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Analysis of Holhymenia histrio genome provides insight into the satDNA evolution in an insect with holocentric chromosomes

Chromosome Research volume 28, pages 369–380 (2020)Cite this article

Abstract

Satellite DNAs (satDNA) are fast-evolving repetitive sequences organized in large tandem arrays, with characteristic enrichment in heterochromatin. Knowledge about evolutionary dynamics of this genome fraction is mostly restricted to its characterization in species with monocentric chromosomes, i.e., localized centromeres. In holocentric species, with non-localized centromeres, satDNAs have been largely ignored. Here we advance the understanding of satDNA evolution among holocentric species by characterization of the most abundant satDNAs in the hemipteran Holhymenia histrio, integrating genomic and chromosomal analyses. High plasticity at chromosomal and molecular levels was noticed for 34 satDNAs populating H. histrio genome. One satDNA family in particular (HhiSat01-184) was highly amplified on multiple chromosomes and also highly polymorphic. Our data support the emergence of a new satDNA family from this abundant satDNA, confined to a single chromosome. Moreover, we present new information about composition of a peculiar chromosome in Coreidae, the m-chromosome, and of the X chromosome. Overall, the molecular and chromosomal patterns for satDNAs in the holocentric species H. histrio seem to be similar to those observed in monocentric species.

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Abbreviations

bp:

base pair

CMA3 :

chromomycin A3

DAPI:

4′,6-diamidino-2-phenylindole

FISH:

fluorescence in situ hybridization

K2P:

Kimura 2-parameter

PCR:

polymerase chain reaction

rDNA:

ribosomal DNA

satDNA:

satellite DNA

SF:

superfamily

SSC:

saline–sodium citrate buffer

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Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process number 2019/19069-7), and by the Conselho Nacional de Desenvolvimento Científiico e Tecnológico (CNPq). VBB acknowledges the scholarship from FAPESP (process number 2018/21772-5) and DCCM is a recipient of a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process number 305300/2017-2).

Funding

We thank Cibele G Sotero-Caio (Sanger Institute) for the English corrections and to anonymous reviewers and the associate editor Dr. Andreas Houben for insightful comments.

Author information

Affiliations

  1. Departamento de Biologia Geral e Aplicada, Instituto de Biociências/IB, UNESP - Universidade Estadual Paulista, Rio Claro, São Paulo, 13506-900, Brazil

    Vanessa Bellini Bardella, Diogo Milani & Diogo Cavalcanti Cabral-de-Mello

Authors
  1. Vanessa Bellini Bardella
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  2. Diogo Milani
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  3. Diogo Cavalcanti Cabral-de-Mello
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Corresponding author

Correspondence to Diogo Cavalcanti Cabral-de-Mello.

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Electronic supplementary material

Supplementary Figure 1.

Molecular data of Superfamily 1 (SF-1). (a) SF-1 alignment based on satDNA consensus sequences showing the identity and the SF-1 consensus. In the box it is highlighted the region with more differences between HhiSat01-184 and HhiSat05-188. (b) Neighbor-joining three with all SF-1 variants. Note that HhiSat05-188 grouped exclusively within a single branch (brown). HhiSat01-184 variants were represented by green. (c) Landscapes (abundance versus divergence) for satDNA families HhiSat01-184 and HhiSat05-188. (JPG 1168 kb)

Supplementary Figure 2.

The five polymorphic variants evidenced at intra-population level for SF-1 in autosomes of Holhymenia histrio. Bivalents harboring signals with similar size (AA), harboring signals with heteromorphic size (Aa) and with presence/absence of signals (A0) are shown. Note the predominance of signals on the large chromosomes. All bivalents are in contact only by one terminus and the insets show the orientation of one bivalent and the X chromosome that is a univalent and their signal distribution. The orientation for the bivalent is valid for all autosomes and the arrowheads indicate the chromosomes termini. The X chromosome is indicated by letter. Bar = 10 μm. (JPG 318 kb)

Supplementary Figure 3.

Chromosomal mapping on metaphase I using SF-1 as probe, revealing differences in size between heteromorphic chromosomes (boxes), i.e. signal restrict to one of the homologous. (a,c) DAPI staining and (b,d) chromosomal distribution of SF-1. Bar = 10 μm. (JPG 1645 kb)

Supplementary Table 1

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Supplementary Table 2

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Bardella, V.B., Milani, D. & Cabral-de-Mello, D.C. Analysis of Holhymenia histrio genome provides insight into the satDNA evolution in an insect with holocentric chromosomes. Chromosome Res 28, 369–380 (2020). https://doi.org/10.1007/s10577-020-09642-1

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  • DOI: https://doi.org/10.1007/s10577-020-09642-1

Key-words

  • Coreidae
  • Hemiptera
  • heterochromatin
  • repetitive DNAs