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Physiological and differential gene expression reveals a trade-off between antioxidant capacity and salt tolerance in Urochondra setulosa and Dichanthium annulatum

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Abstract

Background

Among abiotic stresses, soil salinity is one of the major global constraints to growth and productivity in most of the crop plants, limiting current and future agricultural sustainability. Halophytes are the most suitable host plants to dissect the salinity tolerance phenomenon in natural environment. To elucidate the mechanisms of salinity tolerance is an ever growing research area for genetic engineering of crops to improve the salinity tolerance and ultimately to improve the crop yield and quality.

Methods and results

In the present investigation, two un-explored halophytes, i.e. moderately salt tolerant (Dichanthium annulatum) and extremely salt tolerant (Urochondra setulosa) were studied for unrevealing the contributory role of antioxidative system in salinity tolerance at higher saline intensities of ECe ~30, 40 and 50dSm− 1. Experimental findings indicated that the accumulation of hydrogen peroxide (H2O2) content, Superoxide dismutase (SOD) and ascorbate peroxidase (APX) activities were higher in U. setulosa at all saline treatments. Whereas, higher order of malondialdehyde (MDA) content and catalase (CAT) activity was observed in D. annulatum, although the specific enzyme activities of chemically reactive oxygen species (ROS) system increased with increasing levels of salinity in both the halophytes. This differential physiological mechanism was collaborated with the transcriptomic data generated through High throughput sequencing on Illumina platform. Transcriptome expression analysis depicting that a total of 276 and 66 genes coding for various components of ROS system like antioxidant activity, cell redox and glutathione metabolism were differentially expressed in response to salinity stress in U. setulosa and D. annulatum, respectively. Biochemical analysis indicated that H2O2 is detoxified by increased activities of SOD, APX and CAT in D. annulatum, however, in U. setulosa, POX takes over catalase to remove the higher accumulation of H2O2 along with dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase (MDHAR) significantly associated with the differentially expressed transcripts.

Conclusions

The differentially expressed genes for ROS enzymes and antioxidants clearly differentiate and support the detoxification of H2O2 and survival mechanism of Urochondra setulosa and Dichanthium annulatum at different salinity levels. This study provides the reference information for key regulatory genes responsible for salinity stress tolerance and can be used for increasing salinity tolerance of related crop species.

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Data Availability

The raw data is available with the corresponding author which can be shared on request. Transcriptomics data is submitted at https://www.ncbi.nlm.nih.gov/bioproject/PRJNA561259 and https://www.ncbi.nlm.nih.gov/bioproject/PRJNA665324. The data of differentially expressed genes (DEGs) of both the plants have been deposited in the repository at Mendeley data (https://data.mendeley.com//datasets/c9zwjncxb4/1). Differential antioxidant data has been deposited in the repository at Mendeley data (https://data.mendeley.com/datasets/xd698v9w9s).

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Acknowledgements

We gratefully acknowledge the Indian Council of Agricultural Research (ICAR) for providing us the financial support to conduct the work. We are also thankful to the Director, ICAR-Central Soil Salinity Research, Karnal, Haryana, India for imparting required facilities for carrying out the research work.

Funding

This project was supported by the Indian Council of Agricultural Research (ICAR) - National Agricultural Science Fund (NASF), New Delhi, India (Grant no ABP-6027).

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Authors and Affiliations

  1. ICAR-Central Soil Salinity Research Institute, Karnal, Haryana, India

    Anita Mann, Naresh Kumar, Charu Lata, Arvind Kumar, B. L. Meena & Ashwani Kumar

  2. Present address, Eternal University, Baru Sahib, Himachal Pardesh, India

    Naresh Kumar

  3. ICAR- Indian Institute of Wheat and Barley Research, RRS, Flowerdale, Shimla, India

    Charu Lata

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  1. Anita Mann
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Contributions

A.M. formulated the experiments, organized and prepared the main manuscript, supervision of project. N.K. performed QC, gene validation and bioinformatic analysis, wrote the original manuscript draft. C. L. performed total RNA isolation and physiological enzyme analysis. Ar. K. discussed data presentation design. B.L.M. helped in maintaining salinity throughout the experiment and A.K. interpreted results and performed SAS.

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Correspondence to Anita Mann.

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Communicated by Zhong-Hua Chen.

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10725_2023_1085_MOESM1_ESM.jpeg

Supplementary Material 1: Supplementary Fig. 1. Important pathways operative in ROS system in U. setulosa and D. annulatum at salinity levels of EC 30, 40 & 50 dSm− 1

10725_2023_1085_MOESM2_ESM.jpeg

Supplementary Material 2: Supplementary Fig. 2. GO enrichment of important terms in both the plants at salinity levels of EC 30, 40 & 50 dSm− 1

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Mann, A., Kumar, N., Lata, C. et al. Physiological and differential gene expression reveals a trade-off between antioxidant capacity and salt tolerance in Urochondra setulosa and Dichanthium annulatum. Plant Growth Regul 102, 555–570 (2024). https://doi.org/10.1007/s10725-023-01085-y

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