biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 59:163-170, 2015 | DOI: 10.1007/s10535-014-0476-8

Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass

X. Y. Bai1, Y. J. Dong1,*, Q. H. Wang1, L. L. Xu1, J. Kong1, S. Liu1
1 College of Resources and Environment, Shandong Agricultural University, Tai'an, P.R.China

Hydroponics experiments were conducted to study the effects of sodium nitroprusside (SNP, a donor of NO) on lead toxicity in ryegrass (Lolium perenne L.) seedlings. When the ryegrass seedlings were grown in a nutrient solution containing 500 μM Pb2+ for two weeks, the plant biomass as well as net photosynthetic rate, transpiration rate, chlorophyll and carotenoid content of leaves decreased. The Pb stress also induced the production of superoxide anion (O2 .-) and hydrogen peroxide (H2O2), leading to malondialdehyde (MDA) accumulation. Furthermore, the activities of superoxide dismutase (SOD), peroxidase (POD), and ascorbate peroxidase (APX) decreased in the Pb-treated seedlings, but the catalase (CAT) activity increased. Additionally, the content of Cu in shoots and the content of K, Mg, Fe, and Zn in both shoots and roots decreased, but the content of Ca in shoots and roots increased under the Pb stress. Moreover, Pb accumulated mostly in roots, whereas a small quantity was translocated to shoots. However, the addition of 50, 100, and 200 μM SNP into the solution containing Pb increased the chlorophyll content and net photosynthetic rate, reduced Pb-induced oxidative damages, improved antioxidant enzyme activities, and inhibited translocation of Pb from roots to shoots. In particular, 100 μM SNP had the best effect on promoting growth of the ryegrass seedlings under the Pb toxicity. However, the application of 400 μM SNP had no obvious alleviating effect on Pb toxicity in the ryegrass seedlings.

Keywords: ascorbate peroxidase; carotenoids; catalase; chlorophyll; hydrogen peroxide; Lolium perenne; malondialdehyde; peroxidase; superoxide dismutase
Subjects: lead; nitric oxide; carotenoids; chlorophyll; net photosynthetic rate; transpiration rate; superoxide anion; hydrogen peroxide; malondialdehyde; superoxide dismutase; peroxidase; catalase; ascorbate peroxidase; potassium; calcium; magnesium; iron; copper; zinc; ryegrass

Received: February 18, 2014; Revised: May 8, 2014; Accepted: June 24, 2014; Published: January 1, 2015  Show citation

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Bai, X.Y., Dong, Y.J., Wang, Q.H., Xu, L.L., Kong, J., & Liu, S. (2015). Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biologia plantarum59(1), 163-170. doi: 10.1007/s10535-014-0476-8
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References

  1. Ahamed, M., Javed Siddiqui, M.K.: Environmental lead toxicity and nutritional factors. - Clinical. Nutr. 26: 400-408, 2007. Go to original source...
  2. Ali, N.A., Bernal, M.P., Ater, M.: Tolerance and bioaccumulation of copper in Phragmites australis and Zea mays. - Plant Soil 239: 103-111, 2002. Go to original source...
  3. Alkhatib, R., Maruthavanan, J., Ghoshroy, S., Steiner, R., Sterling, T., Creamer, R.: Physiological and ultrastructural effects of lead on tobacco. - Biol. Plant. 56: 711-716, 2011. Go to original source...
  4. Arienzo, M., Adamo, P., Cozzolino, V.: The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. - Sci. total Environ. 319: 13-25, 2004. Go to original source...
  5. Beligni, M.V., Lamattina, L.: Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. - Planta 208: 337-344, 1999. Go to original source...
  6. Burzynski, M.: The influence of lead and cadmium on the absorption and distribution of potassium, calcium, magnesium and iron in cucumber seedlings. - Acta Physiol. Plant. 9: 229-238, 1987.
  7. Dong, Y.J., Xu, L.L., Wang, Q.H., Fan, Z.Y., Kong, J., Bai, X.Y.: Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. - J. Plant. Interact. 1: 402-411, 2014. Go to original source...
  8. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxyl ammonium-chloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976. Go to original source...
  9. Gopal, R., Rizvi, A.H.: Excess lead alters growth, metabolism and translocation of certain nutrients in radish. - Chemosphere 70: 1539-1544, 2008. Go to original source...
  10. Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplasts: kinetics and stoichiometry of fatty acid peroxidation. - Arch Biochem. Biophys. 125: 189-198, 1968. Go to original source...
  11. Hermes, V.S., Dall'asta, P., Amaral, F.P., Anacleto, K.B., Arisi, A.C.M.: The regulation of transcription of genes related to oxidative stress and glutathione synthesis in Zea mays leaves by nitric oxide. - Biol. Plant. 57: 620-626, 2013. Go to original source...
  12. Hannaway, D., Fransen, S., Cropper, J., Teel, M., Chaney, M., Griggs, T., Halse, R., Hart, J., Cheeke, P., Hansen, D., Klinger, R., Lane, W.: Perennial ryegrass (Lolium perenne L.). - A Pacific Northwest Extension Publication, PNW 503: 1-19, 1999.
  13. Hsu, Y., Kao, C.: Cadmium toxicity is reduced by nitric oxide in rice leaves. - Plant Growth Regul. 42: 227-238, 2004. Go to original source...
  14. Hu, K.D., Hu, L.Y., Li, Y.H., Zhang, F.Q., Zhang, H.: Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. - Plant Growth Regul. 53: 173-183, 2007. Go to original source...
  15. Islam, E., Liu, D., Li, T.Q., Yang, X.E., Jin, X.F., Mahmood, Q., Tian, S.K., Li, J.Y.: Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. - J. Hazard Mater. 154: 914-926, 2008. Go to original source...
  16. Jiang, W.S., Liu, D.H.: Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. - BMC Plant Biol. 10: 1-8, 2010. Go to original source...
  17. Knudson, L.L., Tibbitts, T.W., Edwards, G.E.: Measurement of ozone injury by determination of leaf chlorophyll concentration. - Plant Physiol. 60: 606-608, 1977. Go to original source...
  18. Kopittke, P.M., Asher, C.J., Blamey, F.P.C., Menzies, N.W.: Toxic effects of Pb2+ on the growth and mineral nutrition of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). - Plant Soil 300: 127-136, 2007. Go to original source...
  19. Kopyra, M., Gwozdz, E.A.: Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. - Plant Physiol. Biochem. 41: 1011-1017, 2003. Go to original source...
  20. Lamattina, L., Garcia-Mata, C., Graziano, M., Pagnussat, G.: Nitric oxide: the versatility of an extensive signal molecule. - Annu. Rev. Plant Biol. 54: 109-136, 2003. Go to original source...
  21. Laspina, N.V., Groppa, M.D., Tomaro, M.L., Benavides, M.P.: Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. - Plant Sci. 169: 323-330, 2005. Go to original source...
  22. Liu, T., Liu, S., Guan, H., Ma, L., Chen, Z., Gu, H., Qu, L.J.: Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead. - Environ. exp. Bot. 67: 377-386, 2009. Go to original source...
  23. Mihailovic, N., Drazic, G.: Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. - Plant Soil Environ. 57: 396-401, 2011. Go to original source...
  24. Mittler, R., Vanderauwera, S., Gollery, M., Breusegem, F.V.: Reactive oxygen gene network of plants. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
  25. Nakano, Y., Asada, K.: Hydrogen peroxide scanvenged by ascorbate specific peroxidase in spinach chloroplast. - Plant Cell Physiol. 22: 867-880, 1981.
  26. Nickel, R.S., Cunningham, B.A.: Improved peroxidase assay method using Ieuco 2,3,6-trichlcroindophenol and application to comparative measurements of peroxidase catalysis. - Anal. Biochem. 27: 292-299, 1969. Go to original source...
  27. Orozco-Cardenas, M.L., Ryan, C.A.: Nitric oxide negatively modulates wound signaling in tomato plants. - Plant Physiol. 130: 487-493, 2002. Go to original source...
  28. Pal, R., Banerjee, A., Kundu, R.: Responses of castor bean (Ricinus communis L.) to lead stress. - Proc. nat. Acad. Sci. 83: 643-650, 2013. Go to original source...
  29. Palmgren, M.G., Harper, J.F.: Pumping with plant P-type ATPases. - J. exp. Bot. 50: 883-893, 1999. Go to original source...
  30. Patra, H.L., Kar, M., Mishre, D.: Catalase activity in leaves and cotyledons during plant development and senescence. - Biochem. Pharmacol. 172: 385-390, 1978. Go to original source...
  31. Phang, I.C., Leung, D.W.M., Taylor, H.H., Burritt, D.J.: The protective effect of sodium nitroprusside (SNP) treatment on Arabidopsis thaliana seedlings exposed to toxic level of Pb is not linked to avoidance of Pb uptake. - Ecotoxicol. Environ. Safety 74: 1310-1315, 2011a. Go to original source...
  32. Phang, I.C., Leung, D.W.M., Taylor, H.H., Burritt, D.J.: Correlation of growth inhibition with accumulation of Pb in cell wall and changes in response to oxidative stress in Arabidopsis thaliana seedlings. - Plant Growth Regul. 64: 17-25, 2011b. Go to original source...
  33. Reddy, A.M., Kumar, S.G., Jyonthsnakumari, G., Thimmanaik, S., Sudhakar, C.: Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). - Chemosphere 60: 97-104, 2005. Go to original source...
  34. Samardakiewicz, S., Wo¼ny, A.: Cell division in Lemna minor roots treated with lead. - Aquat. Bot. 83: 289-295, 2005. Go to original source...
  35. Saxena, I., Shekhawat, G.S.: Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. - Nitric Oxide 32: 13-20, 2013. Go to original source...
  36. Stewart, R.C., Bewley, J.D.: Lipid peroxidation associated with accelerated aging of soybean axes. - Plant Physiol. 65: 245-248, 1980. Go to original source...
  37. Tao, Y.M., Chen, Y.Z., Tan, T., Liu, X.C., Yang, D.L., Liang, S.C.: Comparison of antioxidant responses to cadmium and lead in Bruguiera gymnorrhiza seedlings. - Biol. Plant. 56: 149-152, 2012. Go to original source...
  38. Tu, J., Shen, W.B., Xu, L.L.: Regulation of nitric oxide on the aging process of wheat leaves. - Acta. bot. sin. 45: 1055-1062, 2003.
  39. Uchida, A., Jagendorf, A.T., Hibino, T., Takabe, T., Takabe, T.: Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. - Plant Sci. 163: 515-523, 2002. Go to original source...
  40. Velikova, V., Yordanov, I., Edreva, A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci. 151: 59-66, 2000. Go to original source...
  41. Verma, S., Dubey, R.S.: Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. - Plant Sci. 164: 645-655, 2003. Go to original source...
  42. Wang, Q.H., Liang, X., Dong, Y.J., Xu, L.L., Zhang, X.W., Hou, J., Fan, Z.Y.: Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. - Plant Growth Regul. 69: 11-20, 2013a. Go to original source...
  43. Wang, Q.H., Liang, X., Dong, Y.J., Xu, L.L., Zhang, X.W., Kong, J., Liu, S.: Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. - J. Plant Growth Regul. 32: 721-731, 2013b. Go to original source...
  44. Wink, D.A., Mitchell, J.B.: Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. - Free Radical Biol. Med. 25: 434-456, 1998. Go to original source...
  45. Xiao, Q., Ru, Q.M., Wu, F.H., Huang, X., Pei, Z.M., Zheng, H.L.: Nitric oxide alleviates oxidative stress caused by lanthanum in rice leaves. - J. Rare Earths 25: 631-636, 2007. Go to original source...
  46. Xiong, J., An, L.Y., Lu, H., Zhu, C.: Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. - Planta 230: 755-765, 2009. Go to original source...
  47. Xu, J., Wang, W.Y., Yin, H.X., Liu, X.J., Sun, H., Mi, Q.: Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. - Plant Soil 326: 321-330, 2010. Go to original source...
  48. Yan, C.L., Hong, Y.T., Fu, S.Z., Fang, C.H., Lei, J.X., Shen, Q.: Effect of Cd, Pb stress on the activated oxygen scavenging system in tobacco leaves. - Chin. J. Geochem. 17: 372-378, 1998. Go to original source...
  49. Zhang, Y., Han, X., Chen, X., Jin, H., Cui, X.: Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress. - Scientia Hort. 123: 217-223, 2009. Go to original source...
  50. Zhang, Z.Y., Wang, H.H., Wang, X.M., Bi, Y.R.: Nitric oxide enhances aluminum tolerance by affecting cell wall polysaccharides in rice roots. - Plant Cell Rep. 30: 1701-1711, 2011. Go to original source...
  51. Zhou, Y.Q., Huang, S.Z., Yu, S.L., Gu, J.G., Zhao, J.Z., Han, Y.L., Fu, J.J.: The physiological response and sub-cellular localization of lead and cadmium in Iris pseudacorus L. - Ecotoxicology 19: 69-76, 2010. Go to original source...