Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator

Roberto Bonasio, Qiye Li, Jinmin Lian, Navdeep S. Mutti, Lijun Jin, Hongmei Zhao, Pei Zhang, Ping Wen, Hui Xiang, Yun Ding, Zonghui Jin, Steven S. Shen, Zongji Wang, Wen Wang, Jun Wang, Shelley L. Berger, Juergen Liebig, Guojie Zhang, Danny Reinberg

Research output: Contribution to journalArticle

179 Citations (Scopus)

Abstract

Background: Ant societies comprise individuals belonging to different castes characterized by specialized morphologies and behaviors. Because ant embryos can follow different developmental trajectories, epigenetic mechanisms must play a role in caste determination. Ants have a full set of DNA methyltransferases and their genomes contain methylcytosine. To determine the relationship between DNA methylation and phenotypic plasticity in ants, we obtained and compared the genome-wide methylomes of different castes and developmental stages of Camponotus floridanus and Harpegnathos saltator. Results: In the ant genomes, methylcytosines are found both in symmetric CG dinucleotides (CpG) and non-CpG contexts and are strongly enriched at exons of active genes. Changes in exonic DNA methylation correlate with alternative splicing events such as exon skipping and alternative splice site selection. Several genes exhibit caste-specific and developmental changes in DNA methylation that are conserved between the two species, including genes involved in reproduction, telomere maintenance, and noncoding RNA metabolism. Several loci are methylated and expressed monoallelically, and in some cases, the choice of methylated allele depends on the caste. Conclusions: These first ant methylomes and their intra- and interspecies comparison reveal an exonic methylation pattern that points to a connection between DNA methylation and splicing. The presence of monoallelic DNA methylation and the methylation of non-CpG sites in all samples suggest roles in genome regulation in these social insects, including the intriguing possibility of parental or caste-specific genomic imprinting.

Original languageEnglish (US)
Pages (from-to)1755-1764
Number of pages10
JournalCurrent Biology
Volume22
Issue number19
DOIs
StatePublished - Oct 9 2012

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Camponotus floridanus
Ants
Social Class
DNA methylation
DNA Methylation
Formicidae
Genes
Genome
genome
DNA
Methylation
methylation
exons
Exons
caste determination
Genomic Imprinting
Untranslated RNA
RNA Splice Sites
genomic imprinting
genes

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Bonasio, R., Li, Q., Lian, J., Mutti, N. S., Jin, L., Zhao, H., ... Reinberg, D. (2012). Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator. Current Biology, 22(19), 1755-1764. https://doi.org/10.1016/j.cub.2012.07.042

Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator. / Bonasio, Roberto; Li, Qiye; Lian, Jinmin; Mutti, Navdeep S.; Jin, Lijun; Zhao, Hongmei; Zhang, Pei; Wen, Ping; Xiang, Hui; Ding, Yun; Jin, Zonghui; Shen, Steven S.; Wang, Zongji; Wang, Wen; Wang, Jun; Berger, Shelley L.; Liebig, Juergen; Zhang, Guojie; Reinberg, Danny.

In: Current Biology, Vol. 22, No. 19, 09.10.2012, p. 1755-1764.

Research output: Contribution to journalArticle

Bonasio, R, Li, Q, Lian, J, Mutti, NS, Jin, L, Zhao, H, Zhang, P, Wen, P, Xiang, H, Ding, Y, Jin, Z, Shen, SS, Wang, Z, Wang, W, Wang, J, Berger, SL, Liebig, J, Zhang, G & Reinberg, D 2012, 'Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator', Current Biology, vol. 22, no. 19, pp. 1755-1764. https://doi.org/10.1016/j.cub.2012.07.042
Bonasio, Roberto ; Li, Qiye ; Lian, Jinmin ; Mutti, Navdeep S. ; Jin, Lijun ; Zhao, Hongmei ; Zhang, Pei ; Wen, Ping ; Xiang, Hui ; Ding, Yun ; Jin, Zonghui ; Shen, Steven S. ; Wang, Zongji ; Wang, Wen ; Wang, Jun ; Berger, Shelley L. ; Liebig, Juergen ; Zhang, Guojie ; Reinberg, Danny. / Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator. In: Current Biology. 2012 ; Vol. 22, No. 19. pp. 1755-1764.
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AU - Bonasio, Roberto

AU - Li, Qiye

AU - Lian, Jinmin

AU - Mutti, Navdeep S.

AU - Jin, Lijun

AU - Zhao, Hongmei

AU - Zhang, Pei

AU - Wen, Ping

AU - Xiang, Hui

AU - Ding, Yun

AU - Jin, Zonghui

AU - Shen, Steven S.

AU - Wang, Zongji

AU - Wang, Wen

AU - Wang, Jun

AU - Berger, Shelley L.

AU - Liebig, Juergen

AU - Zhang, Guojie

AU - Reinberg, Danny

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N2 - Background: Ant societies comprise individuals belonging to different castes characterized by specialized morphologies and behaviors. Because ant embryos can follow different developmental trajectories, epigenetic mechanisms must play a role in caste determination. Ants have a full set of DNA methyltransferases and their genomes contain methylcytosine. To determine the relationship between DNA methylation and phenotypic plasticity in ants, we obtained and compared the genome-wide methylomes of different castes and developmental stages of Camponotus floridanus and Harpegnathos saltator. Results: In the ant genomes, methylcytosines are found both in symmetric CG dinucleotides (CpG) and non-CpG contexts and are strongly enriched at exons of active genes. Changes in exonic DNA methylation correlate with alternative splicing events such as exon skipping and alternative splice site selection. Several genes exhibit caste-specific and developmental changes in DNA methylation that are conserved between the two species, including genes involved in reproduction, telomere maintenance, and noncoding RNA metabolism. Several loci are methylated and expressed monoallelically, and in some cases, the choice of methylated allele depends on the caste. Conclusions: These first ant methylomes and their intra- and interspecies comparison reveal an exonic methylation pattern that points to a connection between DNA methylation and splicing. The presence of monoallelic DNA methylation and the methylation of non-CpG sites in all samples suggest roles in genome regulation in these social insects, including the intriguing possibility of parental or caste-specific genomic imprinting.

AB - Background: Ant societies comprise individuals belonging to different castes characterized by specialized morphologies and behaviors. Because ant embryos can follow different developmental trajectories, epigenetic mechanisms must play a role in caste determination. Ants have a full set of DNA methyltransferases and their genomes contain methylcytosine. To determine the relationship between DNA methylation and phenotypic plasticity in ants, we obtained and compared the genome-wide methylomes of different castes and developmental stages of Camponotus floridanus and Harpegnathos saltator. Results: In the ant genomes, methylcytosines are found both in symmetric CG dinucleotides (CpG) and non-CpG contexts and are strongly enriched at exons of active genes. Changes in exonic DNA methylation correlate with alternative splicing events such as exon skipping and alternative splice site selection. Several genes exhibit caste-specific and developmental changes in DNA methylation that are conserved between the two species, including genes involved in reproduction, telomere maintenance, and noncoding RNA metabolism. Several loci are methylated and expressed monoallelically, and in some cases, the choice of methylated allele depends on the caste. Conclusions: These first ant methylomes and their intra- and interspecies comparison reveal an exonic methylation pattern that points to a connection between DNA methylation and splicing. The presence of monoallelic DNA methylation and the methylation of non-CpG sites in all samples suggest roles in genome regulation in these social insects, including the intriguing possibility of parental or caste-specific genomic imprinting.

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