Orientation of nonrandomly segregating sex chromosomes in spermatocytes of the flea beetle, Alagoasa bicolor L.

Abstract

In males of the flea beetle, Alagoasa bicolor L., spermatocytes have two achiasmate sex chromosomes, X and Y, each of which is approximately five times larger than the ten pairs of chiasmate autosomes. At metaphase I, these univalent sex chromosomes are located on a spindle domain separated from the autosomal spindle domain by a sheath of mitochondria. A single centriole pair is located at each pole of the spindle. In prometaphase I, each sex chromosome appears to maintain an attachment to both spindle poles via kinetochore microtubules (i.e., amphitelic orientation). Before anaphase I, this orientation changes to the syntelic orientation (both sister kinetochores connected to the same pole), perhaps by the release of microtubule attachments from the more distant pole by each of the chromosomes. The syntelic orientation just prior to anaphase I leaves each sex chromosome attached to the nearest pole via kinetochore microtubules, ensuring nonrandom segregation. As the sex chromosomes reorient, the autosomes follow in a sequential manner, starting with the bivalent closest to the sex spindle domain. We report here data that shed new light on the mechanism of this exceptional meiotic chromosome behavior.

Microtubule distribution during meiosis I in flea-beetle[Alagoasa(Oedionychus)] spermatocytes: evidence for direct connections between unpaired sex chromosomes

“…Virkki mentions the absence of a 'firm connection' between sex chromosomes, based primarily on observations using phasecontrast microscopy (Virkki, 1972). Three other publications claim to find no evidence for microtubule connections between sex chromosomes (Virkki, 1985;Kupfer and Wise, 2000a;Green-Marroquin et al, 2001). Unfortunately, these publications refer to unpublished work or do not present figures that clearly show the region between the sex chromosomes, and therefore there is little or no published evidence for or against a connection.…”

“…Recent data (Forer and Wilson, 2000;Green-Marroquin et al, 2001) have shown that, in fact, the sex-chromosome spindle shares poles with the autosomal spindle. Nevertheless, the behaviour of the chromosomes in flea-beetle primary spermatocytes gives rise to several unanswered questions.…”

“…Although remaining at the cell periphery, the sex chromosomes do make connections to opposite poles and move towards opposite poles, but the details of this process are unknown. For example, it remains unclear how the unpaired sex chromosomes manage to orient to opposite poles; several studies reject the notion that there are connections or physical interactions between the sex chromosomes (Virkki, 1972;Virkki, 1985;Kupfer and Wise, 2000a;Green-Marroquin et al, 2001). With respect to sexchromosome spindle fibres, Virkki (Virkki, 1971;Virkki, 1972;Virkki, 1985) described them as syntelic (i.e.…”

“…each sex chromosome has fibres extending to only one spindle pole); more recently, Green-Marroquin et al argued that the sexchromosome spindle connections are initially amphitelic (i.e. each sex chromosome has fibres extending to both poles) and later become syntelic (Green-Marroquin et al, 2001). Unfortunately, none of the studies provide sufficient evidence to be convincing and none include a comprehensive study of microtubule organization within the two spindles.…”