MicroRNAs and the evolution of complex multicellularity: identification of a large, diverse complement of microRNAs in the brown alga Ectocarpus.

James E. Tarver,Richard S. Taylor,Martina Strittmatter,Alexandre Cormier,Natalia Pinzón,Hervé Seitz,Susana M. Coelho,J. Mark Cock,Wilfrid Carré

doi:10.1093/nar/gkv578

Abstract

There is currently convincing evidence that microRNAs have evolved independently in at least six different eukaryotic lineages: animals, land plants, chlorophyte green algae, demosponges, slime molds and brown algae. MicroRNAs from different lineages are not homologous but some structural features are strongly conserved across the eukaryotic tree allowing the application of stringent criteria to identify novel microRNA loci. A large set of 63 microRNA families was identified in the brown alga Ectocarpus based on mapping of RNA-seq data and nine microRNAs were confirmed by northern blotting. The Ectocarpus microRNAs are highly diverse at the sequence level with few multi-gene families, and do not tend to occur in clusters but exhibit some highly conserved structural features such as the presence of a uracil at the first residue. No homologues of Ectocarpus microRNAs were found in other stramenopile genomes indicating that they emerged late in stramenopile evolution and are perhaps specific to the brown algae. The large number of microRNA loci in Ectocarpus is consistent with the developmental complexity of many brown algal species and supports a proposed link between the emergence and expansion of microRNA regulatory systems and the evolution of complex multicellularity.

Highlights

IntroductionMicroRNAs (miRNAs) are small, 20–24 nucleotide RNA molecules (exceptionally up to 26 nucleotides) that regulate gene expression by affecting the translation or the stability of target gene transcripts
MicroRNAs are small, 20–24 nucleotide RNA molecules that regulate gene expression by affecting the translation or the stability of target gene transcripts. These small RNA molecules are generated from the double stranded regions of hairpincontaining transcripts by the action of RNAseIII endonucleases such as Drosha and Dicer and are incorporated into RNA-induced silencing complexes (RISCs), which use the miRNAs as guides to recognize and bind to specific RNA targets. miRNAs have been shown to play key roles in the regulation of many important processes in both plants and animals [1,2] and it has been suggested that the acquisition of these versatile regulatory molecules may have been a key factor in the evolution of complex multicellularity [3,4,5]
After exclusion of reads corresponding to ribosomal RNA, transfer RNAs and small nucleolar RNAs, the highest coverage of mapped sRNA reads per base pair was for transposable elements (Table 1)

Summary

Introduction

MicroRNAs (miRNAs) are small, 20–24 nucleotide RNA molecules (exceptionally up to 26 nucleotides) that regulate gene expression by affecting the translation or the stability of target gene transcripts These small RNA molecules are generated from the double stranded regions of hairpincontaining transcripts by the action of RNAseIII endonucleases such as Drosha and Dicer and are incorporated into RNA-induced silencing complexes (RISCs), which use the miRNAs as guides to recognize and bind to specific RNA targets. Key components of the miRNA system, such as Dicer endonucleases and Argonaute (which is the central component of RISCs), are found in diverse eukaryotic lineages and are thought to be very ancient and perhaps common to all eukaryotes [10,11] These proteins are thought to have evolved originally as components of systems involving other classes of small RNA, such as the small interfering RNAs (siRNAs), and only later to have been recruited as components of miRNA pathways [9]. Like miRNAs, siRNAs are small RNA molecules generated by endonuclease digestion but they may be derived from diverse sources of double stranded RNA such as viral genomes,

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