SWELLMAP 2, a phyB-Interacting Splicing Factor, Negatively Regulates Seedling Photomorphogenesis in Arabidopsis.

Tingting Yan,Wenwei Wang,Jian Li,Yueqin Heng,Xing Wang Deng

doi:10.3389/fpls.2022.836519

Abstract

Light-triggered transcriptome reprogramming is critical for promoting photomorphogenesis in Arabidopsis seedlings. Nonetheless, recent studies have shed light on the importance of alternative pre-mRNA splicing (AS) in photomorphogenesis. The splicing factors splicing factor for phytochrome signaling (SFPS) and reduced red-light responses in cry1cry2 background1 (RRC1) are involved in the phytochrome B (phyB) signaling pathway and promote photomorphogenesis by controlling pre-mRNA splicing of light- and clock-related genes. However, splicing factors that serve as repressors in phyB signaling pathway remain unreported. Here, we report that the splicing factor SWELLMAP 2 (SMP2) suppresses photomorphogenesis in the light. SMP2 physically interacts with phyB and colocalizes with phyB in photobodies after light exposure. Genetic analyses show that SMP2 antagonizes phyB signaling to promote hypocotyl elongation in the light. The homologs of SMP2 in yeast and human belong to second-step splicing factors required for proper selection of the 3' splice site (3'SS) of an intron. Notably, SMP2 reduces the abundance of the functional REVEILLE 8 a (RVE8a) form, probably by determining the 3'SS, and thereby inhibits RVE8-mediated transcriptional activation of clock genes containing evening elements (EE). Finally, SMP2-mediated reduction of functional RVE8 isoform promotes phytochrome interacting factor 4 (PIF4) expression to fine-tune hypocotyl elongation in the light. Taken together, our data unveil a phyB-interacting splicing factor that negatively regulates photomorphogenesis, providing additional information for further mechanistic investigations regarding phyB-controlled AS of light- and clock-related genes.

Highlights

As one of the most essential environmental factors for plants, light modulates various developmental processes of plants throughout their life cycles
We found that a protein called SWELLMAP 2 (SMP2), whose homolog Slu7/hSlu7 is a second-step splicing factor required for proper 3’ splice site selection (Frank and Guthrie, 1992; Chua and Reed, 1999; Clay and Nelson, 2005), interacted with C-terminal of phytochrome B (phyB)
We further performed co-IP assay using transgenic plant overexpressing YFP-SMP2 (Supplementary Figure 1), and the data show that endogenous phyB protein could be co-immunoprecipitated by YFP-SMP2 in red-light condition (Figure 1D), suggesting that phyB was associated with SMP2 in vivo

Summary

Introduction

As one of the most essential environmental factors for plants, light modulates various developmental processes of plants throughout their life cycles. While grown in the light, seedlings possess short hypocotyls, expanded cotyledons and developed chloroplasts. This seedling photomorphogenesis process is vital for the survival and autotrophic growth. Phytochromes harbor two functional modules: the N-terminal photosensory module (PSM) which perceives light through the chromophore, and the C-terminal output module (OPM) responsible for dimerization, nuclear localization as well as signal transduction (Cheng et al, 2021). Recent evidences have shown that phytochromes regulate alternative pre-mRNA splicing in response to red light (Shikata et al, 2014; Xin et al, 2017, 2019; Dong et al, 2020)

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Conclusion