Academic journal article Genetics

Trans-Centromere Effects on Meiotic Recombination in the Zebrafish

Academic journal article Genetics

Trans-Centromere Effects on Meiotic Recombination in the Zebrafish

Article excerpt


We report that lack of crossover along one chromosome arm is associated with high-frequency occurrence of recombination close to the opposing arm's centromere during zebrafish meiotic recombination. Our data indicate that recombination behavior on the two arms of a chromosome is linked. These results inform mapping strategies for telomeric mutants.

THE zebrafish (Danio rerio) provides the unique opportunity to recover two of the four haploid genomes produced from a single meiosis using a technique known as early pressure (EP) parthenogenesis (Streisinger et al. 1981, 1986). Recombination events can be reconstructed accurately from the genetic analysis of EP parthenogenotes (Streisinger et al. 1986; Johnson et al. 1995) (supporting information, Figure S1). Analysis of these products can reveal how the occurrence of one recombination event may affect subsequent chromosome behaviors at meiosis.

In this study we investigate recombination behavior of two zebrafish chromosomes for which telomeric recessive mutations are available. In the absence of recombination or following even numbers of crossovers along the length of the relevant chromosome arms, the early pressure (EP) half-tetrad progeny produced from heterozygous females will be homozygous for telomeric alleles. Half of such progeny will express the mutant phenotype (Figure S1).We analyzed mutant EP half-tetrad progeny in detail to identify recombination events that produced sister chromatid pairs homozygous for telomeric markers.


A total of 1243 EP larvae were produced from asm+/- heterozygous F1 females that were generated in a mating between a unique asm+/- P0 founder male and a unique asm1/1 P0 female from the wild-type (WT) Tu strain (Figure 1A and Table S1). As illustrated by the representative genotyping analysis (Figure S2), EP parthenogenesis produced 5-day-postfertilization (dpf) offspring in which homologous pairs of chromosomes were derived fromsister chromatid pairs. All asm mutants were genotyped using nine chromosome 18 simple sequence repeat (SSR) markers that were polymorphic between the parental asm- and asm+ chromosomes (Figure S3). On the basis of analysis of these nine markers, 34 mutants lacked evidence of any recombination between the centromere and the asm locus. Two mutants arose from two-strand double crossovers (dco) (Figure S3C), and 3 mutants arose from four-strand dco (Figure S3D). Additionally, one exceptional individual was heterozygous for markers that flank the centromere and therefore likely was not derived only from a single sister chromatid pair (Figure S3E). In sum, 5/39 (13%) EP half-tetrad mutant progeny arose from sister chromatid pairs that experienced dcos. The products of dcos would be anticipated by established linkage maps of zebrafish, which exceed 100 cM inmany cases ( Johnson et al. 1995; Kauffman et al. 1995). Consistent with our genetic analyses, a recent study using the chiasma-specific MLH1 antibody indicated the occasional presence of at least two chiasmata involving a single chromosome arm during zebrafish female meiosis (Kochakpour and Moens 2008). The MLH1-staining did not distinguish between two-, three-, or four-strand dco and at what frequency they occurred. The data presented here show unambiguously that two-strand and four-strand dco occur at measurable frequency in zebrafish.

Among mutant half-tetrad offspring, nonrecombinant along the right (asm) arm of chromosome 18, we found that the left arm pericentric marker Z9194 was heterozygous more often (20 of 34 ¼ 59%) than would be predicted from the published female map distance of 3.7 cM for the Z9194-centromere interval (Figure 1B). As recombination affecting either of the two left arm sister chromatid strands would produce a heterozygous half-tetrad, 7.4% of the EP progeny are expected to be heterozygous. We analyzed 23 randomly chosen phenotypic wild-type half-tetrad siblings (all recombinant on the right armof chromosome 18) and found that only 2 of 23 (8. …

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