Alternative splicing of DSP1 enhances snRNA accumulation by promoting transcription termination and recycle of the processing complex

Abstract

Small nuclear RNAs (snRNAs) are the basal components of the spliceosome and play crucial roles in splicing. Their biogenesis is spatiotemporally regulated. However, related mechanisms are still poorly understood. Defective in snRNA processing (DSP1) is an essential component of the DSP1 complex that catalyzes plant snRNA 3′-end maturation by cotranscriptional endonucleolytic cleavage of the primary snRNA transcripts (presnRNAs). Here, we show that DSP1 is subjected to alternative splicing in pollens and embryos, resulting in two splicing variants, DSP1α and DSP1β. Unlike DSP1α, DSP1β is not required for presnRNA 3′-end cleavage. Rather, it competes with DSP1α for the interaction with CPSF73-I, the catalytic subunit of the DSP1 complex, which promotes efficient release of CPSF73-I and the DNA-dependent RNA polymerease II (Pol II) from the 3′ end of snRNA loci thereby facilitates snRNA transcription termination, resulting in increased snRNA levels in pollens. Taken together, this study uncovers a mechanism that spatially regulates snRNA accumulation.

Spliceosomal snRNAs, the Essential Players in pre‐mRNA Processing in Eukaryotic Nucleus: From Biogenesis to Functions and Spatiotemporal Characteristics

“…[ 145 ] Moreover, DSP4, in collaboration with DSP1, affects multiple aspects of plant development, including male fertility in pollen grains. [ 23,146 ] Due to the essential role of the Integrator complex in snRNA synthesis and other biological processes, its absence usually results in lethality of organisms. [ 146–148 ]…”

DNA-dependent RNA polymerases in plants

“…The termination process involves RNA cleavage by its endoribonuclease subunit, Integrator complex subunit 11 (INTS11), and subsequent RNA release by unknown mechanisms. Transcription termination of snRNA in Arabidopsis is triggered by a smaller version of the Integrator complex comprising DPS1–4 (homologous to INTS7, INTS3, INTS4, and INTS9, subunits of the mammalian Integrator) and a INTS11-like RNA endonuclease ( Liu et al 2016 ; Wang et al 2020 ; Kirstein et al 2021 ).…”

Alternative splicing: transcriptional regulatory network in agroforestry

“…Wang et al. discovered that alternative splicing causes an increased level of snRNA transcripts in pollens which suggests its unique role in the regulation of snRNA biosynthesis in plants ( Wang et al., 2020 ). In this review article, we have summarized recent advances in determining the specific role of AS in the transcriptional regulation of gene expression in plants under the influence of different environmental conditions.…”

“…Beyond the important role of AS in the increased diversity of proteome by producing novel transcript combinations, presumably, many transcript isoforms have a negative influence over protein structure and function, which suggests its role in the posttranscriptional regulation of gene expression (Campbell et al, 2006). Wang et al discovered that alternative splicing causes an increased level of snRNA transcripts in pollens which suggests its unique role in the regulation of snRNA biosynthesis in plants (Wang et al, 2020). In this review article, we have summarized recent advances in determining the specific role of AS in the transcriptional regulation of gene expression in plants under the influence of different environmental conditions.…”