Centromere renewal and replacement in the plant kingdom

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Abstract
Centromere specification has been a topic of intense interest since it became clear that, under the right conditions, human centromeres can form over noncentromeric sites. At least 60 human “neocentromeres” have been described that retain no vestige of the familiar α-satellites and that map to apparently random locations in the genome (1). At the functional and cell biological levels (e.g., association with kinetochore proteins), not a single difference has been detected between standard human centromeres and neocentromeres. These and similar data from Drosophila suggest that animal centromeres are initiated in large part by epigenetic mechanisms (2). In this issue and a recent issue of PNAS, two new articles (3, 4) extend these observations to plants. Lee et al. (3) provide a new evolutionary perspective on centromere evolution, demonstrating that satellite repeats are gained and lost at astonishing rates. Nasuda et al. (4) take the story a step further to show that barley centromeres can move to new positions and that satellite DNA is not necessary for efficient centromere formation. In both plants and animals, the major centromeric DNAs are small 100- to 200-bp satellite repeats that usually are organized in very long arrays. In rice, the major repeat is CentO, and in maize it is CentC. Both are known to interact with the key centromere protein Centromeric Histone H3 (CENH3) (5, 6). Grass centromeres also contain a specialized class of centromeric retroelements (CR elements) that bind to CENH3 and are thoroughly interspersed with the satellites (5). The presumption is that satellite arrays are the primary centromere repeats (5–7), whereas CR elements are either efficient centromere parasites (8) or facilitate the establishment of a centromeric state (9). A central issue in centromere research is the “centromere paradox” (10), the apparent conflict between the importance of centromeric …