Rapid centromere evolution in potato: invasion of the satellite repeats.

In contrast to the gene-rich chromosome arms, the sequence of a typical plant centromere contains a large amount of repetitive DNA, most commonly large tracts of tandemly repeated sequences, or satellite DNA. However, the question of how this arrangement of sequences comes about is still a matter of active debate (reviewed in Malik and Henikoff, 2009). Centromere sequence evolves rapidly, possibly in response to competition among centromeres during female meiosis, where only one out of four meiotic products survives in the oocyte. Recombination, which may homogenize centromere repeats, acts in opposition to mutation and transposon insertion, which alter centromere repeats. Expansion of centromere repeat domains, selected for by competition to survive female meiosis, is counterbalanced by mechanisms to prevent distortion of segregation. In addition to having dynamic sequence and size, centromeres can move, either changing position gradually or forming in other regions of the chromosome (reviewed in Birchler et al., 2011), including regions without typical centromere sequence composition. Epigenetically defined, centromeres can also become inactive to prevent formation of dicentric chromosomes. One of the hallmarks of the epigenetically defined functional centromere is the presence of a centromere-specific histone variant, CENH3. Gong et al. (3559–3574) use this marker to conduct a genome-wide survey of the sequence composition of the potato (Solanum tuberosum) centromere. The authors first identify potato CENH3 and validate its centromere localization, then use anti-CENH3 antibodies to enrich for CENH3-associated DNA fragments by chromatin immunoprecipitation. Highthroughput sequencing of these fragments and alignment to the potato genome revealed that six of the 12 potato chromosomes have tandem repeat–based centromeres, but five centromeres do not contain a tandem repeat. One centromere contains both single/low-copy sequences and satellite repeats. The centromeres that do not contain a tandem repeat have singleor lowcopy sequences and actively transcribed genes, as found by annotation and confirmed by RT-PCR. Among the centromeres with tandem repeats, the repeat sequence is present in the typical megabase-sized arrays. However, the repeat monomer size is substantially longer than the typical centromere satellite (979 bp to 5.4 kb in potato, compared with typical satellites of 135 to 195 bp in other plants). Also, the monomer sequence differed substantially between centromeres; for example, the St24 repeat only hybridizes to the potato chromosome 1 centromere (see figure, top panel). Moreover, examination of these repeats in other Solanum species reveals that the repeats are rapidly evolving; for example, in the closely related Solanum verrucosum, the St24 repeat is on a different chromosome (see figure, bottom panel), and St24 is not present in other tested Solanum species. Indeed, the authors find that five of the six centromere repeats emerged recently in potato, including three repeats that emerged in potato since it diverged from S. verrucosum. This work supports a model in which tandem repeats invade an epigenetically defined centromere, possibly by integration of a large array that amplified de novo. As in potato, different centromeres start with different tandem repeats, but these become homogenized over time. An intriguing model, this leaves many questions for future research, such as why and how a single tandem repeat eventually occupies all centromeres in most species and what mechanism generates the multiple tandem arrays in the potato centromeres.