The spread of satellite DNAs in euchromatin and insights into the multiple sex chromosome evolution in Hemiptera revealed by repeatome analysis of the bug Oxycarenus hyalinipennis

Abstract

Satellite DNAs (satDNAs) are highly repeated tandem sequences primarily located in heterochromatin, although their occurrence in euchromatin has been reported. Here, our aim was to advance the understanding of satDNA and multiple sex chromosome evolution in heteropterans. We combined cytogenetic and genomic approaches to study, for the first time, the satDNA composition of the genome in an Oxycarenidae bug, Oxycarenus hyalinipennis. The species exhibits a male karyotype of 2n = 19 (14A + 2 m + X1X2Y), with a highly differentiated Y chromosome, as demonstrated by C‐banding and comparative genomic hybridization, revealing an enrichment of repeats from the male genome. Additionally, comparative analysis between males and females revealed that the 26 identified satDNA families are significantly biased towards male genome, accumulating in discrete regions in the Y chromosome. Exceptionally, the OhyaSat04‐125 family was found to be distributed virtually throughout the entire extension of the Y chromosome. This suggests an important role of satDNA in Y chromosome differentiation, in comparison of other repeats, which collectively shows similar abundance between sexes, about 50%. Furthermore, chromosomal mapping of all satDNA families revealed an unexpected high spread in euchromatic regions, covering the entire extension, irrespective of their abundance. Only discrete regions of heterochromatin on the Y chromosome and of the m‐chromosomes (peculiar chromosomes commonly observed in heteropterans) were enriched with satDNAs. The putative causes of the intense enrichment of satDNAs in euchromatin are discussed, including the possible existence of burst cycles similar to transposable elements and as a result of holocentricity. These data challenge the classical notion that euchromatin is not enriched with satDNAs.

Dominance of transposable element-related satDNAs results in great complexity of “satDNA library” and invokes the extension towards “repetitive DNA library”

“…In the genome of the Pacific oyster C. gigas we have revealed an unusual, highly scattered organization of relatively short satDNA arrays throughout the genome (Tunjić-Cvitanić et al 2021 ). Similarly, chromosomal mapping of satDNA in the insect Oxycarenus hialinipennis revealed its high spread in the euchromatic regions (Cabral-de-Mello et al 2023 ). These findings contradict the classical concept of satDNAs organization (as outlined in Introduction).…”

“…Randomly selected read pairs of 0.25 × coverage for each species were aligned to dimers of the respective satDNA consensus. The abundance was normalized by dividing the total length mapped to each satDNA by the genome length, following Cabral-de-Mello et al ( 2023 ).…”

Chromosomal Rearrangements and Satellite DNAs: Extensive Chromosome Reshuffling and the Evolution of Neo-Sex Chromosomes in the Genus Pyrrhulina (Teleostei; Characiformes)

“…Repetitive sequences are great tools for the study of sex chromosomes, where species with heteromorphic sex chromosomes show a difference in the accumulation of some sequences between males and females, emphasizing the existence of several W/Y-specific satDNAs [ 13 , 14 , 18 , 75 ]. Despite the presence of a well-differentiated X 1 X 2 Y sex chromosome system, minor differences in haplotype accumulation between males and females were observed ( Figure 6 ).…”

“…Satellite DNAs (satDNAs) are one of the most common repeated sequences, forming extensive arrays of largely similar repeating units (monomers) that make up a significant percentage of genomes (reviewed in [ 10 ]). Recently, given the integration of cytogenetics with high-throughput sequencing data from next-generation sequencing methods (NGS), the whole collection of different satDNA families (satellitome) of several species has been characterized, providing insights into several evolutionary issues, such as karyotype evolution, genome diversity, and phylogenetic relationships [ 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 ]. These satellites (satDNAs) are also thought to play a role in the evolution and structure of sex chromosomes, as well as chromosome-based speciation [ 13 , 14 , 21 , 22 , 23 , 24 , 25 ].…”

Heterochromatin Is Not the Only Place for satDNAs: The High Diversity of satDNAs in the Euchromatin of the Beetle Chrysolina americana (Coleoptera, Chrysomelidae)

“…However, it is now recognized that tandem repeat DNAs, including microsatellites, minisatellites, and satDNAs, can also be found in euchromatin. Recent studies involving the characterization of satellitome and in situ hybridization with low-abundance satDNA families have revealed that many of these satellite DNA sequences are indeed located in euchromatin (see [68,75] for a review). These findings challenge the traditional view and highlight the presence and distribution of satellite DNA in both heterochromatic and euchromatic regions.…”