Originally published as Genetics Published Articles Ahead of Print on October 18, 2007.

Genetics, Vol. 177, 2445-2456, December 2007, Copyright © 2007
doi:10.1534/genetics.107.078717

The Formation of the Central Element of the Synaptonemal Complex May Occur by Multiple Mechanisms: The Roles of the N- and C-Terminal Domains of the Drosophila C(3)G Protein in Mediating Synapsis and Recombination

Jennifer K. Jeffress*,1, Scott L. Page*,2, Suzanne M. Royer{dagger}, Elizabeth D. Belden*, Justin P. Blumenstiel*, Lorinda K. Anderson{dagger} and R. Scott Hawley*,{ddagger},3

* Stowers Institute for Medical Research, Kansas City, Missouri 64110, {dagger} Department of Biology, Colorado State University, Fort Collins, Colorado 80523 and {ddagger} Department of Physiology, University of Kansas School of Medicine, Kansas City, Kansas 66160

3 Corresponding author: Stowers Institute for Medical Research, 1000 E. 50th St., Kansas City, MO 64110.
E-mail: rsh{at}stowers-institute.org

In Drosophila melanogaster oocytes, the C(3)G protein comprises the transverse filaments (TFs) of the synaptonemal complex (SC). Like other TF proteins, such as Zip1p in yeast and SCP1 in mammals, C(3)G is composed of a central coiled-coil-rich domain flanked by N- and C-terminal globular domains. Here, we analyze in-frame deletions within the N- and C-terminal regions of C(3)G in Drosophila oocytes. As is the case for Zip1p, a C-terminal deletion of C(3)G fails to attach to the lateral elements of the SC. Instead, this C-terminal deletion protein forms a large cylindrical polycomplex structure. EM analysis of this structure reveals a polycomplex of concentric rings alternating dark and light bands. However, unlike both yeast and mammals, all three proteins deleted for N-terminal regions completely abolished both SC and polycomplex formation. Both the N- and C-terminal deletions significantly reduce or abolish meiotic recombination similarly to c(3)G null homozygotes. To explain these data, we propose that in Drosophila the N terminus, but not the C-terminal globular domain, of C(3)G is critical for the formation of antiparallel pairs of C(3)G homodimers that span the central region and thus for assembly of complete TFs, while the C terminus is required to affix these homodimers to the lateral elements.