{"title":"哈密尔顿菌共生体通过调节母体蛋白tudor介导的piRNA通路,有利于粉虱受精。","authors":"Xiang Sun, Huan Li, Zhan-Bo Chen, Bing-Qi Liu, Chu-Qiao Li, Zheng-Yang Zhao, Xing-Ye Li, Jun-Bo Luan","doi":"10.1073/pnas.2427053122","DOIUrl":null,"url":null,"abstract":"<p><p>Although it is widely recognized that nutritional symbionts can manipulate host reproduction, the underlying molecular and cellular mechanisms are largely unclear. The facultative symbiont <i>Hamiltonella</i> in bacteriocyte induces female-biased sex ratio of whiteflies. Here, we demonstrate that a maternal gene <i>tudor</i> (<i>tud</i>) and its encoded protein have lower expression levels in ovaries of <i>Hamiltonella-</i>cured whiteflies. Tud family proteins can interlink the various stages of biosynthesis of PIWI-interacting RNA (piRNA), a class of small noncoding RNAs. We find that <i>Hamiltonella</i> affects the abundance of a piRNA through the maternal gene <i>tud</i>, thereby regulating the expression of the <i>vacuolar</i> (<i>H+</i>)<i>-ATPase H subunit</i> (<i>VATPH</i>), which is the switch of activity of the vacuolar (H+)-ATPase that plays a crucial role in maintaining the homeostasis of intracellular energy and supporting mitochondrial respiration. This regulation adjusts the ATP level in ovaries of whiteflies. The ATP level shapes the F-actin pattern in ovaries and eggs of whiteflies, ultimately manipulating whitefly fertilization. Silencing <i>tud</i> inhibited whitefly fertilization by impairing ATP levels and F-actin patterns in ovaries and eggs. This study reveals that symbiont and maternal protein associations can regulate host fertilization by piRNA biosynthesis.</p>","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 24","pages":"e2427053122"},"PeriodicalIF":9.4000,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"<i>Hamiltonella</i> symbionts benefit whitefly fertilization by regulating the maternal protein Tudor-mediated piRNA pathway.\",\"authors\":\"Xiang Sun, Huan Li, Zhan-Bo Chen, Bing-Qi Liu, Chu-Qiao Li, Zheng-Yang Zhao, Xing-Ye Li, Jun-Bo Luan\",\"doi\":\"10.1073/pnas.2427053122\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Although it is widely recognized that nutritional symbionts can manipulate host reproduction, the underlying molecular and cellular mechanisms are largely unclear. The facultative symbiont <i>Hamiltonella</i> in bacteriocyte induces female-biased sex ratio of whiteflies. Here, we demonstrate that a maternal gene <i>tudor</i> (<i>tud</i>) and its encoded protein have lower expression levels in ovaries of <i>Hamiltonella-</i>cured whiteflies. Tud family proteins can interlink the various stages of biosynthesis of PIWI-interacting RNA (piRNA), a class of small noncoding RNAs. We find that <i>Hamiltonella</i> affects the abundance of a piRNA through the maternal gene <i>tud</i>, thereby regulating the expression of the <i>vacuolar</i> (<i>H+</i>)<i>-ATPase H subunit</i> (<i>VATPH</i>), which is the switch of activity of the vacuolar (H+)-ATPase that plays a crucial role in maintaining the homeostasis of intracellular energy and supporting mitochondrial respiration. This regulation adjusts the ATP level in ovaries of whiteflies. The ATP level shapes the F-actin pattern in ovaries and eggs of whiteflies, ultimately manipulating whitefly fertilization. Silencing <i>tud</i> inhibited whitefly fertilization by impairing ATP levels and F-actin patterns in ovaries and eggs. This study reveals that symbiont and maternal protein associations can regulate host fertilization by piRNA biosynthesis.</p>\",\"PeriodicalId\":20548,\"journal\":{\"name\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"volume\":\"122 24\",\"pages\":\"e2427053122\"},\"PeriodicalIF\":9.4000,\"publicationDate\":\"2025-06-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Proceedings of the National Academy of Sciences of the United States of America\",\"FirstCategoryId\":\"103\",\"ListUrlMain\":\"https://doi.org/10.1073/pnas.2427053122\",\"RegionNum\":1,\"RegionCategory\":\"综合性期刊\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/6/12 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"MULTIDISCIPLINARY SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the National Academy of Sciences of the United States of America","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1073/pnas.2427053122","RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/6/12 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
Hamiltonella symbionts benefit whitefly fertilization by regulating the maternal protein Tudor-mediated piRNA pathway.
Although it is widely recognized that nutritional symbionts can manipulate host reproduction, the underlying molecular and cellular mechanisms are largely unclear. The facultative symbiont Hamiltonella in bacteriocyte induces female-biased sex ratio of whiteflies. Here, we demonstrate that a maternal gene tudor (tud) and its encoded protein have lower expression levels in ovaries of Hamiltonella-cured whiteflies. Tud family proteins can interlink the various stages of biosynthesis of PIWI-interacting RNA (piRNA), a class of small noncoding RNAs. We find that Hamiltonella affects the abundance of a piRNA through the maternal gene tud, thereby regulating the expression of the vacuolar (H+)-ATPase H subunit (VATPH), which is the switch of activity of the vacuolar (H+)-ATPase that plays a crucial role in maintaining the homeostasis of intracellular energy and supporting mitochondrial respiration. This regulation adjusts the ATP level in ovaries of whiteflies. The ATP level shapes the F-actin pattern in ovaries and eggs of whiteflies, ultimately manipulating whitefly fertilization. Silencing tud inhibited whitefly fertilization by impairing ATP levels and F-actin patterns in ovaries and eggs. This study reveals that symbiont and maternal protein associations can regulate host fertilization by piRNA biosynthesis.
期刊介绍:
The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.