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Comprehensive insights into the regulatory mechanisms of lncRNA in alkaline-salt stress tolerance in rice

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Abstract

Background

Alkaline-salt is one of the abiotic stresses that slows plant growth and developmental processes and threatens crop yield. Long non-coding RNAs (lncRNAs) are endogenous RNA found in plants that engage in a variety of cellular functions and stress responses.

Method

lncRNAs act as competing endogenous RNAs (ceRNA) and constitute a new set of gene control. The precise regulatory mechanism by which lncRNAs function as ceRNAs in response to alkaline-salt stress remains unclear. We identified alkaline-salt responsive lncRNAs using transcriptome-wide analysis of two varieties including alkaline-salt tolerant [WD20342 (WD)] and alkaline-salt sensitive [Caidao (CD)] rice cultivar under control and alkaline-salt stress treated [WD20342 (WDT, and Caidao (CDT)] conditions.

Results

Investigating the competitive relationships between mRNAs and lncRNAs, we next built a ceRNA network involving lncRNAs based on the ceRNA hypothesis. Expression profiles revealed that a total of 65, 34, and 1549 differentially expressed (DE) lncRNAs, miRNAs, and mRNAs were identified in alkaline-salt tolerant WD (Control) vs. WDT (Treated). Similarly, 75 DE-lncRNAs, 34 DE-miRNAs, and 1725 DE-mRNAs (including up-regulated and down-regulated) were identified in alkaline-salt sensitive CD (Control) vs. CDT (Treated), respectively. An alkaline-salt stress ceRNA network discovered 321 lncRNA-miRNA-mRNA triplets in CD and CDT, with 32 lncRNAs, 121 miRNAs, and 111 mRNAs. Likewise, 217 lncRNA-miRNA-mRNA triplets in WD and WDT revealed the NONOSAT000455-osa_miR5809b-LOC_Os11g01210 triplet with the highest degree as a hub node with the most significant positive correlation in alkaline-salt stress response.

Conclusion

The results of our investigation indicate that osa-miR5809b is dysregulated and plays a part in regulating the defense response of rice against alkaline-salt stress. Our study highlights the regulatory functions of lncRNAs acting as ceRNAs in the mechanisms underlying alkaline-salt resistance in rice.

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Acknowledgements

The authors extend their appreciation to the Researchers Supporting Project number (RSP-2023R369), King Saud University, Riyadh, Saudi Arabia. We are thankful to Bioinformatics and Functional Genomics Labs at National Institute for Genomics and Advanced Biotechnology (NIGAB), Pakistan, for providing the research facilities.

Funding

This research was conducted with the funds of the Sino-Pak Agricultural Breeding Innovations Project for Rapid Yield Enhancement (Project #760). The funders had no role in the design of the study; in the collection, analysis, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Author notes

    Authors and Affiliations

    1. Food Science and Biological Engineering, Jiangsu University, Zhenjiang, Jiangsu, China

      Obaid Ur Rehman & Muhammad Shahbaz Farooq

    2. National Institute for Genomics and Advanced Biotechnology, Park Road, Islamabad, 45500, Pakistan

      Obaid Ur Rehman, Muhammad Uzair, Muhammad Shahbaz Farooq, Bilal Saleem, Umer Farooq & Muhammad Ramzan Khan

    3. Institute of Biotechnology and Genetic Engineering, The University of Agriculture, Peshawar, Pakistan

      Safira Attacha

    4. Department of Biochemistry, Science College, King Saud University, POX, Riyadh, 2455-11451, Saudi Arabia

      Kotb A. Attia

    5. Department of Plant Breeding and Genetics, The University of Haripur, Haripur, 22620, Pakistan

      Sajid Fiaz

    6. Agriculture Research Center, (ARC), Rice Research and Training Center, (RRTC) Sakha, Field Crop Research Institute, Sakha, Egypt

      Wael. H. El-Kallawy

    7. Institute of Science and Technology, Niigata University, Ikarashi-2, Nishi-ku, Niigata, 950-2181, Japan

      Itoh Kimiko

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    1. Obaid Ur Rehman
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    Contributions

    Conceptualization, O.R., and M.U.; methodology, software, and validation, O.R., B.S., S.F., U.F., and M.U.; formal analysis and investigation, O.R., and M.U.; writing—original draft preparation, review, and editing, O.R., M.S.F., M.U., S.A., S.F., W.H.E.K., I.K., K.A.A., and M.R.K.; visualization, M.U.; supervision and funding acquisition, M.R.K. All authors have read and agreed to the published version of the manuscript.

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    Correspondence to Muhammad Uzair, Kotb A. Attia or Muhammad Ramzan Khan.

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    Obaid Ur Rehman and Muhammad Uzair equally contributed.

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    Rehman, O.U., Uzair, M., Farooq, M.S. et al. Comprehensive insights into the regulatory mechanisms of lncRNA in alkaline-salt stress tolerance in rice. Mol Biol Rep 50, 7381–7392 (2023). https://doi.org/10.1007/s11033-023-08648-2

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