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Decoding the antioxidant mechanisms underlying arsenic stress in roots of inoculated peanut plants

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Abstract

Arsenic (As) has aroused worldwide concern due to its accumulation in the food chain. Inoculated peanut plants with Bradyrhizobium sp. strains showing contrasting tolerance to arsenic (As), were exposed to a low arsenate (AsV) for 30 days in order to decipher the participation of the antioxidant system, mainly related to glutathione (GSH) metabolism, together with the arsenate reductase (AR) activity in roots. Results showed that the Bradyrhizobium sp. strain modulates differentially the AR activity. An increase in the enzymatic activities of superoxide dismutase, glutathione peroxidase/peroxirredoxin and glutathione S-transferase (GST) was observed, while glutathione reductase (GR) and monodehydroascorbate reductase activities were diminished. Particularly, ascorbate peroxidase (APX) activity was reduced when C-145 was inoculated. Gene expression assays reported an increase in the expression of transcripts GR, cAPX and GST in peanut roots inoculated with SEMIA6144. In the system peanut-Bradyrhizobium sp. C-145, the cAPX expression remained unchanged. In both symbiotic interactions, the total glutathione (GSHT) and reduced glutathione (GSHR) contents diminished, while oxidized glutathione (GSSG) increased leading to a reduction in the GSHR/(GSHR + GSSG) ratio. We conclude that, irrespectively of the As tolerance that the inoculated strains shows, the antioxidant response is not strain dependent. Thus, glutathione plays a fundamental role not only as an antioxidant metabolite but also as a key molecule to enhance metalloid detoxification in this inoculated crop. Moreover, as the tripeptide participates in the ROS scavenging, acting mainly as a substrate for GST, allow us to describe its activity as a robust biomarker of arsenic contamination in crops.

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Funding

The authors thank CONICET; ANPCyT; SECYT-UNRC; and Ministry of Science, Innovation and Universities together with the European Regional Development Fund (MCIU/AEI/ERDF; PGC2018-098372-B-100) for providing financial assistance for this research. JMP is a CONICET scholarship. CT, EB and AF are members of the research career from CONICET. MCRP is research scientist at EEZ-CSIC. EMM was supported by University Staff Training fellowship (17/04303) from the Spanish Ministry of Education, Culture and Sports (Spain). SC is a researcher-teacher at UNRC. JMP is grateful to the Programa de Movilidad entre Instituciones Asociadas a la Asociación Universitaria Iberoamericana de Postgrado (AUIP, 2017) for supporting a short-term scholarship in EEZ-CSIC and Universidad de Granada (Spain).

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Contributions

JMP carried out all the experiments and wrote the manuscript. EB, CT and SC designed the experimental system and supervised assays carried out in Argentina. EMM collaborated with the gene expression assays. MCRP supervised the gene expression assays carried out in Granada, Spain. All authors read and corrected the manuscript.

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Correspondence to Eliana Bianucci.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Communicated by Hua Wang.

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10725_2022_803_MOESM1_ESM.tif

Figure S1. An integrated scheme for inoculated peanut plants. LDW (Leave dry weight); RDW (Roots dry weight); LL (Leaves lenght); RL (Roots length); LA (Leave area); NN (Nodules number); NDW (Nodules dry weight); [N] (Nitrogen content); Ct (Total chlorophyll); Ca (Chlorophyll a); Cb (Chlorophyll b); NADPHox (NADPH oxidase); SOD (Superoxide dismutase); CAT (Catalase); GST (Glutathione S-transferase); APX (Ascorbate peroxidase); GR (Glutathione reductase); GPX / PRX (Glutathione peroxidase / peroxiredoxin); MDHAR (Monodehydroascorbate reductase); DHAR (Dehydroascorbate reductase); GSHT (Total Glutathione); GSH (Reduced Glutathione); GSSG (Glutathione disulfide); FT (Arsenic translocation factor); TBARs (Thiobarbituric acid reactive substances); C = O (free carbonyl groups) (TIF 171 kb)

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Peralta, J.M., Travaglia, C., Romero-Puertas, M.C. et al. Decoding the antioxidant mechanisms underlying arsenic stress in roots of inoculated peanut plants. Plant Growth Regul 97, 77–90 (2022). https://doi.org/10.1007/s10725-022-00803-2

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