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Schistosomes are dioecious, with egg laying depending on the females\u2019 obligatory pairing with males. Long non-coding RNAs (lncRNAs) are transcripts longer than 200 nucleotides with low or no protein-coding potential that have been involved in other species with reproduction, stem cell maintenance, and drug resistance. In <jats:italic>S<\/jats:italic>. <jats:italic>mansoni<\/jats:italic>, we recently showed that the knockdown of one lncRNA affects the pairing status of these parasites. Here, we re-analyzed public RNA-Seq data from paired and unpaired adult male and female worms and their gonads, obtained from mixed-sex or single-sex cercariae infections, and found thousands of differentially expressed pairing-dependent lncRNAs among the 23 biological samples that were compared. The expression levels of selected lncRNAs were validated by RT-qPCR using an <jats:italic>in vitro<\/jats:italic> unpairing model. In addition, the <jats:italic>in vitro<\/jats:italic> silencing of three selected lncRNAs showed that knockdown of these pairing-dependent lncRNAs reduced cell proliferation in adult worms and their gonads, and are essential for female vitellaria maintenance, reproduction, and\/or egg development. Remarkably, <jats:italic>in vivo<\/jats:italic> silencing of each of the three selected lncRNAs significantly reduced worm burden in infected mice by 26 to 35%. Whole mount <jats:italic>in situ<\/jats:italic> hybridization experiments showed that these pairing-dependent lncRNAs are expressed in reproductive tissues. These results show that lncRNAs are key components intervening in <jats:italic>S<\/jats:italic>. <jats:italic>mansoni<\/jats:italic> adult worm homeostasis, which affects pairing status and survival in the mammalian host, thus presenting great potential as new therapeutic target candidates.<\/jats:p>","DOI":"10.1371\/journal.ppat.1011369","type":"journal-article","created":{"date-parts":[[2023,5,5]],"date-time":"2023-05-05T17:39:14Z","timestamp":1683308354000},"page":"e1011369","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["Long non-coding RNAs are essential for Schistosoma mansoni pairing-dependent adult worm homeostasis and fertility"],"prefix":"10.1371","volume":"19","author":[{"given":"Gilbert O.","family":"Silveira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena S.","family":"Coelho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adriana S. 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