AtDGCR14L contributes to salt-stress tolerance via regulating pre-mRNA splicing in Arabidopsis

Meng Xie, Dimiru Tadesse, Jin Zhang, Tao Yao, Li Zhang, Sara S. Jawdy, Amith Devireddy, Kaijie Zheng, Emily B. Smith, Jennifer Morrell-Falvey, Chongle Pan, Feng Chen, Gerald A. Tuskan, Wellington Muchero, Jin Gui Chen

Research output: Contribution to journalArticlepeer-review

Abstract

In plants, pre-mRNA alternative splicing has been demonstrated to be a crucial tier that regulates gene expression in response to salt stress. However, the underlying mechanisms remain elusive. Here, we studied the roles of DIGEORGE-SYNDROME CRITICAL REGION 14-like (AtDGCR14L) in regulating pre-mRNA splicing and salt stress tolerance. We discovered that Arabidopsis AtDGCR14L is required for maintaining plant salt stress tolerance and the constitutively spliced and active isoforms of important stress- and/or abscisic acid (ABA)-responsive genes. We also identified the interaction between AtDGCR14L and splicing factor U1-70k, which needs a highly conserved three amino acid (TWG) motif in DGCR14. Different from wild-type AtDGCR14L, the overexpression of the TWG-substituted AtDGCR14L mutant did not change salt stress tolerance or pre-mRNA splicing of stress/ABA-responsive genes. Additionally, SWITCH3A (SWI3A) is a core subunit of the SWI/SUCROSE NONFERMENTING (SWI/SNF) chromatin-remodeling complexes. We found that SWI3A, whose splicing depends on AtDGCR14L, actively enhances salt stress tolerance. These results revealed that AtDGCR14L may play an essential role in crosstalk between plant salt-stress response and pre-mRNA splicing mechanisms. We also unveiled the potential role of SWI3A in controlling salt stress tolerance. The TWG motif in the intrinsically disordered region of AtDGCR14L is highly conserved and crucial for DGCR14 functions.

Original languageEnglish
JournalPlant Journal
DOIs
StateAccepted/In press - 2024

Funding

This material is based upon work supported by the Center for Bioenergy Innovation (CBI), which is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Science, Biological and Environmental Research program under Award Number ERKP886. This material is also based upon work supported by the Plant\u2010Microbe Interfaces Scientific Focus Area, supported by the U.S. Department of Energy Office of Science, Biological and Environmental Research program under Award Number ERKP730. The transcriptomic study, proximity labeling experiments, and part of the salt stress study were supported by the Quantitative Plant Science Initiative (QPSI) Scientific Focus Area, supported by the U.S. Department of Energy Office of Science, Biological and Environmental Research program. Part of this research used resources from the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory. Emily B. Smith was funded by the Higher Education Research Experiences (HERE) program at Oak Ridge National Laboratory as an undergraduate student intern. Oak Ridge National Laboratory is managed by UT\u2010Battelle, LLC for the Office of Science of the U.S. Department of Energy under Contract Number DE\u2010AC05\u201000OR22725. Jin Zhang was funded by the National Natural Science Foundation of China (32171814) and the Natural Science Foundation of Zhejiang Province for Distinguished Young Scholars (LR22C160001).

FundersFunder number
U.S. Department of Energy Bioenergy Research Center
Quantitative Plant Science Initiative
Oak Ridge National Laboratory
Center for Bioenergy Innovation
Biological and Environmental Research program
Office of ScienceERKP730
National Natural Science Foundation of China32171814
U.S. Department of EnergyDE‐AC05‐00OR22725
Science Fund for Distinguished Young Scholars of Zhejiang ProvinceLR22C160001
Biological and Environmental ResearchERKP886

    Keywords

    • alternative splicing
    • Arabidopsis thaliana
    • chromatin-remodeling complex
    • DGCR14
    • functional motif
    • salt stress

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