For decades, satellite DNAs have been the hidden part of genomes. Initially considered as junk DNA, there is currently an increasing appreciation of the functional significance of satellite DNA repeats and of their sequences. Satellite DNA families accumulate in the heterochromatin in different parts of the eukaryotic chromosomes, mainly in pericentromeric and subtelomeric regions, but they also span the functional centromere. Tandem repeat sequences may spread from subtelomeric to interstitial loci, leading to the formation of chromosome-specific loci or to the accumulation in equilocal sites in different chromosomes. They also appear as the main components of the heterochromatin in the sex-specific region of sex chromosomes. Satellite DNA, required for chromosome organization, also plays a role in pairing and segregation. Some satellite repeats are transcribed and can participate in the formation and maintenance of heterochromatin structure and in the modulation of gene expression. In addition to the identification of the different satellite DNA families, their characteristics and location, we are interested in determining their impact on the genomes, by identifying the mechanisms leading to their appearance and amplification as well as in understanding how they change over time, the factors affecting these changes, and the influence exerted by the evolutionary history of the organisms. On the other hand, satellite DNA sequences are rapidly evolving sequences that may cause reproductive barriers between organisms and promote speciation. The accumulation of experimental data collected in recent years and the emergence of new approaches based on next-generation sequencing and high-throughput genome analysis are opening new perspectives that are changing our understanding of satellite DNA. This review examines recent data to provide a timely update on the overall information gathered about this part of the genome, focusing on the advances in the knowledge of its origin, its evolution, and its potential functional roles.

Eukaryotic genomes contain large quantities of different classes of repetitive DNA sequences which contribute largely to the absence of correlation between the C-value and the organism's complexity, this hiatus being known as the C-value enigma [Gregory, 2005]. In plants, as in animals, differences in genome size between species may be thousands of orders of magnitude, even between closely related species [Bennet and Leitch, 2005; Gregory, 2005]. Among repetitive sequences, transposable elements are mostly responsible for these pronounced differences, reaching up to 85% of some species of large genomes such as that of maize [Schnable et al., 2009] and explaining C-value differences between related species, as occur between Oryza sativa and its wild relative O. australiensis [Piegu et al., 2006], between Arabidopsis thaliana and A. lyrata[Hu et al., 2011], or between different Orobanchaceae species [Piednoël et al., 2012]. The class I elements or retrotransposons are the most abundant with a predominant presence of LTR-retrotransposons [López-Flores and Garrido-Ramos, 2012; Lee and Kim, 2014]. Nevertheless, not only transposable elements increase the size of plant genomes, but satellite DNAs also contribute greatly to plant genomes. For example, the VicTR-B satellite DNA family represents about 25% of the Vicia sativa genome [Macas et al., 2000] or the FriSAT1 repetitive DNA represents up to 36% of the Fritillaria falcata genome [Ambrožová et al., 2011]. Satellite DNA is a fraction of the eukaryotic genome consisting of highly repetitive noncoding short sequences organized in tandem arrays within the heterochromatin. Satellite DNA sequences are the main component of heterochromatic genome regions, which remain condensed throughout the cell cycle. Even though the satellite DNA is a quantitatively and qualitatively important component of the chromosomes, it remains one of the most enigmatic parts of the eukaryotic genomes. Today, many questions remain unresolved concerning these sequences even though much has been theorized about their origin, function and evolution, and significant experimental advances have been made in those aspects during the last 4 decades. Nonetheless, the individual contributions of different research groups still working on satellite DNA and, in recent years, the thrust of applying new genomic approaches to this topic are revolutionizing the possibilities of gaining breakthroughs in knowledge of the satellite DNA, its role in genomes and its evolution.

For decades, satellite DNA sequences have been considered as ‘junk DNA', probably by erroneously equating junk DNA with ‘noncoding DNA' [Graur et al., 2015]. However, in its original sense, junk DNA is a genomic segment on which selection does not operate [Ohno, 1972], which implies that it has no immediate use but that it might occasionally take on a useful function in the future, although it is expected that the majority of junk DNA will never acquire a function [Doolittle, 2013; Graur et al., 2013]. In terms of encoded information, even DNA fulfilling structural roles would be just junk or worse, ‘selfish DNA' that proliferates for its own benefit, even if cell biology might require it [Doolittle, 2013]. However, from a functional standpoint, DNA may still be classified within 2 categories. Graur et al. [2015] have made an evolutionary classification of genomic function and divided the functional DNA into 2 classes. Functional DNA is any segment in the genome that has a selected-effect function for which it is maintained mostly by purifying selection, although, less frequently, either positive or balancing selection may also contribute. Functional protein-coding genes, RNA-specifying genes, and untranscribed control elements would be ‘literal DNA' (the sequence of nucleotides is under selection). On the other hand, ‘indifferent DNA' includes genomic segments which are functional and needed, but the sequences of which are of little consequence, i.e. sequences whose main function is merely being there, but whose exact sequence is not important such as spacers, fillers, or protectors against frameshifts, etc. Indifferent DNA may also serve nucleotypic functions, such as determining nucleus size or structural roles. Indifferent DNA should show no evidence of selection for or against point mutations, but deletions and insertions should be under selection [Graur et al., 2015]. Contrasting functional DNA, the ‘rubbish DNA' is composed of genomic segments which have no selected-effect function. Graur et al. [2015] further divided the rubbish DNA into 2 classes: ‘junk DNA' and ‘garbage DNA'. The excess DNA in our genomes is junk, harmless and useless; it has no immediate use but might occasionally acquire it [Brenner, 1998; Graur et al., 2015]. When the extra DNA becomes disadvantageous, it would become subject to selection and is instantly converted to garbage [Brenner, 1998; Graur et al., 2015].

In this context, how we classify satellite DNA may be the subject of extensive debate, but it is becoming evident that beyond considering satellite DNA sequences as inert by-products of genome dynamics in heterochromatic regions, satellite DNA evolution is an interplay of stochastic events and selective pressure, which points to a functional significance of satellite sequences [Plohl et al., 2008]. Biological functions have been suggested for different specific satellite DNA families [Pezer et al., 2012; Plohl et al., 2012, 2014]. Thus, arrays of satellite DNA monomers span over the functionally important centromere locus, a specialized locus in chromosome segregation during mitosis and meiosis, and form densely packed heterochromatic genome pericentromeric compartments, primary sites of sister chromatid cohesion [Plohl et al., 2012, 2014]. In addition, other roles for satellite DNAs have also been suggested, such as chromosome organization, pairing and segregation [Plohl et al., 2012]. Furthermore, diverse forms of genome regulation modulated by satellite DNAs may be controlled by selective pressures and could influence the adaptability of the organism [Pezer et al., 2012]: satellite DNA transcripts act as epigenetic signals required for the organization of pericentromeric heterochromatin during embryogenesis, necessary for developmental progression, the epigenetic regulation of heterochromatin establishment, or the modulation of gene expression. In any case, each particular satellite DNA family, as other DNA sequences, would fulfill the precept of Graur et al. [2015] by which the affiliation of a DNA segment to a particular functional category may change during evolution (functional DNA may become junk DNA, junk DNA may become garbage DNA, rubbish DNA may become functional DNA) and that the determination of functionality or nonfunctionality of a genomic sequence must be based on its present status rather than on its potential to change in the future.

Satellite DNAs are organized in large tandem arrays in heterochromatin. Heterochromatin is located mainly in pericentromeric and subtelomeric areas of the chromosomes but also at times may be found at interstitial locations in some of them [López-Flores and Garrido-Ramos, 2012; Plohl et al., 2012]. Satellite DNAs form families that differ in location, nucleotide sequence, sequence complexity, repeat unit length, and abundance. These families experience high rates of genomic change and replacement and usually are species specific or shared by a group of related species, ranging between genus-specific satellite DNAs and satellite DNA families, which are conserved in a whole family or order. In fact, some satellite DNAs exhibit sequence conservation for long evolutionary periods [Quesada del Bosque et al., 2013, 2014; Cafasso and Chinali, 2014; Mehrotra et al., 2014]. This has been interpreted as a clear indication that these sequences fulfill a functional role, but not always [Pezer et al., 2012; Plohl et al., 2012].

Different satellite DNA families can be present within a genome and several genomes can share some or all of these families, which may constitute an ancient library of repetitive sequence families, each amplified differentially in each genome [Fry and Salser, 1977]. The degree of representativeness of each family among species has much to do with the particular evolutionary dynamics of these sequences. The very molecular mechanisms involved in the amplification of a particular family, among others, are responsible for the observed pattern of sequence similarity between the repeats. Thus, repeat units of a family of sequences maintain a high rate of intraspecific homogeneity, while members of the same family of sequences from related species differ greatly from each other [Pérez-Guitérrez et al., 2012]. Later, we will return to the features of the processes affecting evolutionary progression of satellite DNA, whereas in this section, we will focus on structural and organizational characteristics of satellite DNA families. Specifically, we will focus on sequence composition and complexity, repeat unit length, and abundance.

Families of satellite DNA are characterized by a huge variety of sequence compositions. A comparative analysis of tandem repeats from hundreds of species has revealed that repeat monomers are highly variable in sequence composition and show little evidence of sequence conservation [Melters et al., 2013]. In fact, according to theoretical models of satellite DNA evolution and given the experimental evidence, any random sequence can lead to a family of tandem repeats. Nevertheless, the sequence relationship between different satellite DNA families found within the same genome is indicative of common origins of currently highly differentiated satellite DNAs [Navajas-Pérez et al., 2005b]. In general, it has been found that satellite repeats are generally AT rich, especially in the case of centromeric satellite DNAs. AT richness and particularly the periodical distribution of AT tracts cause DNA bending into a super-helical tertiary structure, a sequence-dependent property that is thought to be responsible for the tight packing of DNA and proteins in heterochromatin [Pezer et al., 2012]. However, even the A+T content is not a general rule, since the recent study conducted by Melters et al. [2013] revealed that centromeric satellite DNAs of plant species do not appear to have a preference for AT- or GC-rich tandem repeats, and there is only a slight preference for AT-rich tandem repeats in the case of satellite repeats of animals. Palindrome sequences, which could potentially lead to the formation of dyad structures, are common elements of satellite DNAs. No role has been reliably demonstrated for them, but they might participate in the satellite DNA amplification processes or could mediate in recombination and gene-conversion events acting as targets for enzyme recognition [Krawinkel et al., 1986]. Conserved palindrome sequences are the targets for protein binding in centromeric satellite DNAs [Hall et al., 2003; Luchetti et al., 2003] and could also be targets for transcription factors [Pezer et al., 2012]. Comparison of monomer sequences within different satellite DNAs reveals that some monomer regions are more conserved, while others show higher change rates, indicating a functional constraint on a part of repeat monomers or motifs, probably induced by interaction with satellite DNA-bound proteins [Pezer et al., 2012; Plohl et al., 2012]. Sequence motifs residing within satellite DNAs may participate in homologous recombination as regions of increased similarity and may also represent sequence determinants in epigenetic modifications, which differentiate pericentromeric heterochromatin from centromeric chromatin in Arabidopsis and Zea mays [Hall et al., 2005; Zhang et al., 2008; Plohl et al., 2012]. At times, conserved motifs are remnants of shorter ancestral repeat monomers, regardless of whether they were preserved by selection or just by chance, because current repeats were derived from the duplication and divergence events of an initial shorter repeat [Macas et al., 2006].

In addition to sequence composition, there is also great diversity in repeat sequence length. Mehrotra and Goyal [2014] provided a review of monomer sizes of different plant satellite DNA families. Also, information concerning composition and characteristics can be found in PlantSat, a database that provides a list of satellite DNA sequences for many plant species ( [Macas et al., 2002]. According to Mehrotra and Goyal [2014], plant satellite DNA sequences commonly have monomer unit lengths of 135-195 or 315-375 bp, but repeat length may range between 58 bp of the pAm1 satellite DNA of Avena and 5.9 kb of the 2D8 repeats of Solanum bulbocastanum. According to this classical view of satellite DNA, even shorter monomer length has been found as, for example, the 38 bp of VicTR-B satellite DNA of Vicia [Macas et al., 2006]. However, clearly the term satellite DNA is historical because these kinds of sequences were initially isolated from satellite bands in experiments with gradient centrifugation, but there is an extreme diversity of satellite DNA families, in both animal and plant genomes, regardless of the nucleotide sequence and complexity. Thus, independent of several thousand simple sequence repeats in eukaryotes genomes interspersed in euchromatin, when present and organized in arrays of many thousand copies in heterochromatin, they are also satellite DNAs. Although controversy exists, today the term satellite DNA is generally applied to any tandem repetitive sequence present in blocks of hundreds to thousands of tandem units located in the constitutive heterochromatin regardless of unit size. Thus, in a broad sense, megabase-long arrays of short repeating units of only few base pairs should be considered as satellite DNA [Pedersen et al., 1996; Hudakova et al., 2001; Ananiev et al., 2005]. It is common for satellite DNA repeat monomers of higher lengths to originate from different cycles of amplification and sequence divergence of a basic shorter monomer [Stupar et al., 2002; Navajas-Pérez et al., 2005b; Macas et al., 2006]. In fact, monomer sequences of some satellite DNAs are complex higher-order repeat units formed by concurrent amplification and homogenization of 2 or more monomers adjacent to the original satellite DNA [Plohl et al., 2012].

A great diversity in abundance has also been found for every satellite DNA family studied. The intention here is not to make an extensive and rigorous review of the amount of each satellite DNA studied, partly because the data are not always available, but it can be stated that the genomic content of a satellite DNA can range from 0.1% of the FriSAT1 satellite DNA in several Fritillaria species or 0.3% of satellite DNAs within the genome in Musa [Hribová et al., 2010; Čížková et al., 2013] to 36% of FriSAT1 in F. falcate[Ambrožová et al., 2011]. The relative proportions that a satellite DNA represents in the different genomes are data that must be treated with caution, but it is clear that the amount of satellite DNA present in a genome may be partly responsible for the genome size. The FriSAT1 satellite DNA content between Fritillaria genomes varies from less than 0.1% of most species analyzed to 0.64, 1, 6, 26 and 36% of the genomes of F. camschatcensis, F. pudica, F. glauca, F. affinis, and F. falcate, respectively [Ambrožová et al., 2011]. However, no evidence of a relationship between satellite DNA content and genome size variation has been detected, the latter mostly due to other classes of repetitive DNA such as mobile elements [Ambrožová et al., 2011]. By contrast, the PaB6 satellite DNA of Prospero autumnale significantly contributes to considerable genome size differences found between some of the closely related diploid cytotypes of this species complex [Emadzade et al., 2014].

An additional important feature of satellite DNAs is their location (fig. 1). The following sections will treat this topic by reviewing different satellite DNA families isolated from different chromosomal loci.

Fig. 1

A schematic representation of a hypothetical plant chromosome. The scheme depicts the centromere structure, the Arabidopsis-like telomere sequence, and different classes of subtelomeric and interstitial repeats. See text for details.

Fig. 1

A schematic representation of a hypothetical plant chromosome. The scheme depicts the centromere structure, the Arabidopsis-like telomere sequence, and different classes of subtelomeric and interstitial repeats. See text for details.

Close modal

The centromere nucleates the kinetochore, a proteinaceous structure that regulates chromosome attachment to the spindle microtubules to guide chromosome movement during cell division. This function is common to all eukaryotic species; however, conservation is not the rule for DNA sequences at centromeres [Ma et al., 2007; Wang et al., 2009]. With the exception of the budding yeast Saccharomyces cerevisiae, the centromeres of eukaryotes are composed of large arrays of repetitive DNA. Actually, in most animal and plant species, the centromere contains arrays of satellite DNA sequences which, especially in the case of plants, might be interrupted by transposable elements [Ma et al., 2007; Plohl et al., 2014]. But the sequence of these centromeric satellite DNA repeats varies substantially among species. Centromere tandem monomers are conserved only between closely related species. A recent computational study on hundreds of plant as well as animal satellite DNAs revealed no sequence similarity between repeats from species diverging more than 50 Mya [Melters et al., 2013]. Although some exceptional cases have been identified experimentally, satellite DNA sequences at centromeres can differ greatly, even between closely related species, and furthermore, even between different chromosomes within a species [Macas et al., 2010]. This suggests that satellite arrays undergo rapid evolution through both expansion and shrinkage, resulting in the replacement of the most abundant variant with a different variant [Melters et al., 2013; Zhang et al., 2013b]. Simple sequence repeats are also commonly found forming pericentromeric heterochromatin [Hudakova et al., 2001; Cuadrado and Jouve, 2007; Carmona et al., 2013a; Cuadrado et al., 2013]. In addition to satellite DNA families, centromeric retrotransposons represent an important component of centromeres of a wide range of angiosperm species, implying these families are the key to plant centromere evolution and function [Neumann et al., 2011]. In rice and maize, for example, all centromeres have different retrotransposon families [Nagaki et al., 2005; Bao et al., 2006]. Furthermore, retrotransposons are the main component of banana and some wheat centromeres [Čížková et al., 2013; Li et al., 2013].

Centromeric satellite DNA families in plants and animals are not only fast evolving, but also their repeats do not possess other supposedly conserved properties such as monomer length, AT content, or abundance [Melters et al., 2013]. Human alpha satellite DNA is composed of monomers of about 170 bp in length, which is about the length of a nucleosome, and it has been hypothesized that structural requirements might constrain monomer length. In fact, most plant centromeric repeats are 135-195 bp in length [Macas et al., 2002; Wang et al., 2009; Mehrotra and Goyal, 2014; Plohl et al., 2014]. However, it is clearly not a universal rule, as tandem repeat monomer length is not conserved [Melters et al., 2013]. The centromeres of A. thaliana are composed of arrays of a 178- bp satellite repeat, the CentO centromeric satellite DNA of rice is composed of repeats of 155 bp, and the related repeats composing the centromeric satellite DNA of maize, CentC, have a length of 156 bp [Mehrotra and Goyal, 2014; Plohl et al., 2014]. However, rice has centromeres composed of both the 155-bp CentO satellite repeat and single-copy non-CentO sequences [Zhang et al., 2013b]. In addition, potato and pea centromere repeats differ across chromosomes [Gong et al., 2012; Neumann et al., 2012]. Six of the 12 potato chromosomes have tandem repeat-based centromeres, but 5 centromeres do not contain a tandem repeat. Also, the monomer sequence differed substantially between centromeres [Gong et al., 2012]. In the common bean, 2 unrelated centromere-specific satellite repeats have evolved independently and have undergone chromosome-specific homogenization being predominantly located at subsets of 8 and 3 centromeres, respectively [Iwata et al., 2013]. On the other hand, functional neocentromeres may be formed without the known centromere-specific sequences [Zhang et al., 2013a]. Also, in stable dicentric chromosomes, one of the centromeres was inactive, even containing all the DNA elements found in functional centromeres [Gao et al., 2011; Zhang et al., 2011; Fu et al., 2012].

All these data suggest that the DNA sequences alone are insufficient for centromere formation in plants and that they are not the main determinant of centromere identity and function. In fact, evidence has revealed the importance of epigenetic factors in the establishment of centromeric chromatin. Centromere identity and function is regulated epigenetically through the formation of a specialized chromatin structure (fig. 1). In particular, eukaryotic centromeres, from S. cerevisiae to humans, are characterized by the presence of the centromere-specific histone H3 variant CENH3 [Wang et al., 2009; Plohl et al., 2014]. Centromeres are organized as euchromatic pocket domains of CENH3 flanked by heterochromatic domains. The 178-bp repeats associated with the CENH3-containing chromatin in A. thaliana are hypomethylated compared with the same repeats located in the flanking pericentromeric regions [Zhang et al., 2008]. In addition, the hypomethylation was correlated with a significantly reduced level of H3K9me2 (a mark associated with heterochromatin). A similar hypomethylation of DNA in CEN chromatin was also revealed in maize [Zhang et al., 2008]. Only a portion of centromeric repetitive elements is assembled in CENH3 chromatin, the rest being embedded in heterochromatin [Zhang et al., 2008; Wang et al., 2009]. The CENH3 nucleosomes typically occupy only a portion of the satellite repeats, often in discontinuous blocks, and the same or similar repeats often underlie flanking pericentromeric heterochromatin composed of conventional nucleosomes [Zhang et al., 2013b]. CentO sequences associated with functional centromeres in rice (CENH3-bound) do not significantly differ from the total population of CentO, which includes both centromeric and pericentromeric repeat arrays [Macas et al., 2010]. The total size of CENH3 domains in grass species correlates with the genome size, and chromosomes of different sizes in the same species tend to have CENH3 domains of a similar size, even if they have different sizes of satellite arrays [Zhang et al., 2013b].

It has been proposed that centromeric retrotransposon sequences may help to produce a genomic environment conducive to the establishment of centromeric chromatin [Neumann et al., 2011]. All centromeric retrotransposons tested to date are actively transcribed, and a portion of the centromeric retrotransposons is also associated with the heterochromatin mark H3K9me2. It has been proposed that these elements play a role in RNAi-mediated formation and maintenance of centromeric chromatin. Their transpositional activity contributes to high evolutionary dynamics of centromeres by generating new insertions, which may be further subjected to illegitimate and unequal homologous recombination. In addition, their transcriptional activity is consistent with the notion that the transcription of centromeric retrotransposons has a role in normal centromere function [Neumann et al., 2011]. Satellite DNA repeats are also transcriptionally active in some cases. The CentO transcripts in rice are processed into siRNA, suggesting a potential role of this satellite repeat family in epigenetic chromatin modification [Lee et al., 2006].

Despite the lack of a conserved centromeric sequence, it has been postulated that regular positioning of CENH3 nucleosomes is advantageous for centromere formation [Zhang et al., 2013b]. In this sense, satellites may evolve to stabilize CENH3 nucleosomes, helping to prevent the loss of CENH3 nucleosomes against the pulling forces they undergo during chromosome segregation and to facilitate formation of the kinetochore. Stabilization of CENH3 nucleosomes could explain how new satellites arise and populate centromeres and how the evolutionary transition might proceed from neocentromeres based on unique sequences to mature centromeres based on repeat sequences [Zhang et al., 2013b]. Tandem repeats could invade an epigenetically defined centromere, either by tandem duplication of a sequence with a selective advantage for CENH3 stabilization that amplified de novo or through transposition of existing satellite DNAs [Gong et al., 2012; Zhang et al., 2013b]. Different centromeres starting with different tandem repeats would become homogenized over time [Gong et al., 2012; Zhang et al., 2013b].

Species-specific CENH3 proteins have been identified in all eukaryotes investigated so far, including humans, budding yeast, Drosophila melanogaster, and different plant species [for reviews, see Ma et al., 2007; Plohl et al., 2014]. Furthermore, it has been demonstrated that the evolution of CENH3 is subject to positive selection because of its interactions with changing DNA components [Plohl et al., 2014]. In this context, it has been proposed that coevolution of centromeric satellite DNAs and CENH3 proteins would explain the rapid evolution of the sequences and the proteins at centromeres, a feature which could be linked to reproductive isolation and speciation [Henikoff et al., 2001]. The ‘centromere drive' model [Malik and Henikoff, 2001], a model that proposes selection for the unequal transmission of competing centromeres in female meiosis, would explain the rapid accumulation of sequence differences in the centromere among individuals, leading to reduced compatibility of homologous chromosomes in hybrids and ultimately to postzygotic isolation, thus triggering speciation [Dawe and Henikoff, 2006; Ma et al., 2007; Plohl et al., 2014].

The telomeres are ribonucleoprotein complexes characterized by particular proteins and DNA sequences. The telomeres protect chromosomes from degradation and repair activities, and prevent chromosome shortening resulting from replication of the end of the linear chromosomes [Martínez and Blasco, 2011; Silvestre and Londoño-Vallejo, 2012]. Different telomere-specific proteins are involved in these functions [Martínez and Blasco, 2011]. Telomeric DNA is composed of short tandem repeats of about 6 bp, a eukaryotic ancestral structure [Blackburn and Greider, 1995; Henderson, 1995]: the first cloned telomeres were those of Tetrahymena and the repeated sequence of these telomeres was 5′-TTGGGG-3′, and afterwards, the telomeres of several other species of protozoa, fungi, plants, and animals were studied and proved to be composed of similar repeats or slight variants thereof, including the vertebrate variant 5′- TTAGGG-3′ or the 7-bp plant variant 5′-TTTAGGG-3′ (fig. 1).

However, there are some exceptions to this general rule. In Drosophila, telomere maintenance is based on targeted transposition of 3 non-LTR retrotransposons as an alternative mechanism to the telomerase mechanism [Silva-Sousa et al., 2012]. In plants, no alternative mechanisms such as those observed in Drosophila have been found, but there are sequence variants to the TTTAGGG telomeric sequence in many plant species. In Asparagales, the ends of the chromosomes of most species are composed by the human-type TTAGGG repeats instead of the typical TTTAGGG plant telomeric sequence [Sýkorová et al., 2003a; de la Herrán et al., 2005]. Furthermore, Allium lack any known telomeric sequence [Sýkorová et al., 2006]. Within Solanaceae, the genera Cestrum, Vestia and Sessea lack the plant or the human telomeric motifs at the tips of the chromosomes [Sýkorová et al., 2003b], but recently, the motif TTTTTTAGGG has been found at the telomeres in Cestrum [Peška et al., 2015]. In fact, a broad phylogenetic survey unveiled that the human-type repeat is the most common one and possibly ancestral in eukaryotes, but alternative motifs replaced it along the phylogeny of diverse eukaryotic lineages, some of them several times independently [Fulnečková et al., 2013].

Adjacent to telomeres, there are commonly subtelomeric or telomere-associated sequences, which are tandem repeats with a variety of lengths and degrees of repetitiveness [Henderson, 1995; Louis and Vershinin, 2005; López-Flores and Garrido-Ramos, 2012]. Monomer length is not conserved in subtelomeric satellite DNAs, ranging from 38 bp of the VicTR-B repeats of V. sativa [Macas et al., 2006] to the 2,226 bp of the CL18 repetitive family of banana [Čížková et al., 2013]. Subtelomeres are one of the most dynamic and rapidly evolving regions in eukaryotic genomes [Torres et al., 2011; Richard et al., 2013]. Many satellite DNA sequences at subtelomeric regions are species specific, often chromosome specific, and it is common to find several subtelomeric satellite DNA families within the same species [Cuadrado and Jouve, 1994]. By contrast, there are also highly conserved subtelomeric satellite DNAs. A recent work by Torres et al. [2011] in Solanum is illustrative about the dynamics of satellite DNAs in the subtelomeric regions. The CL14 and CL34 repeats of potato are organized as independent long arrays, up to 1-3 Mb, of 182- and 339-bp monomers, respectively. The CL34 repeat family is younger and more diverse, including the presence of short direct subrepeats and various sequence subfamilies, than the CL14 family. In fact, the CL14 repeat was detected in the subtelomeric regions among highly diverged Solanum species, whereas the CL34 repeat was found only in potato and its closely related species. Some chromosome ends only have CL34, and others have the CL14 family. The same chromosome might have a different family at each end. When both CL14 and CL34 were found at the same chromosomal end, the CL34 repeat array was always proximal to the telomeres. In addition, there are ends which lack either of the 2 families. In fact, the data suggest that there may be other satellite DNA families at subtelomeres in Solanum. The latter is a common situation, as it occurs in subtelomeric regions of the chromosomes of Silene latifolia [Kazama et al., 2006] or Rumex induratus [Navajas-Pérez et al., 2009a]. In S. latifolia, there are at least 4 subfamilies of the same satellite DNA family at the ends of its chromosomes, and each chromosomal end has a characteristic composition of subfamilies [Kazama et al., 2006]. Dynamic rearrangements and sequence exchanges between nonhomologous chromosome ends can result in the formation and amplification of new satellite repeat families or in sequence diversification of existing ones [Macas et al., 2006; Torres et al., 2011].

In Leymus racemosus, 2 satellite DNA families are found in subtelomeric regions, the Tail family composed of 570-bp repeats and a family composed of 350-bp repeats, which were conserved in Secale, Critesion, Pseudoroegeneria, Agropyron, and Australopyrum, although the 350-bp family was independently amplified in each species [Kishii et al., 1999]. In rye, in addition to the 350-bp family, several families with different monomer sizes have been described [Bedbrook et al., 1980; Cuadrado and Jouve, 1994, 1995; Vershinin et al., 1996; Vershinin and Heslop-Harrison, 1998; Contento et al., 2005]. FISH demonstrated a great variation in the relative arrangement of these repetitive sequences in the subtelomeres of rye chromosomes [Cuadrado and Jouve, 1994]. The pSc119.2 satellite DNA family is widely distributed within the Triticeae, and in some Aveneae species, and forms a large and evolutionarily old component of the genome [Contento et al., 2005]. Each of the large blocks of the repeat at chromosomal sites harbored many variants of the 120-bp repeat of different species. The common ancestor of the Triticeae tribe would have multiple sequences of the 120-bp repeat with an ample range of variation being inherited by each genus or species from the single ancestor, and this diversity has been maintained in all species since their split within the Triticeae without intraspecific homogenization [Contento et al., 2005]. The existence of interstitialization phenomena is common in different species through the transference of some of these satellite families from the telomeres towards interstitial sites [Cuadrado and Jouve, 2002; see below]. Banana (Musa spp.) has 2 subtelomeric satellite DNA families, the CL18 and the CL33 [Čížková et al., 2013]. The 2 satellite DNAs showed a high level of sequence conservation within and a high identity between Musa species [Čížková et al., 2013].

A common feature of subtelomeric satellite DNA is the direct attachment to telomere repeats [Sýkorová et al., 2003c]. It is common that telomeric repeats and/or degenerated telomeric repeats are scattered among subtelomeric repeats and even form part of the proper satellite DNA repeat [Bůzek et al., 1997; Garrido-Ramos et al., 1999; Sýkorová et al., 2003c; Navajas-Pérez et al., 2009a; Emadzade et al., 2014]. Interstitial telomeric repeats can be found as short tandem arrays also at centromeres, likely being evolutionary relics derived from chromosomal rearrangements [Lim et al., 2006; Navajas-Pérez et al., 2009a; Emadzade et al., 2014]. However, it also has been found that telomeric repeats might amplify and invade the functional centromeres of chromosomes as in Solanum species [He et al., 2013].

Telomere-associated sequences might not play an essential role in telomere function, but could facilitate chromosome pairing in meiosis or act to buffer terminal genes against the dynamic processes of loss and gain at the ends [Henderson, 1995; Kipling, 1995; Louis and Vershinin, 2005]. Also, subtelomeric repeats or generic subtelomeric heterochromatin may have a supplemental part in chromosome stability by stabilizing the chromosomal ends in the absence of canonical telomeric repeats [Jain et al., 2010]. Recently, Mehrotra et al. [2014] have found that a subtelomeric satellite DNA family previously characterized in Carthamus [Raina et al., 2005] and Centaurea [Suárez-Santiago et al., 2007] is not only conserved in the subfamily Carduoideae (Asteraceae) [Quesada del Bosque et al., 2014], but it is also present across various angiosperm families, suggesting that this satellite DNA may have an indispensible role in regulating cellular events. In Poaceae, the Lt1 subtelomeric satellite DNA family is an ancient family composed of 380-bp repeats conserved within the tribe Triticeae. However, the Lt1 sequences are abundant in the species from which it was isolated, L. triticoides, but absent in its closely related species L. racemosus [Anamthawat-Jónsson et al., 2009]. Together with the previous data reported above, this shows that sequence conservation is not needed to develop any of the different structural roles that may be assigned to these types of repetitive sequences.

The larger chromosome of Muscari comosum is the product of a massive amplification of the MCSAT satellite DNA family, which constitutes 5% of its genome [de la Herrán et al., 2001]. In fact, MCSAT sequences have been differentially amplified in several species of the genus, such as M. matritensis and M. dionysicum, attaining enormous amplification in the genome of M. comosum. MCSAT contribute largely to a progressive increase in the asymmetry of the karyotypes in Muscari species, from symmetrical karyotypes without MCSAT sequences to bimodal karyotypes with 2 sharply distinct size classes of chromosomes, large and small. Intermediate cases were found in M. dionysicum and M. matritensis with MCSAT, comprising 1.8 and 0.8% of their genomes, respectively. Together with the satellite DNAs found in plant sex chromosomes, this is an unusual case of a satellite DNA family exclusive to a single chromosome pair of the karyotype of one species. In addition to these cases of chromosome-specific satellite DNAs, it has been reported that satellite DNAs also accumulate within B chromosomes [Klemme et al., 2013]. Supernumerary chromosomes or B chromosomes are dispensable genetic material found both in plant and animals [Camacho, 2005]. The most widely accepted view is that they are derived from the A chromosome complement [Jamilena et al., 1995a; Martis et al., 2012]. In Secale cereale, although the B chromosomes contained a similar proportion of repeats as the A chromosomes, the 2 differed significantly in composition due to an additional massive accumulation of B-specific satellite repeats [Klemme et al., 2013]. Not all B-enriched sequences are unique to the B, suggesting that B originated from A chromosomes. However, these 2 sets of chromosomes have taken separate evolutionary pathways [Klemme et al., 2013]. Rye satellite repeat families including those clustered on the B chromosome are transcriptionally active. It has been hypothesized that these transcripts could have a function as scaffold RNA in the organization and regulation of Bs [Banaei-Moghaddam et al., 2015]. In addition to supernumerary chromosomes, supernumerary chromosome segments have also been described in plants. As in B chromosomes, some of them are heterochromatic and contain plenty of satellite DNA sequences [Shibata et al., 2000b], but neither all supernumerary chromosomes nor all supernumerary chromosome segments are heterochromatic [Jamilena et al., 1995b; Garrido-Ramos et al., 1998; Camacho, 2005; Houben and Carchilan, 2012; Banaei-Moghaddam et al., 2015].

There are few reports on interstitial satellite DNAs. In Nicotiana, all species belonging to the Tomentosae section have a tandem repeat called GRS at interstitial loci [Lim et al., 2000] that belongs to the HRS60 family of repeats. The HRS60 satellite family of tandem repeats also contains, among others, the elements HRS60, NP3R, and NP4R that, together with the NTS9 element isolated from N. tabacum of the section Sylvestres, were analyzed in the Nicotiana species of the section Alatae [Lim et al., 2006]. Both the NPR3 and the NPR4 repeats, predominantly located at subtelomeric regions, have been expanded to interstitial locations, having a differential distribution between species with a large amplification of NP3R at interstitial loci in N. longiflora [Lim et al., 2006]. The NTS9 is a satellite DNA that is predominantly located close to the centromere of the S9 chromosome of N. tabacum and that has been found at interstitial locations in the chromosomes of some Alatae species. The subtelomeric pSc119.2 satellite DNA tended to spread towards new interstitial sites during the diversification of the most primitive form of the genus Secale towards the most advanced taxa [Cuadrado and Jouve, 2002]. This highly repetitive sequence has supported events of interstitialization also in Hordeum [Carmona et al., 2013b]. Differences in the rates of sequence change were found between interstitial, slower and subtelomeric repeats [Lim et al., 2006]. Interstitialization is compatible with the assumption that subtelomeric regions are presumptive sites where heterochromatin amplification tends to be initiated and from which heterochromatic sequences are dispersed to interstitial sites [Schweizer and Loidl, 1987].

Among flowering plants, the origin of dioecy appears to have independently occurred in about 6% of the genera, and in all cases the appearance of dioecy resulted from quite recent events [Vyskot and Hobza, 2015]. Furthermore, only a few of dioecious plant species have chromosome-mediated sex determination systems [Vyskot and Hobza, 2015]. The most common case is the existence of XX/XY chromosomal complements and a Y-based sex-determining mechanism. However, there appear to be other alternatives, such as complex chromosomal systems (i.e. XX/XY1Y2 systems) and cases in which the sex specification is mediated by the balance between the number of X chromosomes and the number of autosomes (X/A balance). Though sex chromosomes have evolved independently in several different groups of organisms, they share common evolutionary pathways [Vyskot and Hobza, 2015]. Thus, the establishment of a pair of undifferentiated non-heteromorphic sex chromosomes is followed by genetic differentiation between sex chromosomes with a short region in which recombination is suppressed and some heteromorphism is established. The gradual suppression of recombination in a larger region between the sex chromosomes is thought to lead to their progressive divergence and the degeneration by gradual accumulation of deleterious mutations with the loss of function of many genes within the heteromorphic chromosome and the accumulation of a set of diverse repetitive sequences such as mobile elements and satellite DNAs [Charlesworth, 2002].

The genus Rumex is exceptional to study both the evolution of sex chromosomes and the evolution of satellite DNA sequences accumulated within them. American and Eurasian dioecious species of the plant genus Rumex form a clade divided into 2 sister groups, one composed of species with an XX/XY sex chromosome system (R. acetosella and closely related species such as R. graminifolius and R. paucifolius, and R. suffruticosus and R. hastatulus) and the other including species with an XX/XY1Y2 system (R. acetosa and its relatives R. papillaris, R. intermedius, or R. thyrsoides) [Navajas-Pérez et al., 2005a]. Different species represent different stages or degrees of sex chromosome differentiation [Cuñado et al., 2007]: from an undifferentiated stage of genetic differentiation as in R. sagittatus (XX/XY) to an advanced stage of differentiation as in R. acetosa or R. papillaris(XX/XY1Y2) through intermediate stages as in R. suffruticosus or R. acetosella (XX/XY) [Cuñado et al., 2007; Navajas-Pérez et al., 2009b]. The Y chromosomes of XX/XY1Y2 species, but not those of XX/XY species, are heterochromatic and have accumulated a set of diverse repetitive sequences [Shibata et al., 1999, 2000a; Mariotti et al., 2006, 2009; Navajas-Pérez et al., 2006, 2009b; Cuñado et al., 2007; Steflova et al., 2013].

Several satellite DNA families have been found in dioecious Rumex species. The RAYSI family is Y specific and was originally isolated by Shibata et al. [1999]. Several RAYSI subfamilies expand or contract in size presumably by alternating cycles of sudden mechanisms of amplification or elimination [Navajas-Pérez et al., 2006]. A related satellite DNA family, the RAE730 is autosomic [Shibata et al., 2000b; Navajas-Pérez et al., 2005b] and, as the RAYSI repeats, appeared only in the XX/XY1Y2 species of the genus [Navajas-Pérez et al., 2006, 2009b]. The RAE180 satellite DNA [Shibata et al., 2000a] is present in the genomes of all dioecious species [Cuñado et al., 2007; Navajas-Pérez et al., 2005b, 2006, 2009b, c], but in the XX/XY species, RAE180 is located only in a small locus of a pair of autosomes, being poorly represented within their genomes [Cuñado et al., 2007; Navajas-Pérez et al., 2009b, c], and in the XX/XY1Y2 species, in addition to the autosomal locus, the RAE180 repeats have been massively amplified in the Y chromosomes [Cuñado et al., 2007; Navajas-Pérez et al., 2009b, c]. Furthermore, RAYSII and RAYSIII families were identified in the Y chromosomes of R. acetosa[Mariotti et al., 2009]. Recently, following a genomic approach, Steflova et al. [2013] identified Y-chromosome-specific variants of RAE180 and discovered 2 novel satellites: the RA160 satellite dominating on the X chromosome but also present on the Y chromosomes and RA690 localized mostly on the Y1 chromosome. The chromosomal organization of the different satellite DNA sequences in XX/XY and XX/XY1Y2Rumex species demonstrates that active mechanisms of heterochromatin amplification with accumulation and depletion of several kinds of repetitive elements have occurred during sex chromosome evolution and that these mechanisms were accompanied by chromosomal rearrangements, giving rise to the multiple XX/XY1Y2 chromosome systems observed in Rumex. Additionally, Y1 and Y2 chromosomes have undergone further rearrangements that have led to differential patterns of Y heterochromatin distribution between Rumex species with multiple sex chromosome systems [Navajas-Pérez et al., 2009b; Steflova et al., 2013]. Contrary to the accepted picture of Y chromosomes, high rates of colonization by DNA satellites prevented a significant expansion of the transposable elements within the Y chromosomes, although some transposable elements were able to compete with satellites for Y-linked niches, either by a higher insertion rate or a lower removal rate [Steflova et al., 2013]. Kejnovský et al. [2013] have found evidence of microsatellite expansion on the Y chromosome of R. acetosa in contrast to other older Y chromosomes. They have also found that the abundance of microsatellites is higher in the neighborhood of transposable elements, suggesting that microsatellites are probably targets for insertions of transposable elements [Kejnovský et al., 2013]. These authors have suggested that microsatellite expansion would be an early event that shaped Y chromosome evolution, while the accumulation of mobile elements and chromosome shrinkage would have occurred later. Microsatellite accumulation on the Y chromosome in S. latifolia also suggests that the spread of microsatellites predates other structural changes that occurred during the Y chromosome evolution [Kubat et al., 2008].

There are several satellite DNA families within the genome of S. latifolia. One family of repeats composed of several subfamilies is located in the subtelomeric regions of the chromosomes of these species [Bůzek et al., 1997; Garrido-Ramos et al., 1999; Kazama et al., 2006]. In addition, Hobza et al. [2006] characterized a tandem repeat called TRAYC, which has accumulated in the Y chromosome of S. latifolia. This satellite DNA had amplified after the sex chromosomes evolved but before speciation within the section Elisanthe (the species analyzed were the dioecious S. latifolia, S. dioica and S. diclinis). In other species of the genus Silene, this sequence is nearly absent. TRAYC is weakly accumulated within the Y chromosomes near the centromere. Hobza et al. [2006] proposed a role for the centromere as a starting point for the cessation of recombination between the X and Y chromosomes. The absence of TRAYC in other dioecious species, S. otites, supports the idea of 2 independent evolutionary events leading to dioecy in the genus Silene [Hobza et al., 2006]. Cermak et al. [2008] isolated and characterized 2 additional tandem repeats. One of them, STAR-C, was localized at the centromeres of all chromosomes, except the Y chromosome, where it was present on the p arm. Its variant, STAR-Y, carrying a small deletion, was specifically localized on the q arm of the Y chromosome. The tandem repeat TR1 colocalized with the 45S ribosomal RNA genes (rDNA) cluster in the subtelomeres of 5 pairs of autosomes. These 2 studies demonstrate that processes of satellite accumulation are at work even in an early stage of sex chromosome evolution [Hobza et al., 2006]. A high-throughput sequence analysis revealed generally low divergence in repeat composition between the sex chromosomes in S. latifolia, which is consistent with their relatively recent origin [Macas et al., 2011].

The North American endemic R. hastatulus has 2 genetically - but not morphologically - differentiated chromosomal races that differ in their sex chromosome systems [Smith, 1969; Navajas-Pérez et al., 2005a; Quesada del Bosque et al., 2011]. The ‘Texas' race is characterized by a simple XX/XY sex chromosome system, whereas the ‘North Carolina' race has a complex XX/XY1Y2 system. According to molecular data, the North Carolina race of R. hastatulus is classified into the XX/XY group, implying secondary evolution from the XX/XY to the XX/XY1Y2 sex chromosome system [Smith, 1969; Navajas-Pérez et al., 2005a]. An evolutionary change that seems to have occurred independently in 2 lineages of Rumex, one in the ancestor of the XX/XY1Y2 clade (R. acetosa and the Acetosa group) and the other in R. hastatulus, as proposed earlier by Smith [1969]. Despite recent suppression of recombination and low X-Y divergence in both R. hastatulus races, evidence has been found that Y-linked genes have started to undergo gene loss, causing ∼28 and ∼8% hemizygosity of the ancestral and derived X chromosomes, respectively [Hough et al., 2014]. Furthermore, the data gathered by Hough et al. [2014] provide evidence for reduced selection efficiency and ongoing Y chromosome degeneration and indicate that Y degeneration can occur soon after recombination suppression between sex chromosomes. In accordance with those results, Grabowska-Joachimiak et al. [2015] have found heterochromatin in the Y chromosome of the older Texas race, and the heterochromatin found in the Y chromosome of the North Carolina race was largely inherited from the Texas race, which possesses an ancestral XX/XY sex chromosome system and a heterochromatinized Y chromosome. It is plausible that repetitive DNA sequences other than RAE180 repeats are the main component of this heterochromatin in R. hastatulus, since this satellite DNA family is poorly represented in both race genomes [Quesada del Bosque et al., 2011]. It is not common to find plant species with an XX/XY sex chromosome system in which, as in the Texas race of R. hastatulus, the Y chromosome is heterochromatinized. Cannabis sativa is another plant species with a young XX/XY sex chromosome system which bears a heterochromatinized Y chromosome, although the DNA sequences at the Y heterochromatin have not yet been uncovered [Divashuk et al., 2014].

Grabowska-Joachimiak et al. [2015] have demonstrated Smith's postulate that the karyotype of the North Carolina race may have originated from the karyotype of the Texas race in the course of translocation between the autosomes and sex chromosomes. This debate has not been completely resolved with respect to the origin of a multiple sex chromosome system in the Acetosa group of the genus, as 2 alternative explanations have been proposed, i.e. the splitting of one original Y chromosome and the translocation of an autosome onto the X chromosome [Ruiz Rejón et al., 1994; Steflova et al., 2013; Vyskot and Hobza, 2015]. Phylogenetic data gathered by Navajas-Pérez et al. [2005a] do not provide strong support to discriminate between these 2 hypotheses in the section Acetosa, given that the hypothetical XX/XY dioecious ancestor of the Acetosa group of species with XX/XY1Y2 (x = 7) could have had either x = 7 or x = 8 chromosomes, 2 chromosome numbers found in the sister group of dioecious species with an XX/XY system.

Several mechanisms have been proposed to explain the origin of a tandem repeat [Plohl et al., 2012]. Unequal crossing-over is the mechanism that can easily explain the duplication of a sequence in the genome. Strand slippage may also account for the duplication of short stretches of sequences during DNA replication. However, it is difficult to devise a general model describing the forces that explain the emergence, amplification, and spread of a family of tandem repeats. Moreover, it is also useful to separately analyze the molecular mechanisms involved in the appearance of a satellite DNA family and those involved in its subsequent amplification and spreading throughout equilocal sites, according to the concept of equilocality of heterochromatin of Schweizer and Loidl [1987], or wherever non-equilocal sites occur. This is the case even in the event that the same molecular mechanisms may be involved in 3 processes (origin, amplification and spreading) and that origin, amplification and spreading are sometimes used without distinction.

Monomer-repeat sequences give some clues about the mechanisms involved in the origin of a family of tandem repeats. Thus, repeat sequences are often composed of direct subrepeats or motifs that remain as remnants of past events of sequence duplications. For example, RAE730 and RAYSI satellite DNAs of Rumex are composed of repeat DNA sequences of about 727-731 and 922-932 bp, respectively [Navajas-Pérez et al., 2005b]. However, both RAE730 and RAYSI monomers are composed of the repetition of the same basic 120-bp repeat [Navajas-Pérez et al., 2005b]. Two large truncated subrepeats which could have given rise to the current higher-order monomer of 249 bp are identified within the pB6 monomers of P. autumnale. At the same time, each of the 2 subrepeats is typically composed of 3 even smaller secondary subrepeats [Emadzade et al., 2014].

In theory, satellite DNA repeats could be generated by unequal crossing-over of any random sequence. In most cases, however, it is difficult to identify the original sequence seeding the repetitive family. Although, when multiple transitional sequences can be identified, the origin and the complex development of the early stages of satellite repeats can be demonstrated. Intergenic-spacer-derived satellite repeats have been identified in the tomato genome [Jo et al., 2009]. There are several other cases of repetitive DNAs that apparently originated from the tandem duplication of subrepeats of the intergenic spacer of rDNA, which amplified in the genome of the respective species, forming an independent satellite DNA family, e.g. the CC4 repeat family of Phaseolus vulgaris and P. coccineus [Almeida et al., 2012]. Other satellite DNAs with homology to the intergenic spacer of ribosomal DNA were found in the potato and the tobacco genomes [Stupar et al., 2002; Lim et al., 2006]. Furthermore, Jo et al. [2009] found highly divergent genus-specific satellite DNAs that showed sequence similarity with genus-specific intergenic spacers in the family Solanaceae. In this family, the genus-specific satellite DNAs in Solanaceae plants can be generated from differentially organized repeat monomers of the intergenic spacer rather than by accumulation of mutations from pre-existent satellite DNAs [Jo et al., 2009]. In the origin of satellite DNAs, rDNA sequences are not the only sequences involved, since retrotransposons can also give rise to tandem repeats in eukaryotic genomes from successive intrastrand deletions of the mobile elements [Sharma et al., 2013]. Several studies have supported the idea that tandem repetitive families with homology to parts of retrotransposons derive from this class of transposable elements by random recombination and amplification [Macas et al., 2009; Gong et al., 2012].

Molecular mechanisms leading to the appearance of a satellite DNA family and those that imply its copy number increase by amplification and dispersion throughout several sites are intimately related. Satellite DNA represents one of the most dynamic components of genomes, undergoing rapid changes in array size and sequence composition [Plohl et al., 2012]. Rapid amplification/contraction of satellite DNA arrays can appear within short evolutionary time spans. Dramatic amplifications and deletions of satellite DNAs as a result of unequal crossover or large-scale changes, such as transposition, segmental duplications and mechanisms based on rolling-circle replication of extrachromosomal circular DNAs and reinsertion, contribute significantly to the array-length polymorphism as well as to the repeat dispersion throughout the genome [Ma and Jackson, 2006; Navrátilová et al., 2008; Plohl et al., 2012].

Several satellite DNA families may coexist in a genome constituting a library. The library of satellite DNAs represents a permanent source of sequences that can be independently amplified in each specific genome into a dominant satellite DNA, rapidly changing any profile of genomic satellite DNA [Plohl et al., 2012]. Therefore, according to the ‘library' hypothesis [Fry and Salser, 1977], related species share an ancestral set of different conserved satellite DNA families, and each of them may be differentially amplified in each species (fig. 2). The library can persist for long evolutionary periods by reduced action of molecular mechanisms of nonreciprocal exchange [Meštrović et al., 2006]. However, from this library, any of the satellite DNAs may be differentially amplified in each species with the subsequent replacement of one satellite DNA by another in different species. This model of satellite DNA evolution may also explain the differential amplification of monomer variants or subfamilies of a satellite DNA family. The HinfI satellite DNA has been described as a tandem repeat family of sequences [Suárez-Santiago et al., 2007] conserved in the genome of the species of the tribe Cardueae, the largest of the family Compositae [Quesada del Bosque et al., 2014]. At least 9 HinfI subfamilies were present in the common ancestor of Cardueae and each spreads differentially in different genera of every Cardueae subtribes [Quesada del Bosque et al., 2013, 2014].

Fig. 2

A The library model of satellite DNA evolution. Each rectangle represents a repeat unit. Different colors indicate different satellite DNA variants in an ancestral species. Subsequent variation in each species is represented by different color gradients. B Molecular drive is a process that explains intraspecific homogenization and the gradual divergence between species for a family of satellite repeats. See text for details.

Fig. 2

A The library model of satellite DNA evolution. Each rectangle represents a repeat unit. Different colors indicate different satellite DNA variants in an ancestral species. Subsequent variation in each species is represented by different color gradients. B Molecular drive is a process that explains intraspecific homogenization and the gradual divergence between species for a family of satellite repeats. See text for details.

Close modal

Molecular mechanisms of nonreciprocal exchange include the amplification mechanisms discussed above, such as unequal crossover, transposition, segmental duplications, or mechanisms based on rolling-circle replication of extrachromosomal circular DNAs and reinsertion. All these mechanisms, together with gene conversion (another nonreciprocal exchange mechanism), are involved in satellite array homogenization. It might be expected that, in the absence of selective constraints, the sequences of the satellite repeats would freely change so that each one would accumulate specific mutations which make each one unique. However, this is not the case, and members of a satellite DNA family often have an unexpectedly high degree of similarity (fig. 2). Therefore, these family members evolve concertedly with a high rate of intraspecific homogeneity maintained by molecular mechanisms through which mutations spread horizontally to all members of the family [Plohl et al., 2012]. Homogenizing mechanisms would spread new sequence variants appearing in individual repeat units of a family of sequences, and changes would fix in a population of randomly mating individuals by sexual reproduction according to a time-dependent 2-step process called molecular drive, which leads to concerted evolution. This process results in rapid divergence of satellite sequences in reproductively isolated groups of organisms [Dover, 1986; Pérez-Gutiérrez et al., 2012; Plohl et al., 2012]. Pérez-Gutiérrez et al. [2012] demonstrated that in the absence of selective and biological constraints, the rate of concerted evolution of a family of satellite DNA sequences should depend basically on the divergence time between species. In this case, the expected stages of transition during the spread of a sequence variant towards its fixation can be defined [Strachan et al., 1985; Navajas-Pérez et al., 2007]. However, the overall variability profile of satellite DNA monomers in a genome is a complex feature that depends on genomic conservation and divergence of satellite DNAs, distribution and homogenization patterns among variants, putative selective constraints imposed on them, reproduction mode, and population factors [Plohl et al., 2010, 2012]. Therefore, concerted evolution may be slowed down due to satellite DNA location, organization and repeat copy number [Navajas-Pérez et al., 2005b, 2009c], functional constraints [Mravinac et al., 2005], or biological factors [Luchetti et al., 2003; Robles et al., 2004; Suárez-Santiago et al., 2007]. Navajas-Pérez et al. [2005b, 2009c] have shown that reduced rates of recombination diminish the rate of sequence evolution of satellite DNAs. Thus, the RAE180 satellite DNA of Rumex species undergoes a higher sequence change and concerted evolution rates in autosomic than in Y-linked loci [Navajas-Pérez et al., 2009c]. Concerted evolution is usually random, and every version of repeat has an equal probability of being the one that replaces the others. However, some satellite DNAs exhibit sequence conservation of part or of the whole monomer sequence for long evolutionary periods [Cafasso and Chinali, 2014; Mehrotra et al., 2014; Quesada del Bosque et al., 2014]. It has been suggested that functional constraints may be of influence in the preservation of satellite DNAs found in beetles, although biological factors might be responsible for sequence conservation [Pezer et al., 2012]. Gene flow between taxa should reduce the amount of genetic differences between those taxa but should increase the amount of intraspecific variation. Therefore, contrary to the expectations on the concerted evolution model, we should find similar or even higher levels of intraspecific variation than interspecific divergence in an evolutionary scenario of reticulate evolution [Suárez-Santiago et al., 2007; Quesada del Bosque et al., 2013]. In fact, differential speciation pathways gave rise to differential patterns of sequence evolution in different lineages of Centaureinae [Quesada del Bosque et al., 2013] and Cardueae [Quesada del Bosque et al., 2014].

Absence of chromosomal exchanges between nonhomologous chromosomes with lack of chromosome transfer may lead to chromosome-specific subfamilies within a genome [Alexandrov et al., 1988] or even different satellite DNA families [Iwata et al., 2013]. The existence of satellite DNA subfamilies in plants is common [Kazama et al., 2006; Navajas-Pérez et al., 2006; Suárez-Santiago et al., 2007]. In these cases, shared mutations are unambiguously observed in repeats of the same subfamily in exactly the same positions, while at the same sites, all the sequences of the other subfamilies had a different nucleotide. A higher interspecific sequence similarity within subfamilies than between subfamilies is found [Alexandrov et al., 1988; Navajas-Pérez et al., 2006; Quesada del Bosque et al., 2013, 2014].

Genome projects indicated a path leading to exclusion of satellite DNA. Such sequences were relegated and excluded from genome-sequencing projects for obvious reasons, since satellite repeats make their analysis difficult. However, today the arrival of the methodology of high-throughput sequencing of genomes using 454 sequencing or Illumina technologies allows sequencing millions of random fragments of the genome without excluding any sequence, which has opened an exciting prospect for researchers interested in the study of satellite DNA [Macas et al., 2007]. A graph-based clustering and characterization of repetitive sequences in next-generation sequencing data was developed by Novák et al. [2010]. Plant genomes can be efficiently characterized by this graph-based analysis and the graph representation of repeats can be further used to assess the variability and evolutionary divergence of repeat families, discover and characterize novel elements, and aid in subsequent assembly of their consensus sequences [Novák et al., 2010]. RepeatExplorer is a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads [Novák et al., 2013]. The server allows several million sequence reads to be analyzed for the identification of most high and medium copy repeats in genomes [Novák et al., 2013]. The combination of next-generation sequencing and bioinformatics is opening interesting possibilities for an in-depth global genomic analysis, which allows complete information to be compiled about the repeat composition of a specific genome and to uncover new satellite DNA families whose isolation was elusive by conventional methods [Macas et al., 2007, 2011; Hribová et al., 2010; Piednoël et al., 2012; Melters et al., 2013; Steflova et al., 2013; Emadzade et al., 2014; Novák et al., 2014]. In addition, this global perspective will allow different genomes to be compared to gain more accurate information on their different repeat families, repeat copy numbers, intraspecific sequence variability and interspecific sequence divergence, or sequence conservation. In addition, this new approach will allow the current models of satellite DNA evolution to be more efficiently tested. Furthermore, Dodsworth et al. [2015] have recently utilized comparative graph-based clustering of next-generation sequence reads for phylogenetic purposes. Phylogenetic trees are inferred based on the genome-wide abundance of different repeat types treated as continuously varying characters. This methodology may prove especially useful in groups having little genetic differentiation in standard phylogenetic markers, while at the same time providing as data for phylogenetic inference. Also, this method yields a wealth of data for comparative studies of genome evolution [Dodsworth et al., 2015].

Since its discovery 50 years ago, satellite DNA is still one of the most elusive fractions of the eukaryotic genome. Nevertheless, current knowledge of its structure and composition, the abundant data gathered about its origin and evolution, and the exciting perspectives that open new technologies make us optimistic about the possibility that all this knowledge will take satellite DNA out of the rubbish bin.

The research in our laboratory is currently financed by the Ministerio de Ciencia e Innovación and FEDER founds, grant CGL2010-14856 (subprograma BOS).

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