DNA methylation is widespread and associated with differential gene expression in castes of the honeybee,
            <i>Apis mellifera</i>

Elango, Navin; Hunt, Brendan G.; Goodisman, Michael A. D.; Yi, Soojin V.

doi:10.1073/pnas.0900301106

Cited by 307 publications

(447 citation statements)

References 55 publications

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“…3B; Supplemental Tables 11,12), indicating that some genes in ants are distinguished by DNA methylation, similar to the honeybee (see also Bonasio et al 2012;Smith et al 2012). Functional analysis of genes putatively methylated in all seven ant genomes (low CpG O/E) revealed enrichment for housekeeping functions, including transcription, translation, and cellular metabolic function (FDR < 0.05) (Supplemental Tables 13-15), as reported for the honeybee (Elango et al 2009). Next, we computed the average methylation level of genes, grouped by the number of hymenopteran species with orthologs.…”

Section: Ant Conserved Regions Harbor An Abundance Of Regulatory Elemmentioning

confidence: 68%

“…For example, relative depletion of CpG dinucleotides (CpG O/E, a sequence-based signature of DNA methylation) correlates negatively with DNA methylation and distinguishes classes of genes that are differentially expressed between honeybee queens and workers (Elango et al 2009). We found that all seven ants are distinct from the honeybee in exhibiting unimodal CpG O/E distributions and significantly less CpG depletion over exons genome-wide (i.e., higher mean CpG O/E) (Fig.…”

Section: Ant Conserved Regions Harbor An Abundance Of Regulatory Elemmentioning

confidence: 99%

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Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

et al. 2013

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Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations

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Section: Ant Conserved Regions Harbor An Abundance Of Regulatory Elemmentioning

confidence: 68%

Section: Ant Conserved Regions Harbor An Abundance Of Regulatory Elemmentioning

confidence: 99%

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

et al. 2013

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“…Third, the sea squirt Ciona intestinalis has a genome about equally divided between methylated and unmethylated domains, with most gene bodies in the methylated domain (10). Fourth, the DNA of the honey bee, Apis mellifora, contains methylated DNA and Elango et al have found that its genome is equally divided into high-CpG and lowCpG classes (26). These authors suggested that exons are the primary target of DNA methylation and found that the high-CpG genes in A. mellifora are enriched for genes associated with developmental processes.…”

Section: Discussionmentioning

confidence: 99%

CpG island clusters and pro-epigenetic selection for CpGs in protein-coding exons of HOX and other transcription factors

Branciamore¹,

Chen

Riggs

et al. 2010

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

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CpG dinucleotides contribute to epigenetic mechanisms by being the only site for DNA methylation in mammalian somatic cells. They are also mutation hotspots and ∼5-fold depleted genomewide. We report here a study focused on CpG sites in the coding regions of Hox and other transcription factor genes, comparing methylated genomes of Homo sapiens, Mus musculus, and Danio rerio with nonmethylated genomes of Drosophila melanogaster and Caenorhabditis elegans. We analyzed 4-fold degenerate, synonymous codons with the potential for CpG. That is, we studied "silent" changes that do not affect protein products but could damage epigenetic marking. We find that DNA-binding transcription factors and other developmentally relevant genes show, only in methylated genomes, a bimodal distribution of CpG usage. Several genetic code-based tests indicate, again for methylated genomes only, that the frequency of silent CpGs in Hox genes is much greater than expectation. Also informative are NCG-GNN and NCC-GNN codon doublets, for which an unusually high rate of G to C and C to G transversions was observed at the third (silent) position of the first codon. Together these results are interpreted as evidence for strong "pro-epigenetic" selection acting to preserve CpG sites in coding regions of many genes controlling development. We also report that DNA-binding transcription factors and developmentally important genes are dramatically overrepresented in or near clusters of three or more CpG islands, suggesting a possible relationship between evolutionary preservation of CpG dinucleotides in both coding regions and CpG islands.DNA methylation | epigenetics | evolution | gene duplication C pG dinucleotides are of special interest for several reasons. In somatic cells of mammals and other vertebrates, cytosine DNA methylation is almost entirely in CpGs (1, 2) and is an epigenetic mechanism essential for normal development (3, 4). The C in CpGs is highly mutable, with C to T (and complementary G to A) transitions being the most common mutations. The ≈30-fold increased mutation rate for CpG is generally thought to be due to the enzymatic methylation of CpGs, with the formation of 5-methylcytosine ( m C). Deamination of m C then leads to enhanced mutagenesis (5, 6). Most likely for this reason the frequency of CpGs in the mammalian genome is on average ∼5-fold below expectation based on genome-wide nucleotide composition. Importantly, some regions of the genome are not depleted of CpGs and, if >200 bp, are called CpG islands (CGIs) (7,8). As a hallmark feature, CGIs are usually unmethylated. However, some CGIs show tissue-specific methylation, and much evidence indicates that methylated CpG sites ( m CpG) in promoters, enhancers, and other regulatory regions do play an essential role in embryonic development, gene imprinting, and X chromosome inactivation (3, 9, 10). For the above reasons there have been numerous studies of CpGs in promoters (11,12). Over 50% of promoters are in CGIs and there is a strong inverse correlation, especially in c...

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“…DNA methylation is hypothesized to play a key role in developmental responsiveness to environmental factors and may play an important role in social insect caste determination (49). However, the primary targets of DNA methylation in insects appear to be genes with ubiquitous expression across tissues and alternate phenotypes (50)(51)(52). Putatively methylated genes identified from MeDIP analysis in S. invicta were enriched for biological processes related to cellular metabolism and transcription (SI Materials and Methods, Table S1E), as is the case with methylated genes in A. mellifera (50).…”

Section: Vg4mentioning

confidence: 99%

The genome of the fire ant Solenopsis invicta

Wurm

Wang

Riba‐Grognuz

et al. 2011

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

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338

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Ants have evolved very complex societies and are key ecosystem members. Some ants, such as the fire ant Solenopsis invicta, are also major pests. Here, we present a draft genome of S. invicta, assembled from Roche 454 and Illumina sequencing reads obtained from a focal haploid male and his brothers. We used comparative genomic methods to obtain insight into the unique features of the S. invicta genome. For example, we found that this genome harbors four adjacent copies of vitellogenin. A phylogenetic analysis revealed that an ancestral vitellogenin gene first underwent a duplication that was followed by possibly independent duplications of each of the daughter vitellogenins. The vitellogenin genes have undergone subfunctionalization with queen-and worker-specific expression, possibly reflecting differential selection acting on the queen and worker castes. Additionally, we identified more than 400 putative olfactory receptors of which at least 297 are intact. This represents the largest repertoire reported so far in insects. S. invicta also harbors an expansion of a specific family of lipid-processing genes, two putative orthologs to the transformer/feminizer sex differentiation gene, a functional DNA methylation system, and a single putative telomerase ortholog. EST data indicate that this S. invicta telomerase ortholog has at least four spliceforms that differ in their use of two sets of mutually exclusive exons. Some of these and other unique aspects of the fire ant genome are likely linked to the complex social behavior of this species.social insect | caste differences | nonmodel organism | de novo genome assembly

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DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera

Cited by 307 publications

References 55 publications

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

CpG island clusters and pro-epigenetic selection for CpGs in protein-coding exons of HOX and other transcription factors

The genome of the fire ant Solenopsis invicta

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