Region-specific activators of meiotic recombination in Schizosaccharomyces pombe.

Abstract

Schizosaccharomyces pombe rec mutants were previously isolated on the basis of their deficiency in meiotic recombination at the ade6 locus. We surveyed their meiotic recombination deficiencies at and between other loci. In reclO mutants recombinant frequencies in the ~2-Mb region surrounding the ade6 locus were reduced 10-to 100-fold, but recombinant frequencies at or between nine other unlinked loci were reduced <3-fold. The reclO mutations are recessive and are on chromosome I; the ade6 region is on chromosome III. These results indicate that the reclO gene product is required for activation of meiotic recombination in the ~2-Mb region surrounding ade6 but not in the other regions surveyed. Similar ade6 regional specificities were observed for rec8 and recll. We infer that there are multiple activators of meiotic recombination, each specific for a limited set of loci, and we discuss how these regional activators may work. The frequency of homologous recombination is not uniform across chromosomes but is controlled by a complex interplay of special sites and gene products. Control sites have been identified in both prokaryotes and eukaryotes, and in some cases the proteins acting at them have been elucidated (Smith 1988). Recombination can also be locally influenced by other chromosomal processes such as transcription (Voelkel-Meiman et al. 1987;Thomas and Rothstein 1989). In all of these cases, the effects are limited to about a few genes or several kilobases from the control site. We report here that the products of the rec8, reclO, and recll genes (Rec8, ReclO, and Recll) of Schizosaccharomyces pombe are required for high meiotic recombinant frequencies in a region covering about one-half (~2 Mb) of chromosome III; the reductions of recombinant frequencies by the rec8, reclO, and recll mutations are 10-to 100-fold greater in this region than in the other regions examined. These results imply recombination regulatory factors acting only in parts of the genome and over considerably larger distances than in previously reported cases.Meiotic recombination-deficient [rec] mutants of S. pombe were isolated by screening for deficiency of recombination between chromosomal and plasmid-bome alleles of the ade6 locus (Ponticelli and Smith 1989;DeVeaux et al. 1992). They were subsequently shown to be deficient for recombination between homologous chroPiesent address: 1527 143td Avenue SE, Tenino, Washington 98589 USA.mosomes. The 39 recessive mutations analyzed defined 16 complementation groups spread throughout the genome.The rec mutations have a wide range of effects on meiotic recombination (Ponticelli and Smith 1989;DeVeaux et al. 1992). At the ade6 locus, recombinant frequencies are reduced from 3-to 1000-fold, depending on the rec gene mutated. When intragenic recombination (at the ura4 locus) and intergenic recombination (between the pro2 and arg3 loci) were tested, the recombinant frequencies in some rec mutants were reduced much less than those at ade6. These differential reductions might have been attributable...

Linear Element-Independent Meiotic Recombination in Schizosaccharomyces pombe

“…We noted that crossovers in the leu2-lys7 interval (see Figure 1 for location) on chromosome I were reduced in rec10-144 homozygous zygotic crosses, relative to the rec10 1 control (Figure 2). Recombination in this interval was previously reported to be unaltered in rec10-109 homozygous crosses (De Veaux and Smith 1994). Our data using rec10-144 indicate that Rec10 is influencing recombination in intervals outside the previously reported middle regions (De Veaux and Smith 1994).…”

“…This is consistent with the observation that S. cerevisae Red1 null mutants are defective for recombination at some, but not all loci (Rockmill and Roeder 1990). The regional specificity of the rec10-109 mutant shows that Rec10 regulates recombination in the middle region of chromosomes, a pattern similar to that observed for the meiosis-specific cohesins, Rec8 and Rec11, although residual LinEs have been observed in this mutant, suggesting that it is not totally defective in LinE function (De Veaux and Smith 1994;Krawchuk et al 1999;Parisi et al 1999;Lorenz et al 2004). The similar regional pattern of recombination in the rec10-109 and cohesion mutants indicate that there is an intimate functional association between meiotic cohesins and LinEs.…”

“…Recombination in this interval was previously reported to be unaltered in rec10-109 homozygous crosses (De Veaux and Smith 1994). Our data using rec10-144 indicate that Rec10 is influencing recombination in intervals outside the previously reported middle regions (De Veaux and Smith 1994). We examined this further by looking at another interval, his4-lys4, on chromosome II (Figure 1), for which recombination was also previously reported to be rec10 independent (De Veaux and Smith 1994).…”

“…Rec10 is required for regulation of recombination throughout the genome: Rec10-controlled recombination in the middle regions of S. pombe chromosomes has been demonstrated by genetic analysis using rec10-109, a mutant allele generated by chemical mutagenesis (De Veaux and Smith 1994;Krawchuk et al 1999). However, LinEs form in the rec10-109 mutant during meiosis at the appropriate time, albeit with an altered morphological profile, and may retain some function for activation of recombination (Lorenz et al 2004).…”

“…However, until now the question of whether or not LinEs are essential for meiotic recombination remained unanswered (Loidl 2006). Further detailed analysis of one particular rec10 mutant, rec10-109, indicated that 1 Rec10 functions to regulate recombination in a regionspecific fashion (De Veaux and Smith 1994;Krawchuk et al 1999). This is consistent with the observation that S. cerevisae Red1 null mutants are defective for recombination at some, but not all loci (Rockmill and Roeder 1990).…”