Photosynthetica, 2016 (vol. 54), issue 2

Photosynthetica 2016, 54(2):307-316 | DOI: 10.1007/s11099-016-0075-3

Photosynthesis, antioxidant status and gas-exchange are altered by glyphosate application in peanut leaves

D. E. M. Radwan1,2,*, K. A. Fayez1
1 Plant Physiology Laboratory, Botany Department, Faculty of Science, Sohag University, Sohag, Egypt
2 Biology Department, Faculty of Science, Jazan University, Jazan, Kingdom of Saudi Arabia

Glyphosate herbicide caused oxidative stress and exhibited negative effects on photosynthesis and gas exchange of peanut [Arachis hypogaea L. cv. Giza (G) 5 and 6] leaves. We demonstrated that glyphosate caused various morphological symptoms, such as chlorosis, yellowing, and appearance of curly edges in leaves treated with high doses of herbicide in both cultivars; however, the G5 cultivar was more sensitive and showed severer symptoms. Glyphosate lowered photosynthesis and reduced contents of pigments and proteins as well as free amino acids in both cultivars. The gas-exchange parameters, such as photosynthetic (P N) and transpiration rate (E), were highly altered by the glyphosate application. For example, P N and E were reduced by 65 and 61%, respectively, in G5 treated with high dose of glyphosate compared with control. Antioxidant enzymes, such as peroxidase, catalase, ascorbate peroxidase, and superoxide dismutase were induced by both low and high concentrations in the glyphosate-treated leaves. Moreover, the level of lipid peroxidation, indicated by a malondialdehyde content, as well as the hydrogen peroxide content increased in the glyphosate-treated leaves. However, an increase in total antioxidant activity was detected in leaves and this reflected changes in the antioxidant status and accumulation of antioxidants as a defense mechanism against glyphosate toxicity in peanut.

Keywords: antioxidant enzymes; gas exchange; glyphosate; lipid peroxidation; peanut; photosynthesis; reactive oxygen species

Received: April 27, 2015; Accepted: October 6, 2015; Published: June 1, 2016Show citation

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Radwan, D.E.M., & Fayez, K.A. (2016). Photosynthesis, antioxidant status and gas-exchange are altered by glyphosate application in peanut leaves. Photosynthetica, 54(2), 307-316. doi: 10.1007/s11099-016-0075-3.
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    References

    1. Ahsan N., Lee D.G., Lee K.W. et al.: Glyphosate-induced oxidative stress in rice leaves revealed by proteomic approach. - Plant Physiol. Biochem. 46: 1062-1070, 2008. Go to original source...
    2. Alscher R.G., Donahue J.L., Cramer C.L.: Reactive oxygen species and antioxidants: relationships in green cells. - Physiol. Plantarum 100: 224-233, 1997. Go to original source...
    3. Anjum N.A., Umar S., Ahmad A. et al.: Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. - Plant Growth Regul. 54: 271-279, 2008. Go to original source...
    4. Asada K.: Production and action of active oxygen species in photosynthetic tissues. - In: Foyer C., Mullineaux P. (ed.): Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Pp. 77-104. CRC Press, London 1994.
    5. Aydin C.: Some engineering properties of peanut and kernel. - J. Food Eng. 79: 810-816, 2007. Go to original source...
    6. Beauchamp C., Fridovich I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276-287, 1971. Go to original source...
    7. Cerdeira A.L., Duke S.O.: The current status and environmental impacts of glyphosate-resistant crops: A review. - J. Environ. Qual. 35: 1633-1658, 2006. Go to original source...
    8. Chandlee J., Scandalios J.: Analysis of variants affecting the catalase developmental program in maize scutellum. - Theor. Appl. Genet. 69: 71-77, 1984. Go to original source...
    9. Cho U.H., Seo N.H.: Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. - Plant Sci. 168: 113-120, 2005. Go to original source...
    10. Cobb A., Reade J.: Herbicides and Plant Physiology. Pp. 98-99. Wiley-Blackwell, Hoboken 2010. Go to original source...
    11. Dalla Vecchia F., Barbato R., La Rocca N. et al.: Responses to bleaching herbicides by leaf chloroplasts of maize plants grown at different temperatures. - J. Exp. Bot. 52: 811-820, 2001. Go to original source...
    12. de María N., de Felipe M.R., Fernández-Pascual M.: Alterations induced by glyphosate on lupin photosynthetic apparatus and nodule ultrastructure and some oxygen diffusion related proteins. - Plant Physiol. Bioch. 43: 985-996, 2005. Go to original source...
    13. De Prado J.L., De Prado R.A., Shimabukuro R.H.: The effect of diclofop on membrane potential, ethylene induction, and herbicide phytotoxicity in resistant and susceptible biotypes of grasses. - Pestic. Biochem. Phys. 63: 1-14, 1999. Go to original source...
    14. Duke S.O., Baerson S.R., Rimando A.M.: Glyphosate. - In: Plimmer J.R. (ed.): Encyclopedia of Agrochemicals. Pp. 1638. Wiley Online Lib., New York 2003.
    15. Duke S.O., Powles S.B.: Glyphosate: a once-in-a-century herbicide. - Pest Manag. Sci. 64: 319-325, 2008. Go to original source...
    16. Duncan D.B.: A Significance Test for Differences between Ranked Treatments in an Analysis of Variance. - Virginia J. Sci 2: 171-189, 1951).
    17. Fecht-Christoffers M.M., Braun H.-P., Lemaitre-Guillier C. et al.: Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. - Plant Physiol. 133: 1935-1946, 2003.
    18. Fedtke C., Duke S.: Herbicides. - In: Hock B., Elstner F. (ed.): Plant Toxicology. Pp. 247-330. Marcel Dekker, New York 2005.
    19. Foyer C.H., Harbinson J., Mullineaux P.: Oxygen metabolism and the regulation of photosynthetic electron transport. - In: Foyer C.H., Moulineaux P.M. (ed.) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Pp. 1-42. CRC Press, Boca Raton 1994.
    20. Franz J.E., Mao M.K., Sikorski J.A.: Glyphosate: a Unique Global Herbicide. Pp. 189. American Chemical Society, Washington DC 1997).
    21. Geiger D.R., Kapitan S.W., Tucci M.A.: Glyphosate inhibits photosynthesis and allocation of carbon to starch in sugar beet leaves. - Plant Physiol. 82: 468-472, 1986. Go to original source...
    22. Geiger D.R., Tucci M.A., Serviates J.C.: Glyphosate effects on carbon assimilation and gas exchange in sugar beet leaves. - Plant Physiol. 85: 365-369, 1987. Go to original source...
    23. Gomes M.P., Smedbol E., Chalifour A. et al.: Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview. - J. Exp. Bot. 65: 4691-4703, 2014. Go to original source...
    24. Harfouche R., Basu S., Soni S. et al.: Nanoparticle-mediated targeting of phosphatidylinositol-3-kinase signaling inhibits angiogenesis. - Angiogenesis 12: 325-338, 2009. Go to original source...
    25. Hoppe H.H.: Fatty acid biosynthesis - A target site of herbicide action. - In: Böger P., Sandmann G. (ed.): Target Sites of Herbicide Action. Pp. 65-83. CRC Press, Boca Raton 1989.
    26. Jana S., Choudhuri M.A.: Glycolate metabolism of three submersed aquatic angiosperms: effect of heavy metals. - Aquat. Bot. 11: 67-77, 1981. Go to original source...
    27. Jiang L., Yang H.: Prometryne-induced oxidative stress and impact on antioxidant enzymes in wheat. - Ecotoxicol. Environ. Safe. 72: 1687-1693, 2009. Go to original source...
    28. Kellogg E.W., Fridovich I.: Superoxide, hydrogen peroxide, and singlet oxygen in lipid peroxidation by a xanthine oxidase system. - J. Biol. Chem. 250: 8812-8817, 1975.
    29. Kielak E., Sempruch C., Mioduszewska H. et al.: Phytotoxicity of Roundup Ultra 360 SL in aquatic ecosystems: Biochemical evaluation with duckweed (Lemna minor L.) as a model plant. - Pestic. Biochem. Phys. 99: 237-243, 2011. Go to original source...
    30. King C.A., Purcell L.C., Vories E.D.: Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to foliar glyphosate applications. - Agron. J. 93: 179-186, 2001. Go to original source...
    31. Lai C.S., Piette L.H.: Hydroxyl radical production involved in lipid peroxidation of rat liver microsomes. - Biochem. Bioph. Res. Co. 78: 51-59, 1977. Go to original source...
    32. Lichtenthaler H.K., Buschmann C.: Chlorophylls and carotenoids: Measurement and characterization by UV-VIS spectroscopy. - In: Lichtenthaler K. (ed.): Current Protocols in Food Analytical Chemistry. Wiley, New York 2001. Go to original source...
    33. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J.: Protein measurement with the Folin phenol reagent. - J. Biol. Chem. 193: 265-275, 1951.
    34. MacAdam J.W., Nelson C.J., Sharp R.E.: Peroxidase activity in the leaf elongation zone of tall fescue I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. - Plant Physiol. 99: 872-878, 1992. Go to original source...
    35. Mateos-Naranjo E., Redondo-Gómez S., Cox L. et al.: Effectiveness of glyphosate and imazamox on the control of the invasive cordgrass Spartina densiflora. - Ecotoxicol. Environ. Safe. 72: 1694-1700, 2009. Go to original source...
    36. Miteva L.-E., Ivanov S., Alexieva V.: Alterations in glutathione pool and some related enzymes in leaves and roots of pea plants treated with the herbicide glyphosate. - Russ. J. Plant Physl+ 57: 131-136, 2010. Go to original source...
    37. Moore S., Stein W.H.: Photometric ninhydrin method for use in the chromatography of amino acids. - J. Biol. Chem. 176: 367-388, 1948.
    38. Naik G., Priyadarsini K., Satav J. et al.: Comparative antioxidant activity of individual herbal components used in Ayurvedic medicine. - Phytochemistry 63: 97-104, 2003. Go to original source...
    39. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
    40. Olesen C.F., Cedergreen N.: Glyphosate uncouples gas exchange and chlorophyll fluorescence. - Pest Manage. Sci. 66: 536-542, 2010.
    41. Oyinlola A., Ojo A., Adekoya L.: Development of a laboratory model screw press for peanut oil expression. - J. Food Eng. 64: 221-227, 2004. Go to original source...
    42. Pline W.A., Wu J., Hatzios K.K.: Effects of temperature and chemical additives on the response of transgenic herbicideresistant soybeans to glufosinate and glyphosate applications. - Pestic. Biochem. Phys. 65: 119-131, 1999. Go to original source...
    43. Racchi M.: Glyphosate tolerance in plant cell cultures. - In: Sangwan R.S., Sangwan-Norreel B.S. (ed.): The Impact of Biotechnology on Agriculture. Pp. 437-446. Kluwer Academic Press, Dordrecht 1990. Go to original source...
    44. Radwan D.E.M., Soltan D.M.: The negative effects of clethodim in photosynthesis and gas-exchange status of maize plants are ameliorated by salicylic acid pretreatment. - Photosynthetica 50: 171-179, 2012. Go to original source...
    45. Radwan D.E., Lu G., Fayez K.A., Mahmoud S.Y.: Protective action of salicylic acid against bean yellow mosaic virus infection in Vicia faba leaves. - J. Plant Physiol. 165: 845-857, 2008. Go to original source...
    46. Radwan D.E.M.: Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays L.) leaves. - Pestic. Biochem. Phys. 102: 182-188, 2012. Go to original source...
    47. Reddy K.N., Hoagland R.E., Zablotowicz R.M.: Effect of glyphosate on growth, chlorophyll, and nodulation in glyphosate-resistant and susceptible soybean (Glycine max) varieties. - J. New Seeds 2: 37-52, 2001. Go to original source...
    48. Schönbrunn E., Eschenburg S., Shuttleworth W.A. et al.: Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail. - P. Natl. Acad. Sci. USA 98: 1376-1380, 2001. Go to original source...
    49. Sergiev I.G., Alexieva V.S., Ivanov S.V. et al.: The phenylurea cytokinin 4PU-30 protects maize plants against glyphosate action. - Pestic. Biochem. Phys. 85: 139-146, 2006. Go to original source...
    50. Servaites J.C., Tucci M.A., Geiger D.R.: Glyphosate effects on carbon assimilation, ribulose bisphosphate carboxylase activity, and metabolite levels in sugar beet leaves. - Plant Physiol. 85: 370-374, 1987. Go to original source...
    51. Shimada K., Fujikawa K., Yahara K., Nakamura T.: Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. - J. Agric. Food Chem. 40: 945-948, 1992. Go to original source...
    52. Song N.H., Le Yin X., Chen G.F., Yang H.: Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. - Chemosphere 68: 1779-1787, 2007. Go to original source...
    53. Srivalli B., Chinnusamy V., Khanna-Chopra R.: Antioxidant defense in response to abiotic stresses in plants. - J. Plant Biol.-New Delhi 30: 121-140, 2003.
    54. Steinrücken H., Amrhein N.: The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. - Biochem. Bioph. Res. Co. 94: 1207-1212, 1980. Go to original source...
    55. Tan S., Evans R., Singh B.: Herbicidal inhibitors of amino acid biosynthesis and herbicide-tolerant crops. - Amino Acids 30: 195-204, 2006. Go to original source...
    56. Torstensson L.: Behaviour of glyphosate in soils and its degradation. - In: E. Grossbard, Atkinson D. (ed.): The Herbicide Glyphosate. Pp. 137-150. Butterworths, London 1985. Go to original source...
    57. Vencill W.K.: Herbicide Handbook. Pp. 493. Weed Sci. Soc. Amer., Lawrence 2002.
    58. Wiseman H., Halliwell B.: Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. - Biochem. J. 313: 17-29, 1996. Go to original source...
    59. Wong P.: Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614. - Chemosphere 41: 177-182, 2000. Go to original source...
    60. Xue Y.J., Tao L., Yang Z.M.: Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. - J. Agric. Food Chem. 56: 9676-9684, 2008. Go to original source...
    61. Yamauchi Y., Furutera A., Seki K. et al.: Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. - Plant Physiol. Bioch. 46: 786-793, 2008. Go to original source...
    62. Yin X.L., Jiang L., Song N.H., Yang H.: Toxic reactivity of wheat (Triticum aestivum) plants to herbicide isoproturon. - J. Agric. Food Chem. 56: 4825-4831, 2008. Go to original source...
    63. Yu J., Ahmedna M., Goktepe I.: Peanut protein concentrate: Production and functional properties as affected by processing. - Food Chem. 103: 121-129, 2007. Go to original source...
    64. Zhang X.: Research Methodology of Crop Physiology. Pp. 208-211. Agri. Press, Beijing 1992.
    65. Zobiole L.H.S., Kremer R.J., Constantin J.: Glyphosate effects on photosynthesis, nutrient accumulation, and nodulation in glyphosate-resistant soybean. - J. Plant Nutr. Soil Sc. 175: 319-330, 2012. Go to original source...

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