Adverse interactions between micro-RNAs and target genes from different species

Tang, Tian; Kumar, Supriya; Shen, Yang; Lü, Jian; Wu, Mao-Lien; Shi, Suhua; Li, Wen-Hsiung; Wu, Chung‐I

doi:10.1073/pnas.1007591107

Cited by 36 publications

(42 citation statements)

References 43 publications

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“…S4). Phenotypic changes can be strong when "novel miRNAs" are introduced (46). Selection would favor a reduction in error rate in any miRNA as it becomes more highly expressed.…”

Section: Discussionmentioning

confidence: 99%

Testing hypotheses on the rate of molecular evolution in relation to gene expression using microRNAs

Shen

Huang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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There exists an inverse relationship between the rate of molecular evolution and the level of gene expression. Among the many explanations, the "toxic-error" hypothesis is a most general one, which posits that processing errors may often be toxic to the cells. However, toxic errors that constrain the evolution of highly expressed genes are often difficult to measure. In this study, we test the toxic-error hypothesis by using microRNA (miRNA) genes because their processing errors can be directly measured by deep sequencing. A miRNA gene consists of a small mature product (≈22 nt long) and a "backbone." Our analysis shows that (i) like the mature miRNA, the backbone is highly conserved; (ii) the rate of sequence evolution in the backbone is negatively correlated with expression; and (iii) although conserved between distantly related species, the error rate in miRNA processing is also negatively correlated with the expression level. The observations suggest that, as a miRNA gene becomes more highly (or more ubiquitously) expressed, its sequence evolves toward a structure that minimizes processing errors.evolutionary rate | microRNA biogenesis | microRNA evolution

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“…S4). Phenotypic changes can be strong when "novel miRNAs" are introduced (46). Selection would favor a reduction in error rate in any miRNA as it becomes more highly expressed.…”

Section: Discussionmentioning

confidence: 99%

Testing hypotheses on the rate of molecular evolution in relation to gene expression using microRNAs

Shen

Huang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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“…The reason for increased mRNA stability at the region close to the 5 ′ cap in genes without a miRNA target is unknown. One possible explanation is the dynamic gain and loss of miRNA target sites during animal evolution (Tang et al 2010;Xu et al 2013). Given the importance of mRNA secondary structure in miRNA-mediated gene regulation, the sequence of the 5 ′ end of 5 ′ UTRs should be strongly selected for increased mRNA stability when miRNA target sites newly occur in the 3 ′ UTR.…”

Section: Discussionmentioning

confidence: 99%

The role of RNA structure at 5′ untranslated region in microRNA-mediated gene regulation

Xie

et al. 2014

RNA

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Recent studies have suggested that the secondary structure of the 5 ′ untranslated region (5 ′ UTR) of messenger RNA (mRNA) is important for microRNA (miRNA)-mediated gene regulation in humans. mRNAs that are targeted by miRNA tend to have a higher degree of local secondary structure in their 5 ′ UTR; however, the general role of the 5 ′ UTR in miRNA-mediated gene regulation remains unknown. We systematically surveyed the secondary structure of 5 ′ UTRs in both plant and animal species and found a universal trend of increased mRNA stability near the 5 ′ cap in mRNAs that are regulated by miRNA in animals, but not in plants. Intra-genome comparison showed that gene expression level, GC content of the 5 ′ UTR, number of miRNA target sites, and 5 ′ UTR length may influence mRNA structure near the 5 ′ cap. Our results suggest that the 5 ′ UTR secondary structure performs multiple functions in regulating post-transcriptional processes. Although the local structure immediately upstream of the start codon is involved in translation initiation, RNA structure near the 5 ′ cap site, rather than the structure of the full-length 5 ′ UTR sequences, plays an important role in miRNA-mediated gene regulation.

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“…Although some miRNAs are remarkably highly conserved across species, the short sequence lengths and relatively straightforward requirements for processing give them the potential to evolve rapidly (Marco et al 2013). Moreover, their important roles in development make differences in miRNAs attractive potential causes of species-specific differences (Niwa and Slack 2007;Tang et al 2010), although examples of clear roles for miRNAs in speciation have yet to be described.…”

Section: Wwwgenomeorgmentioning

confidence: 99%

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Ren

et al. 2016

Genome Res.

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Hybrid incompatibility (HI) prevents gene flow between species, thus lying at the heart of speciation genetics. One of the most common HIs is male sterility. Two superficially contradictory observations exist for hybrid male sterility. First, an introgression on the X Chromosome is more likely to produce male sterility than on autosome (so-called large-X theory); second, spermatogenesis genes are enriched on the autosomes but depleted on the X Chromosome (demasculinization of X Chromosome). Analysis of gene expression in Drosophila hybrids suggests a genetic interaction between the X Chromosome and autosomes that is essential for male fertility. However, the prevalence of such an interaction and its underlying mechanism remain largely unknown. Here we examine the interaction in nematode species by contrasting the expression of both coding genes and transposable elements (TEs) between hybrid sterile males and its parental nematode males. We use two lines of hybrid sterile males, each carrying an independent introgression fragment from Caenorhabditis briggsae X Chromosome in an otherwise Caenorhabditis nigoni background, which demonstrate similar defects in spermatogenesis. We observe a similar pattern of down-regulated genes that are specific for spermatogenesis between the two hybrids. Importantly, the down-regulated genes caused by the X Chromosome introgressions show a significant enrichment on the autosomes, supporting an epistatic interaction between the X Chromosome and autosomes. We investigate the underlying mechanism of the interaction by measuring small RNAs and find that a subset of 22G RNAs specifically targeting the down-regulated spermatogenesis genes is significantly up-regulated in hybrids, suggesting that perturbation of small RNA-mediated regulation may contribute to the X-autosome interaction.

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Adverse interactions between micro-RNAs and target genes from different species

Cited by 36 publications

References 43 publications

Testing hypotheses on the rate of molecular evolution in relation to gene expression using microRNAs

Testing hypotheses on the rate of molecular evolution in relation to gene expression using microRNAs

The role of RNA structure at 5′ untranslated region in microRNA-mediated gene regulation

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

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