The Role of Satellite DNAs in Genome Architecture and Sex Chromosome Evolution in Crambidae Moths

Cabral-de-Mello, Diogo Cavalcanti; Zrzavá, Magda; Kubı́čková, Svatava; Rendón, Pedro; Marec, František

doi:10.3389/fgene.2021.661417

Cited by 31 publications

(24 citation statements)

References 103 publications

(182 reference statements)

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“…Besides their well-known structural function composing heterochromatin, centromeres or telomeres, a relevant role in chromosomal organization, pairing and segregation has been attributed to satDNA [ 8 , 29 ]. For instance, Cabral-de-Mello et al [ 30 ] have recently reported its involvement in the differentiation of the Z sex chromosome in Crambidae moths. Furthermore, non-coding transcripts of satDNA are involved not only in heterochromatin maintenance and kinetochore assembly [ 31 , 32 ], but also in mosquito embryonic development, promoting gene silencing [ 33 ].…”

Section: Introductionmentioning

confidence: 99%

Satellitome Analysis of Rhodnius prolixus, One of the Main Chagas Disease Vector Species

Montiel

Panzera

Palomeque

et al. 2021

IJMS

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The triatomine Rhodnius prolixus is the main vector of Chagas disease in countries such as Colombia and Venezuela, and the first kissing bug whose genome has been sequenced and assembled. In the repetitive genome fraction (repeatome) of this species, the transposable elements represented 19% of R. prolixus genome, being mostly DNA transposon (Class II elements). However, scarce information has been published regarding another important repeated DNA fraction, the satellite DNA (satDNA), or satellitome. Here, we offer, for the first time, extended data about satellite DNA families in the R. prolixus genome using bioinformatics pipeline based on low-coverage sequencing data. The satellitome of R. prolixus represents 8% of the total genome and it is composed by 39 satDNA families, including four satDNA families that are shared with Triatoma infestans, as well as telomeric (TTAGG)n and (GATA)n repeats, also present in the T. infestans genome. Only three of them exceed 1% of the genome. Chromosomal hybridization with these satDNA probes showed dispersed signals over the euchromatin of all chromosomes, both in autosomes and sex chromosomes. Moreover, clustering analysis revealed that most abundant satDNA families configured several superclusters, indicating that R. prolixus satellitome is complex and that the four most abundant satDNA families are composed by different subfamilies. Additionally, transcription of satDNA families was analyzed in different tissues, showing that 33 out of 39 satDNA families are transcribed in four different patterns of expression across samples.

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Section: Introductionmentioning

confidence: 99%

Satellitome Analysis of Rhodnius prolixus, One of the Main Chagas Disease Vector Species

Montiel

Panzera

Palomeque

et al. 2021

IJMS

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“…The dynamics of the most abundant satDNAs in M. elongatus demonstrates not only their intimate evolution with the highly differentiated heteromorphic W 1 sex chromosome, but also confirms that not only general molecular satDNA evolution is at play; particular characteristics of the species also concomitantly generate diversified satellitomes (Ugarković and Plohl, 2002;Lorite et al, 2004, Lorite et al, 2017Richard et al, 2008;Palacios-Gimenez et al, 2017;Cabral-de-Mello et al, 2021). The ZWbased multiple sex chromosome system in M. elongatus shares a conserved heteromorphic W chromosome with the remaining Megaleporinus; but as seen by the two most prevalent satDNAs in the species their interspecific differences show distinct paces for W/W 1 differentiation.…”

Section: Discussionmentioning

confidence: 57%

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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“…Dalíková et al, 2017b;Cabral-de-Mello et al, 2021). Yet, it seems that abundance of satellite DNA in lepidopteran genomes is very low with scattered distribution and possible enrichment on sex chromosomes (Cabral-de-Mello et al, 2021). This does not reflect distribution of rDNA in Lepidoptera (Nguyen et al, 2010;Provazníková et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Yet we argue that preferential spread of rDNA into terminal regions of lepidopteran chromosomes (Nguyen et al, 2010; Provazníková et al, 2021) favours ectopic recombination as its efficiency depends on proximity of homologous sequences to telomeres (Goldman and Lichten, 1996; Nguyen et al, 2010), whereas ecc-rDNA could be integrated anywhere in the genome as long as a homologous sequence is present. Little is known about satellite DNA in Lepidoptera, which has been studied in detail only in a dozen of species (Lu et al, 1994; Mandrioli et al, 2003; Mahendran et al, 2006; Věchtová et al, 2016; M. Dalíková et al, 2017b; Cabral-de-Mello et al, 2021). Yet, it seems that abundance of satellite DNA in lepidopteran genomes is very low with scattered distribution and possible enrichment on sex chromosomes (Cabral-de-Mello et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Little is known about satellite DNA in Lepidoptera, which has been studied in detail only in a dozen of species (Lu et al, 1994; Mandrioli et al, 2003; Mahendran et al, 2006; Věchtová et al, 2016; M. Dalíková et al, 2017b; Cabral-de-Mello et al, 2021). Yet, it seems that abundance of satellite DNA in lepidopteran genomes is very low with scattered distribution and possible enrichment on sex chromosomes (Cabral-de-Mello et al, 2021). This does not reflect distribution of rDNA in Lepidoptera (Nguyen et al, 2010; Provazníková et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

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The role of repetitive DNA in re-patterning of major rDNA clusters in Lepidoptera

Dalíková

Provazníková

Provazník

et al. 2022

Preprint

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Genes for major ribosomal RNAs (rDNA) are present in multiple copies organized in tandem arrays. Number and position of rDNA loci can change dynamically and their re-patterning is presumably driven by repetitive sequences. We explored a peculiar rDNA organization in several representatives of Lepidoptera with either extremely large or numerous rDNA clusters. We combined molecular cytogenetics with analyses of second and third generation sequencing data to show that rDNA spreads as a transcription unit and reveal association between rDNA and various repeats. Furthermore, we performed comparative long read analyses between the species with derived rDNA distribution and moths with a single rDNA locus, which is considered ancestral. Our results suggest that satellite arrays, rather than mobile elements, facilitate homology-mediated spread of rDNA via either integration of extrachromosomal rDNA circles or ectopic recombination. The latter arguably better explains preferential spread of rDNA into terminal regions of lepidopteran chromosomes as efficiency of ectopic recombination depends on proximity of homologous sequences to telomeres.

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The Role of Satellite DNAs in Genome Architecture and Sex Chromosome Evolution in Crambidae Moths

Cited by 31 publications

References 103 publications

Satellitome Analysis of Rhodnius prolixus, One of the Main Chagas Disease Vector Species

Satellitome Analysis of Rhodnius prolixus, One of the Main Chagas Disease Vector Species

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

The role of repetitive DNA in re-patterning of major rDNA clusters in Lepidoptera

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