Abstract
The regulation of gene expression is of fundamental importance to maintain organismal function and integrity and requires a multifaceted and highly ordered sequence of events. The cyclic nature of gene expression is known as ‘transcription dynamics'. Disruption or perturbation of these dynamics can result in significant fitness costs arising from genome instability, accelerated ageing and disease. We review recent research that supports the idea that an important new role for small RNAs, particularly microRNAs (miRNAs), is in protecting the genome against short-term transcriptional fluctuations, in a process we term ‘microguarding'. An additional emerging role for miRNAs is as ‘micromessengers'—through alteration of gene expression in target cells to which they are trafficked within microvesicles. We describe the scant but emerging evidence that miRNAs can be moved between different cells, individuals and even species, to exert biologically significant responses. With these two new roles, miRNAs have the potential to protect against deleterious gene expression variation from perturbation and to themselves perturb the expression of genes in target cells. These interactions between cells will frequently be subject to conflicts of interest when they occur between unrelated cells that lack a coincidence of fitness interests. Hence, there is the potential for miRNAs to represent both a means to resolve conflicts of interest, as well as instigate them. We conclude by exploring this conflict hypothesis, by describing some of the initial evidence consistent with it and proposing new ideas for future research into this exciting topic.
Highlights
Small RNAs, RNA silencing and microRNA biogenesis Small RNAs are a diverse set of functional, non-coding RNA molecules that are key regulators of expression for many genes in the genome via the process of gene silencing (Bartel and Chen, 2004; Hall and Dalmay, 2013)
These precursors can be transcripts of small RNA genes, pre-messenger RNAs, tRNAs, small nucleolar RNAs and YRNAs
Small RNAs may be cleaved in a sequence- and structure-specific manner from parent RNAs such as YRNAs and tRNAs, with the latter tRNA-derived small RNAs entering RNA-mediated gene silencing pathways (Kumar et al, 2014)
Summary
The regulation of gene expression is of fundamental importance to maintain organismal function and integrity and requires a multifaceted and highly ordered sequence of events. We describe the scant but emerging evidence that miRNAs can be moved between different cells, individuals and even species, to exert biologically significant responses. With these two new roles, miRNAs have the potential to protect against deleterious gene expression variation from perturbation and to themselves perturb the expression of genes in target cells. These interactions between cells will frequently be subject to conflicts of interest when they occur between unrelated cells that lack a coincidence of fitness interests. Heredity (2016) 116, 125–134; doi:10.1038/hdy.2015.84; published online 30 September 2015
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