Figure - available from: Genetica
This content is subject to copyright. Terms and conditions apply.
Southern hybridization of CpSAT-1 probe with Cydia pomonella gDNA digested with XbaI. Note that hybridization signals form a ladder of bands corresponding to the 120 bp multiples, clearly proving that the CpSAT-1 is a tandem repeat
Source publication
Satellite DNA (satDNA) is a non-coding component of eukaryotic genomes, located mainly in heterochromatic regions. Relevance of satDNA began to emerge with accumulating evidence of its potential yet hardly comprehensible role that it can play in the genome of many organisms. We isolated the first satDNA of the codling moth (Cydia pomonella, Tortric...
Citations
... Among the species with holocentric chromosomes, satDNAs have been characterized in a few species, for example, in nematode and insect species (Naclerio et al. 1992;Castagnone-Sereno et al. 1998;Palomeque and Lorite 2008;Dalíková et al. 2017; Bardella et al. 2020) and Rhynchospora (Cyperaceae), Luzula (Juncaceae), and Cuscuta (Convolvulaceae) plants (Heckmann et al. 2013;Ribeiro et al. 2017;Oliveira et al. 2020). Among insects, the few studies in species with holocentric chromosomes demonstrated the location of these sequences mainly in heterochromatic regions, such as subtelomeres, and in sex chromosomes of Lepidoptera and Hemiptera representatives (see for example Lu et al. 1994;Bizzaro et al. 1996;Mandrioli et al. 2003;Palomeque and Lorite 2008;Bardella et al. 2014Bardella et al. , 2020Věchtová et al. 2016;Dalíková et al. 2017;Pita et al. 2017;Cabral-de-Mello et al. 2021a;Montiel et al. 2021). ...
Satellite DNAs (satDNAs) constitute one of the main components of eukaryote genomes and are involved in chromosomal organization and diversification. Although largely studied, little information was gathered about their evolution on holocentric species, i.e., diffuse centromeres, which, due to differences in repeat organization, could result in different evolutionary patterns. Here, we combined bioinformatics and cytogenetic approaches to evaluate the evolution of the satellitomes in Mahanarva holocentric insects. In two species, de novo identification revealed a high number of satDNAs, 110 and 113, with an extreme monomer length range of 18–4228 bp. The overall abundance of satDNAs was observed to be 6.67% in M. quadripunctata and 1.98% in M. spectabilis, with different abundances for the shared satDNAs. Chromosomal mapping of the most abundant repeats of M. quadripunctata and M. spectabilis on other Mahanarva reinforced the dynamic nature of satDNAs. Variable patterns of chromosomal distribution for the satDNAs were noticed, with the occurrence of clusters on distinct numbers of chromosomes and at different positions and the occurrence of scattered signals or nonclustered satDNAs. Altogether, our data demonstrated the high dynamism of satDNAs in Mahanarva with the involvement of this genomic fraction in chromosome diversification of the genus. The general characteristics and patterns of evolution of satDNAs are similar to those observed on monocentric chromosomes, suggesting that the differential organization of genome compartments observed on holocentric chromosomes compared with monocentric chromosomes does not have a large impact on the evolution of satDNAs. Analysis of the satellitomes of other holocentric species in a comparative manner will shed light on this issue.
... Almost half of satDNA families were transcribed in some stages of RPW development and some families were transcribed stably throughout RPW life. In insects, satDNA transcription has previously been described in flies (Lima et al., 2017;Mills et al., 2019), mosquitoes (Halbach et al., 2020), moths (Věchtová et al., 2016), ants (Lorite et al., 2002b), wasps (Renault et al., 1999), sawflies (Rouleux-Bonnin et al., 1996), crickets (Palacios-Gimenez et al., 2018) and beetles Ugarković, 2008, 2009;Feliciello et al., 2015;Mora et al., 2017). The studies of Ugarković (2008, 2009) analyzing the transcription of centromeric satDNAs in two species of the genera Palorus are especially interesting. ...
The red palm weevil, Rhynchophorus ferrugineus, is the most harmful species among those pests affecting palm trees. Its impact causes important economic losses around the World. Nevertheless, the genetic information of Rh. ferrugineus is very scarce. Last year, the first genome assembly was published including a rough description of its repeatome. However, no information has been added about one of the main components of repeated DNA, the satellite DNA. Herein, we presented the characterization of the satellitome of this important species that includes 112 satellite DNA families, the largest number in an insect genome. These satellite DNA families made up around 25% of the genome while the most abundant family, RferSat01-169, alone represented 20.4%. Chromosomal location of most abundant satellite DNA families performed by fluorescence in situ hybridization showed that all of them are dispersed in the euchromatin on all chromosomes but some of them are also specifically accumulated either on the pericentromeric heterochromatic regions of all chromosomes or on specific chromosomes. Finally, the transcription of satellitome families was analyzed through Rh. ferrugineus development. It was found that 55 out of 112 satellite DNA families showed transcription, some families seemed to be transcribed across all stages while a few appeared to be stage-specific, indicating a possible role of those satellite DNA sequences in the development of this species.
... 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). ...
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.
... Together, those results indicated the satellitome is generally expressed in R. prolixus, although each family is transcribed at a different level and at a different pattern, suggesting that satDNA transcription could have a specific role in those tissue environments. Satellite DNA transcription is an accepted feature, as we commented on above, and it has been seen before in other insects, such as Coleoptera [57][58][59], Hymenoptera [60][61][62], Orthoptera [19], Lepidoptera [63] or Diptera [33,34,64]. In D. melanogaster, Mills et al. [34] found that satDNA derived from (AAGA) n tandem repeat is highly transcribed at neuron and testis, being necessary for male fertility. ...
... Another D. melanosgaster satDNA, the 1.688 satDNA family, contains a member with a dense X-linked distribution (1.688 X ), which plays an important role in marking the X chromosome during dosage compensation [65]. In males, the small interfering RNAs generated from 1.688 X sequences promote X localization of the male-specific lethal complex, which increases X-linked gene expression by modification of chromatin [38,63]. In D. buzzatti and D. mojavensis, satDNA families pBuM and CDSTR198 were transcribed, particularly in pupae and male tissues, even when both satDNAs have different genomic environment (heterochromatin and euchromatin, respectively) [64]. ...
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 Tria-toma 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 au-tosomes 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.
... However, low amounts of satDNA appear to be a general feature of lepidopteran genomes, which are generally rather small, ranging from 0.29 pg in Danaus plexippus (Danaidae) to 1.94 pg in Euchlaena irraria (Geometridae) (Gregory, 2020, Animal Genome Size Database). So far, only a total of five satDNAs have been identified in all lepidopteran species investigated (Lu et al., 1994;Mandrioli et al., 2003;Mahendran et al., 2006;Věchtová et al., 2016;Dalíková et al., 2017b). They showed variable patterns of chromosomal distribution including W specific satDNA (Dalíková et al., 2017b), satDNA shared exclusively by Z and W chromosomes (Mandrioli et al., 2003), and satDNAs spread on multiple chromosomes (Mahendran et al., 2006;Věchtová et al., 2016). ...
... So far, only a total of five satDNAs have been identified in all lepidopteran species investigated (Lu et al., 1994;Mandrioli et al., 2003;Mahendran et al., 2006;Věchtová et al., 2016;Dalíková et al., 2017b). They showed variable patterns of chromosomal distribution including W specific satDNA (Dalíková et al., 2017b), satDNA shared exclusively by Z and W chromosomes (Mandrioli et al., 2003), and satDNAs spread on multiple chromosomes (Mahendran et al., 2006;Věchtová et al., 2016). ...
... The interspecies occurrence of the seven satDNAs identified herein is consistent with the library hypothesis (Fry and Salser, 1977). A common feature of these newly identified satDNAs is the enrichment in A + T base pairs (light satDNAs), similar to the other five satDNAs previously described in Lepidoptera (Lu et al., 1994;Mandrioli et al., 2003;Mahendran et al., 2006;Věchtová et al., 2016;Dalíková et al., 2017b). Interestingly, the monomer length of some of the satDNAs identified herein is high, reaching 2,244 bp for Cper-Sat01 in C. perspectalis and more than 1,000 bp for two satDNAs in D. postlineella. ...
Tandem repeats are important parts of eukaryotic genomes being crucial e.g., for centromere and telomere function and chromatin modulation. In Lepidoptera, knowledge of tandem repeats is very limited despite the growing number of sequenced genomes. Here we introduce seven new satellite DNAs (satDNAs), which more than doubles the number of currently known lepidopteran satDNAs. The satDNAs were identified in genomes of three species of Crambidae moths, namely Ostrinia nubilalis, Cydalima perspectalis, and Diatraea postlineella, using graph-based computational pipeline RepeatExplorer. These repeats varied in their abundance and showed high variability within and between species, although some degree of conservation was noted. The satDNAs showed a scattered distribution, often on both autosomes and sex chromosomes, with the exception of both satellites in D. postlineella, in which the satDNAs were located at a single autosomal locus. Three satDNAs were abundant on the W chromosomes of O. nubilalis and C. perspectalis, thus contributing to their differentiation from the Z chromosomes. To provide background for the in situ localization of the satDNAs, we performed a detailed cytogenetic analysis of the karyotypes of all three species. This comparative analysis revealed differences in chromosome number, number and location of rDNA clusters, and molecular differentiation of sex chromosomes.
... Interestingly, in some Rynchospora species, one satDNA is dispersed, acting as holocentromere-specific repeat (Marques et al. 2015;Ribeiro et al. 2017). Among insects, satDNAs were studied only in few representatives of Lepidoptera and Hemiptera (Palomeque and Lorite 2008;Monti et al. 2010;Věchtová et al. 2016;Dalíková et al. 2017;Pita et al. 2017). Variable patterns of satDNA organization, such as clusterization in specific chromosomes, including sex chromosomes (Mandrioli 2003;Dalíková et al. 2017), distribution on multiple chromosomes, forming large blocks (Pita et al. 2017) or scattered as small clusters (Věchtová et al. 2016), were reported. ...
... Among insects, satDNAs were studied only in few representatives of Lepidoptera and Hemiptera (Palomeque and Lorite 2008;Monti et al. 2010;Věchtová et al. 2016;Dalíková et al. 2017;Pita et al. 2017). Variable patterns of satDNA organization, such as clusterization in specific chromosomes, including sex chromosomes (Mandrioli 2003;Dalíková et al. 2017), distribution on multiple chromosomes, forming large blocks (Pita et al. 2017) or scattered as small clusters (Věchtová et al. 2016), were reported. In most cases, the satDNAs are preferentially found in heterochromatic regions, located frequently on subtelomeric regions of holocentric chromosomes (Palomeque and Lorite 2008;Bardella et al. 2014;Pita et al. 2017). ...
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.
... Among insects, satDNA transcription has been described generally in Hymenoptera, Orthoptera, Diptera and Coleoptera [66] and in the lepidopteran species Cydia pomonella [67] and Plodia interpunctella [68]. Differential transcription of satDNAs in this group is related to different developmental stages and tissues and also the sexes [54,69,70]. ...
Background
Satellite DNAs (satDNAs) are organized in repetitions directly contiguous to one another, forming long arrays and composing a large portion of eukaryote genomes. These sequences evolve according to the concerted evolution model, and homogenization of repeats is observed at the intragenomic level. Satellite DNAs are the primary component of heterochromatin, located primarily in centromeres and telomeres. Moreover, satDNA enrichment in specific chromosomes has been observed, such as in B chromosomes, that can provide clues about composition, origin and evolution of this chromosome. In this study, we isolated and characterized a satDNA in A and B chromosomes of Abracris flavolineata by integrating cytogenetic, molecular and genomics approaches at intra- and inter-population levels, with the aim to understand the evolution of satDNA and composition of B chromosomes.
Results
AflaSAT-1 satDNA was shared with other species and in A. flavolineata, was associated with another satDNA, AflaSAT-2. Chromosomal mapping revealed centromeric blocks variable in size in almost all chromosomes (except pair 11) of A complement for both satDNAs, whereas for B chromosome, only a small centromeric signal occurred. In distinct populations, variable number of AflaSAT-1 chromosomal sites correlated with variability in copy number. Instead of such variability, low sequence diversity was observed in A complement, but monomers from B chromosome were more variable, presenting also exclusive mutations. AflaSAT-1 was transcribed in five tissues of adults in distinct life cycle phases.
Conclusions
The sharing of AflaSAT-1 with other species is consistent with the library hypothesis and indicates common origin in a common ancestor; however, AflaSAT-1 was highly amplified in the genome of A. flavolineata. At the population level, homogenization of repeats in distinct populations was documented, but dynamic expansion or elimination of repeats was also observed. Concerning the B chromosome, our data provided new information on the composition in A. flavolineata. Together with previous results, the sequences of heterochromatic nature were not likely highly amplified in the entire B chromosome. Finally, the constitutive transcriptional activity suggests a possible unknown functional role, which should be further investigated.
Electronic supplementary material
The online version of this article (10.1186/s12863-017-0548-9) contains supplementary material, which is available to authorized users.
... Interestingly, none of these W sequence analyses revealed the presence of a satellite DNA, which is considered to be the major component of constitutive heterochromatin. It is noteworthy that so far only four lepidopteran satellite sequences have been described (Lu et al. 1994;Mandrioli et al. 2003;Mahendran et al. 2006;Věchtová et al. 2016). Moreover, information about the satellite DNA (satDNA) distribution in female genomes is not available in all these cases. ...
... However, most of known long tandem repeats in Lepidoptera are present in the W chromosome in some amount. In the case of MBSAT1 in M a m e s t r a b r a s s i c a e a n d F R s a t D N A i n Spodoptera frugiperda (both Noctuidae), the satDNA is mainly located in the W chromosome (Lu et al. 1994;Mandrioli et al. 2003), whereas CpSAT-1 in C. pomonella is underrepresented in the W compared to the Z chromosome and some autosomes (Věchtová et al. 2016). ...
... In this paper, we describe a newly discovered satellite DNA in the Indian meal moth, P. interpunctella, called PiSAT1. Our knowledge of satDNA in Lepidoptera is quite limited, as only four other lepidopteran satDNAs have been described hitherto (Lu et al. 1994;Mandrioli et al. 2003;Mahendran et al. 2006;Věchtová et al. 2016). The cause of such limited amount of information about satDNA in this group of insects probably lies in the composition of lepidopteran genomes as their repetitive DNA is mainly formed by mobile elements (Osanai-Futahashi et al. 2008;The International Silkworm Genome Consortium 2008). ...
The W chromosome of most lepidopteran species represents the largest heterochromatin entity in the female genome. Although satellite DNA is a typical component of constitutive heterochromatin, there are only a few known satellite DNAs (satDNAs) located on the W chromosome in moths and butterflies. In this study, we isolated and characterized new satDNA (PiSAT1) from microdissected W chromosomes of the Indian meal moth, Plodia interpunctella. Even though the PiSAT1 is mainly localized near the female-specific segment of the W chromosome, short arrays of this satDNA also occur on autosomes and/or the Z chromosome. Probably due to the predominant location in the non-recombining part of the genome, PiSAT1 exhibits a relatively large nucleotide variability in its monomers. However, at least a part of all predicted functional motifs is located in conserved regions. Moreover, we detected polyadenylated transcripts of PiSAT1 in all developmental stages and in both sexes (female and male larvae, pupae and adults). Our results suggest a potential structural and functional role of PiSAT1 in the P. interpunctella genome, which is consistent with accumulating evidence for the important role of satDNAs in eukaryotic genomes.
... Among insects, satDNA transcription has been described generally in Hymenoptera, Orthoptera, Diptera and Coleoptera [66] and in the lepidopteran species Cydia pomonella [67] and Plodia interpunctella [68]. Differential transcription of satDNAs in this group is related to different developmental stages and tissues and also the sexes [54,69,70]. ...
Genes for major ribosomal RNAs (rDNA) are present in multiple copies mainly organized in tandem arrays. Number and position of rDNA loci can change dynamically and their re-patterning is presumably driven by other 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 among 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.
