A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of...
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| Veröffentlicht in: | PLoS biology 2022-07, Vol.20 (7), p.e3001472-e3001472 |
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| creator | Issigonis, Melanie Redkar, Akshada B Rozario, Tania Khan, Umair W Mejia-Sanchez, Rosa Lapan, Sylvain W Reddien, Peter W Newmark, Phillip A |
| description | Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of vitellaria for flatworm reproduction (and parasite transmission), little is known about this unique evolutionary innovation. Here, we examine reproductive system development in the planarian
Schmidtea mediterranea
, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this
klf4-like
(
klf4l
) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin. |
| doi_str_mv | 10.1371/journal.pbio.3001472 |
| format | Article |
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Schmidtea mediterranea
, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this
klf4-like
(
klf4l
) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3001472</identifier><identifier>PMID: 35839223</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Analysis ; Animals ; Biology and Life Sciences ; Gametocytes ; Genetic aspects ; Germ cells ; Gonads ; Homology ; Identification and classification ; Insects ; KLF4 protein ; Medicine and Health Sciences ; Oocytes ; Ovaries ; Parasites ; Physical Sciences ; Platyhelminthes ; Pluripotency ; Progenitor cells ; Reproduction ; Reproduction (biology) ; Reproductive organs ; Reproductive system ; Research and Analysis Methods ; Stem cell transplantation ; Stem cells ; Testes ; Transcription factors ; Turbellaria ; Yolk</subject><ispartof>PLoS biology, 2022-07, Vol.20 (7), p.e3001472-e3001472</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Issigonis et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 Issigonis et al 2022 Issigonis et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c672t-37152a7444f0e52e247153fa948e89338c657f0b0b16eead29004e3089e63de13</citedby><cites>FETCH-LOGICAL-c672t-37152a7444f0e52e247153fa948e89338c657f0b0b16eead29004e3089e63de13</cites><orcidid>0000-0002-2818-8389 ; 0000-0003-0793-022X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286257/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286257/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids></links><search><contributor>Ketting, René F.</contributor><creatorcontrib>Issigonis, Melanie</creatorcontrib><creatorcontrib>Redkar, Akshada B</creatorcontrib><creatorcontrib>Rozario, Tania</creatorcontrib><creatorcontrib>Khan, Umair W</creatorcontrib><creatorcontrib>Mejia-Sanchez, Rosa</creatorcontrib><creatorcontrib>Lapan, Sylvain W</creatorcontrib><creatorcontrib>Reddien, Peter W</creatorcontrib><creatorcontrib>Newmark, Phillip A</creatorcontrib><title>A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians</title><title>PLoS biology</title><description>Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of vitellaria for flatworm reproduction (and parasite transmission), little is known about this unique evolutionary innovation. Here, we examine reproductive system development in the planarian
Schmidtea mediterranea
, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this
klf4-like
(
klf4l
) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin.</description><subject>Analysis</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Gametocytes</subject><subject>Genetic aspects</subject><subject>Germ cells</subject><subject>Gonads</subject><subject>Homology</subject><subject>Identification and classification</subject><subject>Insects</subject><subject>KLF4 protein</subject><subject>Medicine and Health Sciences</subject><subject>Oocytes</subject><subject>Ovaries</subject><subject>Parasites</subject><subject>Physical Sciences</subject><subject>Platyhelminthes</subject><subject>Pluripotency</subject><subject>Progenitor cells</subject><subject>Reproduction</subject><subject>Reproduction (biology)</subject><subject>Reproductive organs</subject><subject>Reproductive system</subject><subject>Research and Analysis Methods</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Testes</subject><subject>Transcription 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Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians</title><author>Issigonis, Melanie ; Redkar, Akshada B ; Rozario, Tania ; Khan, Umair W ; Mejia-Sanchez, Rosa ; Lapan, Sylvain W ; Reddien, Peter W ; Newmark, Phillip A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c672t-37152a7444f0e52e247153fa948e89338c657f0b0b16eead29004e3089e63de13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Gametocytes</topic><topic>Genetic aspects</topic><topic>Germ cells</topic><topic>Gonads</topic><topic>Homology</topic><topic>Identification and classification</topic><topic>Insects</topic><topic>KLF4 protein</topic><topic>Medicine and Health Sciences</topic><topic>Oocytes</topic><topic>Ovaries</topic><topic>Parasites</topic><topic>Physical Sciences</topic><topic>Platyhelminthes</topic><topic>Pluripotency</topic><topic>Progenitor cells</topic><topic>Reproduction</topic><topic>Reproduction (biology)</topic><topic>Reproductive organs</topic><topic>Reproductive system</topic><topic>Research and Analysis Methods</topic><topic>Stem cell transplantation</topic><topic>Stem cells</topic><topic>Testes</topic><topic>Transcription factors</topic><topic>Turbellaria</topic><topic>Yolk</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Issigonis, Melanie</creatorcontrib><creatorcontrib>Redkar, Akshada B</creatorcontrib><creatorcontrib>Rozario, Tania</creatorcontrib><creatorcontrib>Khan, Umair W</creatorcontrib><creatorcontrib>Mejia-Sanchez, Rosa</creatorcontrib><creatorcontrib>Lapan, Sylvain W</creatorcontrib><creatorcontrib>Reddien, Peter W</creatorcontrib><creatorcontrib>Newmark, Phillip 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biology</jtitle><date>2022-07-15</date><risdate>2022</risdate><volume>20</volume><issue>7</issue><spage>e3001472</spage><epage>e3001472</epage><pages>e3001472-e3001472</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of vitellaria for flatworm reproduction (and parasite transmission), little is known about this unique evolutionary innovation. Here, we examine reproductive system development in the planarian
Schmidtea mediterranea
, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this
klf4-like
(
klf4l
) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>35839223</pmid><doi>10.1371/journal.pbio.3001472</doi><orcidid>https://orcid.org/0000-0002-2818-8389</orcidid><orcidid>https://orcid.org/0000-0003-0793-022X</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1545-7885 |
| ispartof | PLoS biology, 2022-07, Vol.20 (7), p.e3001472-e3001472 |
| issn | 1545-7885 1544-9173 1545-7885 |
| language | eng |
| recordid | cdi_plos_journals_2703198904 |
| source | Public Library of Science (PLoS) Journals Open Access; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Analysis Animals Biology and Life Sciences Gametocytes Genetic aspects Germ cells Gonads Homology Identification and classification Insects KLF4 protein Medicine and Health Sciences Oocytes Ovaries Parasites Physical Sciences Platyhelminthes Pluripotency Progenitor cells Reproduction Reproduction (biology) Reproductive organs Reproductive system Research and Analysis Methods Stem cell transplantation Stem cells Testes Transcription factors Turbellaria Yolk |
| title | A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians |
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