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Stem–loop binding protein (SLBP) is required for replication-dependent histone mRNA metabolism in mammals. Zebrafish possesses two  slbps , and  slbp1  is necessary for retinal neurogenesis. However, the detailed expression and function of  slbp2  in zebrafish are still unknown. In this study, we first identified zebrafish  slbp2  as an oocyte-specific maternal factor and then generated a maternal-zygotic  slbp2  F3 homozygous mutant (MZ slbp2 Δ4 −/− ) using CRISPR/Cas9. The depletion of maternal Slbp2 disrupted early nuclear cleavage, which resulted in developmental arrest at the MBT stage. The developmental defects could be rescued in  slbp2  transgenic MZ slbp2 Δ4 −/−  embryos. However, homozygous mutant MZ slbp1 Δ1 −/−  developed normally, indicating  slbp1  is dispensable for zebrafish early embryogenesis. Through comparative proteome and transcriptome profiling between WT and MZ slbp2 Δ4 −/−  embryos, we identified many differentially expressed proteins and genes. In comparison with those in WT embryos, four replication-dependent histones, including H2a, H2b, H3, and H4, all reduced their expression, while histone variant  h2afx  significantly increased in MZ slbp2 Δ4 −/−  embryos at the 256-cell stage and high stage. Zebrafish Slbp2 can bind histone mRNA stem–loop in vitro, and the defects of MZ slbp2 Δ4 −/−  embryos can be partially rescued by overexpression of H2b. The current data indicate that maternal Slbp2 plays a pivotal role in the storage of replication-dependent histone mRNAs and proteins during zebrafish oogenesis.

Oocyte-specific maternal Slbp2 is required for replication-dependent histone storage and early nuclear cleavage in zebrafish oogenesis and embryogenesis