Differential nucleosome occupancy modulates alternative splicing in Arabidopsis thaliana.

Ibtissam Jabre,Maria Kalyna,Naeem H. Syed,Weizhong Chen,Cornelia Wilson,Wenbin Guo,Saurabh Chaudhary,Runxuan Zhang,Anireddy S. N. Reddy

doi:10.1111/nph.17062

Abstract

Alternative splicing (AS) is a major gene regulatory mechanism in plants. Recent evidence supports co-transcriptional splicing in plants, hence the chromatin state can impact AS. However, how dynamic changes in the chromatin state such as nucleosome occupancy influence the cold-induced AS remains poorly understood. Here, we generated transcriptome (RNA-Seq) and nucleosome positioning (MNase-Seq) data for Arabidopsis thaliana to understand how nucleosome positioning modulates cold-induced AS. Our results show that characteristic nucleosome occupancy levels are strongly associated with the type and abundance of various AS events under normal and cold temperature conditions in Arabidopsis. Intriguingly, exitrons, alternatively spliced internal regions of protein-coding exons, exhibit distinctive nucleosome positioning pattern compared to other alternatively spliced regions. Likewise, nucleosome patterns differ between exitrons and retained introns, pointing to their distinct regulation. Collectively, our data show that characteristic changes in nucleosome positioning modulate AS in plants in response to cold.

Highlights

Plants employ different strategies to control their transcriptional program during the daily cycles of light-dark and in response to environmental stress to confer adaptive responses (Zhu, 2016; Laloum et al, 2017; Lämke & Bäurle, 2017)
Our results show that characteristic nucleosome occupancy levels are strongly associated with the type and abundance of various Alternative splicing (AS) events under normal and cold temperature conditions in Arabidopsis
Nucleosome patterns differ between exitrons and retained introns pointing to their distinct regulation

Summary

Introduction

Plants employ different strategies to control their transcriptional program during the daily cycles of light-dark and in response to environmental stress to confer adaptive responses (Zhu, 2016; Laloum et al, 2017; Lämke & Bäurle, 2017). Emerging evidence shows that the chromatin environment has a strong bearing on the splicing process by modulating RNAPII processivity and splicing factors (SFs) recruitment (Nojima et al, 2018; Jabre et al, 2019; Kindgren et al, 2019; Li et al, 2020; Yu et al, 2019; Zhu et al, 2020). RNAi lines of a chromatin remodeler gene (ZmCHB101) in maize showed altered nucleosome density, RNAPII elongation rate, and changes in splicing patterns under osmotic stress (Yu et al, 2019). Since cold can influence the RNAPII elongation kinetics in Arabidopsis (Kindgren et al, 2019), we reasoned that rapid cold-induced alternative splicing response in Arabidopsis (Calixto et al, 2018) may be associated with nucleosome remodelling.

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Discussion

Conclusion