Dynamic and Stable Cohesins Regulate Synaptonemal Complex Assembly and Chromosome Segregation

• Published in: Current biology Vol. 26; no. 13; pp. 1688 - 1698
• Main Authors: Gyuricza, Mercedes R., Manheimer, Kathryn B., Apte, Vandana, Krishnan, Badri, Joyce, Eric F., McKee, Bruce D., McKim, Kim S.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 11.07.2016
• Subjects: Animals; Cell Cycle Proteins - genetics; Cell Cycle Proteins - metabolism; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; Chromosome Pairing; Chromosome Segregation; cohesin; Cohesins; cohesion; Drosophila melanogaster - genetics; Drosophila melanogaster - metabolism; Female; Gene Expression Regulation; Insect Proteins - genetics; Insect Proteins - metabolism; meiosis; synaptonemal complex; Synaptonemal Complex - genetics; cohesin; meiosis; cohesion; chromosome segregation; synaptonemal complex
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2016.05.006

Assembly of the synaptonemal complex (SC) in Drosophila depends on two independent pathways defined by the chromosome axis proteins C(2)M and ORD. Because C(2)M encodes a Kleisin-like protein and ORD is required for sister-chromatid cohesion, we tested the hypothesis that these two SC assembly pathways depend on two cohesin complexes. Through single- and double-mutant analysis to study the mitotic cohesion proteins Stromalin (SA) and Nipped-B (SCC2) in meiosis, we provide evidence that there are at least two meiosis-specific cohesin complexes. One complex depends on C(2)M, SA, and Nipped-B. Despite the presence of mitotic cohesins SA and Nipped-B, this pathway has only a minor role in meiotic sister-centromere cohesion and is primarily required for homolog interactions. C(2)M is continuously incorporated into pachytene chromosomes even though SC assembly is complete. In contrast, the second complex, which depends on meiosis-specific proteins SOLO, SUNN, and ORD is required for sister-chromatid cohesion, localizes to the centromeres and is not incorporated during prophase. Our results show that the two cohesin complexes have unique functions and are regulated differently. Multiple cohesin complexes may provide the diversity of activities required by the meiotic cell. For example, a dynamic complex may allow the chromosomes to regulate meiotic recombination, and a stable complex may be required for sister-chromatid cohesion. [Display omitted] •Synaptonemal complex assembly depends on two meiosis-specific cohesin complexes•One complex is required for homolog interactions and crossing over•This cohesin complex is maintained with subunit turnover during pachytene•The other complex is required for cohesion and crossing over Gyuricza et al. find that synaptonemal complex assembly depends on two cohesin complexes. One complex is required only for interhomolog interactions, and the other is required for sister-chromatid interactions. The interhomolog cohesin complex is surprisingly dynamic, which may facilitate regulating SC assembly and crossover formation.