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Journal of Integrative Agriculture  2018, Vol. 17 Issue (03): 579-592    DOI: 10.1016/S2095-3119(17)61676-9
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5-Aminolevulinic acid alleviates herbicide-induced physiological and ultrastructural changes in Brassica napus
XU Ling1, Faisal Islam2, ZHANG Wen-fang3, Muhammad A Ghani4, Basharat Ali2, 5 
1 Key Laboratory of Plant Secondary Metabolism and Regulation of Zhejiang/College of Life Sciences, Zhejiang Sci-Tech University, Hangzhou 310018, P.R.China
2  Institute of Crop Science, Zhejiang University, Hangzhou 310058, P.R.China
3 Jiading District Agro-Technology Extension Service Center, Shanghai 201800, P.R.China
4 Institute of Horticultural Sciences, University of Agriculture, Faisalabad 38040, Pakistan
5 Institute of Crop Science and Resource Conservation, University of Bonn, Bonn 53115, Germany
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Abstract  It is well known that application of 5-aminolevulinic acid (ALA) could promote the plant growth under abiotic stress in oilseed rape (Brassica napus L.).  However, the specifics of its physiological and ultrastructural regulation under herbicide stress conditions are poorly understood.  In the present study, alleviating role of ALA in B. napus was investigated under four levels of herbicide propyl 4-(2-(4,6-dimethoxypyrimidin-2-yloxy) benzylamino) benzoate (ZJ0273) (0, 100, 200 and
500 mg L–1) with or without 1 mg L–1 ALA treated for 48 or 72 h.  Results showed that after 48 h of herbicide stress, the growth of rape seedlings was significantly inhibited with the successive increases of the ZJ0273 concentrations from 0 to 500 mg L–1, but this inhibition was obviously alleviated by exogenous application of ALA.  However, when treatment time prolonged to 72 h, the recovery effects of ALA could not be evaluated due to the death of plants treated with the highest concentration of ZJ0273 (500 mg L-1).  Further, the root oxidizability and activities of antioxidant enzymes (superoxide dismutase, peroxidase and ascorbate peroxidase) were dramatically enhanced by the application of 1 mg L–1 ALA under herbicide stress.  Therefore, plants treated with ALA dynamically modulated their antioxidant defenses to reduce reactive oxygen species (ROS) accumulation and malondialdehyde (MDA) content induced by herbicide stress.  Additionally, exogenously applied ALA improved the ultrastructure’s of chloroplast, mitochondria and nucleus, and induced the production of stress proteins.  Our results suggest that ALA could be considered as a potential plant growth regulator for the improvement of herbicide tolerance through alleviation of the physiological and ultrastructural changes induced by the herbicide in crop production.
Keywords:  Brassica napus L.        ALA        ZJ0273        plant growth        antioxidant enzyme activities        ultrastructure        two-dimensional gel electrophoresis (2-DE)  
Received: 07 February 2017   Accepted:

This work was supported by the Science and Technology Department of Zhejiang Province, China (2016C02050-8, 2016C32089), the Special Fund for Agro-scientific Research in the Public Interest, China (201303022), the Jiangsu Collaborative Innovation Center for Modern Crop Production, China, the Zhejiang Provincial Top Key Discipline of Biology, China, and the Zhejiang Provincial Open Foundation, China (2014C03, 2016D11).

Corresponding Authors:  Correspondence Basharat Ali, Mobile: +49-1771862360, E-mail:   
About author:  XU Ling, E-mail:

Cite this article: 

XU Ling, Faisal Islam, ZHANG Wen-fang, Muhammad A Ghani, Basharat Ali. 2018. 5-Aminolevulinic acid alleviates herbicide-induced physiological and ultrastructural changes in Brassica napus. Journal of Integrative Agriculture, 17(03): 579-592.

Akram N A, Ashraf M. 2013. Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. Journal of Plant Growth Regulation, 32, 663–679.

Akram N A, Ashraf M, Al-Qurainy F. 2012. Aminolevulinic acid-induced regulation in some key physiological attributes and activities of antioxidant enzymes in sunflower (Helianthus annuus L.) under saline regimes. Scientia Horticulturae, 142, 143–148.

Ali B, Gill R A, Yang S, Gill M B, Farooq M A, Liu D, Daud M K, Ali S, Zhou W J. 2015. Regulation of cadmium-induced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L. PLoS ONE, 10, e0123328.

Ali B, Qian P, Jin R, Ali S, Khan M, Aziz R, Tian T, Zhou W. 2014a. Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biologia Plantarum, 58, 131–138.

Ali B, Tao Q J, Zhou Y F, Gill R A, Ali S, Rafiq M T, Xu L, Zhou W J. 2013a. 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, 92, 271–280.

Ali B, Wang B, Ali S, Ghani M A, Hayat M T, Yang C, Xu L, Zhou W J. 2013b. 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity and ultrastructural changes under cadmium stress in Brassica napus L. Journal of Plant Growth Regulation, 32, 604–614.

Ali B, Xu X, Gill R A, Yang S, Ali S, Tahir M, Zhou W J. 2014b. Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Industrial Crops and Products, 52, 617–626.

Bradford M M A. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 25, 248–256.

Bray E A. 1988. Drought and ABA-induced changes in polypeptide and mRNA accumulation in tomato leaves. Plant Physiology, 88, 1210–1214.

Diepenbrock W. 2000. Yield analysis of winter oilseed rape (Brassica napus L.): A review. Field Crops Research, 67, 35–49.

Farooq M A, Gill R A, Islam F, Ali B, Liu H B, Xu J X, He S P, Zhou W J. 2016. Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Frontiers in Plant Science, 7, 468.

Gill R A, Zhang N, Ali B, Farooq M A, Xu J X, Gill M B, Mao B Z, Zhou W J. 2016. Role of exogenous salicylic acid in regulating physio-morphic and molecular changes under chromium toxicity in black- and yellow-seeded Brassica napus L. Environmental Science and Pollution Research, 23, 20483–20496.

Guo X J. 2005. Protein Electrophoresis Experiment Technology. 2nd ed. Science Press, China. (in Chinese)

Hajri H, Mhadhebi R, Ghorbel A, Armstrong J, Salem-fnayou A B. 2016. Physiological and leaf ultrastructural characteristics of perennial ryegrass (Lolium perenne L.) biotypes from Tunisia under sulfonylurea herbicide application. Scientia Horticulturae, 207, 28–32.

Holopainen T, Anttonen S, Wulff A, Palomäki V, Kärenlampi L. 1992. Comparative evaluation of the effects of gaseous pollutants, acid deposition and mineral deficiencies: Structural changes in the cells of forest plants. Agriculture, Ecosystem and Environment, 42, 365–398.

Hotta Y, Tanaka T, Akaoka H, Takeuchi Y, Konnai M. 1997. New physiological effects of 5-aminolevulinic acid in plants: The increase of photosynthesis, chlorophyll content, and plant growth. Bioscience Biotechnology and Biochemistry, 61, 2025–2028.

Hotta Y, Tanaka T, Bingshan L, Takeuchi Y, Konnai M. 1998. Improvement of cold resistance in rice seedlings by 5-aminolevulinic acid. Journal of Pesticide Science, 23, 29–33.

Huffaker E C, Peterson L W. 1974. Protein turnover in plants and possible means of its regulation. Annual Review of Plant Physiology, 25, 363–392.

Inada N, Sakai A, Kuroiwa H, Kuroiwa T. 1998. Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles - Investigations by fluorescence and electron microscopy. Planta, 206, 585–597.

Islam F, Ali B, Wang J, Farooq M A, Gill R A, Ali S, Wang D Y, Zhou W J. 2016. Combined herbicide and saline stress differentially modulates hormonal regulation and antioxidant defense system in Oryza sativa cultivars. Plant Physiology and Biochemistry, 107, 82–95.

Jin Z L, Zhang F, Ahmed Z I, Rasheed M, Naeem M S, Ye Q F, Zhou W J. 2010. Differential morphological and physiological responses of two oilseed Brassica species to a new herbicide ZJ0273 used in rapeseed fields. Pesticide Biochemistry and Physiology, 98, 1–8.

Kaya A, Doganlar Z B. 2016. Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicology and Environmental Safety, 124, 470–479.

Lee J M, Owen M D K. 2000. Comparison of acetolactate synthase enzyme inhibition among resistant and susceptible Xanthium strumarium biotypes. Weed Science, 48, 286–290.

Li N Y, Gao J F, Wang P H. 1998. The characteristics of induced protein in shoots of wheat seedlings under water stress. Acta Phytophysiologica Sinica, 24, 65–71.

Liu D, Pei Z F, Naeem M S, Ming D F, Liu H B, Khan F, Zhou W J. 2011. 5-Aminolevulinic acid activates antioxidative defense system and seedling growth in Brassica napus L. under water-deficit stress. Journal of Agronomy and Crop Science, 197, 284–295.

Momoh E J J, Zhou W J, Kristiansson B. 2002. Variation in the development of secondary dormancy in oilseed rape genotypes under conditions of stress. Weed Research, 42, 446–455.

Naeem M S, Jin Z L, Wan G L, Liu D, Liu H B, Yoneyama K, Zhou W J. 2010. 5-Aminolevulinic acid improves photosynthetic gas exchange capacity and ion uptake under salinity stress in oilseed rape (Brassica napus L.). Plant and Soil, 332, 405–415.

Naeem M S, Rasheed M, Liu D, Jin Z L, Ming D F, Yoneyama K, Takeuchi Y, Zhou W J. 2011. 5-Aminolevulinic acid ameliorates salinity-induced metabolic, water-related and biochemical changes in Brassica napus L. Acta Physiologiae Plantarum, 33, 517–528.

Naeem M S, Warusawitharana H, Liu H B, Liu D, Ahmad R, Waraich E A, Xu L, Zhou W J. 2012. 5-Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. Plant Physiology and Biochemistry, 57, 84–92.

Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou W J. 2011. Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. Journal of Hazardous Materials, 186, 565–574.

Nakano Y, Asada K. 1981. Hydrogen peroxide scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology, 22, 867–880.

Ren A Z, Gao Y B, Liu S. 2000. Effects of Cr, Cd and Pb on free proline content etc in leaves of Brassica chinensis L. Chinese Journal of Applied and Environmental Biology, 6, 112–116. (in Chinese)

Sharma P, Dubey R S. 2005. Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17, 35–52.

Song W J, Zhou W J, Jin Z L, Cao D D, Joel D M, Takeuchi Y, Yoneyama K. 2005. Germination response of Orobanche seeds subjected to conditioning temperature, water potential and growth regulator treatments. Weed Research, 45, 467–476.

Tang Q H, Chen J, Lu L. 2005. An innovative research for novel rape herbicide ZJ0273. Chinese Journal of Pesticides, 44, 496–502.

Wang J, Lv M, Islam F, Gill R A, Yang C, Ali B, Yan G, Zhou W. 2016. Salicylic acid mediates antioxidant defense system and ABA pathway related gene expression in Oryza sativa against quinclorac toxicity. Ecotoxicology and Environmental Safety, 133, 146–156.

Von Wettstein D, Gough S, Kannangara C G. 1995. Chlorophyll biosynthesis. The Plant Cell, 7, 1039–1057.

Wu J, Zhang P Z, Lu L, Yu Q S, Hu X R, Gu J M. 2003. Synthesis and crystal structure of n-propyl-4-[2-(4, 6-dimethoxypyrimidin-2-yloxy) benzylamino] benzoate. Chinese Journal of Structural Chemistry, 22, 613–616.

Xia P G, Guo H B, Zhao H G, Jie J, Deyholos M K, Yan X J, Yan L, Liang Z S. 2016. Optimal fertilizer application for Panax notoginseng and effect of soil water on root rot disease and saponin contents. Journal of Ginseng Research, 40, 38–46.

Xia P G, Li J Z, Wang R L, Zhang Y, Guo H B, Yan X J, Liu Y, Liang Z S. 2015. Comparative study on volatile oils of four Panax genus species in Southeast Asia by gas chromatography-mass spectrometry. Industrial Crops and Products, 74, 478–484.

Xu L, Zhang W F, Ali B, Islam F, Zhu J W, Zhou W J. 2015. Synergism of herbicide toxicity by 5-aminolevulinic acid is related to physiological and ultra-structural disorders in crickweed (Malachium aquaticum L.). Pesticide Biochemistry and Physiology, 125, 53–61.

Yang D F, Ma P D, Liang X, Liang Z S, Zhang M X, Shen S, Liu H Y, Liu Y. 2012. Metabolic profiles and cDNA-AFLP aanalysis of Salvia miltiorrhiza and Salvia castanea Diel f. tomentosa Stib. PLoS ONE, 7, e29678.

Zhang F, Jin Z L, Naeem M S, Ahmed Z I, Gong H J, Lu L, Ye Q F, Zhou W J. 2009. Spatial and temporal changes in acetolactate synthase activity as affected by new herbicide ZJ0273 in rapeseed, barley and water chickweed. Pesticide Biochemistry and Physiology, 95, 63–71.

Zhang F Q, Shi W Y, Jin Z X, Shen Z G. 2003. Response of antioxidative enzymes in cucumber chloroplasts to cadmium toxicity. Journal of Plant Nutrition, 26, 1779–1788.

Zhang M, Fang Y M, Ji Y H, Jiang Z P, Wang L. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. South African Journal of Botany, 85, 1–9.

Zhang W F, Zhang F, Jin Z L, Huang C P, Tang G X, Ye Q F, Zhou W J. 2008a. ALA improving Brassica napus seedling tolerance to herbicide stress. Journal of Nuclear Agricultural Sciences, 22, 488–494.

Zhang W F, Zhang F, Raziuddin R, Gong H J, Yang Z M, Lu L, Ye Q F, Zhou W J. 2008b. Effects of 5-aminolevulinic acid on oilseed rape seedling growth under herbicide toxicity stress. Journal of Plant Growth Regulation, 27, 159–169.

Zhang Y B, Zhou Y. 2000. Plant physiological activity of 5-aminolevulinic acid. World Pesticide, 22, 8–14.

Zhou Q Y, Liu W P, Zhang Y S, Liu K K. 2007. Action mechanisms of acetolactate synthase-inhibiting herbicides. Pesticide Biochemistry and Physiology, 89, 89–96.

Zhou W, Ye Q. 1996. Physiological and yield effects of uniconazole on winter rape (Brassica napus L.). Journal of Plant Growth Regulation, 15, 69–73.

Zhou W J. 2016. Oilseed rape. In: Zhang G P, Zhou W J, eds., Crop Production (2nd edition). Zhejiang University Press, Hangzhou. pp. 173–205. (in Chinese)

Zhou W J, Leul M. 1998. Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regulation, 26, 41–47.

Zhou W J, Leul M. 1999. Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regulation, 27, 99–104.
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