MicroRNAs are deeply linked to the emergence of the complex octopus brain

Zolotarov, Grygoriy; Fromm, Bastian; Legnini, Ivano; Ayoub, Salah; Polese, Gianluca; Maselli, Valeria; Chabot, Peter J.; Vinther, Jakob; Styfhals, Ruth; Seuntjens, Eve; Cosmo, Anna Di; Peterson, Kevin J.; Rajewsky, Nikolaus

doi:10.1101/2022.02.15.480520

Cited by 4 publications

(4 citation statements)

References 48 publications

(60 reference statements)

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“…This is due to the fact that the required syntenic information is often not available and not currently analyzed by our pipeline. Furthermore, MirMachine does not predict species specific microRNAs which can play crucial roles in evolution (Zolotarov et al, 2022). MirMachine predictions are a solid foundation for future smallRNAseq driven annotation efforts of novel microRNAs and synteny-supported annotation of paralogues and orthologues.…”

Section: Discussionmentioning

confidence: 99%

“…Very few of these species have been annotated for microRNAs, or have small RNA sequencing data published, thus, comparatively little progress has been made on the suggested microRNA applications (but see (Fromm et al, 2013; Peterson et al, 2021; Wheeler et al, 2009; Zolotarov et al, 2022) for examples using manual curation). This discrepancy persists because, among other things, no reliable in silico method currently exists to annotate conserved or species-specific microRNA complements from genomic references only.…”

Section: Introductionmentioning

confidence: 99%

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Accurate microRNA annotation of animal genomes using trained covariance models of curated microRNA complements in MirMachine

Umu

Trondsen

Paynter

et al. 2022

Preprint

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Understanding the evolution of organismic complexity and the genomic basis of gene-regulation is one of the main challenges in the postgenomic era. While thousands of new genomes are available today, no accurate methods exist to reliably mine those for microRNAs, an important class of post-transcriptional regulators. Currently, their prediction and annotation depend on the availability of transcriptomics data sets and hands-on expert knowledge leading to the large discrepancy between novel genomes made available and the availability of high-quality microRNA complements. Using the more than 16,000 microRNA entries from the manually curated microRNA gene database MirGeneDB, we generated and trained covariance models for each conserved microRNA family. These models are available in MirMachine, our new pipeline for automated annotation of conserved microRNAs. We show that MirMachine can be used to accurately and precisely predict conserved microRNA complements from genome assemblies, correctly identifying the number of paralogues, and by establishing the novel microRNA score, the completeness of assemblies. Built and trained on representative metazoan microRNA complements, we used MirMachine on a wide range of animal species, including those with very large genomes or additional genome duplications and extinct species such as mammoths, where deep small RNA sequencing data will be hard to produce. With accurate predictions of conserved microRNAs, the MirMachine workflow closes a long-persisting gap in the microRNA field that will not only facilitate automated genome annotation pipelines and can serve as a solid foundation for manual curation efforts, but deeper studies on the evolution of genome regulation, even in extinct organisms. MirMachine is freely available (https://github.com/sinanugur/MirMachine) and also implemented as a web application (www.mirmachine.org).

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Accurate microRNA annotation of animal genomes using trained covariance models of curated microRNA complements in MirMachine

Umu

Trondsen

Paynter

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

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“…Since many miRNAs have evolved through duplication and diversification [ 73 , 75 ], it is tempting to speculate that alternative processing of newly duplicated miRNA loci could contribute to evolution of new miRNAs. Establishment of a previously inabundant 5’ end isomiR as a new dominant miRNA isoform with a new seed could expose new sets of genes to repressive miRNA regulation.…”

Section: Discussionmentioning

confidence: 99%

Global profiling and annotation of templated isomiRs dynamics across Caenorhabditis elegans development

Panzade

Hebbar

et al. 2022

RNA Biology

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microRNAs (miRNAs) are small non-coding RNAs that regulate gene expression through translational repression and mRNA destabilization. During canonical miRNA biogenesis, several miRNA isoforms, or isomiRs, are produced from a single precursor miRNA. Templated isomiRs are generated through Drosha or Dicer cleavage at alternate positions on either the primary or the precursor miRNAs, generating truncated or extended 5’ and/or 3’ miRNA ends. As changes to the mature miRNA sequence can alter miRNA gene target repertoire, we investigated the extent of templated isomiR prevalence, providing a profiling map for templated isomiRs across stages of C. elegans development. While most miRNA loci did not produce abundant templated isomiRs, a substantial number of miRNA loci produced isomiRs were just as, or more, abundant than their annotated canonical mature miRNAs. 3’ end miRNA alterations were more frequent than the seed-altering 5’ end extensions or truncations. However, we identified several miRNA loci that produced a considerable amount of isomiRs with 5’ end alterations, predicted to target new, distinct sets of genes. Overall, the presented annotation of templated isomiR dynamics across C. elegans developmental stages provides a basis for further studies into miRNA biogenesis and the intriguing potential of functional miRNA diversification through isomiR production.

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“…This lack of correlation indicates a combinatorial, or regulatory origin of cellular complexity and it has been proposed to originate in the non-coding part of genomes (Taft et al, 2007). Indeed, the advent of novel microRNAs, ~22 nucleotide short non-coding post-transcriptional gene regulators (Bartel, 2018), strongly correlates both with increasing complexity as found in several metazoan clades including vertebrates and cephalopod mollusks (Deline et al, 2018;Grimson et al, 2008;Heimberg et al, 2008;Sempere et al, 2006;Tanzer & Stadler, 2006;Wheeler et al, 2009;Zolotarov et al, 2022). Their loss also accompanies morphological simplification as seen in, for example, parasitic species (Fromm et al, 2013).…”

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confidence: 99%

Direct observation of the evolution of cell-type specific microRNA expression signatures supports the hematopoietic origin model of endothelial cells

Jenike

Peterson

et al. 2022

Preprint

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The evolution of specialized cell-types is a long-standing interest of biologists but given the deep time-scales very difficult to reconstruct or observe. microRNAs have been linked to the evolution of cellular complexity and may inform on specialization. The endothelium is a vertebrate specific specialization of the circulatory system that enabled a critical new level of vasoregulation. The evolutionary origin of these endothelial cells is unclear. We hypothesized that Mir-126, an endothelial cell-specific microRNA may be informative. We here reconstruct the evolutionary history of Mir-126. Mir-126 likely appeared in the last common ancestor of vertebrates and tunicates, a species without an endothelium, within an intron of the evolutionary much older EGF Like Domain Multiple (Egfl) locus. Mir-126 has a complex evolutionary history due to duplications and losses of both the host gene and the microRNA. Taking advantage of the strong evolutionary conservation of the microRNA among Olfactores, and using RNA in situ hybridization (RISH), we localized Mir-126 in the tunicate Ciona robusta. We found exclusive expression of the mature Mir-126 in granular amebocytes, supporting a long-proposed scenario that endothelial cells arose from hemoblasts, a type of proto-endothelial amoebocyte found throughout invertebrates. This observed change of expression of Mir-126 from proto-endothelial amoebocytes in the tunicate to endothelial cells in vertebrates is the first direct observation of the evolution of a cell-type in relation to microRNA expression indicating that microRNAs can be a prerequisite of cell-type evolution.

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MicroRNAs are deeply linked to the emergence of the complex octopus brain

Cited by 4 publications

References 48 publications

Accurate microRNA annotation of animal genomes using trained covariance models of curated microRNA complements in MirMachine

Accurate microRNA annotation of animal genomes using trained covariance models of curated microRNA complements in MirMachine

Global profiling and annotation of templated isomiRs dynamics across Caenorhabditis elegans development

Direct observation of the evolution of cell-type specific microRNA expression signatures supports the hematopoietic origin model of endothelial cells

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