Identification of Two Proteins Required for Conjunction and Regular Segregation of Achiasmate Homologs in Drosophila Male Meiosis

Abstract

In Drosophila males, homologous chromosomes segregate by an unusual process involving physical connections not dependent on recombination. We have identified two meiotic proteins specifically required for this process. Stromalin in Meiosis (SNM) is a divergent member of the SCC3/SA/STAG family of cohesin proteins, and Modifier of Mdg4 in Meiosis (MNM) is one of many BTB-domain proteins expressed from the mod(mdg4) locus. SNM and MNM colocalize along with a repetitive rDNA sequence known to function as an X-Y pairing site to nucleolar foci during meiotic prophase and to a compact structure associated with the X-Y bivalent during prometaphase I and metaphase I. Additionally, MNM localizes to autosomal foci throughout meiosis I. These proteins are mutually dependent for their colocalization, and at least MNM requires the function of teflon, another meiotic gene. SNM and MNM do not colocalize with SMC1, suggesting that the homolog conjunction mechanism is independent of cohesin.

Meiotic Pairing and Disjunction of Mini-X Chromosomes in Drosophila Is Mediated by 240-bp rDNA Repeats and the Homolog Conjunction Proteins SNM and MNM

“…A plausible alternative is that the 240-bp repeats mediate X-Y pairing during early prophase I, the period when homologous sequences are intimately paired, independently of SNM and MNM, and that SNM and MNM are recruited to already paired X and Y chromosomes to stabilize their association during the later stages of meiosis I. This scenario is consistent with our finding that SNM and MNM are dispensable for pairing of homologous autosomal sequences during early prophase I (Thomas et al 2005) and with previous suggestions that cytologically visible X-Y connections (sometimes referred to as ''collochores'') during prometaphase I and metaphase I are near but distinct from the rDNA arrays (Cooper 1964).…”

“…During prophase I, MNM and SNM localize to multiple foci in the nucleolus where the 240-bp repeats also reside. Following chromosome condensation and nucleolar dissolution at prometaphase I, MNM and SNM colocalize to a dense focus associated with the X-Y bivalent and coincident with the 240-bp repeats (Thomas et al 2005). However, the mechanism by which SNM and MNM associate with the X-Y pairing region is not understood.…”

“…Recent data show that stable conjunction and accurate segregation of all four homolog pairs in Drosophila male meiosis depends upon two proteins: stromalin in meiosis (SNM), a homolog of the SCC3/SA cohesin proteins, and Mod(mdg4) in meiosis (MNM), a BTB domain protein (Thomas et al 2005). SNM and MNM colocalize to meiotic chromosomes throughout prophase I and metaphase I but disappear at the onset of anaphase I, suggesting that they function directly in stabilization of pairing, i.e., as substitutes for chiasmata.…”

“…Achiasmate segregation, i.e., segregation of homologs without chiasmata, is found in one sex or the other in several groups of eukaryotes (Wolf 1994). In Drosophila male meiosis, crossing over is normally completely absent and the homologs fail to form either synaptonemal complexes or chiasmata, yet homologs are stably conjoined during late prophase I and metaphase I and segregate from one another with great regularity during anaphase I.Recent data show that stable conjunction and accurate segregation of all four homolog pairs in Drosophila male meiosis depends upon two proteins: stromalin in meiosis (SNM), a homolog of the SCC3/SA cohesin proteins, and Mod(mdg4) in meiosis (MNM), a BTB domain protein (Thomas et al 2005). SNM and MNM colocalize to meiotic chromosomes throughout prophase I and metaphase I but disappear at the onset of anaphase I, suggesting that they function directly in stabilization of pairing, i.e., as substitutes for chiasmata.…”

Localization of the Genetic Determinants of Meiosis Suppression in Daphnia pulex

“…Because sex-specific meiosis genes are known to exist in Drosophila (Baker 1975;Bopp et al 1999;Tomkiel et al 2001;Hirai et al 2004;Thomas et al 2005), and sex-specific differences exist in meiotic progression and dysfunction in mammals (Morelli and Cohen 2005), the restriction of a meiosis-suppressing gene to one sex may entail no special requirements.…”