ATM/p53-Associated Apoptosis Contributes to Sterility in Allotriploid Crucian Carp

During meiosis, ataxia telangiectasia mutated (ATM) kinase senses DNA double-strand breaks (DSBs) and regulates multiple downstream processes, including DSB repair and p53-mediated apoptosis. The allotriploid crucian carp (3nAT, 3n = 150), derived from distant hybridization between female diploid red crucian carp (2nRCC) and male allotetraploid hybrids (4nAT), is sterile and exhibits extensive germ cell apoptosis associated with abnormal meiosis. Here, we used the ATM kinase inhibitor KU55933, to investigate the sterility mechanism. Following intraperitoneal treatment with KU55933 (KU-3nAT), germ cell apoptosis was markedly reduced, and a small number of morphologically abnormal gametes were produced. Meiosis- and gamete maturation-related genes were upregulated, whereas pro-apoptotic genes were downregulated, indicating that meiotic arrest was partially attenuated. However, KU-3nAT sperm exhibited abnormal structures with rounded heads, retained cytoplasm, and absent or malformed flagella. Self-crossed and hybrid embryos with 2nRCC arrested at gastrulation, while a few KU-3nAT ♀ × 4nAT ♂ embryos hatched. These results suggest that ATM/p53-associated apoptosis contributes to germ cell loss at the proposed pachytene checkpoint in 3nAT, while ATM inhibition permits limited gamete production but does not restore normal gamete function or embryonic development.