Abstract

Alternative pre-mRNA splicing (AS) is prevalent in plants and is involved in many interactions between plants and environmental stresses. However, the patterns and underlying mechanisms of AS evolution in plants remain unclear. By analyzing the transcriptomes of four eudicot species, we revealed that the divergence of AS is largely due to the gains and losses of AS events among orthologous genes. Furthermore, based on a subset of AS, in which AS can be directly associated with specific transcripts, we found that AS that generates transcripts containing premature termination codons (PTC), are likely more conserved than those that generate non-PTC containing transcripts. This suggests that AS coupled with nonsense-mediated decay (NMD) might play an important role in affecting mRNA levels post-transcriptionally. To understand the mechanisms underlying the divergence of AS, we analyzed the key determinants of AS using a machine learning approach. We found that the presence/absence of alternative splice site (SS) within the junction, the distance between the authentic SS and the nearest alternative SS, the size of exon–exon junctions were the major determinants for both alternative 5′ donor site and 3′ acceptor site among the studied species, suggesting a relatively conserved AS mechanism. The comparative analysis further demonstrated that variations of the identified AS determinants significantly contributed to the AS divergence among closely related species in both Solanaceae and Brassicaceae taxa. Together, these results provide detailed insights into the evolution of AS in plants.

Highlights

  • Due to their sessile lifestyle, plants have evolved various mechanisms to respond to environmental stresses

  • To provide an overview of Alternative pre-mRNA splicing (AS) evolution among different plant families, we studied the genome-wide AS in A. thaliana, soybean (Glycine max), tomato (Solanum lycopersicum), and wild tobacco (N. attenuata), from which comparable transcriptomic datasets are available from the same tissues and they represent a wide-range of eudicots

  • More than 75% of the splice junctions that were identified from the full dataset can be detected from these randomly selected 17 million uniquely mapped reads (Supplementary Figure S3A), indicating the 17M reads is sufficient to reveal the AS evolution pattern among species

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Summary

Introduction

Due to their sessile lifestyle, plants have evolved various mechanisms to respond to environmental stresses. Alternative splicing (AS), a mechanism by which different mature RNAs are formed by removing different introns or using different splice sites (SS) from the same pre-mRNA, is known to be important for stress-induced responses in plants (Mastrangelo et al, 2012; Staiger and Brown, 2013) Both biotic and abiotic stresses such as herbivores (Ling et al, 2015), pathogens (Howard et al, 2013), and cold and salt (Ding et al, 2014) can all induce genome-wide changes in AS in plants. The strong association between AS and environmental stimuli suggests that AS is involved in adaptation processes and may have evolved rapidly

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