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Three key events are related to RNA degradation: oocyte meiotic resumption, fertilization, and zygotic genome activation (ZGA). In this study, we unexpectedly discover that the UPR (unfolded protein response) protein IRE1\u03b1 is critical for post-fertilization maternal messenger mRNA (mRNA) degradation. IRE1\u03b1 is specifically expressed from the metaphase II oocytes to four-cell embryos, with its translation dependent on the ERK1\/2 pathway. Oocyte-specific deletion of the IRE1\u03b1 RNase domain resulted in female infertility, characterized by embryonic developmental arrest at the one-cell\u00a0or two-cell stage, and failure to degrade maternal mRNAs destined for elimination. Using IRE1\u03b1-Flag knock-in mouse model and LACE-seq, as well as in vitro analysis, we show that IRE1\u03b1 can directly bind and cleave maternal mRNAs after fertilization. Moreover, IRE1\u03b1-mediated mRNA\u00a0decay is essential for ZGA and histone modifications. This study unveils an important function of IRE1\u03b1 in early embryonic development through regulated IRE1\u03b1-dependent decay, independent of the canonical IRE1\u03b1\u2013XBP1 signaling pathway, thereby revealing a novel molecular mechanism underlying maternal mRNA degradation triggered by fertilization.<\/jats:p>","DOI":"10.1093\/nar\/gkaf520","type":"journal-article","created":{"date-parts":[[2025,6,27]],"date-time":"2025-06-27T14:17:53Z","timestamp":1751033873000},"source":"Crossref","is-referenced-by-count":4,"title":["IRE1\u03b1 RNase activity is critical for early embryo development by degrading maternal transcripts"],"prefix":"10.1093","volume":"53","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7451-9364","authenticated-orcid":false,"given":"Chao","family":"Li","sequence":"first","affiliation":[{"name":"Guangdong Second Provincial General Hospital, Postdoctoral Research Station of Basic Medicine, School of Medicine, Jinan University , Guangzhou 510317 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Reproductive Medicine Center, Guangdong Second Provincial General Hospital , Guangzhou 510317 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li-Tao","family":"Yi","sequence":"additional","affiliation":[{"name":"School of Basic Medical Sciences, Southern Medical University Department of Developmental Biology, , Guangzhou 510515 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guang","family":"Wang","sequence":"additional","affiliation":[{"name":"Guangzhou Key Laboratory of Metabolic Diseases and Reproductive Health, Guangdong\u2013Hong Kong Metabolism & Reproduction Joint Laboratory, Reproductive Medicine Center, Guangdong Second Provincial General Hospital , Guangzhou 510317 ,","place":["China"]},{"name":"International Joint Laboratory for Embryonic Development & Prenatal Medicine, Division of Histology and Embryology, Medical College, Jinan University , Guangzhou 510632 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