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Multiple heterochromatin diversification events in the genome of fungus-farming ants: insights from repetitive sequences

Abstract

A substantial portion of the eukaryotic genome includes repetitive DNA, which is important for its stability, regulation, and architecture. Fungus-farming ant genomes show remarkable structural rearrangement rates that were necessary for the establishment of their agriculture-based lifestyle, highlighting the relevance of this peculiar group in understanding the repetitive portion of ant genome. Chromosomal banding studies are in accordance with genomic data because they show that repetitive heterochromatic sequences of basal and derivative Attina species are GC-rich, an uncommon trait in Formicidae. To understand the evolutionary dynamics of heterochromatin in Attina, we compared GC-rich heterochromatin patterns between the Paleoattina and Neoattina clades of this subtribe. To this end, we hybridized the Mrel-C0t probe (highly and moderately repetitive DNA) obtained from Mycetomoellerius relictus, Neoattina with GC-rich heterochromatin, in karyotypes of Paleoattina and Neoattina species. Additionally, we mapped the repetitive sequences (GA)15 and (TTAGG)6 in species of the two clades to investigate their organization and evolutionary patterns in the genome of Attina. The Mrel-C0t probe marked the heterochromatin in M. relictus, in other Mycetomoellerius spp., and in species of Mycetarotes, Cyphomyrmex, and Sericomyrmex (Neoattina). In Mycetomoellerius urichii, only pericentromeric heterochromatin was marked with Mrel-C0t. No marking was observed in Paleoattina species or in Atta and Acromyrmex (Neoattina). These results indicated that different evolutionary events led to heterochromatin differentiation in Attina. The most likely hypothesis is that GC-rich heterochromatin arose in the common ancestor of the two clades and accumulated various changes throughout evolution. The sequences (GA)15 and (TTAGG)6 located in euchromatin and telomeres, respectively, showed more homogeneous results among the species.

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Acknowledgements

We would like to thank Dr. Cléa S. F. Mariano for kindly providing Acromyrmex echinatior samples, Dr. Jacques H. C. Delabie for species identification, and Jérôme Orivel for the use of laboratory to process the Myrmicocrypta sp. samples. We also acknowledge Laboratório de Sistemética Molecular (Beagle) of the Universidade Federal de Viçosa (UFV) and Marina Souza da Cunha for technical support. GAT thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarships granted. Financial support for this study was provided by the Programa de Auxílio ao Pesquisador – PAPESQ/UNIFAP.

Funding

Financial support for this study was provided by the Programa de Auxílio ao Pesquisador – PAPESQ/UNIFAP and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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All the authors were involved in the project design, data collection, and data interpretation; GAT performed the experiments; All the authors participated in writing the paper, read, and approved the final manuscript.

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Correspondence to Luísa Antônia Campos Barros.

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The authors declare no competing interests.

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Supplementary Fig. 1

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High Resolution Image Fig. S1 Female metaphases submitted to C-banding technique showing heterochromatin location (dark regions) in different species of fungus-farming ants included in the Neoattina clade: (a) centromeric regions of Mycetomoellerius relictus (2n = 20), and (b) centromeric and pericentromeric regions of Mycetomoellerius urichii (2n = 18). Bars: 5 µm (TIF 349 KB)

Supplementary Fig. 2

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High Resolution Image Fig. S2 Fluorescence in situ hybridization (FISH) using C0t-DNA probe from Mycetomoellerius relictus and counterstained with DAPI (blue regions) in different species of fungus-farming ants included in the Paleoattina clade: (a), (b), (c) Mycocepurus goeldii (2n = 8), (d), (e), (f) Apterostigma madidiense (n = 23), (g), (h), (i) Apterostigma steigeri (2n = 22) and (j), (k), (l) Myrmicocrypta sp. (2n = 30). Bar: 5 µm (TIF 3239 KB)

Supplementary Fig. 3

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High Resolution Image Fig. S3 Fluorescence in situ hybridization (FISH) using the C0t-DNA probe from Mycetomoellerius relictus and counterstained with DAPI (blue regions) in different species of fungus-farming ants included in the Neoattina clade: (a), (b), (c) Atta bisphaerica (2n = 22), ( d), (e), (f) Acromyrmex balzani (2n = 38), (g), (h), (i) Acromyrmex echinatior (2n = 38), (j), (k), (l) Acromyrmex niger (2n = 38) and (m), (n), (o) Acromyrmex rugosus (2n = 38). Bar: 5 µm(TIF 6346 KB)

Supplementary Fig. 4

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High Resolution Image Fig. S4 Female karyotypes of (a) Mycocepurus goeldii (2n = 8) and (b) Sericomyrmex sp. (2n = 50) submitted to fluorescence in situ hybridization (FISH) with the (GA)15 microsatellite probe (red regions) and counterstained with DAPI (blue regions). Bars: 5 µm (TIF 553 KB)

Supplementary Fig. 5

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High Resolution Image Fig. S5 Metaphases of Mycetomoellerius spp. submitted to DAPI fluorochrome: (a) Mycetomoellerius urichii (2n = 18), (b) Mycetomoellerius sp. (2n = 22), (c) Mycetomoellerius holmgreni (2n = 20), (d) Mycetomoellerius relictus (2n = 20). Dimension lines in (a) indicate centromeric and pericentromeric regions. Bar: 5 µm (TIF 5085 KB)

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Teixeira, G.A., Barros, L.A.C., de Aguiar, H.J.A.C. et al. Multiple heterochromatin diversification events in the genome of fungus-farming ants: insights from repetitive sequences. Chromosoma 131, 59–75 (2022). https://doi.org/10.1007/s00412-022-00770-7

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  • DOI: https://doi.org/10.1007/s00412-022-00770-7

Keywords

  • Attina
  • C 0 t-DNA
  • Microsatellites
  • Chromosome evolution
  • Telomeres
  • Biodiversity