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Effects of Nitrate toxicity on free Proline accumulation, chlorophyll degradation and photosynthetic efficiency in Chlorella vulgaris Beyerinck [Beijerinck]

Year 2019, Volume 6, Issue 1, 10 - 19, 16.03.2019
https://doi.org/10.21448/ijsm.471036

Abstract

The effects of high nitrate concentrations on alterations in maximal photochemical efficiency of PSII ratio (Fv/Fm), chlorophyll content, chlorophyll degradation, growth rate and proline accumulation in Chlorella vulgaris Beyerinck [Beijerinck] were investigated in this study. The Fv/Fm ratio was observed in response to the increased nitrate concentration. The Fv/Fm ratio decreased in C. vulgaris following 44 h in 12.99 mM NaNO3-enriched media. Experimental results showed that, growth rates and chlorophyll content declined by increasing nitrate concentration. The decrease in the ratio of chlorophyll a/b with enrichment of high nitrate concentration (6.5 mM and 12.99 mM NaNO3) was also caused by a decrease in chlorophyll a and an increase in chlorophyll b concentration in C. vulgaris cultures. The results showed that 6.5 and 12.99 mM nitrate concentration increased proline content in treated cells, which suggests that nitrate stress lead to proline accumulation in C. vulgaris.

References

  • [1] Madison, R.J., Burnett, J.O. (1985). Overview of the occurrence of nitrate in groundwater of the United States. US Geological Survey Water-Supply Paper, 2275, 93–100.
  • [2] Viaroli, P., Bartoli, M., Bondavalli, C., Naldi, M. (1995). Oxygen fluxes and dystrophy in a coastal lagoon colonized by Ulva rigida (Sacca di Goro, Po River Delta, northern Italy). Fresenius Environmental Bulletin, 4, 381–386.
  • [3] Herndon, J., Cochlan, W.P. (2007). Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6, 260–270.
  • [4] Rouse, J.D., Bishop, C.A., Struger, J. (1999). Nitrogen pollution: an assessment of its threat to amphibian survival. Environmental Health Perspective, 107, 799-803.
  • [5] Pierce, R.H., Weeks, J.M., Prappas, J.M. (1993). Nitrate toxicity to five species of marine fish. Journal of The World Aquaculture Society, 24, 105-107.
  • [6] Bates, S.S., Worms, J., Smith, J.C. (1993). Effects of ammonium and nitrate on growth and domoic acid production by Nitzschia pungens in batch culture. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1248-1254
  • [7] Rijstenbil, J.W., Dehairs, F., Ehlich, R., Wijnholds, J.A. (1998). Effect of the nitrogen status on copper accumulation and pools of metal-binding peptides in the planktonic diatom Thalassiosira pseudonana. Aquatic Toxicology, 42, 187-209.
  • [8] Menéndez, M. (2005). Effect of nutrient pulses on photosynthesis of Chaetomorpha linum from a shallow Mediterranean coastal lagoon. Aquatic Botany, 82, 181–192.
  • [9] Schobert, B. Is there an osmotic regulatory mechanism in algae and higher plants? Journal of Theoretical Biology, 68, (1977) 17-26.
  • [10] Ashraf, M., Foolad, M.R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59, 206-216.
  • [11] Blum, A., Ebercon, A. (1976). Genotypic response in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Science, 16, 361-367.
  • [12] Ahmad, I., Hellebust, J.A. (1988). The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiology, 88, 348-354.
  • [13] Smirnoff, N., Cumbes, Q.J. (1989). Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry, 28, 1057-1060.
  • [14] Charest, C., Phan, C.T. (1990). Cold acclimation of wheat (Triticum aestivum): Properties of ezymes involved in proline metabolism. Plant Physiology, 80, 159-168.
  • [15] Cao, W., & Tibbtts, T.W. (1998). Response of potatoes to nitrogen concentrations differ with nitrogen forms. Journal of Plant Nutrition, 21, 615-623.
  • [16] Jones, J.B. (1997). Hydroponics: a pratical guide for the soilless grower (pp 30-32). Boca Raton, Florida: St. Luice Press.
  • [17] Zhang, G.W., Liu, Z.L., Zhou, J.G., Zhu, Y.L. (2008). Effects of Ca(NO3)2 stress on oxidative damage, antioxidant enzymes activities and polyamine contents in roots of grafted and non-grafted tomato plants. Plant Growth Regulations, 56, 7-19.
  • [18] Tang, D., Shi, S., Li, D., Hu, C., Liu, Y. (2007). Physiological and biochemical responses of Scytonema javanicum (cyanobacterium) to salt stress. Journal of Arid Environments, 71, 312-320.
  • [19] Rudic, V., & Dudnicenco, T. (2000). Process for cultivation of green alga Haeamatococcus pluvialis (Flotow). MD Patent Nr. a 2000 0154.
  • [20] Strasser, R.J., Srivastava, A., (1995). Govindjee Polyphasic chlorophyll a fluorescence transients in plant and cyanobacteria. Photochemistry and Photobiology, 61, 32-42.
  • [21] Jeffrey, S.W., & Humphrey, G.F. (1975). New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants and natural phytoplankton. Biochemie und Physiologie der Pflanzen, 165, 191–194.
  • [22] Bates, L.S., Waldren, R.P., Tear, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil, 39, 205–207.
  • [23] Báckor, M., Fahselt, D., Wu, C.T. (2004). Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta). Plant Science, 167, 151-157.
  • [24] Touzet, N., Franco, J.M., Raine, R. (2007). Influence of inorganic nutrition on growth and PSP toxin production of Alexandrium minutum (Dinophyceae) from Cork Harbour, Ireland. Toxion, 50, 106–119.
  • [25] Leong, S.C.Y., Murata, A., Nagashima, Y., Taguchi, S. (2004). Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon 43, 407–415.
  • [26] Shi, Y., Hu, H., Cong, W. (2005). Positive effects of continuous low nitrate levels on growth and photosynthesis of Alexandrium tamarense (Gonyaulacales, Dinophyceae). Phycological Research, 53, 43–48.
  • [27] Hwang, D.F., & Lu, Y.H. (2000). Influence of environmental and nutritional factors on growth toxicity and toxin profile of dinoflagellate Alexandrium minutum. Toxicon, 38, 1491–1503.
  • [28] Chen, W., Zhang, Q., Dai, S. (2009). Effects of nitrate on intracellular nitrite and growth of Microcystis aeruginosa. Journal of Applied Phycology, 21, 701-706.
  • [29] Sivasankar, S., & Oaks, A. (1996). Nitrate assimilation in higher plants: the effect of metabolities and light. Plant Physiology and Biochemistry, 34, 609-620.
  • [30] Crawford, B. (1989). Photosynthetic carbon assimilation and the suppression of photorespiration in the cyanobacteria, Aquatic Botany, 34, 211-231.
  • [31] Tylova-Munzarova, E., Lorenzen, B., Brix, H., Votrubova, O. (2005). The effects of NH4+and NO3- on growth, resource allocation and nitrogen uptake kinetics of Phragmites australis and Glyceria maxima. Aquatic Botany, 81, 326–342.
  • [32] Spiller, H., & Boger, P. (1977). Photosynthetic nitrite reduction by dithioerythritol and the effect of nitrite on electron transport in isolated chloroplasts. Photochemistry and Photobiology, 26, 397–402.
  • [33] Loranger, C., & Carpentier, R. (1994). A fast bioassay for phytotoxicity measurements using immobilized photosynthetic membranes. Biotechnology and Bioengineering, 44, 178–183.
  • [34] Almeida, J.S., Júlio, S.M., Reis, M.A.M., Carrondo, M.J.T. (1995). Nitrite inhibition of denitrification by Pseudomonas fluorescens. Biotechnology and Bioengineering, 46, 194–201.
  • [35] Yang, S., Wang, J., Cong, W., Cai, Z.L., Fan, O.Y. (2004). Utilization of nitrite as nitrogen source by Botryococcus braunii. Biotechnology Letter, 26, 239–243.
  • [36] Puckett, K.J., Nieboer, E., Flora, W.P., Richardson, D.H.S. (1973). Sulphur dioxide:its effect on photosynthetic 14C fixation in lichens and suggested mechanisms of phytotoxicity. New Phytologist, 72, 141-154.
  • [37] Chettri, M.K., Cook, C.M., Vardaka, E., Sawidis, T., Lanaras, T. (1998). The effect of Cu, Zn, and Pb on the chlorophyll content of the lichens Cladonia convoluta and Cladonia rangiformis. Environmental and Experimental Botany, 39, 1-10.
  • [38] Sandmann, G., & Böger, O. (1980). Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiology, 66, 797-800.
  • [39] Tanaka, A., & Tanaka, R. (2006). Chlorophyll metabolism; a review. Current Opinion in Plant Biology, 9, 248-255.
  • [40] Leigh, R.A., Ahmad, N., Wyn Jones, R.G. (1981). Assessment of glycine betaine and proline compartmentation by analysis isolated beet vacuoles. Planta, 153, 34-41.
  • [41] Binzel, M.L., Hasegawa, P.M., Rhodes, D., Handa, S., Handa, A.K., Bressan, R.A. (1987). Solute accumulation in tobacco cells adapted to NaCl. Plant Physiology, 84, 1408-1415.
  • [42] Ketchum, R.E.B., Warren, R.C., Klima, L.J., Lopez-Gutierrez, F., Nabors, M.W., (1991). The mechanism and regulation of proline accumulation in suspension cultures of halophytic grass Distichlis spicata L. Journal of Plant Physiology, 137, 368-374.
  • [43] Wu, J.T., Hsieh, M.T., Kow, L.C. (1998). Role of proline accumulation in response to toxic copper in Chlorella sp. (Chlorophyceae) cells. Journal of Phycology, 34, 113-117.
  • [44] Lutts, S., Majerus, V., Kinet J.M., (1999). NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Plant Physiology, 105, 450-458.
  • [45] De-Lacerda, C.F., Cambraia, J., Oliva, M.A., Ruiz, H.A., Prisco, J.T. (2003). Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environmental and Experimental Botany, 49, 107-120.
  • [46] Sánchez, E., López-Lefebre, L.R., Garcia, P.C., Rivero, R.M., Ruiz, J.M., Romero, L., (2001). Proline metabolism in response to highest nitrogen dosages in green bean plants (Phaseolus vulgaris L. cv. Strike). Journal of Plant Physiology, 158, 593-598.

Effects of Nitrate toxicity on free Proline accumulation, chlorophyll degradation and photosynthetic efficiency in Chlorella vulgaris Beyerinck [Beijerinck]

Year 2019, Volume 6, Issue 1, 10 - 19, 16.03.2019
https://doi.org/10.21448/ijsm.471036

Abstract

The effects of high nitrate concentrations on alterations in maximal photochemical efficiency of PSII ratio (Fv/Fm), chlorophyll content, chlorophyll degradation, growth rate and proline accumulation in Chlorella vulgaris Beyerinck [Beijerinck] were investigated in this study. The Fv/Fm ratio was observed in response to the increased nitrate concentration. The Fv/Fm ratio decreased in C. vulgaris following 44 h in 12.99 mM NaNO3-enriched media. Experimental results showed that, growth rates and chlorophyll content declined by increasing nitrate concentration. The decrease in the ratio of chlorophyll a/b with enrichment of high nitrate concentration (6.5 mM and 12.99 mM NaNO3) was also caused by a decrease in chlorophyll a and an increase in chlorophyll b concentration in C. vulgaris cultures. The results showed that 6.5 and 12.99 mM nitrate concentration increased proline content in treated cells, which suggests that nitrate stress lead to proline accumulation in C. vulgaris.

References

  • [1] Madison, R.J., Burnett, J.O. (1985). Overview of the occurrence of nitrate in groundwater of the United States. US Geological Survey Water-Supply Paper, 2275, 93–100.
  • [2] Viaroli, P., Bartoli, M., Bondavalli, C., Naldi, M. (1995). Oxygen fluxes and dystrophy in a coastal lagoon colonized by Ulva rigida (Sacca di Goro, Po River Delta, northern Italy). Fresenius Environmental Bulletin, 4, 381–386.
  • [3] Herndon, J., Cochlan, W.P. (2007). Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6, 260–270.
  • [4] Rouse, J.D., Bishop, C.A., Struger, J. (1999). Nitrogen pollution: an assessment of its threat to amphibian survival. Environmental Health Perspective, 107, 799-803.
  • [5] Pierce, R.H., Weeks, J.M., Prappas, J.M. (1993). Nitrate toxicity to five species of marine fish. Journal of The World Aquaculture Society, 24, 105-107.
  • [6] Bates, S.S., Worms, J., Smith, J.C. (1993). Effects of ammonium and nitrate on growth and domoic acid production by Nitzschia pungens in batch culture. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1248-1254
  • [7] Rijstenbil, J.W., Dehairs, F., Ehlich, R., Wijnholds, J.A. (1998). Effect of the nitrogen status on copper accumulation and pools of metal-binding peptides in the planktonic diatom Thalassiosira pseudonana. Aquatic Toxicology, 42, 187-209.
  • [8] Menéndez, M. (2005). Effect of nutrient pulses on photosynthesis of Chaetomorpha linum from a shallow Mediterranean coastal lagoon. Aquatic Botany, 82, 181–192.
  • [9] Schobert, B. Is there an osmotic regulatory mechanism in algae and higher plants? Journal of Theoretical Biology, 68, (1977) 17-26.
  • [10] Ashraf, M., Foolad, M.R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59, 206-216.
  • [11] Blum, A., Ebercon, A. (1976). Genotypic response in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Science, 16, 361-367.
  • [12] Ahmad, I., Hellebust, J.A. (1988). The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiology, 88, 348-354.
  • [13] Smirnoff, N., Cumbes, Q.J. (1989). Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry, 28, 1057-1060.
  • [14] Charest, C., Phan, C.T. (1990). Cold acclimation of wheat (Triticum aestivum): Properties of ezymes involved in proline metabolism. Plant Physiology, 80, 159-168.
  • [15] Cao, W., & Tibbtts, T.W. (1998). Response of potatoes to nitrogen concentrations differ with nitrogen forms. Journal of Plant Nutrition, 21, 615-623.
  • [16] Jones, J.B. (1997). Hydroponics: a pratical guide for the soilless grower (pp 30-32). Boca Raton, Florida: St. Luice Press.
  • [17] Zhang, G.W., Liu, Z.L., Zhou, J.G., Zhu, Y.L. (2008). Effects of Ca(NO3)2 stress on oxidative damage, antioxidant enzymes activities and polyamine contents in roots of grafted and non-grafted tomato plants. Plant Growth Regulations, 56, 7-19.
  • [18] Tang, D., Shi, S., Li, D., Hu, C., Liu, Y. (2007). Physiological and biochemical responses of Scytonema javanicum (cyanobacterium) to salt stress. Journal of Arid Environments, 71, 312-320.
  • [19] Rudic, V., & Dudnicenco, T. (2000). Process for cultivation of green alga Haeamatococcus pluvialis (Flotow). MD Patent Nr. a 2000 0154.
  • [20] Strasser, R.J., Srivastava, A., (1995). Govindjee Polyphasic chlorophyll a fluorescence transients in plant and cyanobacteria. Photochemistry and Photobiology, 61, 32-42.
  • [21] Jeffrey, S.W., & Humphrey, G.F. (1975). New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants and natural phytoplankton. Biochemie und Physiologie der Pflanzen, 165, 191–194.
  • [22] Bates, L.S., Waldren, R.P., Tear, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil, 39, 205–207.
  • [23] Báckor, M., Fahselt, D., Wu, C.T. (2004). Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta). Plant Science, 167, 151-157.
  • [24] Touzet, N., Franco, J.M., Raine, R. (2007). Influence of inorganic nutrition on growth and PSP toxin production of Alexandrium minutum (Dinophyceae) from Cork Harbour, Ireland. Toxion, 50, 106–119.
  • [25] Leong, S.C.Y., Murata, A., Nagashima, Y., Taguchi, S. (2004). Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon 43, 407–415.
  • [26] Shi, Y., Hu, H., Cong, W. (2005). Positive effects of continuous low nitrate levels on growth and photosynthesis of Alexandrium tamarense (Gonyaulacales, Dinophyceae). Phycological Research, 53, 43–48.
  • [27] Hwang, D.F., & Lu, Y.H. (2000). Influence of environmental and nutritional factors on growth toxicity and toxin profile of dinoflagellate Alexandrium minutum. Toxicon, 38, 1491–1503.
  • [28] Chen, W., Zhang, Q., Dai, S. (2009). Effects of nitrate on intracellular nitrite and growth of Microcystis aeruginosa. Journal of Applied Phycology, 21, 701-706.
  • [29] Sivasankar, S., & Oaks, A. (1996). Nitrate assimilation in higher plants: the effect of metabolities and light. Plant Physiology and Biochemistry, 34, 609-620.
  • [30] Crawford, B. (1989). Photosynthetic carbon assimilation and the suppression of photorespiration in the cyanobacteria, Aquatic Botany, 34, 211-231.
  • [31] Tylova-Munzarova, E., Lorenzen, B., Brix, H., Votrubova, O. (2005). The effects of NH4+and NO3- on growth, resource allocation and nitrogen uptake kinetics of Phragmites australis and Glyceria maxima. Aquatic Botany, 81, 326–342.
  • [32] Spiller, H., & Boger, P. (1977). Photosynthetic nitrite reduction by dithioerythritol and the effect of nitrite on electron transport in isolated chloroplasts. Photochemistry and Photobiology, 26, 397–402.
  • [33] Loranger, C., & Carpentier, R. (1994). A fast bioassay for phytotoxicity measurements using immobilized photosynthetic membranes. Biotechnology and Bioengineering, 44, 178–183.
  • [34] Almeida, J.S., Júlio, S.M., Reis, M.A.M., Carrondo, M.J.T. (1995). Nitrite inhibition of denitrification by Pseudomonas fluorescens. Biotechnology and Bioengineering, 46, 194–201.
  • [35] Yang, S., Wang, J., Cong, W., Cai, Z.L., Fan, O.Y. (2004). Utilization of nitrite as nitrogen source by Botryococcus braunii. Biotechnology Letter, 26, 239–243.
  • [36] Puckett, K.J., Nieboer, E., Flora, W.P., Richardson, D.H.S. (1973). Sulphur dioxide:its effect on photosynthetic 14C fixation in lichens and suggested mechanisms of phytotoxicity. New Phytologist, 72, 141-154.
  • [37] Chettri, M.K., Cook, C.M., Vardaka, E., Sawidis, T., Lanaras, T. (1998). The effect of Cu, Zn, and Pb on the chlorophyll content of the lichens Cladonia convoluta and Cladonia rangiformis. Environmental and Experimental Botany, 39, 1-10.
  • [38] Sandmann, G., & Böger, O. (1980). Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiology, 66, 797-800.
  • [39] Tanaka, A., & Tanaka, R. (2006). Chlorophyll metabolism; a review. Current Opinion in Plant Biology, 9, 248-255.
  • [40] Leigh, R.A., Ahmad, N., Wyn Jones, R.G. (1981). Assessment of glycine betaine and proline compartmentation by analysis isolated beet vacuoles. Planta, 153, 34-41.
  • [41] Binzel, M.L., Hasegawa, P.M., Rhodes, D., Handa, S., Handa, A.K., Bressan, R.A. (1987). Solute accumulation in tobacco cells adapted to NaCl. Plant Physiology, 84, 1408-1415.
  • [42] Ketchum, R.E.B., Warren, R.C., Klima, L.J., Lopez-Gutierrez, F., Nabors, M.W., (1991). The mechanism and regulation of proline accumulation in suspension cultures of halophytic grass Distichlis spicata L. Journal of Plant Physiology, 137, 368-374.
  • [43] Wu, J.T., Hsieh, M.T., Kow, L.C. (1998). Role of proline accumulation in response to toxic copper in Chlorella sp. (Chlorophyceae) cells. Journal of Phycology, 34, 113-117.
  • [44] Lutts, S., Majerus, V., Kinet J.M., (1999). NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Plant Physiology, 105, 450-458.
  • [45] De-Lacerda, C.F., Cambraia, J., Oliva, M.A., Ruiz, H.A., Prisco, J.T. (2003). Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environmental and Experimental Botany, 49, 107-120.
  • [46] Sánchez, E., López-Lefebre, L.R., Garcia, P.C., Rivero, R.M., Ruiz, J.M., Romero, L., (2001). Proline metabolism in response to highest nitrogen dosages in green bean plants (Phaseolus vulgaris L. cv. Strike). Journal of Plant Physiology, 158, 593-598.

Details

Primary Language English
Subjects Biology
Published Date March
Journal Section Articles
Authors

İnci TÜNEY KIZILKAYA (Primary Author)
EGE UNIVERSITY, FACULTY OF SCIENCE
0000-0003-0293-6964
Türkiye


Dilek UNAL
BILECIK SEYH EDEBALI UNIVERSITY
Türkiye

Publication Date March 16, 2019
Published in Issue Year 2019, Volume 6, Issue 1

Cite

APA Tüney Kızılkaya, İ. & Unal, D. (2019). Effects of Nitrate toxicity on free Proline accumulation, chlorophyll degradation and photosynthetic efficiency in Chlorella vulgaris Beyerinck [Beijerinck] . International Journal of Secondary Metabolite , 6 (1) , 10-19 . DOI: 10.21448/ijsm.471036

International Journal of Secondary Metabolite (IJSM)

ISSN-e: 2148-6905