Endogenous Small-Noncoding RNAs and Potential Functions in Desiccation Tolerance in Physcomitrella Patens

Jing Xia,Weixiong Zhang,Xiaoqin Wang,Ralph Quatrano,Yikun He,Pierre-François Perroud

doi:10.1038/srep30118

Abstract

Early land plants like moss Physcomitrella patens have developed remarkable drought tolerance. Phytohormone abscisic acid (ABA) protects seeds during water stress by activating genes through transcription factors such as ABSCISIC ACID INSENSITIVE (ABI3). Small noncoding RNA (sncRNA), including microRNAs (miRNAs) and endogenous small-interfering RNAs (endo-siRNAs), are key gene regulators in eukaryotes, playing critical roles in stress tolerance in plants. Combining next-generation sequencing and computational analysis, we profiled and characterized sncRNA species from two ABI3 deletion mutants and the wild type P. patens that were subject to ABA treatment in dehydration and rehydration stages. Small RNA profiling using deep sequencing helped identify 22 novel miRNAs and 6 genomic loci producing trans-acting siRNAs (ta-siRNAs) including TAS3a to TAS3e and TAS6. Data from degradome profiling showed that ABI3 genes (ABI3a/b/c) are potentially regulated by the plant-specific miR536 and that other ABA-relevant genes are regulated by miRNAs and ta-siRNAs. We also observed broad variations of miRNAs and ta-siRNAs expression across different stages, suggesting that they could potentially influence desiccation tolerance. This study provided evidence on the potential roles of sncRNA in mediating desiccation-responsive pathways in early land plants.

Highlights

Land plants such as moss Physcomitrella patens have developed remarkable drought tolerance for survival, whereas modern vascular plants have only retained drought tolerance in a few specialized tissues like seeds and spores[1]
abscisic acid (ABA) is a potent regulator of abiotic stress signaling in plants including moss, and ABA pretreatment is required for moss (P. patens) to confer desiccation tolerance[31]
Our results showed that the miR536 family functioned as regulators of the ABI3 genes on the ABA signaling pathway

Summary

Introduction

Land plants such as moss Physcomitrella patens have developed remarkable drought tolerance for survival, whereas modern vascular plants have only retained drought tolerance in a few specialized tissues like seeds and spores[1]. ABA activates genes that have stress-tolerance functions through transcription factors such as ABSCISIC ACID INSENSITIVE 3 (ABI3)[6]. It has been shown that miRNAs play important roles in gene regulation in response to ABA treatment in plants. In P. patens, miRNAs have been shown to induce hypermethylation of their target genes and consequential transcriptional silencing upon ABA treatment[23]. ABA-induced accumulation of miR1026 subsequently leads to hypermethylation and down-regulation of the PpbHLH gene, indicating that miRNAs function in epigenetic control of stress-responsive genes[23]. Like miRNAs, endo-siRNAs in plants play important roles in gene regulation. We identified novel miRNAs and endo-siRNAs derived from long hairpin RNAs, miRNA-cleaved transcripts, and putative target genes of small RNAs by investigating data from degradome profiling of P. patens. Differential expression analyses revealed a broad alteration of small RNA expressions across different conditions, indicating the involvement of small RNAs in the plant’s adaptation to dynamic environmental changes

Methods

Results

Conclusion