ABSTRACT
Homologous chromosome pairing is a prerequisite to establish physical linkage between homologs, which is critical for faithful chromosome segregation during meiosis I. The establishment of pairing is genetically separable from subsequent synapsis, defined as stabilization of pairing by the synaptonemal complex (SC). The underlying mechanism of presynaptic pairing is poorly understood. In the nematode Caenorhabditis elegans, a unique cis-acting element, the pairing center (PC), is essential for presynaptic pairing; however, it is not known whether and how the remainder of the chromosome contributes to presynaptic pairing. Here we report direct evidence for presynaptic pairing activity intrinsic to non-PC regions, which is facilitated by a conserved chromodomain protein, MRG-1. In mrg-1 loss-of-function mutants, pairing is compromised specifically in non-PC regions, leading to nonhomologous SC assembly. Our data support a model in which presynaptic alignment in non-PC regions collaborates with initial PC pairing to ensure correct homologous synapsis.
Subject(s)
Caenorhabditis elegans Proteins/genetics , Caenorhabditis elegans Proteins/metabolism , Caenorhabditis elegans/genetics , Caenorhabditis elegans/metabolism , Chromosome Pairing/genetics , Chromosome Pairing/physiology , Animals , Animals, Genetically Modified , Caenorhabditis elegans/cytology , Genes, Helminth , Meiosis/genetics , Meiosis/physiology , Mutation , Synaptonemal Complex/genetics , Synaptonemal Complex/metabolismABSTRACT
Although Mendel's first law predicts that crosses between XY (or XO) males and XX females should yield equal numbers of males and females, individuals in a wide variety of metazoans transmit their sex chromosomes unequally and produce broods with highly skewed sex ratios. Here, we report two modifications to the cellular programme of spermatogenesis, which, in combination, help to explain why males of the free-living nematode species Rhabditis sp. SB347 sire <5% male progeny. First, the spermatogenesis programme involves a modified meiosis in which chromatids of the unpaired X chromosome separate prematurely, in meiosis I. Second, during anaphase II, cellular components essential for sperm motility are partitioned almost exclusively to the X-bearing sperm. Our studies reveal a novel cellular mechanism for the differential transmission of X-bearing sperm and suggest Rhabditis sp. SB347 as a useful model for studying sex chromosome drive and the evolution of new mating systems.
