Effect of lead (Pb) on antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens)

doi:10.1016/j.ecoenv.2016.12.020

Ecotoxicology and Environmental Safety

Volume 138, April 2017, Pages 71-77

https://doi.org/10.1016/j.ecoenv.2016.12.020 Get rights and content

Highlights

•
Moso bamboo roots tissue accumulated higher Pb content.
•
Antioxidative enzymes were effectively activated by Pb stress.
•
Photosynthetic pigment contents enhanced by Pb toxicity.
•
Moso bamboo could be suitable for remediation of low Pb contaminated soils.

Abstract

The antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens), which is a valuable remediation material with large biomass and rapid growth rate were studied in hydroponics and pot experiments. In hydroponics experiment, TBARS concentrations and SOD activities decreased with increase of Pb treatments. The activities of POD boost up with elevated Pb treatments, and reached peak level with application of 400 μM Pb. Proline concentrations reduced with application of 20 μM Pb and then enhanced consistently with application of 100 and 400 μM Pb. The biomass of Moso bamboo improved with increase of Pb treatments upto 400 mg kg⁻¹, and then decreased with application of each additional increment of Pb in pot experiment. Application of 800 mg kg⁻¹ Pb showed significant increase of photosynthetic pigments, however, non significant variation was observed for other treatments. The Pb concentration in roots, stems and leaves attained 523 mg kg⁻¹, 303 mg kg⁻¹ and 222 mg kg⁻¹ respectively with application of 1600 mg kg⁻¹ Pb compared with control. Analysis of TEM-EDX revealed that Pb in cell was mostly concentrated in cytoplasm then in cell wall and followed by vacuole. It is concluded that Moso bamboo may be potential remediation species for phytoremediation in low Pb contaminated soils.

Introduction

The quality of soil environment reported by Chinese government revealed more than 16.1% contaminated soils in China which include 1.5% lead contaminated soils (Chen et al., 2016). Major sources of lead (Pb) in soils are mining activities, industrial emissions and pesticide application. Pb in soil has not only affected yield and quality of crops but it has also affected human health through food chain and mental development of children (Harguinteguy et al., 2015, Mazumdar and Das, 2015, Sosa et al., 2016). Pb pollution in soils has become one of the major environmental problems of the world (Liu et al., 2015, Mani et al., 2015b).

Pb is not an essential element for plants, it will harm plants due to high concentration level. Pb will destroy cell structure, metabolism and chlorosis of leaves (Elkhatib et al., 2014, Hu et al., 2012). Excessive Pb induces accumulation of reactive oxygen species (ROS) and increase the level of lipid peroxidation (Gupta et al., 2013, Tauqeer et al., 2015). However, under heavy metal exposure, antioxidant enzyme system, including superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT), will effectively eliminate the plant excessive reactive oxygen free radicals to alleviate toxicity of heavy metal (Pb) in plants (Chen et al., 2015b, Gill and Tuteja, 2010).

Phytoremediation is a kind of green environmental, and economic remediation technology (Ahmadpour et al., 2012, Tangahu et al., 2011). The remediation species are mostly grown around the area of heavy metals pollution, and characteristics of these plants are mainly accumulation of heavy metals with high tolerant ability (Kamran et al., 2014, Salazar and Pignata, 2014). Several plants can grow in heavy metal contaminated soils because they use avoidance strategy, limiting heavy metal uptake by plant, e.g. by chelating metal ions in rhizosphere or binding in mycorrhizal fungi (Meier et al., 2012, Rajkumar et al., 2012). Growth of Moso bamboo (Phyllostachys pubescens (Pradelle) Mazel ex J.Houz.) was observed in old Pb/Zn mine area including surrounding Sedum alfredii H, Violaye doensis M, Juncus eflasus L etc. (Zhang et al., 2006), which has additional advantages such as quick growth, and its biomass production could reach 82 t hm⁻² of dry weight compared to other plants (Chen, 1998, Song et al., 2013).

The purpose of this study was to evaluate relationship between activity of antioxidant enzymes and Pb toxicity on growth and chlorophyll concentrations of Moso bamboo. The transmission electron microscopy-energy dispersive X-ray detector (TEM-EDX) technology was employed to study organs of Moso bamboo cell accumulating Pb which will provide theoretical basis for further studies on mechanism of Pb toxicity in plants.

Section snippets

Hydroponics experiment

Plants were grown under glasshouse environment with natural light, day/night temperature of 25/30 °C, and day/night humidity of 70/90%. Seeds of Phyllostachys pubescens collected from Guilin of Guangxi Province, China were sown in special nutritional substrates containing perlite and vermiculite (3:1 v/v), moistened with distilled water. The nutrients solution was applied until seedlings had two leaves pairs. The composition of nutrients solution was as follows (mg L⁻¹) (Chen et al., 2015a): 57.1

Effects of Pb on antioxidation system of leaves and Pb concentration of plants in hydroponics

The Pb was mostly concentrated in roots of Moso bamboo grown in hydroponics experiment (Fig. 1). The Pb concentration in Moso bamboo was in sequence of roots >leaves>stems with application of 20–100 μM Pb. Application of 400 μM Pb revealed Pb concentration sequence of roots >stems >leaves. Pb concentration in roots, stems and leaves has reached 1409 mg kg⁻¹, 238 mg kg⁻¹ and 179 mg kg⁻¹ with application of 400 μM Pb compared with control.

The concentrations of TBARS and activities of SOD in leaves of Moso

Discussions

The reactive oxygen species were produced due to oxidative stress caused by variety of harmful effects in plant cells including lipid peroxidation when exposed to Pb (Mihailovic et al., 2014). TBARS concentrations was produced in plant tissues under stress caused by oxidative stress lipid over oxidation of the final product, and level of concentrations reflects plant victimization (Hu et al., 2015). The change of TBARS concentrations is often used to show how an organism can resist pressure (

Conclusions

All considered parameters suggested that Moso bamboo can tolerate stress of 1600 mg kg⁻¹ of Pb. Moso bamboo has relatively strong absorption capacity for Pb. Our results showed improved POD activity with increased application of Pb. However, TBARS concentrations and SOD activity decreased with the increase of Pb. TEM-EDX analysis revealed, Pb accumulation mainly in cytoplasm and cell wall for reduced toxicity. Our results provided helpful reference for phytoremediation of Pb contaminated soils by

Acknowledgement

The study was financially supported through a grant from the Natural Science Foundation of China (31670617) and key research and development project of Science Technology Department of Zhejiang Province (2015C03G 4010004).

References (46)

Alia et al.
Proline accumulation under heavy metal stress
J. Plant Physiol.
(1991)
J. Chen
Organic acid compounds in root exudation of Moso Bamboo ( Phyllostachys pubescens) and its bioactivity as affected by heavy metals
Environ. Sci. Pollut. Res.
(2016)
M. Chen
Bioaccumulation and tolerance characteristics of a submerged plant (Ceratophyllum demersum L.) exposed to toxic metal lead
Ecotoxicol. Environ. Saf.
(2015)
S.S. Gill et al.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
Plant Physiol. Biochem.
(2010)
C.A. Harguinteguy
Nickel, lead and zinc accumulation and performance in relation to their use in phytoremediation of macrophytes Myriophyllum aquaticum and Egeria densa
Ecol. Eng.
(2015)
E. Islam
Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi
J. Hazard. Mater.
(2007)
E. Islam
Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi
J. Hazard. Mater.
(2008)
S. Malar
Effect of lead on phytotoxicity, growth, biochemical alterations and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation
Ecotoxicol. Environ. Saf.
(2014)
D. Mani
Integrated micro-biochemical approach for phytoremediation of cadmium and zinc contaminated soils
Ecotoxicol. Environ. Saf.
(2015)
R. Mittler
Reactive oxygen gene network of plants
Trends Plant Sci.
(2004)

M. Rajkumar

Perspectives of plant-associated microbes in heavy metal phytoremediation

Biotechnol. Adv.

(2012)

M.J. Salazar et al.

Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation

J. Geochem. Explor.

(2014)

P. Ahmadpour

Phytoremediation of heavy metals: a green technology

Afr. J. Biotechnol.

(2012)

K. Bauddh et al.

Assessment of metal uptake capacity of castor bean and mustard for phytoremediation of nickel from contaminated soil

Bioremediation J.

(2015)

H. Chen

Study on biomass and productivity of phyllostachys heterocycla cv.pubescens forest in the north of fujian

Sci. Silvae Sin.

(1998)

J.R. Chen

Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens)

Sci. Rep.

(2015)

Y. Ekmekçi

A crop tolerating oxidative stress induced by excess lead: maize

Acta Physiol. Plant.

(2009)

A.A. Elkhatib

Bioaccumulation potential and physiological responses of aquatic macrophytes to Pb pollution

Int. J. Phytoremediat.

(2014)

E. Gajewska et al.

Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress

Acta Physiol. Plant.

(2005)

C.N. Giannopolitis et al.

Superoxide dismutases: i. Occurrence in higher plants

Plant Physiol.

(1977)

D.K. Gupta

Lead tolerance in plants: strategies for phytoremediation

Environ. Sci. Pollut. Res.

(2013)

F.J. Hu

Effects of Pb stress on the growth, development and Pb enrichment properties of Toona ciliata Roem saplings

J. Agro-Environ. Sci.

(2012)

Z. Hu

Growth responses of two tall fescue cultivars to Pb stress and their metal accumulation characteristics

Ecotoxicology

(2015)

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¹: These authors contributed equally to this work.

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Effect of lead (Pb) on antioxidation system and accumulation ability of Moso bamboo (Phyllostachys pubescens)

Highlights

Abstract

Introduction

Section snippets

Hydroponics experiment

Effects of Pb on antioxidation system of leaves and Pb concentration of plants in hydroponics

Discussions

Conclusions

Acknowledgement

J. Plant Physiol.

Environ. Sci. Pollut. Res.

Ecotoxicol. Environ. Saf.

Plant Physiol. Biochem.

Ecol. Eng.

J. Hazard. Mater.

J. Hazard. Mater.

Ecotoxicol. Environ. Saf.

Ecotoxicol. Environ. Saf.

Trends Plant Sci.

Biotechnol. Adv.

J. Geochem. Explor.

Phytoremediation of heavy metals: a green technology

Afr. J. Biotechnol.

Assessment of metal uptake capacity of castor bean and mustard for phytoremediation of nickel from contaminated soil

Bioremediation J.

Study on biomass and productivity of phyllostachys heterocycla cv.pubescens forest in the north of fujian

Sci. Silvae Sin.

Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens)

Sci. Rep.

A crop tolerating oxidative stress induced by excess lead: maize

Acta Physiol. Plant.

Bioaccumulation potential and physiological responses of aquatic macrophytes to Pb pollution

Int. J. Phytoremediat.

Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress

Acta Physiol. Plant.

Superoxide dismutases: i. Occurrence in higher plants

Plant Physiol.

Lead tolerance in plants: strategies for phytoremediation

Environ. Sci. Pollut. Res.

Effects of Pb stress on the growth, development and Pb enrichment properties of Toona ciliata Roem saplings

J. Agro-Environ. Sci.

Growth responses of two tall fescue cultivars to Pb stress and their metal accumulation characteristics

Ecotoxicology