Evolution of the Small Family of Alternative Splicing Modulators Nuclear Speckle RNA-binding Proteins in Plants.

Leandro Lucero,Martín D Crespi,Fernando Ibañez,Federico Ariel,Jeremie Bazin,Johan Rodriguez Melo

doi:10.3390/genes11020207

Abstract

RNA-Binding Protein 1 (RBP1) was first identified as a protein partner of the long noncoding RNA (lncRNA) ENOD40 in Medicago truncatula, involved in symbiotic nodule development. RBP1 is localized in nuclear speckles and can be relocalized to the cytoplasm by the interaction with ENOD40. The two closest homologs to RBP1 in Arabidopsis thaliana were called Nuclear Speckle RNA-binding proteins (NSRs) and characterized as alternative splicing modulators of specific mRNAs. They can recognize in vivo the lncRNA ALTERNATIVE SPLICING COMPETITOR (ASCO) among other lncRNAs, regulating lateral root formation. Here, we performed a phylogenetic analysis of NSR/RBP proteins tracking the roots of the family to the Embryophytes. Strikingly, eudicots faced a reductive trend of NSR/RBP proteins in comparison with other groups of flowering plants. In Medicago truncatula and Lotus japonicus, their expression profile during nodulation and in specific regions of the symbiotic nodule was compared to that of the lncRNA ENOD40, as well as to changes in alternative splicing. This hinted at distinct and specific roles of each member during nodulation, likely modulating the population of alternatively spliced transcripts. Our results establish the basis to guide future exploration of NSR/RBP function in alternative splicing regulation in different developmental contexts along the plant lineage.

Highlights

RNA-binding proteins (RBPs) participate in the control of gene expression at every step after transcription, including Alternative Splicing (AS), silencing, RNA decay, and translational control [1].In Arabidopsis thaliana, several hundreds of proteins have been predicted to bind RNAs [2]
In order to explore the evolutionary relationships of Nuclear Speckle RNA-binding proteins (NSRs) proteins in plants, inferred through phylogenetic analysis, we first used Arabidopsis thaliana NSRa and NSRb protein sequences as queries to perform BLASTP searches against Chlorophyte and Embryophyte available genomes (Supplementary Table S1)
No hits were obtained in the basal Embriophyte species Physcomitrella patens and Sphagnum fallax, but four NSRs genes were identified in the genome of the Bryophyte Marchantia polymorpha (Supplementary Table S1)

Summary

Introduction

RNA-binding proteins (RBPs) participate in the control of gene expression at every step after transcription, including Alternative Splicing (AS), silencing, RNA decay, and translational control [1].In Arabidopsis thaliana, several hundreds of proteins have been predicted to bind RNAs [2]. RNA binding proteins (NSRs) are a family of RBPs that act as regulators of AS and auxin-regulated developmental processes such as lateral root formation in Arabidopsis thaliana [3]. These proteins were shown to interact with some of their alternatively spliced mRNA targets and with a structured noncoding. Overexpression of ASCO was shown to affect AS of a subset of mRNA regulated by NSRs, in a similar manner as in nsra/b double mutants, and ASCO was shown to compete in vitro with the binding of one AS mRNA target These observations led to proposing that plant lncRNAs are able to modulate AS by hijacking RBPs such as NSRs [4]. A genome-wide analysis was performed to monitor the global role of NSRs in RNA processing and AS, as well as the direct interacting mRNAs of NSRs [5]

Methods

Results

Conclusion