The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast

Abstract

During meiosis, homologous chromosomes pair at close proximity to form the synaptonemal complex (SC). This association is mediated by transverse filament proteins that hold the axes of homologous chromosomes together along their entire length. Transverse filament proteins are highly aggregative and can form an aberrant aggregate called the polycomplex that is unassociated with chromosomes. Here, we show that the Ecm11-Gmc2 complex is a novel SC component, functioning to facilitate assembly of the yeast transverse filament protein, Zip1. Ecm11 and Gmc2 initially localize to the synapsis initiation sites, then throughout the synapsed regions of paired homologous chromosomes. The absence of either Ecm11 or Gmc2 substantially compromises the chromosomal assembly of Zip1 as well as polycomplex formation, indicating that the complex is required for extensive Zip1 polymerization. We also show that Ecm11 is SUMOylated in a Gmc2-dependent manner. Remarkably, in the unSUMOylatable ecm11 mutant, assembly of chromosomal Zip1 remained compromised while polycomplex formation became frequent. We propose that the Ecm11-Gmc2 complex facilitates the assembly of Zip1 and that SUMOylation of Ecm11 is critical for ensuring chromosomal assembly of Zip1, thus suppressing polycomplex formation.

Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSγ-Mediated Crossover Formation

“…We also used DAPI staining on wholemount cells cultured on solid sporulation media to measure the frequency of meiocytes, at multiple time points, that had undergone a meiotic division ( Figure S2B). Consistent with a prior study, we found that ecm11 mutants exhibit a delay in exiting meiotic prophase ( Figure S2 and Humphryes et al 2013). In our liquid sporulation time course experiment, by 28 hr, 50% of surface-spread nuclei from wild-type meiocytes had progressed beyond the pachytene stage and a substantial fraction were undergoing meiotic divisions.…”

Superresolution expansion microscopy reveals the three-dimensional organization of theDrosophilasynaptonemal complex

“…Some organisms, such as mammals, yeast, and flies, use pairs of TF homodimers [SYCP1, Zip1, and C(3)G, respectively] to span the CR of the SC, whereas worms use multiple SC components (SYP1-4) staggered across the CR (13,(32)(33)(34). In addition, multiple SC components are thought to make up the CE in both mice (SYCE1-3, TEX12) and yeast (Ecm11, Gmc2), whereas only one CE protein (CONA) has been identified in flies (30,(35)(36)(37)(38)(39).…”

Recombination, Pairing, and Synapsis of Homologs during Meiosis

“…For example, dimers of the large coiled-coil protein Zip1/SCP1/ SYCP1/C(3)G/SYP-1/ZEP1/ZIP1 form the transverse filaments of the SC central region in all organisms (e.g., Higgins et al 2005;Hawley 2011;Miao et al 2013). They were previously thought to be the sole SC central element components, but they are in fact associated with additional proteins different in number, localization, and perhaps function from one organism to the other: SYCE1, SYCE2, SYCE3, and Tex12 in mammals; Cona in Drosophila, SYP-2, SYP-3, SYP-4 in worm; and Ecm11, Gmc2 in budding yeast (reviewed in Bolcun-Filas et al 2007;Hawley 2011;Schild-Prüfert et al 2011;Davies et al 2012;Fraune et al 2012;Gó mez et al 2013;Humphryes et al 2013). However, despite the identification of several new AE and central region components in recent years, we are only beginning to understand how they interact precisely to form the SC (Davies et al 2012), how they are regulated, and, more importantly, what is/are the function(s) of the SC.…”