Great Abundance of Satellite DNA in &lt;b&gt;&lt;i&gt;Proceratophrys&lt;/i&gt;&lt;/b&gt; (Anura, Odontophrynidae) Revealed by Genome Sequencing

Silva, Marcelo J da; Destro, Raquel Fogarin; Gazoni, Thiago; Narimatsu, Hideki; Santos, Paulo S Pereira Dos; Haddad, Célio F. B.; Parise-Maltempi, Patrícia Pasquali

doi:10.1159/000506531

Cited by 16 publications

(18 citation statements)

References 36 publications

(45 reference statements)

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“…Scarce information about satellite DNA obtained by genome-wide analysis confirms the high amount of satellite DNA present in amphibian genomes (e.g. 15.7% in Proceratophrys boiei 16 ).…”

Section: Introductionmentioning

confidence: 58%

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Identification and characterization of a new family of long satellite DNA, specific of true toads (Anura, Amphibia, Bufonidae)

Guzmán

Roco

Stöck

et al. 2022

Sci Rep

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Amphibians have some of the most variable genome sizes among vertebrates. Genome size variation has been attributed to repetitive and noncoding DNA, including satellite repeats, transposable elements, introns, and nuclear insertions of viral and organelle DNA. In vertebrates, satellite DNAs have been widely described in mammals, but few molecular studies have been carried out in amphibians. Here, we provide a detailed characterization of a new family of satellite DNA, present in all 15 examined species of the family Bufonidae. Southern-blot analysis and PCR reveal that this satellite is formed by monomers of 807 bp, is organized in tandem arrays, and has an AT-content of 57.4%. Phylogenetic analyses show that most clades exhibit species-specific variances, indicating that this satellite DNA has evolved by concerted evolution. The homogenization/fixation process is heterogeneous in Bufonidae, where the genera Bufo and Bufotes do not show species-specific differences, while populations from Rhinella marina exhibit population-specific changes. Additionally, variants of this satellite DNA have been identified in Duttaphrynus melanostictus and R. marina, supporting the ‘library hypothesis’ (a set, ‘library’, of satellite DNAs is shared by a species group). Physical mapping in Bufo bufo, Bufo spinosus, Epidalea calamita and Bufotes viridis provides evidence that this repetitive DNA is not dispersed in the karyotype, but accumulated in pericentromeric regions of some chromosomal pairs. This location, together with its presence in the transcriptomes of bufonids, could indicate a role in centromere function or heterochromatin formation and maintenance.

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“…Scarce information about satellite DNA obtained by genome-wide analysis confirms the high amount of satellite DNA present in amphibian genomes (e.g. 15.7% in Proceratophrys boiei 16 ).…”

Section: Introductionmentioning

confidence: 58%

“…Monomers of such length have not been identified when amphibian repetitive elements are characterized from next-generation sequence reads, e.g. in Proceratophrys boiei 16 .…”

Section: Discussionmentioning

confidence: 99%

Identification and characterization of a new family of long satellite DNA, specific of true toads (Anura, Amphibia, Bufonidae)

Guzmán

Roco

Stöck

et al. 2022

Sci Rep

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“…For M. elongatus, the male has lower copy numbers and a dispersed organization, since it did not present any FISH signals. This loss of autosomal clusters might have contributed to the homogenization in W 1 in M. elongatus, and generated the enriched and duplicated regions in this chromosome, fixating in the female genome as described for many other organisms (Dalíková et al, 2017;Palacios-Gimenez et al, 2017;da Silva et al, 2020;Ferretti et al, 2020;Rovatsos et al, 2021).…”

Section: Discussionmentioning

confidence: 95%

“…Regardless of the library size of satDNAs, usually one or very few satDNA families are the most predominant in each species ( Ruiz-Ruano et al, 2016 ; Silva et al, 2017 ; Bardella et al, 2020 ; da Silva et al, 2020 ) and the best candidates were none other but the two most abundant satDNA in M. elongatus , MelSat01-36 and MelSat02-26. Both satDNAs have concomitant origins in both sexes of M. elongatus and M. macrocephalus, but they have different evolutionary pathways in each species and concerted evolution might be acting separately for each of them.…”

Section: Discussionmentioning

confidence: 99%

Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs

et al. 2021

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Neotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W1 and, in MelSat02-26’s case, also harbored by Z2 and W2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.

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“…In amphibians, abundant repeats of satDNAs seem not to be dispersed in the karyotype, and even in specific chromosomes, but rather clustered in peri/centromeric regions, and possibly playing a role in the organization, regulation and maintenance of these chromosomal regions. In summary, this feature was detailed for the anuran genera Physalaemus, Proceratophrys, and Bufo (Vittorazzi et al, 2011;Da Silva et al, 2020;Guzmán et al, 2022, respectively), and, for all cases, the chromosomal location of abundant satDNAs indicates a role in centromere function or in the formation and maintenance of heterochromatin in these regions.…”

Section: Discussionmentioning

confidence: 96%

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

et al. 2023

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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.

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Great Abundance of Satellite DNA in <b><i>Proceratophrys</i></b> (Anura, Odontophrynidae) Revealed by Genome Sequencing

Cited by 16 publications

References 36 publications

Identification and characterization of a new family of long satellite DNA, specific of true toads (Anura, Amphibia, Bufonidae)

Identification and characterization of a new family of long satellite DNA, specific of true toads (Anura, Amphibia, Bufonidae)

Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs

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

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