Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes.

Abstract

Zipl is a yeast synaptonemal complex (SC) central region component and is required for normal meiotic recombination and crossover interference. Physical analysis of meiotic recombination in a zipi mutant reveals the following: Crossovers appear later than normal and at a reduced level. Noncrossover recombinants, in contrast, seem to appear in two phases: (i) a normal number appear with normal timing and (ii) then additional products appear late, at the same time as crossovers. Also, Holliday junctions are present at unusually late times, presumably as precursors to late-appearing products. Redl is an axial structure component required for formation of cytologically discernible axial elements and SC and maximal levels of recombination. In a redi mutant, crossovers and noncrossovers occur at coordinately reduced levels but with normal timing. If Zipl affected recombination exclusively via SC polymerization, a zip] mutation should confer no recombination defect in a redi strain background. But a red] zip] double mutant exhibits the sum of the two single mutant phenotypes, including the specific deficit of crossovers seen in a zipi strain. We infer that Zipl plays at least one role in recombination that does not involve SC polymerization along the chromosomes. Perhaps some Zipl molecules act first in or around the sites of recombinational interactions to influence the recombination process and thence nucleate SC formation. We propose that a Zipldependent, pre-SC transition early in the recombination reaction is an essential component of meiotic crossover control. A molecular basis for crossover/noncrossover differentiation is also suggested.In meiosis, crossovers ensure the disjunction of homologs at the first division. The number and distribution of crossovers are tightly controlled (1-6). One manifestation of control is crossover interference: the presence of a crossover at one position along a chromosome reduces the probability that a crossover will also be found nearby. Crossover interference may act upon an array of undifferentiated recombinational interactions causing certain ones to mature into crossovers and others to mature into noncrossovers (e.g., refs. 3 and 4).In yeast, meiotic recombination initiates via meiosis-specific double strand breaks (DSBs) (7,8), which occur prior to bulk polymerization of the synaptonemal complex between the structural axes of paired homologs (9). Resected DSBs then invade an intact duplex to form double Holliday junctions; invasion and ensuing steps are approximately concomitant with initiation and progression of SC polymerization, respectively (10). Double Holliday junctions persist throughout much of the period when SC is full-length ("pachytene"). Mature crossover and noncrossover products form an hour or so after Holliday junctions appear, at about the time that SC disappears (9), but not dependent upon SC disassembly (11,12 In this model, all undifferentiated recombinational interactions are placed under "stress"; in addition, each interaction has an intrinsic "...

MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

“…For example, association with Ndj1p and Mps3p could stabilize telomere structure and, by contributing to anchoring at the nuclear envelope, bring about structural changes in the chromosomes that regulate the distribution of crossovers (see ref. 15), perhaps by means of tension (7,45,46). Alternatively, or in addition, telomere-promoted movements themselves may contribute to the normal pattern of crossovers, perhaps in part by promoting stable homologous interactions, pairing and synapsis.…”

Evolutionary history of the mammalian synaptonemal complex

“…TNs now localize between the LEs and contain proteins, such as RPA, MSH4, BLM helicase and topoisomerase, which are implicated in the resolution of most of the early DNA-DNA interactions (Moens et al 2002). Results from mice (Tarsounas et al 1999;Baudat et al 2000;Bolcun-Filas et al 2009) and from yeast (Storlazzi et al 1996;Agarwal and Roeder 2000) research further suggest that some recombination nodules at this stage may function as initiation sites for synapsis. At these sites, the assembly of the CR starts and spreads into both directions to connect the homologs over their entire length.…”

Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks

“…SC assembly requires Zip2 and Zip3, which form discrete Spo11-dependent complexes that colocalize with the earliest central element (Zip1) structures and which are thus thought to nucleate central element polymerization (31,32). Zip2͞Zip3 complexes localize to a subset of recombination sites (31,32), and the Zip proteins are required for processing crossover-designated recombination intermediates (33,51).…”