (2007) Asparagine in plants. Ann Appl Biol 150:1–26
Li ZG, Ding XJ, Du PF (2013) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747
Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933
Machingura M, Ebbs SD (2010) Increased beta-cyanoalanine synthase and asparaginase activity in nitrogen-deprived wheat exposed to cyanide. J Plant Nutr Soil Sci 173:808–810
Misra N, Gupta AK (2005) Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci 169:331–339
Neuberg M, Pavlíková D, Pavlík M, Balík J (2010) The effect of different nitrogen nutrition on proline and asparagine content in plant. Plant Soil Environ 56:305–311
Noctor G, Novitskaya L, Lea P, Foyer C (2002) Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation. J Exp Bot 53:939–945
O’Leary B, Preston GM, Sweetlove LJ (2014) Increased β-cyanoalanine nitrilase activity improves cyanide tolerance and assimilation in Arabidopsis. Mol Plant 7:231–243
Okuma E, Murakami Y, Shimoishi Y, Tada M, Murata Y (2004) Effects of exogenous application of proline and betaine on the growth of tobacco cultured cells under saline conditions. Soil Sci Plant Nutr 50:1301–1305
Pavlíková D, Pavlík M, Staszková L, Motyka V, Száková J, Tlustoš P, Balík J (2008) Glutamate kinase as a potential biomarker of heavy metal stress in plants. Ecotoxicol Environ Saf 70:223–230
Piotrowski M, Schonfelder S, Weiler EW (2001) The Arabidopsis thaliana isogene NIT4 and its orthologs in tobacco encode beta-cyano-l-alanine hydratase/nitrilase. J Biol Chem 276:2616–2621
Ramajulu S, Sudhakar C (2000) Proline metabolism during dehydration in two mulberry genotypes with contrasting drought tolerance. J Plant Physiol 157:81–85
Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-deltaaminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271
Savouré A, Jaoua S, Hua XJ, Ardiles W, Van Montagu M, Verbruggen N (1995) Isolation, characterization, and chromosomal location of a gene encoding the DELTA-1pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett 372:13–19
Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482
Szabados L, Savouré A (2010) Proline: a mulitfunctional amino acid. Trends Plant Sci 15:89–97
Tripathi SB, Gurumurthi K, Panigrahi AK, Shaw BP (2007) Salinity induced changes in proline and betaine contents and synthesis in two aquatic macrophytes differing in salt tolerance. Biol Plant 51:110–115
Tsai KJ, Lin CY, Ting CY, Shih MC (2016) Ethylene-regulated glutamate dehydrogenase fine-tunes metabolism during anoxia-reoxygenation. Plant Physiol 172:1548–1562
Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103:771–781
Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008) Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146:310–320
Wen JF, Yang SH, Gong M (2011) Biochemical pathways of Cd stress-induced proline accumulation and inhibitory effects of exogenous proline on Cd-induced H2O2 production in Tobacco (Nicotiana tabacum L.) suspension cells. Plant Physiol J 47:392–398 (in Chinese)
Wen JF, Gong M, Liu Y, Hu JL, Deng MH (2013) Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci Hortic 164:366–371
Whankaew S, Machingura M, Rhanor T, Triwitayakorn K, Ebbs S (2014) Cyanide as an alternative source of nitrogen for sorghum (Sorghum bicolor) and wheat (Triticum aestivum). J Soil Sci Plant Nutr 14:332–347
Wu JT, Chang SC, Chen KS (1995) Enhancement of intracellular proline level in cells of Anacystis nidulans (Cyanobacteria) exposed to deleterious concentration of copper. J Phycol 31:376–379
Yu XZ, Zhang FZ (2012) Activities of nitrate reductase and glutamine synthetase in rice seedlings during cyanide metabolism. J Hazard Mater 225–226:190–194
Yu XZ, Lei SY, Lin YJ, Zhang Q (2019a) Interaction of cyanate uptake by rice seedlings with nitrate assimilation: gene expression analysis. Environ Sci Pollut Res 220:300–313
Yu XZ, Lu CJ, Lin YJ, Li YH (2019b) Cr-induced disturbance on expression of six COX genes in rice seedlings. Int J Environ Sci Technol 16:2385–2394
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River, pp 231–261
Zushi K, Matsuzoe N (2006) Free amino acid contents of tomato fruit grown under water and salinity stresses. Acta Hortic 724:91–96
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The authors wish to thank all who assisted in conducting this work.
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This work was financially supported by the National Natural Science Foundation of China (No: 41877493).
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Xiao-Zhang Yu has received the grants from the National Natural Science Foundation of China. The other authors, Wei Liu, Sheng-Yu Lei, Li Yang and Yu-Juan Lin, declare that they have no conflict of interest.
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Liu, W., Yu, XZ., Lei, SY. et al. Assessment of ammonium fertilization as a stimulus for proline accumulation in Oryza sativa L. during cyanide assimilation. Int. J. Environ. Sci. Technol. 17, 2811–2818 (2020). https://doi.org/10.1007/s13762-020-02686-0
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DOI: https://doi.org/10.1007/s13762-020-02686-0