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

By Thomas, Sharon E.; McKee, Bruce D. | Genetics, October 2007 | Go to article overview

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


Thomas, Sharon E., McKee, Bruce D., Genetics


ABSTRACT

In most eukaryotes, segregation of homologous chromosomes during meiosis is dependent on crossovers that occur while the homologs are intimately paired during early prophase. Crossovers generate homolog connectors known as chiasmata that are stabilized by cohesion between sister-chromatid arms. In Drosophila males, homologs pair and segregate without recombining or forming chiasmata. Stable pairing of homologs is dependent on two proteins, SNM and MNM, that associate with chromosomes throughout meiosis I until their removal at anaphase I. SNM and MNM localize to the rDNA region of the X-Y pair, which contains 240-bp repeats that have previously been shown to function as cis-acting chromosome pairing/segregation sites. Here we show that heterochromatic mini-X chromosomes lacking native rDNA but carrying transgenic 240-bp repeat arrays segregate preferentially from full-length sex chromosomes and from each other. Mini-X pairs do not form autonomous bivalents but do associate at high frequency with the X-Y bivalent to form trivalents and quadrivalents. Both disjunction of mini-X pairs and multivalent formation are dependent on the presence of SNM and MNM. These results imply that 240-bp repeats function to mediate association of sex chromosomes with SNM and MNM.

PAIRING of homologous chromosomes is an essential step in meiosis, setting the stage for the segregation of homologs to opposite poles (Page and Hawley 2003; McKee 2004). In most eukaryotes, pairing is accompanied by high frequencies of recombination and by formation of synaptonemal complexes, proteinaceous structures that connect homologs from end to end during the pachytene stage of meiotic prophase. Segregation of homologs requires not only that they pair but also that they undergo at least one crossover. Crossovers generate cytologically visible linkers known as chiasmata, which are essential tomaintaining bivalent integrity throughout late prophase I and metaphase I (Hawley 1988).

However, synaptonemal complexes, crossing over, and chiasmata are not universal prerequisites for meiotic chromosome segregation. 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, andMod(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.

Segregation of the X and Y chromosomes in Drosophila also depends upon pairing between specific sites located in the central region of the proximal X heterochromatin and on the short arm of the Y near the centromere. These sites coincide approximately with the locations of the X and Y rDNA arrays, which consist of 200-250 tandem copies of the genes for the 18S, 28S, and 5.8S ribosomal RNAs (rRNAs) (Ritossa 1976). Several findings have implicated therDNAin X-Ypairing.X heterochromatic deletions that remove all of the rDNA causeX-Y pairing failure andX-Y nondisjunction (NDJ) during meiosis I(McKeeandLindsley1987)but deletions that retain as few as six to eight rDNA repeats also retain pairing and disjunctional ability (Appels and Hilliker 1982;McKee andLindsley 1987). Similarly, mini-Xchromosomes generated by deletion of most of the euchromatin and variableamounts of the heterochromatin have been shown to segregate regularly from attached-XY chromosomes if they retain part of therDNA locus but to disjoin randomly from attached-XYs if they are completely deficient for the rDNA (LINDSLEY and SANDLER 1958; PARK and YAMAMOTO 1995; KARPEN et al. …

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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
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