Independently Regulated Neocentromere Activity of Two Classes of Tandem Repeat Arrays

Abstract

Tandem repeat arrays often are found in interstitial (i.e., normally gene-rich) regions on chromosomes. In maize, genes on abnormal chromosome 10 induce the tandem repeats that make up knobs to move poleward on the meiotic spindle. This so-called neocentromere activity results in the preferential recovery, or meiotic drive, of the knobs in progeny. Here we show that two classes of repeats differ in their capacity to form neocentromeres and that their motility is controlled in trans by at least two repeat-specific activators. Microtubule dynamics appear to contribute little to the movement of neocentromeres (they are active in the presence of taxol), suggesting that the mechanism of motility involves microtubule-based motors. These data suggest that maize knob repeats and their binding proteins have coevolved to ensure their preferential recovery in progeny. Neocentromere-mediated drive provides a plausible mechanism for the evolution and maintenance of repeat arrays that occur in interstitial positions. INTRODUCTIONMany plants and animals have long arrays of tandem repeats in interstitial positions on chromosome arms (John and Miklos, 1979;Rodionov, 1999). Two such repeats in maize, one that is 180 bp and another that is 350 bp (TR-1), occupy condensed regions known as knobs (Peacock et al., 1981;Dennis and Peacock, 1984;Ananiev et al., 1998a). Knobs are found at 22 different positions in the karyotype and are strikingly polymorphic, making them excellent cytological markers (Longley, 1938;Kato, 1984). They also have the capacity to behave like centromeres, or "neocentromeres," in the presence of an unusual form of chromosome 10 ( Rhoades and Vilkomerson, 1942). In strains carrying normal chromosome 10 (N10), the knobs are quiescent, whereas in strains carrying abnormal chromosome 10 (Ab10), knobs at all positions in the genome move rapidly poleward on the meiotic spindle, dragging their chromosome arms with them (Rhoades and Vilkomerson, 1942). The mechanism of neocentromere activity remains a mystery, although it is known that neocentromeres lack two major kinetochore proteins, CENPC and MAD2 Yu, 2000), and interact with microtubules in a lateral manner instead of in the end-on manner typical of maize centromeres (Yu et al., 1997).Neocentromere activity plays an integral role in an associated phenotype known as meiotic drive. Meiotic drive has been documented in a variety of organisms (Lyttle, 1993), in which it is usually associated with several linked loci that collectively confer a segregation advantage to the linkage group. Meiotic drive systems presumably have evolved to "beat Mendel's rules" and therefore maximize their representation in the population (Sandler and Novitski, 1957). In some organisms, meiotic drive is a result of unusual chromosome segregation in meiosis (Rhoades, 1952;Cazemajor et al., 2000), and in others, it is caused by events that follow meiosis (Raju, 1996;Merrill et al., 1999). In maize, meiotic neocentromere activity at the large knob on Ab10 is thought to preferentially pull Ab10...

Human centromere repositioning “in progress”

“…The extent of the neocentromere phenomenon in lower organisms remains unknown because of the fact that these organisms are infrequently karyotyped. In addition to humans, neocentromere formation has been reported in Drosophila (26,35,36) and a number of plant species (43). The most extensively studied neocentromeres in plants are ''maize knobs,'' which have been shown to act as facultative centromeres at meiosis and provide meiotic drive advantage (43,44).…”

The Maize Ab10 Meiotic Drive System Maps to Supernumerary Sequences in a Large Complex Haplotype

“…In addition, although acentric fragments are generally immobile, neocentromere activity draws the knobbed acentric fragment poleward. The knob on Inv3a contains long arrays of both the 180-bp and TR-1 repeats (Hiatt et al 2002), and neocentromere activity of either alone is probably sufficient to move the fragment.…”

“…The Ab10 haplotype domains were computationally extracted and straightened (Dawe et al 1994). For visual assays of neocentromere activity, cells were processed for fluorescent in situ hybridization (FISH) to reveal the TR-1 and 180-bp repeats as previously described (Hiatt et al 2002).…”

“…There are three different types of maize knobs: those composed primarily of 180-bp repeats, those composed primarily of TR-1 repeats, and those containing both repeats in separate parts of the knob (Ananiev et al 1998;Hiatt et al 2002). Both 180-bp-containing and TR-1-containing knobs behave as neocentromeres, although they are controlled by different trans-acting factors on Ab10 (Hiatt et al 2002).…”

“…Both 180-bp-containing and TR-1-containing knobs behave as neocentromeres, although they are controlled by different trans-acting factors on Ab10 (Hiatt et al 2002). A mutant of meiotic drive (Smd1) with reduced neocentromere activity has been described (Dawe and Cande 1996).…”