Analysis in Proceratophrys boiei genome illuminates the satellite DNA content in a frog from the Brazilian Atlantic forest

Abstract

Satellite DNAs (satDNAs) are one of the most abundant elements in genomes. Characterized as tandemly organized sequences that can be amplified into multiple copies, mainly in heterochromatic regions. The frog P. boiei (2n = 22, ZZ♂/ZW♀) is found in the Brazilian Atlantic forest and has an atypical pattern of heterochromatin distribution when compared to other anuran amphibians, with large pericentromeric blocks on all chromosomes. In addition, females of Proceratophrys boiei have a metacentric sex chromosome W showing heterochromatin in all chromosomal extension. In this work, we performed high-throughput genomic, bioinformatic, and cytogenetic analyses to characterize the satellite DNA content (satellitome) in P. boiei, mainly due to high amount of C-positive heterochromatin and the highly heterochromatic W sex chromosome. After all the analyses, it is remarkable that the satellitome of P. boiei is composed of a high number of satDNA families (226), making P. boiei the frog species with the highest number of satellites described so far. Consistent with the observation of large centromeric C-positive heterochromatin blocks, the genome of P. boiei is enriched with high copy number of repetitive DNAs, with total satDNA abundance comprising 16.87% of the genome. We successfully mapped via Fluorescence in situ hybridization the two most abundant repeats in the genome, PboSat01-176 and PboSat02-192, highlighting the presence of certain satDNAs sequences in strategic chromosomal regions (e.g., centromere and pericentromeric region), which leads to their participation in crucial processes for genomic organization and maintenance. Our study reveals a great diversity of satellite repeats that are driving genomic organization in this frog species. The characterization and approaches regarding satDNAs in this species of frog allowed the confirmation of some insights from satellite biology and a possible relationship with the evolution of sex chromosomes, especially in anuran amphibians, including P. boiei, for which data were not available.

Satellitome Analysis in the Southern Lapwing (Vanellus chilensis) Genome: Implications for SatDNA Evolution in Charadriiform Birds

“…Comparative analyses between the sexes have demonstrated that satellite DNAs are of great importance for the differentiation of sex chromosomes [16,26,27,[68][69][70][71][72][73]. The Z and W chromosomes of all birds are descended from the same ancestral autosomal pair, most likely between 60 and 100 million years ago [74].…”

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

“…A similar scenario has already been reported in other animal species, such as the frog Proceratophrys boiei . Despite having a simple and heteromorphic ZZ/ZW sex chromosome system, it is distinguished by the absence of sex-specific satDNAs and low sex divergence, indicating their early stage of sex chromosome differentiation [ 77 ].…”

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

“…This approach has allowed the characterization of satDNAs in the genomes of numerous non‐model species from different groups. For example, satDNAs have been studied in insects (Anjos et al, 2023; Cabral‐de‐Mello et al, 2021; Mora et al, 2020; Pita et al, 2017), mollusks (Tunjić‐Cvitanić et al, 2021), fishes (Goes et al, 2022; Kretschmer et al, 2022), frogs (da Silva et al, 2020; da Silva et al, 2023), mammals (Gutiérrez et al, 2022) and plants (Heitkam et al, 2021; Sader et al, 2021). Consequently, low‐abundance satDNAs have been characterized, and some of them have been found in euchromatin (Cabral‐de‐Mello et al, 2021; Milani et al, 2021; Montiel et al, 2021; Pita et al, 2017).…”