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; Jürgen Liebig; Guojie Zhang; Danny Reinberg

doi:10.1016/j.cub.2012.07.042

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, Jürgen Liebig, Guojie Zhang, Danny Reinberg

Institute for Health Informatics

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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 language	English (US)
Pages (from-to)	1755-1764
Number of pages	10
Journal	Current Biology
Volume	22
Issue number	19
DOIs	https://doi.org/10.1016/j.cub.2012.07.042
State	Published - Oct 9 2012

Bibliographical note

Funding Information:
We thank T. Bloss and K. Haight for ant colony maintenance; B. Kopenhaver for technical help; D. Beck, C. Desplan, D. Simola, and S. Tu for critical reading of the manuscript; and H. Shao for help with the mC detection pipeline. R.B. was supported by a Helen Hay Whitney Foundation postdoctoral fellowship. This work was funded by a Howard Hughes Medical Institute Collaborative Innovation Award (#2009005) to S.L.B., D.R., and J.L.

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Bonasio, R., Li, Q., Lian, J., Mutti, N. S., Jin, L., Zhao, H., Zhang, P., Wen, P., Xiang, H., Ding, Y., Jin, Z., Shen, S. S., Wang, Z., Wang, W., Wang, J., Berger, S. L., Liebig, J., Zhang, G., & 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

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

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title = "Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator",

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.",

author = "Roberto Bonasio and Qiye Li and Jinmin Lian and Mutti, {Navdeep S.} and Lijun Jin and Hongmei Zhao and Pei Zhang and Ping Wen and Hui Xiang and Yun Ding and Zonghui Jin and Shen, {Steven S.} and Zongji Wang and Wen Wang and Jun Wang and Berger, {Shelley L.} and J{\"u}rgen Liebig and Guojie Zhang and Danny Reinberg",

note = "Funding Information: We thank T. Bloss and K. Haight for ant colony maintenance; B. Kopenhaver for technical help; D. Beck, C. Desplan, D. Simola, and S. Tu for critical reading of the manuscript; and H. Shao for help with the mC detection pipeline. R.B. was supported by a Helen Hay Whitney Foundation postdoctoral fellowship. This work was funded by a Howard Hughes Medical Institute Collaborative Innovation Award (#2009005) to S.L.B., D.R., and J.L. ",

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T1 - Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator

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, Jürgen

AU - Zhang, Guojie

AU - Reinberg, Danny

N1 - Funding Information: We thank T. Bloss and K. Haight for ant colony maintenance; B. Kopenhaver for technical help; D. Beck, C. Desplan, D. Simola, and S. Tu for critical reading of the manuscript; and H. Shao for help with the mC detection pipeline. R.B. was supported by a Helen Hay Whitney Foundation postdoctoral fellowship. This work was funded by a Howard Hughes Medical Institute Collaborative Innovation Award (#2009005) to S.L.B., D.R., and J.L.

PY - 2012/10/9

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

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