Germ cells are distinct from somatic cells in their immortality, totipotency, and ability to undergo meiosis. Candidates for components that guide the unique germline program are the distinctive granules observed in germ cells of many species. We show that a component of germ granules is essential for fertility in C. elegans and that its primary function is in germline proliferation. This role has been revealed by molecular and genetic analyses of pgl-1. PGL-1 is a predicted RNA-binding protein that is present on germ granules at all stages of development. Elimination of PGL-1 results in defective germ granules and sterility. Interestingly, PGL-1 function is required for fertility only at elevated temperatures, suggesting that germline development is inherently sensitive to temperature.
Meiotic chromosomes are organized about a proteinaceous core that forms between replicated sister chromatids. We have isolated a Caenorhabditis elegans gene, him-3, which encodes a meiosis-specific component of chromosome cores with some similarity to the yeast lateral element protein Hop1p. Antibodies raised against HIM-3 localize the protein to condensing chromosomes in early prophase I and to the cores of both synapsed and desynapsed chromosomes. In RNA interference experiments, chromosomes appear to condense normally in the absence of detectable protein but fail to synapse and form chiasmata, indicating that HIM-3 is essential for these processes. Hypomorphs of him-3, although being synapsis proficient, show severe reductions in the frequency of crossing-over, demonstrating that HIM-3 has a role in establishing normal levels of interhomolog exchange. Him-3 mutants also show defects in meiotic chromosome segregation and the persistence of the protein at the chromosome core until the metaphase I-anaphase I transition suggests that HIM-3 may play a role in sister chromatid cohesion. The analysis of him-3 provides the first functional description of a chromosome core component in a multicellular organism and suggests that a mechanistic link exists between the early meiotic events of synapsis and recombination, and later events such as segregation. [Key Words: C. elegans; chromosome core; synapsis; crossing-over; segregation]Received April 12, 1999; revised version accepted July 19, 1999. Meiosis is two specialized cell divisions that result in daughter cells with half the chromosome number of the parental cell. This is accomplished by a single round of DNA replication followed by two divisions, anaphase I and II. Anaphase I is unique in that it segregates homologous chromosomes, each composed of a pair of sister chromatids joined by a single kinetochore, from each other. Most organisms use crossing-over, cytologically evident as chiasmata, to direct the segregation of chromosomes at this division. A decrease in the frequency of crossing-over generally leads to an increase in the nondisjunction of chromosome pairs (for review, see Hawley 1988). For exchange to occur in most organisms, homologous chromosomes must find one another in the prophase nucleus and align themselves throughout their lengths, a process that usually culminates in the formation of a tripartite proteinaceous structure, the synaptonemal complex (SC) (Moses 1968;von Wettstein et al. 1984;Heyting 1996). A prerequisite to the assembly of the mature SC is the polymerization of single proteinaceous axes between sister chromatids, which have been referred to as axial elements or chromosome cores (Moses 1968). The axial elements of homologous chromosomes become aligned and equidistantly separated by the proteins that constitute the central region of the SC and are then referred to as lateral elements. The conserved, highly ordered nature of the SC has raised questions concerning its function and protein composition. Although the localization of axi...
PGL-1 is a constitutive protein component of C. elegans germ granules, also known as P granules. Maternally supplied PGL-1 is essential for germline development but only at elevated temperature, raising the possibility that redundant factors provide sufficient function at lower temperatures. We have identified two PGL-1-related proteins, PGL-2 and PGL-3, by sequence analysis of the C. elegans genome and by a yeast two-hybrid screen for proteins that interact with PGL-1. PGL-3 is associated with P granules at all stages of development, while PGL-2 is associated with P granules only during postembryonic development. All three PGL proteins interact with each other in vitro. Furthermore, PGL-1 and PGL-3 are co-immunoprecipitated from embryo extracts, indicating that they are indeed in the same protein complex in vivo. Nevertheless, each PGL protein localizes to P granules independently of the other two. pgl-2 or pgl-3 singlemutant worms do not show obvious defects in germline development. However, pgl-1; pgl-3 (but not pgl-2; pgl-1) double-mutant hermaphrodites and males show significantly enhanced sterility at all temperatures, compared to pgl-1 alone. Mutant hermaphrodites show defects in germline proliferation and in production of healthy gametes and viable embryos. Our findings demonstrate that both PGL-2 and PGL-3 are components of P granules, both interact with PGL-1, and at least PGL-3 functions redundantly with PGL-1 to ensure fertility in both sexes of C. elegans.
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