MicroRNA Gene Evolution in Arabidopsis lyrata and Arabidopsis thaliana

Noah Fahlgren,Lisa M Smith,Kristin D Kasschau,James C Carrington,Sanjuro Jogdeo,Scott A Givan,Elisabeth J Chapman,Christopher M Sullivan,Sascha Laubinger,Mark Dasenko,Detlef Weigel

doi:10.1105/tpc.110.073999

Noah Fahlgren, Lisa M Smith + Show 9 more

Open Access

https://doi.org/10.1105/tpc.110.073999

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Abstract

MicroRNAs (miRNAs) are short regulatory RNAs processed from partially self-complementary foldbacks within longer MIRNA primary transcripts. Several MIRNA families are conserved deeply through land plants, but many are present only in closely related species or are species specific. The finding of numerous evolutionarily young MIRNA, many with low expression and few if any targets, supports a rapid birth-death model for MIRNA evolution. A systematic analysis of MIRNA genes and families in the close relatives, Arabidopsis thaliana and Arabidopsis lyrata, was conducted using both whole-genome comparisons and high-throughput sequencing of small RNAs. Orthologs of 143 A. thaliana MIRNA genes were identified in A. lyrata, with nine having significant sequence or processing changes that likely alter function. In addition, at least 13% of MIRNA genes in each species are unique, despite their relatively recent speciation (approximately 10 million years ago). Alignment of MIRNA foldbacks to the Arabidopsis genomes revealed evidence for recent origins of 32 families by inverted or direct duplication of mostly protein-coding gene sequences, but less than half of these yield miRNA that are predicted to target transcripts from the originating gene family. miRNA nucleotide divergence between A. lyrata and A. thaliana orthologs was higher for young MIRNA genes, consistent with reduced purifying selection compared with deeply conserved MIRNA genes. Additionally, target sites of younger miRNA were lost more frequently than for deeply conserved families. In summary, our systematic analyses emphasize the dynamic nature of the MIRNA complement of plant genomes.

Highlights

MicroRNA are a class of small RNA encoded in the genomes of plants, animals, algae, some other unicellular organisms, and many DNA viruses (Carthew and Sontheimer, 2009; Cullen, 2009; Voinnet, 2009)
What are the rates of gain and loss of young MIRNA genes in the Arabidopsis lineage? It is difficult to measure birth and death rates directly because the presence and absence of a gene in two extant species could be interpreted as a gain in one or a loss in the other
In some cases the presence of the gene in an outgroup species parsimoniously indicates that the gene was lost in one lineage, as was the case with several MIRNA found in C. rubella and either A. thaliana (MIR830 and MIR865) or A. lyrata (MIR395g and h, MIR399g-I, and MIR3435)

Summary

Introduction

MicroRNA (miRNA) are a class of small RNA encoded in the genomes of plants, animals, algae, some other unicellular organisms, and many DNA viruses (Carthew and Sontheimer, 2009; Cullen, 2009; Voinnet, 2009). Evidence of extensive sequence similarity between foldback sequences and proteincoding loci was found for several young Arabidopsis MIRNA genes, suggesting that MIRNA can form by inverted duplication events (Allen et al, 2004; Rajagopalan et al, 2006; Axtell et al, 2007; Fahlgren et al, 2007). These MIRNA would have a high degree of complementarity to the parental locus and, if expressed, could produce small RNA that target the parental transcript. The inverted repeats found in some classes of transposable elements could be the raw material for hairpin RNA that, if processed, might generate small RNA that target similar repetitive sequences integrated into transcribed genes (Smalheiser and Torvik, 2005, 2006; Piriyapongsa and Jordan, 2007; Piriyapongsa et al, 2007)

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