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Here, we demonstrate that AGO3 and AGO4, but not AGO2, localize to the sex chromatin of pachytene spermatocytes, where they are required for the transcriptional silencing of XY-linked genes that characterizes Meiotic Sex Chromosome Inactivation (MSCI). Previous findings showed that deletion of\n                    <jats:italic>Ago4<\/jats:italic>\n                    (\n                    <jats:italic>Ago4<\/jats:italic>\n                    <jats:sup>\n                      <jats:italic>-\/-<\/jats:italic>\n                    <\/jats:sup>\n                    <jats:italic>)<\/jats:italic>\n                    mildly impairs MSCI and normal spermatozoa production. By contrast, loss of\n                    <jats:italic>Ago3<\/jats:italic>\n                    (\n                    <jats:italic>Ago3<\/jats:italic>\n                    <jats:sup>\n                      <jats:italic>-\/-<\/jats:italic>\n                    <\/jats:sup>\n                    <jats:italic>)<\/jats:italic>\n                    does not produce these defects, while combined deletion of\n                    <jats:italic>Ago1<\/jats:italic>\n                    ,\n                    <jats:italic>Ago3<\/jats:italic>\n                    , and\n                    <jats:italic>Ago4<\/jats:italic>\n                    (\n                    <jats:italic>Ago413<\/jats:italic>\n                    <jats:sup>\n                      <jats:italic>-\/-<\/jats:italic>\n                    <\/jats:sup>\n                    ) leads to severely reduced fertility, accompanied by disrupted autosomal and sex chromosome gene regulation and altered chromatin accessibility in spermatocytes. In\n                    <jats:italic>Ago413<\/jats:italic>\n                    <jats:sup>\n                      <jats:italic>-\/-<\/jats:italic>\n                    <\/jats:sup>\n                    mice, premature overexpression of spermiogenesis genes during prophase I results in reduced sperm production, abnormal sperm morphology, and impaired fertilization capacity. Together, AGO3 and AGO4 act during prophase I to ensure the timely expression of meiosis-related genes during prophase I while maintaining repression of spermiogenesis-associated genes. These results indicate that AGO3 and AGO4 act in a coordinated fashion in the male germline to orchestrate cell progression in spermatogenesis through temporal regulation of autosomal and sex chromosome genes.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1012217","type":"journal-article","created":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T17:40:24Z","timestamp":1782754824000},"page":"e1012217","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Argonaute proteins orchestrate Meiotic Sex Chromosome Inactivation and timing of the spermatogenic transcriptional program"],"prefix":"10.1371","volume":"22","author":[{"given":"Maria de las Mercedes","family":"Carro","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6621-0700","authenticated-orcid":true,"given":"Alexis","family":"Dziubek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Touey-May","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth A.","family":"Popkowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-5358-231X","authenticated-orcid":true,"given":"Mark","family":"Abdelmassih","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3129-019X","authenticated-orcid":true,"given":"Leah E.","family":"Simon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie L.","family":"Tanis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Faraz","family":"Ahmed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0928-7971","authenticated-orcid":true,"given":"Jennifer K.","family":"Grenier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew","family":"Grimson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2050-6979","authenticated-orcid":true,"given":"Paula E.","family":"Cohen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,6,29]]},"reference":[{"key":"pgen.1012217.ref001","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.scr.2018.04.009","article-title":"Spermatogonial stem cells and spermatogenesis in mice, monkeys and men","volume":"29","author":"AP Fayomi","year":"2018","journal-title":"Stem Cell Res"},{"key":"pgen.1012217.ref002","article-title":"Control of meiotic crossovers: From double-strand break formation to designation","author":"S Gray","year":"2016","journal-title":"Annual Reviews Inc"},{"key":"pgen.1012217.ref003","doi-asserted-by":"crossref","unstructured":"Lenzi ML, Smith J, Snowden T, Kim M, Fishel R, Poulos BK, et al. 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