5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots

Ecotoxicology and Environmental Safety

Volumn 92, Issue , 2013, Pages 271-280

  Ali, Basharat ^a   Tao, Qiaojing ^a   Zhou, Yuanfei ^a   Gill, Rafaqat A ^a   Ali, Shafaqat ^b   Rafiq, Muhammad T ^c   Xu, Ling ^a   Zhou, Weijun ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b GOVERNMENT COLLEGE UNIVERSITY   (Pakistan)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

5 aminolevulinic acid; Antioxidant enzymes; Cadmium; Oilseed rape; Reactive oxygen species; Root morphology; Root ultra structures

Indexed keywords

AMINOLEVULINIC ACID; ASCORBATE PEROXIDASE; CADMIUM; CATALASE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; MALONALDEHYDE; PEROXIDASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANGIOSPERM; ANTIOXIDANT; BIOCHEMISTRY; CADMIUM; CONCENTRATION (COMPOSITION); ECOTOXICOLOGY; ENZYME; MEMBRANE; MITOCHONDRION; MORPHOLOGY; ROOT; TOXICITY; ULTRASTRUCTURE;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL SHAPE; CELL ULTRASTRUCTURE; CELL WALL; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HYDROPONICS; MITOCHONDRION; NONHUMAN; PLANT GROWTH; PLANT STRESS; PROTEIN CONTENT; RAPESEED; ROOT CELL; ROOT MORPHOLOGY;

AMINOLEVULINIC ACID; ANIMALS; BRASSICA NAPUS; CADMIUM; CATALASE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL REMEDIATION; GLUTATHIONE; GLUTATHIONE REDUCTASE; MALONDIALDEHYDE; OXIDATION-REDUCTION; PEROXIDASE; PLANT LEAVES; PLANT ROOTS; PROTECTIVE AGENTS; REACTIVE OXYGEN SPECIES; SOIL POLLUTANTS; SUPEROXIDE DISMUTASE;

BRASSICA NAPUS;

EID: 84876974758     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2013.02.006     Document Type: Article

References (77)

1. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
2. Alcantara E., Romera F.J., Canete M., De La Guardia M.D. Effects of heavy metals on both induction and function of root Fe(III) reductase in Fe-deficient cucumber (Cucumis sativus L.) plants. J. Exp. Bot. 1994, 45:1893-1898.
3. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55:373-399.
4. Arisi A.C.M., Mocquot B., Lagriffoul A., Mench M., Foyer C.H., Jouanin L. Responses to cadmium in leaves of transformed poplars over expressing T glutamyl cysteine synthetase. Physiol. Plant. 2000, 109:143-149.
5. Arnon D.I., Hoagland D.R. Crop production in artificial solution with special reference to factors affecting yield and absorption of inorganic nutrients. Soil Sci. 1940, 50:463-485.
6. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:601-639.
7. Bachir M.L.D., Wu F.B., Zhang G.P., Wu H.X. Genotypic difference in effect of cadmium on the development and mineral concentrations of cotton. Commun. Soil Sci. Plant Anal. 2004, 35:285-299.
8. Bhaya D., Castelfranco P.A. Chlorophyll biosynthesis and assembly into chlorophyll protein complexes in isolated developing chloroplasts. Proc. Natl. Acad. Sci. USA 1985, 82:5370-5374.
9. Bradford N.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
10. Caasilit M., Whitecross M.I., Nayudu M., Tanner G.J. UV-B irradiation induce differential leaf damage, ultrastructural changes and accumulation of specific phenolic compounds in rice cultivars. Aust. J. Plant Physiol. 1997, 24:261-274.
11. Castelfranco P.A., Jones O.T.G. Protoheme turnover and chlorophyll synthesis in greening barley tissue. Plant Physiol. 1975, 55:485-490.
12. Choudhury S., Panda S.K. Role of salicylic acid in regulating cadmium induced oxidative stress in Oryza sativa L. roots. Bulg. J. Plant Physiol. 2004, 30(3-4):95-110.
13. Daud M.K., Yuqiang S., Dawood M., Hayat Y., Variath M.T., Wu Y.X., Raziuddin, Mishkat U., Salahuddin, Najeeb U., Zhu S.J. Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J. Hazard. Mater. 2009, 161(1):463-473.
14. Dazy M., Masfaraud J.F., Ferard J.F. Induction of oxidative stress biomarkers associated with heavy metal stress in Fontinalis antipyretica Hedw. Chemosphere 2009, 75:297-302.
15. Dietz K.J., Baier M., Kramer U. Free radicals and reactive oxygen species as mediator of heavy metal toxicity in plants. Heavy Metal Stress in Plants. From Molecules to Ecosystem 1999, 73-89. Springer-Verlag, Berlin. M.N.V. Prasad, J. Hagemeyer (Eds.).
16. El-Tayeb M.A. Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul. 2005, 45:215-224.
17. Folgar S., Torres E., Perez-Rama M., Cid A., Herrero C., Abalde J. Dunaliella salina as marine microalga highly tolerant to but a poor remover of cadmium. J. Hazard. Mater. 2009, 165:486-493.
18. Gullner G., Dodge A.D. Accumulation of glutathione in pea leaf discs exposed to the photooxidative herbicides acifluorfen and 5-aminolevulinic acid. J. Plant Physiol. 2000, 156:111-117.
19. Gunes A., Inal A., Bagci E.G., Coban S., Sahin O. Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. Biol. Plant. 2007, 51:571-574.
20. Gouia H., Ghorbal M., Meyer C. Effect of cadmium on activity of nitrate reductase and other enzymes of the nitrate assimilation pathway in bean. Plant Physiol. Biochem. 2000, 38:629-638.
21. Halliwell B., Gutteridge J.M.C., Aruoma O. The deoxyribose method: a simple 'test tube' assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 1987, 165:215-219.
22. Hasan S.A., Fariduddin Q., Ali B., Hayat S., Ahmad A. Cadmium: toxicity and tolerance in plants. J. Environ. Biol. 2009, 30:165-174.
23. Hayat S., Ahmad A. Salicylic acid: a plant hormone. Role of salicylic acid in the induction of abiotic stress tolerance 2007, 91-150. Springer, Dordrecht. T. Janda, E. Horváth, G. Szalai, E. Paldi (Eds.).
24. Hendry G.A.F., Baker A.J.M., Ewart C.F. Cadmium tolerance and toxicity, oxygen radical processes and molecular damage in cadmium-tolerant and cadmium sensitive clones of Holcus lanatus. Acta Bot. Neerl. 1992, 41:271-281.
25. Hull H.M., Morton H.L., Wharrie J.R. Environmental influence on cuticle development and resultant foliar penetration. Bot. Rev. 1975, 41:421-451.
26. Islam E., Yang X., Li T., Liu D., Jin X., Meng F. Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J. Hazard. Mater. 2007, 147:806-816.
27. Jalil A., Selles F., Clarke J.M. Effect of cadmium on growth and uptake of cadmium and other elements by Durum wheat. J. Plant Nutr. 1994, 17:1839-1858.
28. Jiang M., Zhang J. Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol. 2001, 42:1265-1273.
29. Jiang M., Zhang J. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 2002, 53:2401-2410.
30. Jin X., Yang X., Islam E., Liu D., Mahmood Q. Effects of cadmium on ultra-structure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredi Hance. J. Hazard. Mater. 2008, 156:387-397.
31. Keramat B., Kalantari K.M., Arvin M.J. Effects of methyl jasmonate in regulating cadmium induced oxidative stress in soybean plant (Glycine max L.). Afr. J. Microbiol. Res. 2009, 3:240-244.
32. Kupper H., Lombi E., Zhao F.J., McGrath S.P. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 2000, 212:75-84.
33. Law M.Y., Charles S.A., Halliwell B. Glutathione and ascorbic-acid in spinach (Spinacia oleracea) chloroplasts-the effect of hydrogen-peroxide and of paraquat. Biochem. J. 1983, 210:899-903.
34. Leul M., Zhou W.J. Alleviation of waterlogging damage in winter rape by uniconazole application: effects on enzyme activity, lipid peroxidation and membrane integrity. J. Plant Growth Regul. 1999, 18:9-14.
35. 2+ on root growth and cell division of Allium cepa. Acta Sci. Circumstantiae 1992, 12:439-446.
36. Liu D., Kottke I. Subcellular localization of cadmium in the root cells of Allium cepa by electron energy loss spectroscopy and cytochemistry. J. Biosci. 2004, 29:329-335.
37. Liu D., Jiang W., Gao X. Effect of cadmium on root growth, cell division and nucleoli in root tip cells of garlic. Biol. Plant. 2003, 47:79-83.
38. Liu D., Jiang W., Wang W., Zhai L. Evaluation of metal ion toxicity on root tip cells by the Allium test. Isr. J. Plant Sci. 1995, 43:125-133.
39. Liu D., Pei Z.F., Naeem M.S., Ming D.F., Liu H.B., Khan F., Zhou W.J. 5-Aminolevulinic acid activates antioxidative defence system and seedling growth in Brassica napus L. under water-deficit stress. J. Agron. Crop Sci. 2011, 197:284-295.
40. Meng H.B., Hua S.J., Shamsi I.H., Jilani G., Li Y.L., Jiang L.X. Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul. 2009, 58:47-59.
41. Mohamed A.A., Castagna A., Ranieri A., Sanita di toppi L. Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol. Biochem. 2012, 57:15-22.
42. Momoh E.J.J., Zhou W.J. Growth and yield responses to plant density and stage of transplanting in winter oilseed rape (Brassica napus L.). J. Agron. Crop Sci. 2001, 186:253-259.
43. Naeem M.S., Rasheed M., Liu D., Jin Z.L., Ming D.F., Yoneyama K., Takeuchi Y., Zhou W.J. 5-Aminolevulinic acid ameliorates salinity-induced metabolic, water-related and biochemical changes in Brassica napus L. Acta Physiol. Plant. 2011, 33:517-528.
44. Naeem M.S., Warusawitharana H., Liu H.B., Liu D., Ahmad R., Waraich E.A., Xu L., Zhou W.J. 5-Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. Plant Physiol. Biochem. 2012, 57:84-92.
45. Najeeb U., Jilani G., Ali S., Sarwar M., Xu L., Zhou W.J. Insight into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J. Hazard. Mater. 2011, 186:565-574.
46. Nakano Y., Asada K. Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 1981, 22:867-880.
47. Nishihara E., Takahashi K., Nakata N., Tanaka K., Watanabe K. Effect of 5-aminolevulinic acid (ALA) on photosyntheticrate, hydrogen peroxide content, antioxidant level and active oxygen-scavenging enzymes in spinach (Spinacia oleracea L.). J. Jpn. Soc. Hortic. Sci. 2001, 70:346-352.
48. Nishihara E., Kondo K., Masud Parvez M., Takahashi K., Watanabe K., Tanaka K. Role of 5-aminolevulinic acid (ALA) on active oxygen-scavenging system in NaCl-treated spinach (Spinacia oleracea). Plant Physiol. 2003, 160:1085-1091.
49. Panda S.K., Upadhyay R.K. Salt stress induces oxidative alterations and antioxidative defense in the roots of Lemna minor. Biol. Plant. 2004, 48:249-253.
50. Panda S.K., Chaudhury I., Khan I.M.H. Heavy metal induced lipid peroxidation and affect antioxidants in wheat leaves. Biol. Plant. 2003, 46:289-294.
51. Papazoglou E.G., Karantounias G.A., Vemmos S.N., Bouranis D.L. Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni. Environ. Int. 2005, 31:243-249.
52. Purvis A.C. Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 1997, 100:165-170.
53. Roy C.B., Vivekanandan M. Role of aminolevulinic acid in improving biomass production in Vigna catjung, V. mungo, and V. radiata. Biol. Plant. 1998, 41:211-215.
54. Schutzendubel A., Schwanz P., Teichmann T., Gross K., LangenfeldHeyser R., Godbold D.L., Polle A. Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 2001, 127:887-898.
55. Schwarz D., Grosch R. Influence of nutrient solution concentration and a root pathogen on tomato root growth and morphology. Sci. Hortic. 2003, 97:109-120.
56. Shah K., Dubey R.S. Effect of cadmium on RNA level as well as activity and molecular forms of ribonuclease in growing rice seedlings. Plant Physiol. Biochem. 1995, 33:577-584.
57. Shah K., Kumar R.G., Verma S., Dubey R.S. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedling. Plant Sci. 2001, 161:1135-1144.
58. Shani U., Ben-Gal A. Long-term response of grapevines to salinity: osmotic effects and ion toxicity. Am. J. Enol. Vitic. 2005, 56:148-154.
59. Singh N., Ma L.Q., Srivastava M., Rathinasabapathi B. Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci. 2006, 170:274-282.
60. Sinha S., Basant A., Malik A., Singh K.P. Multivariate modeling of chromium-induced oxidative stress and biochemical changes in plants of Pistia stratiotes L. Ecotoxicology 2009, 8:555-566.
61. Song A., Li Z., Zhang J., Xue G., Fan F., Liang Y. Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J. Hazard. Mater. 2009, 172:74-83.
62. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18:321-336.
63. Stohs S.J., Bagchi D., Hassoun E., Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J. Environ. Pathol. Toxicol. Oncol. 2000, 19:201-213.
64. Stoyanova D., Chakalova E. The effect of cadmium on the structure of photosynthetic apparatus in Elodea canadensis Rich. Plant Physiol. 1990, 16:18-26.
65. Thian X., Li Y. Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol. Plant. 2006, 50:775-778.
66. Van Huystee R.B. A study of peroxidase synthesis by means of double labeling and affinity chromatography. Can. J. Bot. 1976, 54:876-880.
67. Velikova V., Yordanov I., Edreva A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci. 2000, 151:59-66.
68. Vitoria A.P., Rodriguez A.P.M., Cunha M., Lea P.J., Azevedo R.A. Structural changes in radish seedlings (Raphanus sativus) exposed to cadmium. Biol. Plant. 2004, 47:561-568.
69. Watanabe K., Tanaka T., Kuramochi H., Takeuchi Y. Improving salt tolerance of cotton seedling with 5-aminolevulinic acid. Plant Growth Regul. 2000, 32:97-101.
70. Yamamoto Y., Kobayashi Y., Mutsumoto H. Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol. 2001, 125:199-208.
71. Youssef T., Awad M.A. Mechanisms of enhancing photosynthetic gas exchange in date palm seedlings (Phoenix dactylifera L.) under salinity stress by a 5-aminolevulinic acid-based fertilizer. J. Plant Growth Regul. 2008, 27:1-9.
72. Zengin F.K., Munzuroglu O. Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus Vulgaris L.) seedlings. Acta Biol. Cracov. Bot. 2005, 47:157-164.
73. Zhang Z.J., Li H.Z., Zhou W.J., Takeuchi Y., Yoneyama K. Effect of 5-aminolevulinic acid on development and salt tolerance of potato (Solanum tuberosum L.) microtubers in vitro. Plant Growth Regul. 2006, 49:27-34.
74. Zhang Z.F., Zhang F., Raziuddin, Gong H.J., Yang Z.M., Lu L., Ye Q.F., Zhou W.J. Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. J. Plant Growth Regul. 2008, 27:159-169.
75. Zhou W.J., Lin X.Q. Effects of water logging at different growth stages on physiological characteristics and seed yield of winter rape (Brassica napus L.). Field Crops Res. 1995, 44:103-110.
76. Zhou W.J., Leul M. Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul. 1998, 26:41-47.
77. Zhou W.J., Leul M. Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul. 1999, 27:99-104.