The expansion of the metazoan microRNA repertoire

Hertel, Jana; Lindemeyer, Manuela; Missal, Kristin; Fried, Claudia; Tanzer, Andrea; Hofacker, Ivo L.; Stadler, Peter F.

doi:10.1186/1471-2164-7-25

Cited by 316 publications

(245 citation statements)

References 71 publications

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“…Remarkably, the rate of miRNA family gain accelerated significantly in the therian lineage, leading to substantially larger miRNA family repertoires in extant therian species. Previous attempts to assess miRNA expansions did not uncover this expansion due to noncomparable and limited data (Hertel et al 2006). The therian rate increase might be associated, for example, with the evolution of new developmental programs in therians (e.g., the switch from egg-laying to a lifebearing reproductive mode).…”

Section: Discussionmentioning

confidence: 99%

Birth and expression evolution of mammalian microRNA genes

et al. 2012

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MicroRNAs (miRNAs) are major post-transcriptional regulators of gene expression, yet their origins and functional evolution in mammals remain little understood due to the lack of appropriate comparative data. Using RNA sequencing, we have generated extensive and comparable miRNA data for five organs in six species that represent all main mammalian lineages and birds (the evolutionary outgroup) with the aim to unravel the evolution of mammalian miRNAs. Our analyses reveal an overall expansion of miRNA repertoires in mammals, with threefold accelerated birth rates of miRNA families in placentals and marsupials, facilitated by the de novo emergence of miRNAs in host gene introns. Generally, our analyses suggest a high rate of miRNA family turnover in mammals with many newly emerged miRNA families being lost soon after their formation. Selectively preserved mammalian miRNA families gradually evolved higher expression levels, as well as altered mature sequences and target gene repertoires, and were apparently mainly recruited to exert regulatory functions in nervous tissues. However, miRNAs that originated on the X chromosome evolved high expression levels and potentially diverse functions during spermatogenesis, including meiosis, through selectively driven duplicationdivergence processes. Overall, our study thus provides detailed insights into the birth and evolution of mammalian miRNA genes and the associated selective forces.

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Section: Discussionmentioning

confidence: 99%

Birth and expression evolution of mammalian microRNA genes

et al. 2012

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“…As a key component in virtually all gene regulatory networks they are deeply linked to lineage-specific adaptations and morphological innovations (Heimberg et al, 2008;Tarver et al, 2013). A least in the Metazoa they fall into hundreds of groups of evolutionarily unrelated groups (Kozomara and Griffiths-Jones, 2014) that in most cases originated de novo from transcribed regions (Hertel et al, 2006;Prochnik et al, 2007). They have been advocated as excellent, nearly homoplasyfree genetic markers and have been claimed to resolve several clades in the ToL (Wheeler et al, 2009;Campo-Paysaa et al, 2011).…”

Section: Micrornasmentioning

confidence: 99%

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

et al. 2016

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Our understanding of the early evolution of animals will be greatly improved if a final solution can be found to the evolutionary relationships between Porifera, Placozoa, Ctenophora, Cnidaria, and Bilateria. There have been many recent attempts to solve this key issue at the base of the metazoan tree of life, and these have sparked heated discussions and highlighted fundamental analytical problems. We argue that solving this problem will necessitate analysis of disparate data types, including phylogenomic data, larger scale genomic characters, developmental data, and morphological characters. At the least, morphological and developmental data must be used to cross-validate phylogenomic conclusions, but ideally solutions should be sought to the problems of combining disparate data sources with appropriate character weighting and algorithm choice.

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“…In addition, Zuckerkandl (1992) notes that Kimura's selectively neutral mutations are selectively equivalent and thus do not preclude them being functional. The first few hundred miRNAs to be discovered are highly conserved ), but hundreds of more recently discovered miRNAs are not, being lineage-or even species-specific (Berezikov et al 2006a,b;Piriyapongsa and Jordan 2007;) and expanding in the mammalian lineage (Hertel et al 2006). There are also thousands of recently discovered small RNAs (piRNAs) expressed in testis that are not conserved between mouse and other species (Aravin et al 2006;Girard et al 2006;Lau et al 2006).…”

Section: Different Rates Of Evolution Of Functional Sequencesmentioning

confidence: 99%

Raising the estimate of functional human sequences: Figure 1.

Pheasant¹,

Mattick²

2007

Genome Res.

222

170

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While less than 1.5% of the mammalian genome encodes proteins, it is now evident that the vast majority is transcribed, mainly into non-protein-coding RNAs. This raises the question of what fraction of the genome is functional, i.e., composed of sequences that yield functional products, are required for the expression (regulation or processing) of these products, or are required for chromosome replication and maintenance. Many of the observed noncoding transcripts are differentially expressed, and, while most have not yet been studied, increasing numbers are being shown to be functional and/or trafficked to specific subcellular locations, as well as exhibit subtle evidence of selection. On the other hand, analyses of conservation patterns indicate that only ∼5% (3%-8%) of the human genome is under purifying selection for functions common to mammals. However, these estimates rely on the assumption that reference sequences (usually ancient transposon-derived sequences) have evolved neutrally, which may not be the case, and if so would lead to an underestimate of the fraction of the genome under evolutionary constraint. These analyses also do not detect functional sequences that are evolving rapidly and/or have acquired lineage-specific functions. Indeed, many regulatory sequences and known functional noncoding RNAs, including many microRNAs, are not conserved over significant evolutionary distances, and recent evidence from the ENCODE project suggests that many functional elements show no detectable level of sequence constraint. Thus, it is likely that much more than 5% of the genome encodes functional information, and although the upper bound is unknown, it may be considerably higher than currently thought.

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The expansion of the metazoan microRNA repertoire

Cited by 316 publications

References 71 publications

Birth and expression evolution of mammalian microRNA genes

Birth and expression evolution of mammalian microRNA genes

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

Raising the estimate of functional human sequences: Figure 1.

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