The DEAD-box RNA helicase SHI2 functions in repression of salt-inducible genes and regulation of cold-inducible gene splicing

Authors: BANGSHING, WANG - Texas Tech University; HAOXI, CHAI - Texas Tech University; YINGLI, ZHONG - Texas Tech University; YUN, SHEN - Texas Tech University; WANNIAN, YANG - Texas Tech University; Chen, Junping; Xin, Zhanguo; HUAZHONG, SHI - Texas Tech University

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/19/2019
Publication Date: 11/20/2019
Citation: Bangshing, W., Haoxi, C., Yingli, Z., Yun, S., Wannian, Y., Chen, J., Xin, Z., Huazhong, S. 2019. The DEAD-box RNA helicase SHI2 functions in repression of salt-inducible genes and regulation of cold-inducible gene splicing. Journal of Experimental Botany. 71(4):1598–1613. https://doi.org/10.1093/jxb/erz523.
DOI: https://doi.org/10.1093/jxb/erz523

Interpretive Summary: Abiotic stresses account for 80% of the losses in the potential genetic yield of crops. Understanding the mechanisms of plants to adapt to abiotic stresses is important for food security. As sessile organisms, plants must regulate the expression of many genes in response to changes in environmental conditions. However, it is not well understood how genes are activated or repressed during exposure to environmental stresses. In collaboration with Texas Tech University, ARS scientists from Lubbock, Texas identified a gene, Shi2 (Shiny2), from Arabidopsis that is responsible for repressing salt-inducible genes. Shi 2 gene also mediates RNA splicing to produce the mature mRNA and stabilizes mRNAs by adding Cap and Poly A tail. The Shi2 gene provides a novel way to regulate gene expression and stress tolerance in plants.

Technical Abstract: Gene regulation is central for growth, development and adaptation to environmental changes in all living organisms. In addition to the constitutively expressed housekeeping genes essential for maintaining the normal function of cell, many genes are induced by environmental cues or developmental signals. The expression of these inducible genes is often repressed under normal conditions, but the molecular mechanisms of gene repression is not fully understood. In this study, we show that SHI2 gene is important for salt-inducible gene repression and plays a role in cold stress response. The shi2 mutant was isolated from a mutagenized Arabidopsis line that has has a transgene of luciferase driven by the promoter of Sot12, a salt-inducible gene. The shi2 mutant exhibited exaggerated expression of luciferase activity in response to salt treatment and hypersensitivity to cold, ABA and LiCl. SHI2 encodes a DEAD (Asp-Glu-Ala-Asp) box RNA helicase with similarity to a yeast splicing factor. The shi2 mutation resulted in mis-splicing of the pre-mRNAs of cold-responsive genes. The SHI2 gene was also found to be involved in 5’ capping and polyadenylation site selection. Transcriptomic analysis showed that the shi2 mutation rendered a stronger response to salt stress but resulted in reduced number of genes in response to cold. However, many more genes were differentially expressed between the mutant and wild type in response to cold stress than to salt stress. We deduce that SHI2 represses inducible gene expression by serving in a repressor complex at the promoter under normal growth conditions, while SHI2 is also a component in the active transcription machinery for transcription and co-transcriptional processes once the inducible genes are activated by environmental signals.