scholarly journals Bumblebee worker castes show differences in allele-specific DNA methylation and allele-specific expression

2020 ◽  
Author(s):  
H. Marshall ◽  
A.R.C. Jones ◽  
Z.N. Lonsdale ◽  
E.B. Mallon

AbstractAllele-specific expression is when one allele of a gene shows higher levels of expression compared to the other allele, in a diploid organism. Genomic imprinting is an extreme example of this, where some genes exhibit allele-specific expression in a parent-of-origin manner. Recent work has identified potentially imprinted genes in species of Hymenoptera. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals DNA methylation is often associated with imprinted genes. DNA methylation systems have been described in species of Hymenoptera, providing a candidate imprinting mechanism. Using previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive castes and the proportion of allele-specific expression bias generally varies between colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both castes. There is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that DNA methylation does not directly drive genome-wide allele-specific expression in this species. Only a small number of the genes identified may be ‘imprinted’ and it may be these genes which are associated with allele-specific DNA methylation. Future work utilising reciprocal crosses to identify parent-of-origin DNA methylation will further clarify the role of DNA methylation in parent-of-origin allele-specific expression.

2020 ◽  
Vol 12 (8) ◽  
pp. 1471-1481
Author(s):  
Hollie Marshall ◽  
Alun R C Jones ◽  
Zoë N Lonsdale ◽  
Eamonn B Mallon

Abstract Allele-specific expression is when one allele of a gene shows higher levels of expression compared with the other allele, in a diploid organism. Recent work has identified allele-specific expression in a number of Hymenopteran species. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals, DNA methylation is often associated with genes which show allele-specific expression. DNA methylation systems have been described in species of Hymenoptera, providing a candidate mechanism. Using previously generated RNA-Seq and whole-genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers, we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive and sterile workers and the proportion of allele-specific expression bias generally varies between genetically distinct colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both reproductive and sterile workers, with reproductive workers showing significantly more genes with allele-specific methylation. Finally, there is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that cis-acting DNA methylation does not directly drive genome-wide allele-specific expression in this species.


2021 ◽  
Author(s):  
Hollie Marshall ◽  
Moi T Nicholas ◽  
Jelle S van Zweden ◽  
Felix Wäckers ◽  
Laura Ross ◽  
...  

Genomic imprinting is defined as parent-of-origin allele-specific expression. In order for genes to be expressed in this manner an `imprinting' mark must be present to distinguish the parental alleles within the genome. In mammals imprinted genes are primarily associated with DNA methylation. Genes exhibiting parent-of-origin expression have recently been identified in two species of Hymenoptera with functional DNA methylation systems; Apis mellifera and Bombus terrestris. We carried out whole genome bisulfite sequencing of parents and offspring from reciprocal crosses of two B. terrestris subspecies in order to identify parent-of-origin DNA methylation. We were unable to survey a large enough proportion of the genome to draw a conclusion on the presence of parent-of-origin DNA methylation however we were able to characterise the sex- and caste-specific methylomes of B. terrestris for the first time. We find males differ significantly to the two female castes, with differentially methylated genes involved in many histone modification related processes. We also analysed previously generated honeybee whole genome bisulfite data to see if genes previously identified as showing parent-of-origin DNA methylation in the honeybee show consistent allele-specific methylation in independent data sets. We have identified a core set of 12 genes in female castes which may be used for future experimental manipulation to explore the functional role of parent-of-origin DNA methylation in the honeybee. Finally, we have also identified allele-specific DNA methylation in honeybee male thorax tissue which suggests a role for DNA methylation in ploidy compensation in this species.


2015 ◽  
Author(s):  
Harindra E Amarasinghe ◽  
Bradley J Toghill ◽  
Despina Nathanael ◽  
Eamonn B Mallon

Methylation has previously been associated with allele specific expression in ants. Recently, we found methylation is important in worker reproduction in the bumblebee Bombus terrestris. Here we searched for allele specific expression in twelve genes associated with worker reproduction in bees. We found allele specific expression in Ecdysone 20 monooxygenase and IMP-L2-like. Although we were unable to confirm a genetic or epigenetic cause for this allele specific expression, the expression patterns of the two genes match those predicted for imprinted genes.


2015 ◽  
Author(s):  
Harindra E Amarasinghe ◽  
Bradley J Toghill ◽  
Despina Nathanael ◽  
Eamonn B Mallon

Methylation has previously been associated with allele specific expression in ants. Recently, we found methylation is important in worker reproduction in the bumblebee Bombus terrestris. Here we searched for allele specific expression in twelve genes associated with worker reproduction in bees. We found allele specific expression in Ecdysone 20 monooxygenase and IMP-L2-like. Although we were unable to confirm a genetic or epigenetic cause for this allele specific expression, the expression patterns of the two genes match those predicted for imprinted genes.


2018 ◽  
Author(s):  
Sahar V. Mozaffari ◽  
Michelle M. Stein ◽  
Kevin M. Magnaye ◽  
Dan L. Nicolae ◽  
Carole Ober

AbstractGenomic imprinting is the phenomena that leads to silencing of one copy of a gene inherited from a specific parent. Mutations in imprinted regions have been involved in diseases showing parent of origin effects. Identifying genes with evidence of parent of origin expression patterns in family studies allows the detection of more subtle imprinting. Here, we use allele specific expression in lymphoblastoid cell lines from 306 Hutterites related in a single pedigree to provide formal evidence for parent of origin effects. We take advantage of phased genotype data to assign parent of origin to RNA-seq reads in individuals with gene expression data. Our approach identified known imprinted genes, two putative novel imprinted genes, and 14 genes with asymmetrical parent of origin gene expression. We used gene expression in peripheral blood leukocytes (PBL) to validate our findings, and then confirmed imprinting control regions (ICRs) using DNA methylation levels in the PBLs.Author SummaryLarge scale gene expression studies have identified known and novel imprinted genes through allele specific expression without knowing the parental origins of each allele. Here, we take advantage of phased genotype data to assign parent of origin to RNA-seq reads in 306 individuals with gene expression data. We identified known imprinted genes as well as two novel imprinted genes in lymphoblastoid cell line gene expression. We used gene expression in PBLs to validate our findings, and DNA methylation levels in PBLs to confirm previously characterized imprinting control regions that could regulate these imprinted genes.


2021 ◽  
Author(s):  
Tie-Bo Zeng ◽  
Nicholas Pierce ◽  
Piroska Szabo

Unlike regular imprinted genes, non-canonical imprinted genes are known to not depend on gamete-specific DNA methylation difference. Instead, the paternal allele-specific expression of these genes in the extra-embryonic lineages depends on an H3K27me3-based imprint in the oocyte, but this marking is not maintained beyond pre-implantation development. The maintenance of non-canonical imprinting corresponds to maternal allele-specific DNA methylation and paternal allele-specific H3K4me3 at their somatic DMRs, which occur at ERVK repeats. We hypothesized that EHMT2, the main euchromatic H3K9 methyltransferase, also has a role in this process. Using reciprocal mouse crosses and allele-specific RNA-seq analysis, we found that the maternal allele of each known non-canonical imprinted gene was derepressed from its ERVK promoter in the Ehmt2−/− ectoplacental cone of somite-matched 8.5 dpc embryos. In the Ehmt2−/− embryos, loss of DNA methylation accompanied the derepression of both parental alleles of those ERVK promoters. Our study identifies EHMT2 as an essential player that maintains the repressed chromosomal state in non-canonical imprinting.


2020 ◽  
Author(s):  
◽  
Alwyn Clark Go

Speciation occurs when reproductive barriers prevent the exchange of genetic information between individuals. A common form of reproductive barrier between species capable of interbreeding is hybrid sterility. Genomic incompatibilities between the divergent genomes of different species contribute to a reduction in hybrid fitness. These incompatibilities continue to accumulate after speciation, therefore, young divergent taxa with incomplete reproductive isolation are important in understating the genetics leading to speciation. Here, I use two Drosophila subspecies pairs. The first is D. willistoni consisting of D. w. willistoni and D. w. winge. The second subspecies pair is D. pseudoobscura, which is composed of D. p. pseudoobscura and D. p. bogotana. Both subspecies pairs are at the early stages of speciation and show incomplete reproductive isolation through unidirectional hybrid male sterility. In this thesis, I performed an exploratory survey of genome-wide expression analysis using RNA-sequencing on D. willistoni and determined the extent of regulatory divergence between the subspecies using allele-specific expression analysis. I found that misexpressed genes showed a degree of tissue specificity and that the sterile male hybrids had a higher proportion of misexpressed genes in the testes relative to the fertile hybrids. The analysis of regulatory divergence between this subspecies pair found a large (66-70%) proportion of genes with conserved regulatory elements. Of the genes showing evidence or regulatory divergence between subspecies, cis-regulatory divergence was more common than other types. In the D. pseudoobscura subspecies pair, I compared sequence and expression divergence and found no support for directional selection driving gene misexpression in their hybrids. Allele-specific expression analysis revealed that compensatory cis-trans mutations partly explained gene misexpression in the hybrids. The remaining hybrid misexpression occurs due to interacting gene networks or possible co-option of cis-regulatory elements by divergent transacting factors. Overall, the results of this thesis highlight the role of regulatory interactions in a hybrid genome and how these interactions could lead to hybrid breakdown by disrupting gene interaction networks.


2019 ◽  
Vol 116 (12) ◽  
pp. 5653-5658 ◽  
Author(s):  
Lin Shao ◽  
Feng Xing ◽  
Conghao Xu ◽  
Qinghua Zhang ◽  
Jian Che ◽  
...  

Utilization of heterosis has greatly increased the productivity of many crops worldwide. Although tremendous progress has been made in characterizing the genetic basis of heterosis using genomic technologies, molecular mechanisms underlying the genetic components are much less understood. Allele-specific expression (ASE), or imbalance between the expression levels of two parental alleles in the hybrid, has been suggested as a mechanism of heterosis. Here, we performed a genome-wide analysis of ASE by comparing the read ratios of the parental alleles in RNA-sequencing data of an elite rice hybrid and its parents using three tissues from plants grown under four conditions. The analysis identified a total of 3,270 genes showing ASE (ASEGs) in various ways, which can be classified into two patterns: consistent ASEGs such that the ASE was biased toward one parental allele in all tissues/conditions, and inconsistent ASEGs such that ASE was found in some but not all tissues/conditions, including direction-shifting ASEGs in which the ASE was biased toward one parental allele in some tissues/conditions while toward the other parental allele in other tissues/conditions. The results suggested that these patterns may have distinct implications in the genetic basis of heterosis: The consistent ASEGs may cause partial to full dominance effects on the traits that they regulate, and direction-shifting ASEGs may cause overdominance. We also showed that ASEGs were significantly enriched in genomic regions that were differentially selected during rice breeding. These ASEGs provide an index of the genes for future pursuit of the genetic and molecular mechanism of heterosis.


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