Dosage-sensitive miRNAs trigger modulation of gene expression during genomic imbalance in maize

Abstract

The genomic imbalance caused by varying the dosage of individual chromosomes or chromosomal segments (aneuploidy) has more detrimental effects than altering the dosage of complete chromosome sets (ploidy). Previous analysis of maize (Zea mays) aneuploids revealed global modulation of gene expression both on the varied chromosome (cis) and the remainder of the genome (trans). However, little is known regarding the role of microRNAs (miRNAs) under genomic imbalance. Here, we report the impact of aneuploidy and polyploidy on the expression of miRNAs. In general, cis miRNAs in aneuploids present a predominant gene-dosage effect, whereas trans miRNAs trend toward the inverse level, although other types of responses including dosage compensation, increased effect, and decreased effect also occur. By contrast, polyploids show less differential miRNA expression than aneuploids. Significant correlations between expression levels of miRNAs and their targets are identified in aneuploids, indicating the regulatory role of miRNAs on gene expression triggered by genomic imbalance.

MicroRNAs play regulatory roles in genomic balance

“…To address this question, global miRNA expression levels in the maize mature leaf tissue of a collection of maize aneuploid series containing various copies of chromosomal segments covering 82.1% of the maize W22 genome were examined in a recent study. [ 73–76 ] miRNAs for each aneuploid were partitioned into ones that are present on the varied chromosomal segment ( cis ) versus ones that are located in the remainder of the genome ( trans ). By comparing the miRNA expression levels in aneuploidy with the respective diploid or haploid control, the results showed that aneuploidy causes altered miRNA expression both in cis and in trans .…”

“…By comparing the miRNA expression levels in aneuploidy with the respective diploid or haploid control, the results showed that aneuploidy causes altered miRNA expression both in cis and in trans . [ 76 ] While the global trend of cis miRNA modulation could hardly be examined due to the limited number of cis miRNAs, trans miRNAs in different aneuploids exhibited a predominant trend of modulation toward the inverse level when assayed globally, although both positive and negative modulations were observed. In addition, results of differential miRNA expression analysis comparing tetrasomy to trisomy demonstrated that there are progressive cis and trans effects on a subset of miRNAs in aneuploids, with greater chromosomal dosage producing greater effects.…”

“…In addition, results of differential miRNA expression analysis comparing tetrasomy to trisomy demonstrated that there are progressive cis and trans effects on a subset of miRNAs in aneuploids, with greater chromosomal dosage producing greater effects. [ 76 ]…”

“…In addition, a trend of varied miRNA modulation is not detectable from triploids and tetraploids. [ 76 ]…”

“…By quantifying the expression of individual miRNAs in the aneuploidy and ploidy series and performing differential miRNA expression analysis, it was found that a gene‐dosage effect is the plurality trend for individual cis DEM (differentially expressed miRNAs) expression with varied chromosomal dosage whereas other types of responses such as dosage compensation and negative dosage effect were also observed (Figure 1). [ 76 ] In rare conditions, a nonlinear correlation was found between expression levels of cis DEMs and the chromosomal dosage, with miRNA expression modulated toward the same direction in aneuploids compared with the control regardless of increased or decreased chromosomal dosage. For trans DEMs, there is a coexistence of linear and nonlinear relationships between the direction of genomic modulation and chromosomal dosage.…”