Abstract
ABSTRACTMutations in structural maintenance of chromosomes (Smc) proteins are frequently associated with chromosomal abnormalities commonly observed in developmental disorders. However, the role of Smc proteins in development still remains elusive. To investigate Smc5/6 function during early embryogenesis we examined smc5 and smc6 mutants of the fruit fly Drosophila melanogaster using a combination of reverse genetics and microscopy approaches. Smc5/6 exhibited a maternally contributed function in maintaining chromosome stability during early embryo development, which manifested as female subfertility in its absence. Loss of Smc5/6 caused an arrest and a considerable delay in embryo development accompanied by fragmented nuclei and increased anaphase-bridge formation, respectively. Surprisingly, early embryonic arrest was attributable to the absence of Smc5/6 during oogenesis, which resulted in insufficient repair of pre-meiotic and meiotic DNA double-strand breaks. Thus, our findings contribute to the understanding of Smc proteins in higher eukaryotic development by highlighting a maternal function in chromosome maintenance and a link between oogenesis and early embryogenesis.
Highlights
During the development of multicellular organisms such as insects, worms, and mammals, chromosomes are coordinated for replication, transcription, repair, and segregation
We discovered a maternal function of Smc5/6 in maintaining chromosome stability during both oogenesis and early embryogenesis
Mutants of Smc5/6 display reduced embryo viability To study the function of Smc5/6 during embryogenesis we utilized a previously described loss-of-function allele smc5P7E8 (Li et al, 2013) (Fig. S1A)
Summary
During the development of multicellular organisms such as insects, worms, and mammals, chromosomes are coordinated for replication, transcription, repair, and segregation. Conserved proteins critical to maintaining chromosome dynamics, organization, and integrity throughout these processes have evolved. Structural maintenance of chromosomes (Smc) proteins belong to an evolutionarily conserved protein family that assemble into three major and distinct complexes. The sisterchromatid cohesion (SMC1/3)-, the chromosome condensation (SMC2/4)-, and the SMC5/6-complex regulate most aspects of chromosome biology to ensure genome integrity (Hirano, 2002). The Smc5/6 complex, hereby referred to as Smc5/6, is the least characterized complex of all three. Smc5/6 is implicated in DNA recombination and repair, chromosome replication and
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