Responses of Plants to Pesticide Toxicity: an Overview

SHARMA, A.; KUMAR, V.; THUKRAL, A.K.; BHARDWAJ, R.; SHARMA, A.; KUMAR, V.; THUKRAL, A.K.; BHARDWAJ, R.

doi:10.1590/s0100-83582019370100065

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Planta Daninha

Print version ISSN 0100-8358On-line version ISSN 1806-9681

Planta daninha vol.37 Viçosa 2019 Epub Aug 19, 2019

https://doi.org/10.1590/s0100-83582019370100065

Literature Review

Responses of Plants to Pesticide Toxicity: an Overview

Respostas de Plantas à Toxicidade de Pesticidas: Uma Visão Geral

A. SHARMA¹^*
http://orcid.org/0000-0002-5251-9045

V. KUMAR¹

A.K. THUKRAL¹

R. BHARDWAJ¹

^¹ Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Amritsar-143005, India.

ABSTRACT:

Pesticides are applied all over the world to protect plants from pests. However, their application also causes toxicity to plants, which negatively affects the growth and development of plants. Pesticide toxicity results in reduction of chlorophyll and protein contents, accompanied by decreased photosynthetic efficiency of plants. Pesticide stress also generates reactive oxygen species which causes oxidative stress to plants. To attenuate the negative effects of oxidative stress, the antioxidative defense system of plants gets activated, and it includes enzymatic antioxidants as well as non-enzymatic antioxidants. The present review gives an overview of various physiological responses of plants under pesticide toxicity in tabulated form.

Keywords: physiological responses; antioxidative defense system; oxidative stress

RESUMO:

Os pesticidas são aplicados no mundo todo para proteger as plantas contra as pragas. No entanto, essa aplicação também causa toxicidade às plantas, o que afeta de forma negativa o crescimento e o desenvolvimento delas. A toxicidade dos pesticidas resulta na redução dos teores de clorofila e proteína, acompanhada de menor eficiência fotossintética das plantas. O estresse causado por pesticidas também gera espécies reativas de oxigênio, que causam estresse oxidativo às plantas. Para atenuar os efeitos negativos do estresse oxidativo, o sistema de defesa antioxidante das plantas é ativado, e isso inclui antioxidantes enzimáticos e não enzimáticos. A presente revisão fornece uma visão geral de várias respostas fisiológicas de plantas sob toxicidade de pesticidas, em forma de tabela.

Palavras-chave: respostas fisiológicas; sistema de defesa antioxidante; estresse oxidativo

INTRODUCTION

A pesticide is a compound which is utilized to repel, kill or prevent any pest. On the basis of the target killed, pesticides are mainly classified as herbicides, fungicides and insecticides. The increased demand of food on account of population explosion has compelled man to use pesticides for better crop production (^{Tomer, 2013}). Pesticides are used to protect crops in the field as well as during post-harvest storage to minimize crop damage. Crop plants are attacked by a variety of pests which include soil insects, cut worms, leaf rollers, aphids etc., and pesticides are mostly used to control these pests (^{Goh et al., 2011}). Nowadays, there are other alternatives to control these insect pests which include the use of bio-pesticides and development of pest resistant transgenic varieties. However, the use of chemical pesticides is still the best and most widely applied strategy to protect crops from pests and results in high yield production of crops. It has been reported that approximately two million tonnes of pesticides are consumed annually throughout the world (^{De et al., 2014}). Global pesticide consumption includes 47.55% of herbicides, 29.5% of insecticides, 17.5% of fungicides and 5.5% of other pesticides.

Transpiration pull helps in the absorption of water soluble pesticides and their entry into the plant system. Volatile pesticides indirectly come into the atmosphere via leaves through stomata during transpiration. Plants absorb pesticides via roots, leaf surface or roots. A number of factors are involved in pesticide uptake and its metabolism in the plant system which include external environmental factors (temperature, humidity and precipitation) and physiochemical properties of soil and pesticides (^{Finlayson and MacCarthy, 1973}). Uptake of pesticides via the root system and their metabolism in the plant system is affected by factors such as mode of application, amount of pesticide, physiochemical and biochemical properties of pesticides and their reaction with soil and stage of plant development (^{Führ, 1991}). Absorption of pesticides by plants is also determined by their degree of water solubility. Pesticide uptake takes place either by active absorption via the root system, or by passive absorption. Absorbed pesticides are either metabolized by the plant system or accumulate in plants, causing bio-magnification in the ecosystem (^{Mwevura, 2000}).

Pesticide application also causes toxicity to plants, which can be seen in the form of necrosis, chlorosis, stunting, burns and twisting of leaves (^{Sharma et al., 2018a}). The excessive use of pesticides is one of the major causes of reduction of the diversity of structural vegetation (^{Donald, 2004}). Sensitive or stressed plants may be extra vulnerable to phytotoxicity. Toxicity depends upon many factors such as use of pesticides, rate of application, spraying technique, climate conditions, organization of flora, humidity and properties of soil such as moisture, temperature, pH, texture and microbial activity. It has been found that pesticide application negatively affects plant growth and development (Sharma et al., 2015, ^2016a, ^{Shahzad et al., 2018}). Pesticide application causes oxidative stress to plants as a result of the generation of reactive oxygen species (ROS) ^{Sharma et al., 2018b}). This oxidative stress results in degradation of chlorophyll pigments and proteins and it ultimately causes a reduction in the photosynthetic efficiency of plants (^{Xia et al., 2006}; Sharma et al., 2015). To cope up with oxidative stress, the antioxidative defense system of plants is activated, which involves enzymatic and non-enzymatic antioxidants (^{Xia et al., 2009}; Sharma et al., 2015; 2016b,c,^d). Activation of the antioxidative defense system aids with ROS scavenging and reduces the oxidative stress in plants caused by pesticide toxicity (Sharma et al., 2015, ^2017a,^b). The present review has been planned to give a detailed overview of various physiological changes in plants subjected to pesticide treatment. Physiological responses of plants to pesticide application have been summarized in tabulated form.

PHYSIOLOGICAL RESPONSES OF PLANTS TO PESTICIDE TOXICITY

Table 1, 2 and 3 show oxidative stress markers, enzymatic antioxidants and non-enzymatic antioxidants, respectively, whereas supplementary Tables 1, 2 and 3 give a detailed overview for growth parameters, pigment system, photosynthetic parameters and protein content, respectively, in plants against pesticide toxicity.

It has been concluded that pesticide application causes oxidative stress in plants by production of reactive oxygen species. This ultimately leads to retarded growth and photosynthetic efficiency of plants. Plants try to ameliorate pesticide toxicity by activation of their internal antioxidative defense system which includes antioxidative enzymes and non-enzymatic antioxidants.

Table 1 Effect of pesticides on oxidative stress markers in plants

Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Effect of pesticide on oxidative stress markers		Reference
Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Parameter	Effect
Amide	Acetochlor	Vitis vinifera L. × Vitis labrusca L.	Soil	22460 g a.i. ha^-1	30 d	Leaves (upper node)	O₂·^- MDA	Increase Increase	Tan et al. (2012)
	Napropamide	Brassica napus L.	Seedling	8 mg L^-1	5 d	Leaves	TBARS	Increase	Cui et al. (2010)
	Napropamide	Brassica napus L.	Seedling	8 mg L^-1	5 d	Root	TBARS	Increase	Cui et al. (2010)
	Rac-metolachlor	Oryza sativa L.	Culture solution	6.2 µM L^-1	5 d	Root	MDA	Increase	Liu et al. (2012)
	Rac-metolachlor	Zea mays L.	Culture solution	74.4 µM L^-1	5 d	Root	MDA	Increase
	S-metolachlor	O. sativa L.	Culture solution	6.2 µM L^-1	5 d	Root	MDA	Increase
	S-metolachlor	Z. mays L.	Culture solution	74.4 µM L^-1	5 d	Root	MDA	Increase
Cyclohexene oxime	Clethodim	Z. mays L.	Soil	200 ppm	21 d	Leaves	H₂O₂ MDA	Increase Increase	Radwan (2012)
Dinitroaniline	Pendimethalin	Vigna mungo L. var. Shekhar	Soil	10 ppm	15 d	Leaves	MDA	Decrease	Singh et al. (2012)
Diphenyl ether	Fluoroglycofen	V. vinifera L. × V. labrusca L.	Soil	375 g a.i. ha^-1	30 d	Leaves (upper node)	O₂·^- MDA	Increase Increase	Tan et al. (2012)
Imidazolinone	Imazapic	Nicotiana tabacum L.	Spray	0.12 mM	9 d	Leaves	MDA	Increase	Kaya and Doganlar (2016)
	R (-)-imazethapyr	Arabidopsis thaliana L.	Culture solution	2.5 µg L^-1	28 d	Plantlets	O₂·^- H₂O₂ MDA	Increase Increase Increase	Qian et al. (2011)
	S (+)-imazethapyr	A. thaliana L.	Culture solution	2.5 µg L^-1	28 d	Plantlets	O₂·^- H₂O₂ MDA	Increase Increase No change	Qian et al. (2011)
Neonicotinoid	Imidacloprid	Oryza sativa L.	Sand	0.015%	12 d	Seedlings	O₂·^- H₂O₂ MDA	Increase Increase Increase	Sharma et al. (2015)
Neonicotinoid	Imidacloprid	Oryza sativa L.	Sand	0.02%	12 d	Seedlings	MDA	Increase	Sharma et al. (2013)
Organophosphorus	Chlorpyrifos	O. sativa L.	Sand	0.04%	12 d	Seedlings	O₂·^- H₂O₂ MDA	Increase Increase Increase	Sharma et al. (2015)
		O. sativa L.	Sand	0.06%	12 d	Seedlings	MDA	Increase	Sharma et al. (2012)
		Vigna radiata L.	Spray	15 mM	10 d	Leaves	TBARS	Increase	Parween et al. (2012)
	Dimethoate	V. radiata L.	Culture soln.	150 ppm	4 d	Leaves	O₂·^- H₂O₂ MDA OH^-	Increase Increase Increase Increase	Singh et al. (2014)
	Glyphosate	Glycine max L. var. DM48	Spray	0.94 %	24 h	Leaves	MDA	Increase	Moldes et al. (2008)
		Glycine max L. var. DM48	Spray	0.94 %	24 h	Root	MDA	Increase
		G. max L. var. DM4800RG	Spray	0.94 %	24 h	Leaves	MDA	Increase
		G. max L. var. DM4800RG	Spray	0.94 %	24 h	Root	MDA	Decrease
		G. max L. var. MSOY7501	Spray	0.94 %	24 h	Leaves	MDA	Increase
		G. max L. var. MSOY7501	Spray	0.94 %	24 h	Root	MDA	Increase
		G. max L. var. MSOY7575RR	Spray	0.94 %	24 h	Leaves	MDA	Increase
		G. max L. var. MSOY7575RR	Spray	0.94 %	24 h	Root	MDA	Increase
		Z. mays L. var. Kneza-640	Spray	10 mM	10 d	Leaves	H₂O₂ MDA Electrolyte leakage	Increase Increase Increase	Sergiev et al. (2006)
Phenoxy	Clodinafop-propargyl	Secale cereale L.	Spray	800 µg L^-1	7 d	Leaves	O₂·^-	Increase	Lukatkin et al. 2013
		Triticum aestivum L.	Spray	800 µg L^-1	7 d	Leaves	O₂·^-	Increase
		Z. mays L.	Spray	800 µg L^-1	7 d	Leaves	O₂·^-	Increase
	Fluazifop-P-butyl	Acanthospermum hispidum DC.	Shoot immersing	10 µM	24 h	Leaves	MDA	Increase	Luo et al. (2004)
	Fluazifop-P-butyl	Avena sativa L.	Shoot immersing	10 µM	24 h	Leaves	MDA	Increase	Luo et al. (2004)
	Fusilade	Arachis hypogaea L.	Spray	60 ppm	14 d	Leaves	H₂O₂ MDA	Increase Increase	Fayez et al. (2014)
	Quizalofop-p-ethyl	Helianthus. annuus L.	Spray	0.8 mM	15 d	Leaves	MDA	Increase	Bayram et al. (2015)
	R-diclofop-methyl	A. thaliana L.	Culture medium	1 mg L^-1	28 d	Plantlets	MDA	Increase	Zhang et al. (2012)
	S-diclofop-methyl	A. thaliana L.	Culture medium	1 mg L^-1	28 d	Plantlets	MDA	Increase	Zhang et al. (2012)
Pyrethroid	Deltamethrin	G. max L. Merr.	Spray	0.20 %	10 d	Leaves	MDA	Increase	Bashir et al. (2007)
Pyridine	Fluroxypyr	O. sativa L.	Culture soln.	0.8 mg L^-1	6 d	Leaves	O·̄₂ H₂O₂ MDA	Increase Increase Increase	Wu et al. (2010)
Quaternary ammonium	Paraquat	Papaver somniferum L.	Spray	0.48 %	24 h	Leaves	MDA Electrolyte leakage	Increase Increase	Zhao et al. (2010)
Triazine	Atrazine	Acorus calamus L.	Culture soln.	8 mg L^-1	15 d	Leaves	MDA	Increase	Wang et al. (2015)
		Lythrum salicaria L.	Culture soln.	8 mg L^-1	15 d	Leaves	MDA	Increase	Wang et al. (2015)
		O. sativa L.	Hoagland medium	0.4 mg L^-1	6 d	Leaves	O₂·^- H₂O₂ TBARS	Increase Increase Increase	Zhang et al. (2014)
		Pennisetum americanum L.	Soil	10 mg kg^-1	38 d	Shoot	MDA	Increase	Jiang et al. (2016)
		Pennisetum americanum L.	Soil	10 mg kg^-1	38 d	Root	MDA	Increase	Jiang et al. (2016)
		Scirpus tabernaemontani P.	Culture soln.	8 mg L^-1	15 d	Leaves	MDA	Increase	Wang et al. (2015)
		Vicia faba L.	Spray	1.79 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Hassan and Alla (2005)
		Z. mays L.	Spray	1.79 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Hassan and Alla (2005)
			Spray	78 mM	5 d	Leaves	MDA	Increase	Akbulut and Yigit (2010)
			Hoagland medium	10 mg L^-1	3 d	Shoot	MDA	No change	Li et al. (2012)
			Hoagland medium	10 mg L^-1	3 d	Root	MDA	Increase	Li et al. (2012)
		Z. mays L. Hybrid 351	Soil	1.79 kg ha^-1	8 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Alla and Hassan (2006)
		Z. mays L. Giza 2	Soil	1.79 kg ha^-1	8 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Alla and Hassan (2006)
	Prometryne	T. aestivum L.	Soil	12 mg kg^-1	10 d	Leaves	TBARS	Increase	Jiang and Yang (2009)
	Prometryne	T. aestivum L.	Soil	12 mg kg^-1	10 d	Root	TBARS	Increase	Jiang and Yang (2009)
Urea	Chlorotoluron	T. aestivum L.	Soil	25 mg kg^-1	10 d	Leaves	O₂·^- H₂O₂ TBARS	Increase Increase Increase	Song et al. (2007)
	Chlorimuron-ethyl	T. aestivum L.	Soil	300 µg kg^-1	24 h	Leaves	MDA	Increase	Wang and Zhou (2006)
	Chlorimuron-ethyl	T. aestivum L.	Soil	300 µg kg^-1	24 h	Root	MDA	Increase	Wang and Zhou (2006)
	Fluometuron	V. faba L.	Spray	2.98 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Hassan and Alla (2005)
	Fluometuron	Z. mays L.	Spray	2.98 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Hassan and Alla (2005)
	Granstar	Avena fatua L.	Spray	300 µg L^-1	3 d	Leaves	O₂·^- MDA	Increase Increase	Gar’kova et al. (2011)
		Secale cereale L.	Spray	300 µg L^-1	3 d	Leaves	O₂·^- MDA	Increase Increase
		Secale cereale L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	O₂·^-	Increase
		T. aestivum L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	O₂·^-	Increase
		T. aestivum L.	Spray	300 µg L^-1	3 d	Leaves	O₂·^- MDA	Increase Increase
		Z. mays L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	O₂·^-	Increase
		Z. mays L.	Spray	300 µg L^-1	3 d	Leaves	O₂·^- MDA	Increase Increase
	Isoproturon	P. sativum L.	Sand	10 mM	15 d	Leaves	H₂O₂ MDA Electrolyte leakage	Increase Increase Increase	Singh et al. (2016)
		T. aestivum L.	Soil	2.5 L ha^-1	15 d	Shoot	H₂O₂ MDA	Increase Increase	Alla and Hassan (2014)
				4 mg kg^-1	10 d	Shoot	O₂·^- H₂O₂ TBARS	Increase Increase Increase	Liang et al. (2012)
						Root	TBARS	Increase
						Leaves	H₂O₂	Increase
				10 mg kg^-1	10 d	Leaves	TBARS	Increase	Yin et al. (2008)
				10 mg kg^-1	10 d	Root	TBARS	No change	Yin et al. (2008)
	Rimsulfuron	V. faba L.	Spray	0.015 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase Increase	Hassan and Alla (2005)
	Rimsulfuron	Z. mays L.	Spray	0.015 kg a.i. ha^-1	12 d	Shoot	H₂O₂ MDA C=O	Increase Increase No change	Hassan and Alla (2005)
Unclassified	Dichlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Root	H₂O₂	Increase	San Miguel et al. (2012)
	Dichlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Leaves	H₂O₂	Decrease	San Miguel et al. (2012)
	Flurochloridone	H. annuus L.	Spray	11 mM	15 d	Leaves	MDA	Increase	Kaya and Yigit (2014)
	Monochlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Root	H₂O₂	Increase	San Miguel et al. (2012)
	Monochlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Leaves	H₂O₂	No change
	Trichlorobenzene	Z. mays L.	Hoagland medium	40 mg L^-1	7 d	Root	H₂O₂	Increase
	Trichlorobenzene	Z. mays L.	Hoagland medium	40 mg L^-1	7 d	Leaves	H₂O₂	Increase

Table 2 Effect of pesticides on enzymatic antioxidants in plants

Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Effect of pesticide on enzymatic antioxidants		Reference
Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Parameter	Effect
Amide	Acetochlor	Vitis vinifera L. × Vitis labrusca L.	Soil	22460 g a.i.ha^-1	30 d	Leaves (upper node)	APOX CAT POD SOD	Decrease Decrease Decrease Decrease	Tan et al. (2012)
	Alachlor	Lactuca sativa L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	Increase Increase Increase	Stajner et al. (2003)
		Phaseolus vulgaris L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	Increase Increase Increase
		Pisum sativum L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	Increase Increase Increase
	Fomesafen	Glycine max L. Merr.	Spray	1000 g ha^-1	2 d	Leaves	GST	Increase	Andrews et al. (2005)
	Metolachlor	L. sativa L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	No change Decrease Increase	Stajner et al. (2003)
		P. vulgaris L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	Increase Increase Increase
		P. sativum L.	Hoagland medium	2 µM	24 d	Leaves	CAT POD SOD	Decrease Increase Increase
	Metosulam	Vicia faba L.	Seedling’s root immersing	10^-4 %	24 h	Leaves	APOX CAT POD	Increase Increase Decrease	Badr et al. (2013)
	Napropamide	Brassica napus L.	Seedling	8 mg L^-1	5 d	Leaves	APOX CAT GST POD SOD	Increase Increase Increase Increase Increase	Cui et al. (2010)
	Rac-metolachlor	Oryza. sativa L.	Culture solution	6.2 µM L^-1	5 d	Root	CAT POD	Decrease Decrease	Liu et al. (2012)
	Rac-metolachlor	Zea mays L.	Culture solution	74.4 µM L^-1	5 d	Root	CAT POD SOD	Decrease Decrease Decrease
	S-metolachlor	O. sativa L.	Culture solution	6.2 µM L^-1	5 d	Root	CAT POD	Decrease Decrease
	S-metolachlor	Z. mays L.	Culture solution	74.4 µM L^-1	5 d	Root	CAT POD SOD	Decrease Decrease Decrease
Cyclohexene oxime	Clethodim	Z. mays L.	Soil	200 ppm	21 d	Leaves	APOX CAT POD SOD	Increase Decrease Increase Decrease	Radwan (2012)
Diphenyl ether	Fluoroglycofen	V. vinifera L. × V. labrusca L.	Soil	375 g ai ha^-1	30 d	Leaves (upper node)	APOX CAT POD SOD	Decrease Decrease Decrease Decrease	Tan et al. (2012)
Diphenyl ether	Oxyfluorfen	G. max L. Merr.	Spray	2500 g ha^-1	2 d	Leaves	GST	Increase	Andrews et al. (2005)
Imidazolinone	Imazapic	Nicotiana tabacum L.	Spray	0.12 mM	9 d	Leaves	APOX CAT GR GST	Increase Increase Increase Increase	Kaya and Doganlar (2016)
	R (-)-imazethapyr	Arabidopsis thaliana L.	Culture solution	2.5 µg L^-1	28 d	Plantlets	APOX CAT GPOX SOD	Decrease Decrease Increase Decrease	Qian et al. (2011)
	S (+)-imazethapyr	A. thaliana L.	Culture solution	2.5 µg L^-1	28 d	Plantlets	APOX CAT GPOX SOD	Increase Decrease Increase Decrease	Qian et al. (2011)
Neonicotinoid	Imidacloprid	Brassica juncea L.	Soil	300 mg kg^-1	65 d	Leaves	GR GST POD	Increase Increase Increase	Sharma et al. (2016b)
		Brassica juncea L.	Soil	300 mg kg^-1	80 d	Green pods	APOX GPOX GR GST POD	Increase Increase Increase Increase Increase	Sharma et al. (2017c)
		O. sativa L.	Sand	0.01%	12 d	Seedlings	APOX CAT DHAR GR MDHAR POD SOD	Increase Decrease Increase Increase Increase Decrease Increase	Sharma et al. (2013)
		O. sativa L.	Sand	0.015%	12 d	Seedlings	APOX CAT DHAR GR MDHAR POD SOD	Increase Increase Decrease Increase Increase Decrease Increase	Sharma et al. (2015)
Organochlorine	DDT	G. max L.	Soil	63.5 ng g^-1	60 d	Leaves Root	GST GST	Decrease Increase	Mitton et al. (2016)
Organochlorine	DDT	Medicago sativa L.	Soil	63.5 ng g^-1	60 d	Leaves Root	GST GST	Increase Increase	Mitton et al. (2016)
Organophosphorus	Chlorpyrifos	Vigna radiata L.	Spray	15 mM	10 d	Leaves	APOX CAT GR SOD	Increase Decrease Increase Increase	Parween et al. (2012)
	Dimethoate	V. radiata L.	Culture soln.	30 ppm	4 d	Leaves	CAT DHAR GR SOD	Increase Increase Increase Increase	Singh et al. (2014)
	Dimethoate	V. radiata L.	Culture soln.	150 ppm	4 d	Leaves	CAT DHAR GR SOD	Decrease Decrease Decrease Increase	Singh et al. (2014)
	Glyphosate	G. max L. var. DM48	Spray	0.94 %	24 h	Leaves	APOX CAT POD	Increase Increase Increase	Moldes et al. (2008)
		G. max L. var. DM48	Spray	0.94 %	24 h	Roots	APOX CAT POD	Increase Increase Decrease
		G. max L. var. DM4800RG	Spray	0.94 %	24 h	Leaves	APOX CAT POD	Increase Decrease Increase
		G. max L. var. DM4800RG	Spray	0.94 %	24 h	Root	APOX CAT POD	Increase Decrease Increase
		G. max L. var. MSOY7501	Spray	0.94 %	24 h	Leaves	APOX CAT POD	Increase Decrease Increase
		G. max L. var. MSOY7501	Spray	0.94 %	24 h	Root	APOX CAT POD	Increase Decrease Increase
		G. max L. var. MSOY7575RR	Spray	0.94 %	24 h	Leaves	APOX CAT POD	Increase Increase Increase
		G. max L. var. MSOY7575RR	Spray	0.94 %	24 h	Roots	APOX CAT POD	Increase Increase Increase
		V. radiate L. var. PDM11	Seed	10 mM	12 d	Root	CAT GST POD	Increase Increase Increase	Basantani et al. (2011)
		V. radiate L. var. PDM54	Seed	10 mM	12 d	Root	CAT POD GST	Increase Increase Increase	Basantani et al. (2011)
		Z. mays L. var. Kneza-640	Spray	10 mM	10 d	Leaves	CAT GST POD	Increase Increase Increase	Sergiev et al. (2006)
Phenoxy	Clodinafop-propargyl	Secale cereale L.	Spray	800 µg L^-1	7 d	Leaves	CAT APOX	Increase Increase	Lukatkin et al. 2013
		Triticum aestivum L.	Spray	800 µg L^-1	7 d	Leaves	CAT APOX	Increase Increase
		Z. mays L.	Spray	800 µg L^-1	7 d	Leaves	CAT APOX	Increase Increase
	Fenoxaprop-p-ethyl	T. aestivum L.	Spray	250 g ha^-1	15 d	Leaves	CAT POD	Increase Increase	Sing et al. (2013)
	Fusilade	Arachis hypogaea L.	Spray	60 ppm	14 d	Leaves	APOX CAT POD SOD	Increase Decrease Increase Decrease	Fayez et al. (2014)
	Haloxyfop-ethoxyethyl	Triticum vulgare L.	Drop on leaf	50 µM	12 h	Leaves	APOX CAT POD SOD	Increase Increase Increase Decrease	Janicka et al. (2008)
	Quizalofop-p-ethyl	Helianthus annuus L.	Spray	0.8 mM	15 d	Leaves	APOX POD	Increase Increase	Bayram et al. (2015)
	R-diclofop-methyl	A. thaliana L.	Culture medium	1 mg L^-1	28 d	Plantlets	CAT POD SOD	Decrease Increase Increase	Zhang et al. (2012)
	S-diclofop-methyl	A. thaliana L.	Culture medium	1 mg L^-1	28 d	Plantlets	CAT POD SOD	Increase Increase Decrease	Zhang et al. (2012)
Pyrethroid	Deltamethrin	G. max L. Merr.	Spray	0.20 %	10 d	Leaves	APOX CAT GR SOD	Increase Decrease Increase Increase	Bashir et al. (2007)
Pyridine	Fluroxypyr	O. sativa L.	Culture soln.	0.8 mg L^-1	6 d	Leaves	APOX CAT POD SOD	No change Decrease Increase Increase	Wu et al. (2010)
Quaternary ammonium	Paraquat	Papaver somniferum L.	Spray	0.48 %	24 h	Leaves	CAT POD SOD	Increase Decrease Increase	Zhao et al. (2010)
Triazine	Atrazine	Acorus calamus L.	Culture soln.	8 mg L^-1	15 d	Leaves	POD	Increase	Wang et al. (2015)
		Lythrum salicaria L.	Culture soln.	8 mg L^-1	15 d	Leaves	POD	Decrease	Wang et al. (2015)
		O. sativa L.	Hoagland medium	0.4 mg L^-1	6 d	Leaves	APOX CAT GR GST POD SOD	Increase Increase Increase Increase Increase Increase	Zhang et al. (2014)
		O. sativa L.	Hoagland medium	0.4 mg L^-1	6 d	Root	APOX CAT GR GST POD SOD	Increase Increase Increase Decrease Increase Increase	Zhang et al. (2014)
		Pennisetum americanum L.	Soil	10 mg kg^-1	38 d	Shoot	APOX CAT POD SOD	Increase Increase Increase Increase	Jiang et al. (2016)
		Pennisetum americanum L.	Soil	10 mg kg^-1	38 d	Root	APOX CAT POD SOD	Increase Increase Increase Increase	Jiang et al. (2016)
		Scirpus tabernaemontani P.	Culture soln.	8 mg L^-1	15 d	Leaves	POD	Decrease	Wang et al. (2015)
		V. faba L.	Spray	1.79 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Decrease Decrease Decrease Decrease	Hassan and Alla (2005)
		Z. mays L.	Spray	1.79 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Decrease Decrease Decrease Increase	Hassan and Alla (2005)
			Spray	78 mM	5 d	Leaves	APOX POD	Increase Increase	Akbulut and Yigit (2010)
			Hoagland medium	10 mg L^-1	3 d	Shoot	CAT POD SOD	Increase Increase Increase	Li et al. (2012)
			Hoagland medium	10 mg L^-1	3 d	Root	CAT POD SOD	Increase Increase Increase	Li et al. (2012)
		Z. mays L. Hybrid 351	Soil	1.79 kg ha^-1	8 d	Shoot	APOX CAT POD GST SOD	Increase Decrease Decrease Increase Increase	Alla and Hassan (2006)
		Z. mays L. Giza 2	Soil	1.79 kg ha^-1	8 d	Shoot	APOX CAT POD GST SOD	Decrease Decrease Decrease Decrease Decrease	Alla and Hassan (2006)
	Prometryn	T. aestivum L.	Soil	12 mg kg^-1	10 d	Leaves	APOX CAT GST POD SOD	Increase Increase Increase Increase Increase	Jiang and Yang (2009)
	Prometryn	T. aestivum L.	Soil	12 mg kg^-1	10 d	Root	APOX CAT GST POD SOD	Increase Increase Increase Increase Increase	Jiang and Yang (2009)
Urea	Chlorotoluron	T. aestivum L.	Soil	25 mg kg^-1	10 d	Root	APOX CAT POD SOD	Increase Decrease Increase Increase	Song et al. (2007)
	Chlorimuron-ethyl	T. aestivum L.	Soil	300 µg kg^-1	24 h	Leaves	POD	Increase	Wang and Zhou (2006)
	Chlorimuron-ethyl	T. aestivum L.	Soil	300 µg kg^-1	24 h	Root	POD	Increase	Wang and Zhou (2006)
	Fluometuron	Z. mays L.	Spray	2.98 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Decrease Decrease Decrease Decrease	Hassan and Alla (2005)
	Fluometuron	V. faba L.	Spray	2.98 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Decrease Decrease Decrease Decrease	Hassan and Alla (2005)
	Granstar	S. cereale L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	APOX CAT SOD	Increase Increase Increase	Gar’kova et al. (2011)
		T. aestivum L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	APOX CAT SOD	Increase Increase Increase
		Z. mays L.	Leaf disk immersing	300 µg L^-1	3 h	Leaves	APOX CAT SOD	Increase Increase Increase
	Isoproturon	P. sativum L.	Sand	10 mM	15 d	Leaves	APOX CAT GPOX SOD	Increase Increase Decrease Increase	Singh et al. (2016)
		T. aestivum L. .	Soil	2.5 L ha^-1	15 d	Shoot	APOX CAT SOD	Decrease Decrease Decrease	Alla and Hassan, (2014)
				4 mg kg^-1	10 d	Shoot	APOX CAT GR GST POD SOD	Increase Decrease Increase Increase Increase Increase	Liang et al. (2012)
				4 mg kg^-1	10 d	Root	APOX CAT GR GST POD SOD	Increase Decrease Increase Increase Increase Increase	Liang et al. (2012)
				10 mg kg^-1	10 d	Leaves	APOX CAT GST POD SOD	Increase Decrease Increase Increase Increase	Yin et al. (2008)
				10 mg kg^-1	10 d	Root	APOX CAT GST POD SOD	Increase Increase Increase Increase Increase	Yin et al. (2008)
			Spray	1 kg ha^-1	15 d	Leaves	CAT POD	Increase Increase	Sing et al. (2013)
	Rimsulfuron	V. faba L.	Spray	0.015 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Increase Increase Increase Increase	Hassan and Alla (2005)
	Rimsulfuron	Z. mays L.	Spray	0.015 kg a.i. ha^-1	12 d	Shoot	APOX CAT POD SOD	Increase Increase Increase Increase	Hassan and Alla (2005)
	Sulfosulfuron	T. aestivum L.	Spray	800 g ha^-1	15 d	Leaves	CAT POD	Increase Increase	Sing et al. (2013)
Unclassified	Dichlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Root	GR POD	Increase Decrease	San Miguel et al. (2012)
	Dichlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Leaves	GR POD	Decrease Decrease	San Miguel et al. (2012)
	Flurochloridone	H. annuus L.	Spray	11 mM	15 d	Leaves	APOX CAT GR GST SOD	Decrease Decrease Increase Increase Increase	Kaya and Yigit (2014)
	Flurochloridone	V. sativa L.	Spray	32 mM	15 d	Leaves	GR GST	Increase Increase	Kaya and Yigit (2012)
	Monochlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Roots	GR POD	Increase Increase	San Miguel et al. (2012)
	Monochlorobenzene	Z. mays L.	Hoagland medium	80 mg L^-1	7 d	Leaves	GR POD	Decrease Increase
	Trichlorobenzene	Z. mays L.	Hoagland medium	40 mg L^-1	7 d	Root	GR POD	Increase No change
	Trichlorobenzene	Z. mays L.	Hoagland medium	40 mg L^-1	7 d	Leaves	GR POD	Decrease No change

Table 3 Effect of pesticides on non-enzymatic antioxidants in plants

Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Effect of pesticide on non-enzymatic antioxidants		Reference
Type of pesticide	Pesticide name	Plant name	Mode of application	Concentration of pesticide	Time after treatment	Plant part analyzed	Parameter	Effect	Reference
Amide	Fomesafen	Glycine max L. Merr.	Spray	1000 g ha^-1	2 d	Leaves	HGSH	Increase	Andrews et al. (2005)
	Metosulam	Vicia faba L.	Seedling’s root immersing	10^-4 %	24 h	Leaves	Proline	Increase	Badr et al. (2013)
						Stems	Proline	Increase
						Root	Proline	Increase
Cyclohexene oxime	Clethodim	Zea mays L.	Soil	200 ppm	21 d	Leaves	Total phenolics	Increase	Radwan (2012)
Diamide	Chlorantraniliprole	Z. mays L.	Seed	0.5 ppm	7 d	Leaves	Proline	Increase	Kilic et al. (2015)
Dinitroaniline	Pendimethalin	Foeniculum vulgare L.	Soil	8.5 mg L^-1	84 d	Leaves	Total phenolics	Increase	El-Awadi and Hassan et al. 2011
Diphenyl ether	Oxyfluorfen	G. max L. Merr.	Spray	2500 g ha^-1	2 d	Leaves	HGSH	Increase	Andrews et al. (2005)
Imidazolinone	Imazapic	Nicotiana tabacum L.	Spray	0.12 mM	9 d	Leaves	GSH	Increase	Kaya and Doganlar (2016)
Neonicotinoid	Imidacloprid	Brassica juncea L.	Soil	300 mg kg^-1	60 d	Leaves	Ascorbate GSH Tocopherol Polyphenols Total phenolics	Increase Increase Increase Increase Increase	Sharma et al. (2016c)
					65 d	Leaves	GSH	Increase	Sharma et al. (2016b)
					80 d	Green pods	GSH	Increase	Sharma et al. (2017c)
		Oryza sativa L.	Sand	0.02%	12 d	Seedling	Proline	Increase	Sharma et al. (2013)
		Oryza sativa L.	Sand	0.015%	12 d	Seedling	Proline	Increase	Sharma et al. (2015)
Organophosphorus	Chlorpyrifos	O. sativa L.	Sand	0.06%	12 d	Seedling	Proline	Increase	Sharma et al. (2012)
		O. sativa L.	Sand	0.04%	12 d	Seedling	Proline	Increase	Sharma et al. (2015)
		Vigna radiata L.	Spray	15 mM	10 d	Leaves	Proline Ascorbate GSH	Increase Decrease Increase	Parween et al. (2012)
	Dimethoate	V. radiata L.	Culture soln.	30 ppm	4 d	Leaves	GSH Ascorbate	Increase Increase	Singh et al. (2014)
	Dimethoate	V. radiata L.	Culture soln.	150 ppm	4 d	Leaves	GSH Ascorbate	Decrease Decrease	Singh et al. (2014)
	Glyphosate	Z. mays L. var. Kneza-640	Spray	10 mM	10 d	Leaves	Proline GSH	Increase Increase	Sergiev et al. (2006)
Phenoxy	Fluzifop-p-butyl	Arachis hypogaea L. var. Giza 5	Spray	0.156 g L^-1	14 d	Leaves	Proline	Increase	Fayez et al. (2011)
Phenoxy	Quizalofop-p-ethyl	Helianthus annuus L.	Spray	0.8 mM	15 d	Leaves	Total phenolics	Increase	Bayram et al. (2015)
Pyrethroid	Deltamethrin	G. max L. Merr.	Spray	0.20 %	10 d	Leaves	Proline Ascorbate GSH	Increase Increase Increase	Bashir et al. (2007)
Pyridine	Fluroxypyr	O. sativa L.	Culture soln.	0.8 mg L^-1	6 d	Leaves	Proline	Increase	Wu et al. (2010)
Triazine	Atrazine	Z. mays L. Hybrid 351	Soil	1.79 kg ha^-1	8 d	Shoot	GSH Ascorbate	Increase Increase	Alla and Hassan (2006)
Triazine	Atrazine	Z. mays L. Giza 2	Soil	1.79 kg ha^-1	8 d	Shoot	GSH Ascorbate	Decrease Decrease	Alla and Hassan (2006)
Urea	Chlorotoluron	Triticum aestivum L.	Soil	25 mg kg^-1	10 d	Leaves	Proline	Increase	Song et al. (2007)
	Diuron	G. max L. var. Clark	Soil	2 ppm	7 d	Leaves	Proline	Increase	Fayez (2000)
	Diuron	G. max L. var. Crawford	Soil	2 ppm	7 d	Leaves	Proline	Increase	Fayez (2000)
	Isoproturon	T. aestivum	Soil	2.5 L ha^-1	15 d	Shoot	GSH	Decrease	Alla and Hassan (2014)
Unclassified	Bentazon	A. hypogaea L. var. Giza 6	Spray	1.6 g L^-1	14 d	Leaves	Proline	Increase	Fayez et al. (2011)
Unclassified	Flurochloridone	Vicia sativa L.	Spray	32 mM	15d	Leaves	GSH	Increase	Kaya and Yigit (2012)

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Received: August 21, 2017; Accepted: September 18, 2017

* Corresponding author: <anketsharma@gmail.com>

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