Abstract
While DNA methylation carries genetic signals and is instrumental in the evolution of organismal complexity, small RNAs (sRNAs), ~18–24 ribonucleotide (nt) sequences, are crucial mediators of methylation as well as gene silencing. However, scant study deals with sRNA evolution via featuring their expression dynamics coupled with species of different evolutionary time. Here we report an atlas of sRNAs and microRNAs (miRNAs, single-stranded sRNAs) produced over time at seed-set of two major spermatophytes represented by populations of Picea glauca and Arabidopsis thaliana with different seed-set duration. We applied diverse profiling methods to examine sRNA and miRNA features, including size distribution, sequence conservation and reproduction-specific regulation, as well as to predict their putative targets. The top 27 most abundant miRNAs were highly overlapped between the two species (e.g., miR166,−319 and−396), but in P. glauca, they were less abundant and significantly less correlated with seed-set phases. The most abundant sRNAs in libraries were deeply conserved miRNAs in the plant kingdom for Arabidopsis but long sRNAs (24-nt) for P. glauca. We also found significant difference in normalized expression between populations for population-specific sRNAs but not for lineage-specific ones. Moreover, lineage-specific sRNAs were enriched in the 21-nt size class. This pattern is consistent in both species and alludes to a specific type of sRNAs (e.g., miRNA, tasiRNA) being selected for. In addition, we deemed 24 and 9 sRNAs in P. glauca and Arabidopsis, respectively, as sRNA candidates targeting known adaptive genes. Temperature had significant influence on selected gene and miRNA expression at seed development in both species. This study increases our integrated understanding of sRNA evolution and its potential link to genomic architecture (e.g., sRNA derivation from genome and sRNA-mediated genomic events) and organismal complexity (e.g., association between different sRNA expression and their functionality).
Highlights
Epigenetic mechanisms exert functional roles in the upper dimension of gene regulatory networks (GRNs) and are more important to the transcription machinery than have hitherto been thought
This study accentuated that roles of small RNAs (sRNAs) in phenotypic variation are canalized at the reproductive period and coupled with species of different evolutionary time, which, metaphorically like writing on a palimpsest for the generation, sets molecular imprinting on phenotypes that will be expressed in the adult stage for local adaptation
Notwithstanding deeply conserved miRNA families play an important role across a plurality of plants, few studies isolate conserved miRNAs and sRNAs to comparatively uncover the frequent presence and absence of sRNAs in large quantities and its evolutionary significance shaped by natural selection
Summary
Epigenetic mechanisms exert functional roles in the upper dimension of gene regulatory networks (GRNs) and are more important to the transcription machinery than have hitherto been thought. Myriad MIRNAs (miRNA genes) are expanded but unrevealed (Fattash et al, 2007; Nozawa et al, 2012), or young MIRNAs are spawned, weakly expressed and eventually frequently lost (Fahlgren et al, 2007). This indicates that lineage-specific miRNAs have undergone rapid turnover in evolution (e.g., 1.2–3.3 genes per Myr in Arabidopsis, Fahlgren et al, 2010) and MIRNAs evolve adaptively, possibly driven by positive selection. Duplication of MIRNAs, especially those from whole-genome duplication (WGD), may be conducive to miRNA diversity and their regulatory complexity (Maher et al, 2006; Vanneste et al, 2014), indicative of coevolution of MIRNAs, miRNAs and their targets in the context of WGD events (or genome evolution)
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