Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications

Abstract

Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. Here we discuss some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome, which may represent an important source of robustness and evolvability.

The functions of long noncoding RNAs in development and stem cells

“…As reviewed in detail elsewhere (Kapusta and Feschotte, 2014;Ulitsky, 2016), and as touched upon above, studies suggest that lncRNAs evolve rapidly, with gains and losses occurring much more frequently than in other gene classes. This complicates the identification of homologs for study in model organisms.…”

“…Based on the criteria listed above, the human genome encodes tens of thousands of lncRNAs, as do the genomes of non-human primates, and at least thousands of lncRNAs are found in other vertebrate species. Large numbers of lncRNAs have also been found in every multicellular organism subjected to in-depth RNA-seq analysis, including vertebrates, insects, nematodes, sponges and plants (Kapusta and Feschotte, 2014;Ulitsky, 2016). Although there are no clear orthologous lncRNAs between these groups of species, there are some prominent similarities between them.…”

Long Noncoding RNAs in HPV-Induced Oncogenesis

“…In the past few years, an important component of ncRNA class has been studied: the long ncRNAs (lncRNAs) that are defined as RNAs longer than 200 nucleotides. 53 Strong evidences describe that human genome has more than 14000 lncRNA genes units, associated with the regulation of distinct mechanisms and harboring expression patterns depending on the cell type, developmental stage, or disease situation, such as cancer. [54][55][56][57] lncRNAs can regulate several processes in eukaryotic organisms, although most of their functions and biochemical properties are still unknown.…”

L’apophénie d’ENCODE ou Pangloss examine le génome humain

“…Il n'est pas étonnant qu'il soit entièrement transcrit, au moins à faible niveau. Le très fort taux de turnover de ces sites de fixation et de ces transcrits au cours de l'évolution, ainsi que la difficulté à leur trouver quelque fonction biologique, montrent qu'ils ne sont très vraisemblablement pas indispensables [34]. La petite taille des motifs reconnus par les facteurs de transcription explique très simplement la forte probabilité d'apparition d'un tel site dans un quelconque fragment d'ADN [16].…”