Evolutionary dynamics and sites of illegitimate recombination revealed in the interspersion and sequence junctions of two nonhomologous satellite DNAs in cactophilic Drosophila species

Abstract

Satellite DNA (satDNA) is a major component of genomes but relatively little is known about the fine-scale organization of unrelated satDNAs residing at the same chromosome location, and the sequence structure and dynamics of satDNA junctions. We studied the organization and sequence junctions of two nonhomologous satDNAs, pBuM and DBC-150, in three species from the neotropical Drosophila buzzatii cluster (repleta group). In situ hybridization to microchromosomes, interphase nuclei and extended DNA fibers showed frequent interspersion of the two satellites in D. gouveai, D. antonietae and, to a lesser extent, D. seriema. We isolated by PCR six pBuM Â DBC-150 junctions: four are exclusive to D. gouveai and two are exclusive to D. antonietae. The six junction breakpoints occur at different positions within monomers, suggesting independent origin. Four junctions showed abrupt transitions between the two satellites, whereas two junctions showed a distinct 10 bp tandem duplication before the junction. Unlike pBuM, DBC-150 junction repeats are more variable than randomly cloned monomers and showed diagnostic features in common to a 3-monomer higher-order repeat seen in the sister species D. serido. The high levels of interspersion between pBuM and DBC-150 repeats suggest extensive rearrangements between the two satellites, maybe favored by specific features of the microchromosomes. Our interpretation is that the junctions evolved by multiples events of illegitimate recombination between nonhomologous satDNA repeats, with subsequent rounds of unequal crossing-over expanding the copy number of some of the junctions.

Characterization and Genomic Organization of <i>PERI</i>, a Repetitive DNA in the <i>Drosophila buzzatii</i> Cluster Related to <i>DINE-1</i> Transposable Elements and Highly Abundant in the Sex Chromosomes

“…In another study, Casals et al [2005Casals et al [ , 2006 showed a preferential accumulation of several class-II transposable elements in pericentromeric zones of polytene chromosomes, defined as transitions between heterochromatin and euchromatin (probably ␤ -heterochromatin). Finally, using PCR, we did not find evidence of interspersion between one of the class II TE elements ( Galileo ) analysed by Casals et al [2005Casals et al [ , 2006, and satDNA repeats [Kuhn et al, 2009]. Thus, the available information suggests non-overlapping patterns or low levels of interspersion between the verified TEs and satDNAs in the buzzatii cluster.…”

“…The microchromosomes (also known as 'dot' chromosomes) are also highly heterochromatic. In previous studies, we determined the chromosome location of 2 satDNA families, pBuM and DBC-150, on the metaphase chromosomes of several species of the buzzatii cluster [Kuhn et al, 2007[Kuhn et al, , 2008[Kuhn et al, , 2009. In D. serido , fig.…”

Non-parental banding patterns in recombinant inbred line population of maize with SSR markers

“…The ability of these sequences to change their copy number is thought to promote chromosomal rearrangements (Badaeva et al, 2007). For example, satellite DNA families are involved in recombination events in Drosophila (Kuhn et al, 2009) and play a central role in chromosome evolution in plants (Raskina et al, 2008). The role of several SSRs in chromosome organization has also been demonstrated in wheat and rye (Cuadrado and Schwarzacher, 1998).…”

The non-regular orbit: three satellite DNAs in Drosophila martensis (buzzatii complex, repleta group) followed three different evolutionary pathways

“…Alternatively, the three DBC-150 variants of D. martensis may be part of a higher-order repeat, i.e., multimers with a number of diverged monomers. For example, in one species of the BCS, D. antonietae, we found DBC-150 repeat units made up of dimers (2-mer) displaying 12.2% variability between the two subrepeats, but 6% between the dimers (Kuhn et al 2009). Unfortunately, we could not examine the genomic and/or chromosomal organization of DBC-150 variants in D. martensis because living strains are no longer available in Drosophila stock centers.…”

“…The DBC-150 repeats from D. martensis were clearly allocated in a specific branch, separated from all other DBC-150 variants found in the BCS, including the more differentiated higher-order repeats of D. serido and the DBC-150 repeats from some sequence junctions found in D. gouveai and D. antonietae (Kuhn et al 2009). The 11 DBC-150 repeats from D. martensis further splits into three main branches corresponding to the three main variants of DBC-150 found in this species.…”