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Modulation of growth, ascorbate-glutathione cycle and thiol metabolism in rice (Oryza sativa L. cv. MTU-1010) seedlings by arsenic and silicon

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Abstract

Arsenic is a carcinogenic metalloid, exists in two important oxidation states—arsenate (As–V) and arsenite (As-III). The influence of arsenate with or without silicate on the growth and thiol metabolism in rice (Oryza sativa L. cv. MTU-1010) seedlings were investigated. Arsenate was more toxic for root growth than shoot growth where the root lengths were short, characteristically fragile and root tips turned brown. The multiple comparison analysis using Tukey’s HSD (honest significant difference) tests indicated that the rate of arsenate accumulation and its conversion to arsenite by arsenate reductase were significantly increased in all arsenate treated seedlings while in seedlings treated jointly with arsenate and silicate, arsenate accumulation and its conversion to arsenite decreased. Silicate content was detected in the seedlings treated with silicate alone and under co-application of arsenate with silicate. In the test seedlings arsenic toxicity increased ascorbate and glutathione contents along with the activities of their regulatory enzymes, viz., ascorbate peroxidase, glutathione reductase, glutathione peroxidase and glutathione–s-transferase to reduce the toxicity level induced by arsenic whereas ascorbate oxidase activity was decreased to maintain sufficient ascorbate pool under arsenate treatment. Phytochelatins production were increased in both root and shoot of the test seedlings under arsenate exposure to alter the detrimental effects of arsenic by chelation with arsenite and their subsequent sequestration into vacuole. Thus, joint application of silicate along with arsenate showed significant alterations on all the parameters tested compared to arsenate treatment alone due to less availability of arsenic in the tissue leading to better growth and metabolism in rice seedlings. Thus use of silicon in arsenic contaminated medium may help to grow rice with improved vigour.

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Abbreviations

AA :

ascorbic acid or ascorbate

AOX :

ascorbate oxidase

ACN :

acetonitrile

APX :

ascorbate peroxidase

AR :

arsenate reductase

As :

arsenic

As(V) :

arsenate

As(III) :

arsenite

BSA :

bovine serum albumin

Ca(NO 3 ) 2 :

calcium nitrate

CDNB :

1-chloro-2,4-dinitrobenzene

CuSO 4 :

copper sulfate

DHA :

dehydroascorbate

DHAR :

dehydroascorbate reductase

DNPH :

2,4-dinitrophenylhydrazine

DTNB :

5,5-dithiobis-2-nitrobenzoic acid

DTPA :

diethylene triamine penta acetic acid

DTT :

dithiothreitol

DW :

dry weight

EDTA :

ethylene diamine tetra acetic acid

FW :

fresh weight

GSH :

glutathione reduced

GSSG :

glutathione oxidized

GPx :

glutathione peroxidase

GR :

glutathione reductase

GST :

glutathione-S-transferase

H 2 O :

water

H 2 O 2 :

hydrogen peroxide

H 2 SO 4 :

sulfuric acid

H 3 BO 3 :

boric acid

HCl :

hydrochloric acid

HEPES :

4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid

HF :

hydrofluoric acid

HNO 3 :

nitric acid

HPLC :

high-performance liquid chromatography

KI :

potassium iodide

KNO 3 :

potassium nitrate

mBBr :

monobromobimane

MDHA :

monodehydroascorbate

MDHAR :

monodehydroascorbate reductase

MES :

2-(N-morpholino)ethanesulfonic acid

MgSO 4 :

magnesium sulfate

MnCl 2 :

manganese chloride

MOPS :

3-(N-morpholino)propanesulfonic acid

MSA :

methanesulfonic acid

NaBH 4 :

sodium tetrahydridoborate

NaCl :

sodium chloride

NaFeEDTA :

ethylenediaminetetraacetic acid ferric sodium salt

NaOCl :

sodium hypochlorite

NH 4 NO 3 :

ammonium nitrate

OD :

optical density

PCs :

phytochelatins

PFD :

photon flux density

PMSF :

phenylmethane sulfonyl fluoride or phenylmethylsulfonyl fluoride

PVP :

polyvinyl pyrrolidone

ROS :

reactive oxygen species

RT :

retention time

Rt :

root

SE :

standard error

Sh :

shoot

Si :

silicon or silicate

SSA :

sulphosalicylic acid

TCA :

trichloroacetic acid

TFA :

trifluoroacetic acid

ZnSO 4 :

zinc sulfate

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Acknowledgements

The authors are grateful to the Department of Science & Technology, Government of India, New Delhi for providing DST-INSPIRE Fellowship (No. DST/INSPIRE Fellowship/2015/IF150003) to S.D. and Centre of advanced studies of the department for providing infrastructural facilities in completion of the work. The authors are also grateful to Dr. Baidya Nath Pal, Associate Scientist ‘A’ of Indian Statistical Institute, Kolkata for his valuable guidance during statistical analysis. The authors are thankful to Scientific Research Laboratory, Kolkata for analysis of arsenic, arsenite and silicate contents from the samples.

Authors' contributions

SD performed the experiments, statistically analyzed the data and drafted the manuscript. BM did part of the experiments. AKB conceived the study, supervised the experimental design and gave final shape of the manuscript. All authors read and are in agreement of the final manuscript.

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Correspondence to Asok K. Biswas.

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The authors declare that they have no conflict of interest.

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The research article ensures objectivity and transparency in research and secures that accepted principles of ethical and professional conduct have been followed. This original research article does not contain any studies with human participants and animals performed by any of the authors.

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Das, S., Majumder, B. & Biswas, A.K. Modulation of growth, ascorbate-glutathione cycle and thiol metabolism in rice (Oryza sativa L. cv. MTU-1010) seedlings by arsenic and silicon. Ecotoxicology 27, 1387–1403 (2018). https://doi.org/10.1007/s10646-018-1994-5

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  • DOI: https://doi.org/10.1007/s10646-018-1994-5

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