Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans

Abstract

The synaptonemal complex (SC) is a key structure of meiosis, mediating the stable pairing (synapsis) of homologous chromosomes during prophase I. Its remarkable tripartite structure is evolutionarily well conserved and can be found in almost all sexually reproducing organisms. However, comparison of the different SC protein components in the common meiosis model organisms Saccharomyces cerevisiae, Arabidopsis thaliana, Caenorhabditis elegans, Drosophila melanogaster, and Mus musculus revealed no sequence homology. This discrepancy challenged the hypothesis that the SC arose only once in evolution. To pursue this matter we focused on the evolution of SYCP1 and SYCP3, the two major structural SC proteins of mammals. Remarkably, our comparative bioinformatic and expression studies revealed that SYCP1 and SYCP3 are also components of the SC in the basal metazoan Hydra. In contrast to previous assumptions, we therefore conclude that SYCP1 and SYCP3 form monophyletic groups of orthologous proteins across metazoans.

Fig. 1.

Schematic comparison of SYCP1 proteins of rat (GenBank accession no. NM_012810) and Hydra (GenBank accession no. JQ906934). Sequence identity and sequence similarity (in parentheses) at the amino acid level are given (%). The gray boxes represent putative coiled coil domains. Position of conserved motifs CM1 (amino acids 106–188 in the rat; amino acids 56–138 in Hydra) and CM2 (amino acids 724–754 in the rat; amino acids 674–704 in Hydra) is denoted by red boxes. NLS, nuclear localization signal.

Fig. 2.

Schematic comparison of SYCP3 proteins of rat (GenBank accession no. NM_013041) and Hydra (GenBank accession no. JQ906932). Sequence identity and sequence similarity (in parentheses) at the amino acid level are given (%). The gray boxes represent putative coiled coil domains. Position of conserved motifs CM1 (amino acids 86–105 in the rat; amino acids 64–82 in Hydra) and CM2 (amino acids 252–257 in the rat; amino acids 230–235 in Hydra) is denoted by red boxes.

Fig. 3.

Identification and characterization of Hydra SYCP1 and SYCP3. Expression pattern of SYCP1 (A) and SYCP3 (B) mRNAs as shown by RT-PCR. Expression pattern of SYCP1 (C) and SYCP3 (D) at the protein level as shown by immunoblotting. Testis-specific expression of SYCP1 (E and F, arrow) and SYCP3 (G and H, arrow) mRNA as shown by in situ hybridization on whole-mount Hydra.

Fig. 4.

Ultrastructure of a Hydra SC showing the typical components: LE, CE, and NE, nuclear envelope (A). Immunolocalization of SYCP1 and SYCP3 on cryosections of Hydra testis (B). Sg, Spermatogonia; Sp, Spermatocytes; St, Spermatids. Bar, 20 μm.

Fig. 5.

Immunolocalization of SYCP1 and SYCP3 on spread meiotic chromosomes as shown by confocal microscopy. During zygotene and pachytene, SYCP1 selectively localizes to the synapsed areas of homologous chromosomes (arrows) and SYCP3 labels the whole length of lateral elements. During diplotene, SYCP1 dissociates from the lateral elements (arrows). Image enlargements of diplotene SCs show the localization of SYCP3 in the two aligned LEs (arrows); whereas, SYCP1 is restricted to the synapsed regions in between. Bar, 10 μm.

Fig. 6.

Molecular phylogeny of SYCP1 proteins. The tree was calculated from an 83 amino acid alignment using Bayesian inference [MrBayes (36); posterior probability values are indicated]. CCDC39 sequences were used as an outgroup. Phylogenetic grouping of SYCP1 proteins was also supported using the neighbor-joining method (34).

Fig. 7.

Molecular phylogeny of SYCP3 proteins. The tree was calculated from a 171 amino acid alignment corresponding to the Cor1/Xlr/Xmr conserved region (CM1 to CM2) using the neighbor-joining method [(34); 1,000 pseudosamples; bootstrap values are indicated]. SYCP2 sequences were used as an outgroup. Phylogenetic grouping of SYCP3 proteins was also supported using Bayesian inference MrBayes (36).