An SMC-like protein binds and regulates Caenorhabditis elegans condensins

• Published in: PLoS genetics Vol. 13; no. 3; p. e1006614
• Main Authors: Chao, Lucy Fang-I, Singh, Meha, Thompson, James, Yates, 3rd, John R, Hagstrom, Kirsten A
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 16.03.2017; Public Library of Science (PLoS)
• Subjects: Adenosine triphosphatase; Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Amino Acid Sequence; Animals; Animals, Genetically Modified; ATPases; Biology; Biology and Life Sciences; Caenorhabditis elegans; Caenorhabditis elegans - embryology; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; Caenorhabditis elegans Proteins - classification; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Cell division; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; Chromosomes; Compensation; Condensin; Deoxyribonucleic acid; DNA; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Drug dosages; Eukaryotes; Gene expression; Gene Expression Regulation, Developmental; Genetic aspects; Genetic engineering; Genomes; Hydrolysis; Lethality; Localization; Meiosis; Meiosis - genetics; Microscopy, Confocal; Mitosis; Mitosis - genetics; Multiprotein Complexes - genetics; Multiprotein Complexes - metabolism; Mutation; Nematodes; Nuclear Proteins - genetics; Nuclear Proteins - metabolism; Overexpression; Phylogeny; Physiology; Protein Binding; Protein Subunits - genetics; Protein Subunits - metabolism; Proteins; Recombination; Research and Analysis Methods; Sequence Homology, Amino Acid; X Chromosome - genetics; X Chromosomes; La Jolla California
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1006614

Structural Maintenance of Chromosomes (SMC) family proteins participate in multisubunit complexes that govern chromosome structure and dynamics. SMC-containing condensin complexes create chromosome topologies essential for mitosis/meiosis, gene expression, recombination, and repair. Many eukaryotes have two condensin complexes (I and II); C. elegans has three (I, II, and the X-chromosome specialized condensin IDC) and their regulation is poorly understood. Here we identify a novel SMC-like protein, SMCL-1, that binds to C. elegans condensin SMC subunits, and modulates condensin functions. Consistent with a possible role as a negative regulator, loss of SMCL-1 partially rescued the lethal and sterile phenotypes of a hypomorphic condensin mutant, while over-expression of SMCL-1 caused lethality, chromosome mis-segregation, and disruption of condensin IDC localization on X chromosomes. Unlike canonical SMC proteins, SMCL-1 lacks hinge and coil domains, and its ATPase domain lacks conserved amino acids required for ATP hydrolysis, leading to the speculation that it may inhibit condensin ATPase activity. SMCL-1 homologs are apparent only in the subset of Caenorhabditis species in which the condensin I and II subunit SMC-4 duplicated to create the condensin IDC- specific subunit DPY-27, suggesting that SMCL-1 helps this lineage cope with the regulatory challenges imposed by evolution of a third condensin complex. Our findings uncover a new regulator of condensins and highlight how the duplication and divergence of SMC complex components in various lineages has created new proteins with diverse functions in chromosome dynamics.