Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes

Abstract

We carried out a global survey of all major types of transposable elements in Silene latifolia, a model species with sex chromosomes that are in the early stages of their evolution. A shotgun genomic library was screened with genomic DNA to isolate and characterize the most abundant elements. We found that the most common types of elements were the subtelomeric tandem repeat X-43.1 and Gypsy retrotransposons, followed by Copia retrotransposons and LINE non-LTR elements. SINE elements and DNA transposons were less abundant. We also amplified transposable elements with degenerate primers and used them to screen the library. The localization of elements by FISH revealed that most of the Copia elements were accumulated on the Y chromosome. Surprisingly, one type of Gypsy element, which was similar to Ogre elements known from legumes, was almost absent on the Y chromosome but otherwise uniformly distributed on all chromosomes. Other types of elements were ubiquitous on all chromosomes. Moreover, we isolated and characterized two new 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 second tandem repeat, TR1, co-localized with the 45S rDNA cluster in the subtelomeres of five pairs of autosomes. FISH analysis of other Silene species revealed that some elements (e.g., Ogre-like elements) are confined to the section Elisanthe while others (e.g. Copia or Athila-like elements) are present also in more distant species. Similarly, the centromeric satellite STAR-C was conserved in the genus Silene whereas the subtelomeric satellite X-43.1 was specific for Elisanthe section. Altogether, our data provide an overview of the repetitive sequences in Silene latifolia and revealed that genomic distribution and evolutionary dynamics differ among various repetitive elements. The unique pattern of repeat distribution is found on the Y chromosome, where some elements are accumulated while other elements are conspicuously absent, which probably reflects different forces shaping the Y chromosome.

The role of repetitive DNA in structure and evolution of sex chromosomes in plants

“…The different evolutionary pressures acting on non-recombining regions influence TE distribution and affect sex chromosome evolution. We speculate that for some TEs recombination is an essential condition for transposition (Cermak et al, 2008). We can also speculate that different repetitive elements occupy the nonrecombining part of the Y chromosome in different evolutionary steps of X-Y diversification.…”

“…It is interesting that the CENP-B satellite is absent on the Y chromosome in a number of mammalian species from the only centromere in the genome that does not have a pairing partner in meiosis (Kipling and Warburton, 1997). Similarly, centromeric satellites STAR-C and STAR-Y are underrepresented only in centromeres of the Y chromosome in Silene latifolia Cermak et al, 2008).…”

“…The first active MITE elements in S. latifolia were described by Bergero et al (2008). A comprehensive systematic study of repetitive DNA in S. latifolia showed that Copia retroelements are the most abundant DNA element on the Y chromosome (Cermak et al, 2008). Cermak et al (2008) also showed the enigmatic distribution of the Ogre-like retroelement, which colonizes only recombining parts of the genome of S. latifolia (is absent in non-recombining parts of the Y chromosome).…”

“…A comprehensive systematic study of repetitive DNA in S. latifolia showed that Copia retroelements are the most abundant DNA element on the Y chromosome (Cermak et al, 2008). Cermak et al (2008) also showed the enigmatic distribution of the Ogre-like retroelement, which colonizes only recombining parts of the genome of S. latifolia (is absent in non-recombining parts of the Y chromosome). This distribution of Ogre-like elements could be explained either by their spreading in connection with the recombination machinery or by their activity only in females, for example, because of some inhibition mechanisms (for example, RNAi) present only Repetitive DNA and plant sex chromosomes E Kejnovsky et al in males.…”

“…Most TEs are distributed uniformly along both the X and Y chromosomes. Two exceptions are Retand elements, which are localized at subtelomeres (Kejnovsky et al, 2006b) and Ogre-like elements, which are present on whole X chromosome but restricted to the PAR region of the Y chromosome (Cermak et al, 2008). Tandem repeats colonize the centromeres (STAR-C) and subtelomeres (X-43.1) of X chromosome, whereas in the Y chromosome STAR-C and STAR-Y are located in the middle of both arms and X-43.1 is at the subtelomere of the q-arm.…”