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Abstract
Benzoapyrene (B[a]P) pollution poses a threat to the environment and the food chain and consequently to human health. However, the alleviation of the harmful effects of B[a]P pollution in perennial ryegrass (Lolium perenne L.) by the application of exogenous nitric oxide (NO) has been ignored. Thus, in this paper the effects of exogenous sodium nitroprusside (SNP, a NO donor) on the growth, photosynthetic fluorescence characteristics, and antioxidant enzyme activity of ryegrass exposed to B[a]P stress are investigated. B[a]P stress induced the reduction of the aboveground and belowground dry weights, chlorophyll (a, b), the total chlorophyll contents, the carotenoid content, the net photosynthetic rate (Pn), the intercellular carbon dioxide concentration (Ci), the water use efficiency (WUE), the photosystem II (PSII) potential activity (Fv/F0), the maximum quantum yield of PSII photochemistry (Fv/Fm), the steady-state fluorescence yield (Fs), and the non-photochemical quenching (qN), while enhancement was recorded in response to the foliar spray of SNP at 200 and 300 μmol L-1 under B[a]P stress. Gray correlation and principal component analyses show that 200 μmol L-1 of SNP more drastically alleviated the damage caused by B[a]P stress than 300 μmol L -1 of SNP. The exogenous NO-mediated alleviation of B[a]P toxicity in ryegrass was associated with preserved photosynthetic characteristics and activation of antioxidant enzymes.
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Copyright (c) 2023 Yue Li, Junqiang Ma, Yu Wang, Sunan Xu, Lei Jiang, Lihong Zhang, Wei Hou
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Fig. 1. Effect of different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP), a NO donor, on the biomass of ryegrass seedlings under benzoapyrene (B[a]P) stress. (A) Aboveground dry weight, (B) Belowground dry weight, (C) Aboveground fresh weight, (D) Belowground fresh weight, (E) Aboveground plant height, (F) Belowground root length. Data are mean ± standard deviation, n = 3. Different letters indicate significant differences at p < 0.05.
Fig. 2. Effect of different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP), a NO donor, on the photosynthetic pigment content of ryegrass seedlings under benzoapyrene (B[a]P) stress. (A) Chlorophyll a content, (B) Chlorophyll b content, (C) Carotenoid content, (D) Total chlorophyll content. FW – fresh weight. Data are mean ± standard deviation, n = 3. Different letters indicate significant differences at p < 0.05.
Fig. 3. Effect of different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP), a NO donor, on photosynthetic gas exchange parameters of ryegrass seedlings under benzoapyrene (B[a]P) stress. (A) Net photosynthetic rate (Pn), (B) Stomatal conductance (Gs), (C) Intercellular carbon dioxide concentration (Ci), (D) Transpiration rate (Tr), (E) Water use efficiency (WUE). Data are mean ± standard deviation, n = 3. Different letters indicate significant differences at p < 0.05.
Fig. 4. Effect of different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP), a NO donor, on chlorophyll fluorescence parameters of ryegrass seedlings under benzoapyrene (B[a]P) stress. (A) PSII potential activity (Fv/F0), (B) PSII maximum light energy conversion efficiency (Fv/Fm), (C) Actual quantum yield of PSII photochemistry (ФPSII), (D) Steady-state fluorescence (Fs), (E) Photochemical quenching coefficient (qP), (f) Non-photochemical quenching coefficient (qN). Data are mean ± standard deviation, n = 3. Different letters indicate significant differences at p < 0.05.
Fig. 5. Effect of different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP), a NO donor, on antioxidant enzyme activity of ryegrass seedlings under benzoapyrene (B[a]P) stress. (A) Superoxide dismutase (SOD) activity. (B) Catalase (CAT) activity. (C) Peroxidase (POD) activity. Data are mean ± standard deviation, n = 3. U – unit of enzyme activity, FW – fresh weight. Different letters indicate significant differences at p < 0.05.
Fig. 6. Principal component analysis (PCA) plots of growth, photosynthetic characteristics and chlorophyll fluorescence parameters and antioxidant enzyme activity of ryegrass for different concentrations (100, 200, 300 and 400 μmol L-1) of sodium nitroprusside (SNP) in combination with benzoapyrene (B[a]P) as well as control.
References
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- Ahmad, P., Ahanger, M.A., Alyemeni, M.N., Wijaya, L., Alam, P., 2018: Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255, 79-93.
- Ahmad, A., Khan, W.U., Shah, A.A., Yasin, N.A., Naz, S., Ali, A., Tahir, A., Batool, A. I., 2021: Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance, and reduction of arsenic uptake in Brassica juncea. Chemosphere 262, 128384.
- Ali, Q., Daud, M.K., Haider, M.Z., Ali, S., Rizwan, M., Aslam, N., Noman A., Lqbal, N., Shahzad, F., Deeba, F., Ali, L., Zhu, S.J., 2017: Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiology and Biochemistry 119, 50-58.
- Arnon, D.I., 1949: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
- Dąbrowski, P., Pawluśkiewicz, B., Baczewska, A.H., Oglęcki, P., Kalaji, H., 2015: Chlorophyll a florescence of perennial ryegrass (Lolium perenne L.) varieties under long term exposure to shade. Zemdirbyste 102, 305-312.
- Dai, Z., Rizwan, M., Gao, F., Yuan, Y., Huang, H., Hossain, M.M., Xiong, S., Cao, M., Liu, Y., Tu, S., 2020: Nitric oxide alleviates selenium toxicity in rice by regulating antioxidation, selenium uptake, speciation and gene expression. Environmental Pollution 257, 113540.
- Ding K., Luo Y., Liu S., Li Z., 2002: Remediation of phenanthrene contaminated soil by growing Lolium multiflorum Lam. Soils 34, 233-236 (in Chinese).
- Duan, J., He, S., Feng, Y.F., Yu, Y.L., Xue, L.H., Yang, L.Z., 2017: Floating ryegrass mat for the treatment of low-pollution wastewater. Ecological Engineering 108, 172-178.
- Fancy, N.N., Bahlmann, A.K., Loake, G.J., 2017: Nitric oxide function in plant abiotic stress. Plant, Cell and Environment 40, 462-472.
- Fismes, J., Perrin‐Ganier, C., Empereur‐Bissonnet, P., Morel, J.L., 2002: Soil‐to‐root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. Journal of Environmental Quality 31, 1649-1656.
- Gadelha, C.G., Miranda, R.S., Alencar, N.L.M., Costa, J.H., Prisco, J.T., Gomes-Filho, E., 2017: Exogenous nitric oxide improves salt tolerance during establishment of Jatropha curcas seedlings by ameliorating oxidative damage and toxic ion accumulation. Journal of Plant Physiology 212, 69-79.
- He, J.Y., Ren, Y.F., Chen, X.L., Chen, H., 2014: Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicology and Environment Safety 108, 114-119.
- Li, Q., Huang, W., Xiong, C., Zhao, J., 2018: Transcriptome analysis reveals the role of nitric oxide in Pleurotuseryngii responses to Cd2+ stress. Chemosphere 201, 294-302.
- Lichtenthaler, H.K., 1987: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
- Murchie, E.H., Lawson, T., 2013: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64, 3983–3998.
- Nagel, M., Alqudah, A.M., Bailly, M., Rajjou, L., Pistrick, S., Matzig, G., Kranner, I., 2019: Novel loci and a role for nitric oxide for seed dormancy and preharvest sprouting in barley. Plant, Cell and Environment 42, 1318-1327.
- Ncube, S., Kunene, P., Tavengwa, N.T., Tutu, H., Richards, H., Cukrowska, E., Chimuka, L., 2017: Synthesis and characterization of a molecularly imprinted polymer for the isolation of the 16 US-EPA priority polycyclic aromatic hydrocarbons (PAHs) in solution. Journal of Environmental Management 199, 192-200.
- Pinhero, R.G., Rao, M.V., Paliyath, G., Murr, D.P., Fletcher, R.A., 1997: Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiology 114, 695-704.
- Reda, M., Golicka, A., Kabała, K., Janicka, M., 2018: Involvement of NR and PM-NR in NO biosynthesis in cucumber plant subjected to salt stress. Plant Science 267, 55-64.
- Schreiber, U., Bilger, W., Neubauer, C., 1995: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze, E.D., Caldwell, M.M. (eds.), Ecophysiology of Photosynthesis, 49-70. Springer, Berlin, Heidelberg.
- Silveira, N.M., Frungillo, L., Marcos, F.C., Pelegrino, M.T., Miranda, M.T., Seabra, A.B., Salgado, L., Machado, E.C., Ribeiro, R.V., 2016: Exogenous nitric oxide improves sugarcane growth and photosynthesis under water deficit. Planta 244(1), 181-190.
- Song, L.L., Yue, L.L., Zhao, H.Q., Hou, M., 2013: Protection effect of nitric oxide on photosynthesis in rice under heat stress. Acta Physiologiae Plantarum 35, 3323-3333.
- Souri, Z., Karimi, N., Farooq, M.A., Sandalio, L.M., 2020: Nitric oxide improves tolerance to arsenic stress in Isatis cappadocica desv. shoots by enhancing antioxidant defenses. Chemosphere 239, 124523
- Tandy, N.E., Di Giulio, R.T., Richardson, C.J., 1989: Assay and electrophoresis of superoxide dismutase from red spruce (Picea rubens Sarg.), loblolly pine (Pinus taeda L.), and scotch pine (Pinus sylvestris L.): A Method for Biomonitoring. Plant Physiology 90, 742-748.
- Tiwari, S., Verma, N., Singh, V.P., Prasad, S.M., 2019: Nitric oxide ameliorates aluminium toxicity in Anabaena PCC 7120: regulation of aluminium accumulation, exopolysaccharides secretion, photosynthesis and oxidative stress markers. Environmental and Experimental Botany 161, 218-227.
- Wei, L.J., Zhang, M.L., Wei, S.H., Zhang, J., Wang, C.L., Liao, W.B., 2020: Roles of nitric oxide in heavy metal stress in plants: cross-talk with phytohormones and protein S-nitrosylation. Environmental Pollution 259, 113943.
- Xiao, Y., Yang, Z.F., Nie, G., Han, J.T., Shuai, Y., Zhang, X.Q., 2021: Multi-trait evaluation of yield and nutritive value of 12 Lolium multiflorum varieties or lines in Chengdu Plain. Acta Prataculturae Sinica 30, 174. (in Chinese)
- Xie, H., Ma, Y., Wang, Y., Sun, F., Liu, R., Liu, X., Xu, Y., 2021: Biological response and phytoremediation of perennial ryegrass to halogenated flame retardants and Cd in contaminated soils. Journal of Environmental Chemical Engineering 9, 106526.
- Yan, F., Liu, Y., Sheng, H., Wang, Y., Kang, H., Zeng, J., 2016: Salicylic acid and nitric oxide increase photosynthesis and antioxidant defense in wheat under UV-B stress. Biologia Plantarum 60, 686-694.
- Ye, X., Ma, J., Wei, J., Sun, K., Xiong, Q., 2019: Comparison of the bioavailability of benzo[a]pyrene (B[a]P) in a B[a]P-contaminated soil using the different addition approaches. Scientific Reports 9, 1-9.
- Zhang, J., Yang, N.N., Geng, Y.N., Zhou, J.H., Lei, J., 2019: Effects of the combined pollution of cadmium, lead and zinc on the phytoextraction efficiency of ryegrass (Lolium perenne L.). RSC advances 9(36), 20603-20611.
References
Ahanger, M.A., Aziz, U., Alsahli, A.A., Alyemeni, M.N., Ahmad, P., 2019: Influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed Vigna angularis. Biomolecules 10, 42.
Ahmad, P., Ahanger, M.A., Alyemeni, M.N., Wijaya, L., Alam, P., 2018: Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255, 79-93.
Ahmad, A., Khan, W.U., Shah, A.A., Yasin, N.A., Naz, S., Ali, A., Tahir, A., Batool, A. I., 2021: Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance, and reduction of arsenic uptake in Brassica juncea. Chemosphere 262, 128384.
Ali, Q., Daud, M.K., Haider, M.Z., Ali, S., Rizwan, M., Aslam, N., Noman A., Lqbal, N., Shahzad, F., Deeba, F., Ali, L., Zhu, S.J., 2017: Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiology and Biochemistry 119, 50-58.
Arnon, D.I., 1949: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Dąbrowski, P., Pawluśkiewicz, B., Baczewska, A.H., Oglęcki, P., Kalaji, H., 2015: Chlorophyll a florescence of perennial ryegrass (Lolium perenne L.) varieties under long term exposure to shade. Zemdirbyste 102, 305-312.
Dai, Z., Rizwan, M., Gao, F., Yuan, Y., Huang, H., Hossain, M.M., Xiong, S., Cao, M., Liu, Y., Tu, S., 2020: Nitric oxide alleviates selenium toxicity in rice by regulating antioxidation, selenium uptake, speciation and gene expression. Environmental Pollution 257, 113540.
Ding K., Luo Y., Liu S., Li Z., 2002: Remediation of phenanthrene contaminated soil by growing Lolium multiflorum Lam. Soils 34, 233-236 (in Chinese).
Duan, J., He, S., Feng, Y.F., Yu, Y.L., Xue, L.H., Yang, L.Z., 2017: Floating ryegrass mat for the treatment of low-pollution wastewater. Ecological Engineering 108, 172-178.
Fancy, N.N., Bahlmann, A.K., Loake, G.J., 2017: Nitric oxide function in plant abiotic stress. Plant, Cell and Environment 40, 462-472.
Fismes, J., Perrin‐Ganier, C., Empereur‐Bissonnet, P., Morel, J.L., 2002: Soil‐to‐root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. Journal of Environmental Quality 31, 1649-1656.
Gadelha, C.G., Miranda, R.S., Alencar, N.L.M., Costa, J.H., Prisco, J.T., Gomes-Filho, E., 2017: Exogenous nitric oxide improves salt tolerance during establishment of Jatropha curcas seedlings by ameliorating oxidative damage and toxic ion accumulation. Journal of Plant Physiology 212, 69-79.
He, J.Y., Ren, Y.F., Chen, X.L., Chen, H., 2014: Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicology and Environment Safety 108, 114-119.
Li, Q., Huang, W., Xiong, C., Zhao, J., 2018: Transcriptome analysis reveals the role of nitric oxide in Pleurotuseryngii responses to Cd2+ stress. Chemosphere 201, 294-302.
Lichtenthaler, H.K., 1987: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Murchie, E.H., Lawson, T., 2013: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64, 3983–3998.
Nagel, M., Alqudah, A.M., Bailly, M., Rajjou, L., Pistrick, S., Matzig, G., Kranner, I., 2019: Novel loci and a role for nitric oxide for seed dormancy and preharvest sprouting in barley. Plant, Cell and Environment 42, 1318-1327.
Ncube, S., Kunene, P., Tavengwa, N.T., Tutu, H., Richards, H., Cukrowska, E., Chimuka, L., 2017: Synthesis and characterization of a molecularly imprinted polymer for the isolation of the 16 US-EPA priority polycyclic aromatic hydrocarbons (PAHs) in solution. Journal of Environmental Management 199, 192-200.
Pinhero, R.G., Rao, M.V., Paliyath, G., Murr, D.P., Fletcher, R.A., 1997: Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiology 114, 695-704.
Reda, M., Golicka, A., Kabała, K., Janicka, M., 2018: Involvement of NR and PM-NR in NO biosynthesis in cucumber plant subjected to salt stress. Plant Science 267, 55-64.
Schreiber, U., Bilger, W., Neubauer, C., 1995: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze, E.D., Caldwell, M.M. (eds.), Ecophysiology of Photosynthesis, 49-70. Springer, Berlin, Heidelberg.
Silveira, N.M., Frungillo, L., Marcos, F.C., Pelegrino, M.T., Miranda, M.T., Seabra, A.B., Salgado, L., Machado, E.C., Ribeiro, R.V., 2016: Exogenous nitric oxide improves sugarcane growth and photosynthesis under water deficit. Planta 244(1), 181-190.
Song, L.L., Yue, L.L., Zhao, H.Q., Hou, M., 2013: Protection effect of nitric oxide on photosynthesis in rice under heat stress. Acta Physiologiae Plantarum 35, 3323-3333.
Souri, Z., Karimi, N., Farooq, M.A., Sandalio, L.M., 2020: Nitric oxide improves tolerance to arsenic stress in Isatis cappadocica desv. shoots by enhancing antioxidant defenses. Chemosphere 239, 124523
Tandy, N.E., Di Giulio, R.T., Richardson, C.J., 1989: Assay and electrophoresis of superoxide dismutase from red spruce (Picea rubens Sarg.), loblolly pine (Pinus taeda L.), and scotch pine (Pinus sylvestris L.): A Method for Biomonitoring. Plant Physiology 90, 742-748.
Tiwari, S., Verma, N., Singh, V.P., Prasad, S.M., 2019: Nitric oxide ameliorates aluminium toxicity in Anabaena PCC 7120: regulation of aluminium accumulation, exopolysaccharides secretion, photosynthesis and oxidative stress markers. Environmental and Experimental Botany 161, 218-227.
Wei, L.J., Zhang, M.L., Wei, S.H., Zhang, J., Wang, C.L., Liao, W.B., 2020: Roles of nitric oxide in heavy metal stress in plants: cross-talk with phytohormones and protein S-nitrosylation. Environmental Pollution 259, 113943.
Xiao, Y., Yang, Z.F., Nie, G., Han, J.T., Shuai, Y., Zhang, X.Q., 2021: Multi-trait evaluation of yield and nutritive value of 12 Lolium multiflorum varieties or lines in Chengdu Plain. Acta Prataculturae Sinica 30, 174. (in Chinese)
Xie, H., Ma, Y., Wang, Y., Sun, F., Liu, R., Liu, X., Xu, Y., 2021: Biological response and phytoremediation of perennial ryegrass to halogenated flame retardants and Cd in contaminated soils. Journal of Environmental Chemical Engineering 9, 106526.
Yan, F., Liu, Y., Sheng, H., Wang, Y., Kang, H., Zeng, J., 2016: Salicylic acid and nitric oxide increase photosynthesis and antioxidant defense in wheat under UV-B stress. Biologia Plantarum 60, 686-694.
Ye, X., Ma, J., Wei, J., Sun, K., Xiong, Q., 2019: Comparison of the bioavailability of benzo[a]pyrene (B[a]P) in a B[a]P-contaminated soil using the different addition approaches. Scientific Reports 9, 1-9.
Zhang, J., Yang, N.N., Geng, Y.N., Zhou, J.H., Lei, J., 2019: Effects of the combined pollution of cadmium, lead and zinc on the phytoextraction efficiency of ryegrass (Lolium perenne L.). RSC advances 9(36), 20603-20611.