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Comparative study on the influence of silicon and selenium to mitigate arsenic induced stress by modulating TCA cycle, GABA, and polyamine synthesis in rice seedlings

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Abstract

Arsenic contamination of groundwater is a major concern for its usage in crop irrigation in many regions of the world. Arsenic is absorbed by rice plants mainly from arsenic contaminated water during irrigation. It hampers growth and agricultural productivity. The aim of the study was to mitigate the toxic effects of arsenate (As-V) [25 μM, 50 μM, and 75 μM] by silicon (Si) [2 mM] and selenium (Se) [5 μM] amendments on the activity of the TCA cycle, synthesis of γ-aminobutyric acid (GABA) and polyamines (PAs) in rice (Oryza sativa L. cv. MTU-1010) seedlings and to identify which chemical was more potential to combat this threat. As(V) application decreased the activities of tested respiratory enzymes and increased the levels of organic acids (OAs) in the test seedlings. Application of Si with As(V) and Se with As(V) increased the activities of respiratory enzymes and the levels of OAs. The effects were more pronounced during Si amendments. The activities of GABA synthesizing enzymes along with accumulation of GABA were increased under As(V) stress. During joint application of Si with As(V) and Se with As(V) the activity and the level of said parameters were decreased that indicating defensive role of these chemicals to resist As(V) toxicity in rice and Si amendments showed greater potential to reduce As(V) induced damages in the test seedlings. PAs trigger tolerance mechanism against As(V) in plants. PAs such as putrescine, spermidine and spermine were synthesized more during Si and Se amendments in As(V) contaminated rice seedlings to combat the toxic effects of As(V). Si amendments substantially modulated the toxic effects caused by As(V) over Se amendments in the As(V) challenged test seedlings. Thus, in future application of Si enriched fertilizer will be beneficial to grow rice plants with normal vigor in arsenic contaminated soil.

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Fig. 1: Influence of increasing concentrations of As(V) with or without Si and Se on PDH activity in 3 weeks old rice seedlings.
Fig. 2: Influence of increasing concentrations of As(V) with or without Si and Se on IDH activity in 3 weeks old rice seedlings.
Fig. 3: Influence of increasing concentrations of As(V) with or without Si and Se on α-KGDH activity in 3 weeks old rice seedlings.
Fig. 4: Influence of increasing concentrations of As(V) with or without Si and Se on SDH activity in 3 weeks old rice seedlings.
Fig. 5: Influence of increasing concentrations of As(V) with or without Si and Se on fumarase activity in 3 weeks old rice seedlings.
Fig. 6: Influence of increasing concentrations of As(V) with or without Si and Se on MDH activity in 3 weeks old rice seedlings.
Fig. 7: Influence of increasing concentrations of As(V) with or without Si and Se on CS activity in 3 weeks old rice seedlings.
Fig. 8: Influence of increasing concentrations of As(V) with or without Si and Se on GABA contents in 3 weeks old rice seedlings.
Fig. 9: Influence of increasing concentrations of As(V) with or without Si and Se on glutamate dehydrogenase activity in 3 weeks old rice seedlings.
Fig. 10: Influence of increasing concentrations of As(V) with or without Si and Se on glutamate decarboxylase activity in 3 weeks old rice seedlings.
Fig. 11: Influence of increasing concentrations of As(V) with or without Si and Se on GABA transaminase activity in 3 weeks old rice seedlings.
Fig. 12: Influence of As(V), As(V) + Si, and As(V) + Se on Put contents in 3 weeks old rice (cv. MTU-1010) seedlings.
Fig. 13: Influence of As(V), As(V) + Si, and As(V) + Se on Spd contents in 3 weeks old rice (cv. MTU-1010) seedlings.
Fig. 14: Influence of As(V), As(V) + Si, and As(V) + Se on Spm contents in 3 weeks old rice (cv. MTU-1010) seedlings.
Fig. 15: Overall schematic representation showing events toward mitigation of arsenic induced toxicity by silicon and selenium on TCA cycle, GABA and polyamine metabolism in 21 days old rice seedling.

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Abbreviations

ACN:

Acetonitrile

AMP:

Adenosine monophosphate

ANOVA:

Analysis of variance

As:

Arsenic

As(V):

Arsenate

As(III):

Arsenite

α-KGDH:

α-ketoglutarate dehydrogenase

BSA:

Bovine serum albumin

CaCl2 :

Calcium chloride

Co-A:

Coenzyme A

CH3COOC2H5 :

Ethyl acetate

C/N:

Carbon/Nitrogen

CNS:

Carbon nitrogen sulfur

CS:

Citrate synthase

DNPH:

2,4-Dinitrophenylhydrazine

DTT:

Dithiothreitol

DTNB:

5,5′-dithiobis-(2-nitrobenzoic acid)

EDTA:

Ethylenediaminetetraacetic acid

GABA:

γ-aminobutyric acid

GABA-T:

GABA transaminase

GAD:

Glutamate decarboxylase

GDH:

Glutamate dehydrogenase

h:

hour

H2SO4 :

Sulfuric acid

HCl:

Hydrochloric acid

HClO4 :

Perchloric acid

HEPES:

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

HPLC:

High performance liquid chromatography

HSD:

Honest significant difference

IDH:

Isocitrate dehydrogenase

INT:

Iodonitrotetrazolium or 2-(4-iodophenyl)-3-(4-nitrophenyl)-5-phenyl-2H-tetrazolium

KOH:

Potassium hydroxide

MDH:

Malate dehydrogenase

min:

minutes

MgCl2 :

Magnesium chloride

MnSO4 :

Manganese(II) sulfate

MOPS:

3-(N-morpholino)propanesulfonic acid

Na2CO3 :

Sodium carbonate

NAD:

Nicotinamide adenine dinucleotide

NADPH:

Nicotinamide adenine dinucleotide phosphate hydrogen

NaH2PO4 :

Monosodium phosphate

NaOCl:

Sodium hypochlorite

NaOH:

Sodium hydroxide

NH4OH:

Ammonium hydroxide

(NH4)2SO4 :

Ammonium sulfate

NO:

Nitric oxide

OA:

Organic acid

OAA:

Oxaloacetic acid

OD:

Optical density

PAs:

Polyamines

PDH:

Pyruvate dehydrogenase

Put:

Putrescine

PVP:

Polyvinylpyrrolidone

RFs:

Retention factors

ROS:

Reactive oxygen species

rpm:

revolutions per minute

s:

seconds

Se:

Selenium

SDH:

Succinate dehydrogenase

Si:

Silicon

SPD:

Spermidine

SPM:

Spermine

SPSS:

Statistical package for the social sciences

TCA:

Trichloroacetic acid

TLC:

Thin layer chromatography

TPP:

Thiamine pyrophosphate

UQH2 :

Ubiquinol

UQ:

Ubiquinone.

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Acknowledgements

The authors would acknowledge the Department of Science & Technology, Government of India for providing DST-Inspire Fellowship (No. DST/INSPIRE Fellowship/2015/IF150003) to S.D. We are thankful to the Center for advanced study, Department of Botany, University of Calcutta for providing the infrastructure facility.

Author contribution

S.D. designed and carried out the experiments, did all data analysis and drafted the manuscript. B.M. helped in drafting of the manuscript. A.K.B. conceived the study, helped to design experiments, analyzed results and finalized the manuscript.

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  1. Plant Physiology and Biochemistry Laboratory, Centre of Advanced Studies, Department of Botany, University of Calcutta, 35 Ballygunge Circular Road, Kolkata, 700019, India

    Susmita Das, Barsha Majumder & Asok K. Biswas

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  1. Susmita Das
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  2. Barsha Majumder
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Das, S., Majumder, B. & Biswas, A.K. Comparative study on the influence of silicon and selenium to mitigate arsenic induced stress by modulating TCA cycle, GABA, and polyamine synthesis in rice seedlings. Ecotoxicology 31, 468–489 (2022). https://doi.org/10.1007/s10646-022-02524-8

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