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Genome Biol., Mar 21 2025, 26 (1) 65 | https://doi.org/10.1186/s13059-025-03529-2
Global profiling of CPL3-mediated alternative splicing reveals regulatory mechanisms of DGK5 in plant immunity and phosphatidic acid homeostasis
Sung‑Il Kim 1, Xiyu Ma 2, Liang Kong 1, Wenbin Guo 3, Lahong Xu 2, Libo Shan 1, Runxuan Zhang 3* and Ping He 1,2*
1Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA
2Department of Biochemistry & Biophysics, Texas a&M University, College Station, TX 77843, USA
3Information and Computational Sciences Department, The James Hutton Institute, Dundee, UK
*Corresponding authors: correspondence to Runxuan Zhang or Ping He
2Department of Biochemistry & Biophysics, Texas a&M University, College Station, TX 77843, USA
3Information and Computational Sciences Department, The James Hutton Institute, Dundee, UK
*Corresponding authors: correspondence to Runxuan Zhang or Ping He
Abstract
Background
Alternative splicing of precursor mRNAs serves as a crucial mechanism to enhance gene expression plasticity for organismal adaptation. However, the precise regulation and function of alternative splicing in plant immune gene regulation remain elusive.
Results
Here, by deploying in-depth transcriptome profiling with deep genome coverage coupled with differential expression, differential alternative splicing, and differential transcript usage analysis, we reveal profound and dynamic changes in alternative splicing following treatment with microbial pattern flg22 peptides in Arabidopsis. Our findings highlight RNA polymerase II C-terminal domain phosphatase-like 3 (CPL3) as a key regulator of alternative splicing, preferentially influencing the splicing patterns of defense genes rather than their expression levels. CPL3 mediates the production of a flg22-induced alternative splicing variant, diacylglycerol kinase 5α (DGK5α), which differs from the canonical DGK5β in its interaction with the upstream kinase BIK1 and subsequent phosphorylation, resulting in reduced flg22-triggered production of phosphatidic acid and reactive oxygen species. Furthermore, our functional analysis suggests that DGK5β, but not DGK5α, contributes to plant resistance against virulent and avirulent bacterial infections.
Conclusions
These findings underscore the role of CPL3 in modulating alternative splicing dynamics of defense genes and DGK5 isoform-mediated phosphatidic acid homeostasis, shedding light on the intricate mechanisms underlying plant immune gene regulation.
Alternative splicing of precursor mRNAs serves as a crucial mechanism to enhance gene expression plasticity for organismal adaptation. However, the precise regulation and function of alternative splicing in plant immune gene regulation remain elusive.
Results
Here, by deploying in-depth transcriptome profiling with deep genome coverage coupled with differential expression, differential alternative splicing, and differential transcript usage analysis, we reveal profound and dynamic changes in alternative splicing following treatment with microbial pattern flg22 peptides in Arabidopsis. Our findings highlight RNA polymerase II C-terminal domain phosphatase-like 3 (CPL3) as a key regulator of alternative splicing, preferentially influencing the splicing patterns of defense genes rather than their expression levels. CPL3 mediates the production of a flg22-induced alternative splicing variant, diacylglycerol kinase 5α (DGK5α), which differs from the canonical DGK5β in its interaction with the upstream kinase BIK1 and subsequent phosphorylation, resulting in reduced flg22-triggered production of phosphatidic acid and reactive oxygen species. Furthermore, our functional analysis suggests that DGK5β, but not DGK5α, contributes to plant resistance against virulent and avirulent bacterial infections.
Conclusions
These findings underscore the role of CPL3 in modulating alternative splicing dynamics of defense genes and DGK5 isoform-mediated phosphatidic acid homeostasis, shedding light on the intricate mechanisms underlying plant immune gene regulation.
논문정보
- Research article
- 2025년 03월 (BRIC 등록일 2025-03-27)
- 국외 연구진
- 생명과학 > 유전자발현
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