Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles

Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi.

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Main Authors: Guernsey, Michael W., van Kruistum, Henri, Reznick, David N., Pollux, Bart J.A., Baker, Julie C.
Format: Article/Letter to editor biblioteca
Language:English
Subjects:Poeciliopsis, placenta, transcriptome,
Online Access:https://research.wur.nl/en/publications/molecular-signatures-of-placentation-and-secretion-uncovered-in-p
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spelling dig-wur-nl-wurpubs-5699582024-10-30 Guernsey, Michael W. van Kruistum, Henri Reznick, David N. Pollux, Bart J.A. Baker, Julie C. Article/Letter to editor Molecular Biology and Evolution 37 (2020) 9 ISSN: 0737-4038 Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles 2020 Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi. en application/pdf https://research.wur.nl/en/publications/molecular-signatures-of-placentation-and-secretion-uncovered-in-p 10.1093/molbev/msaa121 https://edepot.wur.nl/531528 Poeciliopsis placenta transcriptome https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic Poeciliopsis
placenta
transcriptome
Poeciliopsis
placenta
transcriptome
spellingShingle Poeciliopsis
placenta
transcriptome
Poeciliopsis
placenta
transcriptome
Guernsey, Michael W.
van Kruistum, Henri
Reznick, David N.
Pollux, Bart J.A.
Baker, Julie C.
Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
description Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi.
format Article/Letter to editor
topic_facet Poeciliopsis
placenta
transcriptome
author Guernsey, Michael W.
van Kruistum, Henri
Reznick, David N.
Pollux, Bart J.A.
Baker, Julie C.
author_facet Guernsey, Michael W.
van Kruistum, Henri
Reznick, David N.
Pollux, Bart J.A.
Baker, Julie C.
author_sort Guernsey, Michael W.
title Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
title_short Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
title_full Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
title_fullStr Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
title_full_unstemmed Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles
title_sort molecular signatures of placentation and secretion uncovered in poeciliopsis maternal follicles
url https://research.wur.nl/en/publications/molecular-signatures-of-placentation-and-secretion-uncovered-in-p
work_keys_str_mv AT guernseymichaelw molecularsignaturesofplacentationandsecretionuncoveredinpoeciliopsismaternalfollicles
AT vankruistumhenri molecularsignaturesofplacentationandsecretionuncoveredinpoeciliopsismaternalfollicles
AT reznickdavidn molecularsignaturesofplacentationandsecretionuncoveredinpoeciliopsismaternalfollicles
AT polluxbartja molecularsignaturesofplacentationandsecretionuncoveredinpoeciliopsismaternalfollicles
AT bakerjuliec molecularsignaturesofplacentationandsecretionuncoveredinpoeciliopsismaternalfollicles
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