Sex and fetal genome influence gene expression in pig endometrium at the end of gestation

Abstract Background A fine balance of feto-maternal resource allocation is required to support pregnancy, which depends on interactions between maternal and fetal genetic potential, maternal nutrition and environment, endometrial and placental functions. In particular, some imprinted genes have a ro...

Full description

Bibliographic Details
Main Authors: Agnes Bonnet, Lisa Bluy, Laure Gress, Laurianne Canario, Laure Ravon, Aurelie Sécula, Yvon Billon, Laurence Liaubet
Format: Article
Language:English
Published: BMC 2024-03-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10144-1
_version_ 1797247446066135040
author Agnes Bonnet
Lisa Bluy
Laure Gress
Laurianne Canario
Laure Ravon
Aurelie Sécula
Yvon Billon
Laurence Liaubet
author_facet Agnes Bonnet
Lisa Bluy
Laure Gress
Laurianne Canario
Laure Ravon
Aurelie Sécula
Yvon Billon
Laurence Liaubet
author_sort Agnes Bonnet
collection DOAJ
description Abstract Background A fine balance of feto-maternal resource allocation is required to support pregnancy, which depends on interactions between maternal and fetal genetic potential, maternal nutrition and environment, endometrial and placental functions. In particular, some imprinted genes have a role in regulating maternal-fetal nutrient exchange, but few have been documented in the endometrium. The aim of this study is to describe the expression of 42 genes, with parental expression, in the endometrium comparing two extreme breeds: Large White (LW); Meishan (MS) with contrasting neonatal mortality and maturity at two days of gestation (D90-D110). We investigated their potential contribution to fetal maturation exploring genes-fetal phenotypes relationships. Last, we hypothesized that the fetal genome and sex influence their endometrial expression. For this purpose, pure and reciprocally crossbred fetuses were produced using LW and MS breeds. Thus, in the same uterus, endometrial samples were associated with its purebred or crossbred fetuses. Results Among the 22 differentially expressed genes (DEGs), 14 DEGs were differentially regulated between the two days of gestation. More gestational changes were described in LW (11 DEGs) than in MS (2 DEGs). Nine DEGs were differentially regulated between the two extreme breeds, highlighting differences in the regulation of endometrial angiogenesis, nutrient transport and energy metabolism. We identified DEGs that showed high correlations with indicators of fetal maturation, such as ponderal index at D90 and fetal blood fructose level and placental weight at D110. We pointed out for the first time the influence of fetal sex and genome on endometrial expression at D90, highlighting AMPD3, CITED1 and H19 genes. We demonstrated that fetal sex affects the expression of five imprinted genes in LW endometrium. Fetal genome influenced the expression of four genes in LW endometrium but not in MS endometrium. Interestingly, both fetal sex and fetal genome interact to influence endometrial gene expression. Conclusions These data provide evidence for some sexual dimorphism in the pregnant endometrium and for the contribution of the fetal genome to feto-maternal interactions at the end of gestation. They suggest that the paternal genome may contribute significantly to piglet survival, especially in crossbreeding production systems.
first_indexed 2024-04-24T19:58:49Z
format Article
id doaj.art-07467bb6270a4ac78a6b2ec6c3eb874f
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-04-24T19:58:49Z
publishDate 2024-03-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-07467bb6270a4ac78a6b2ec6c3eb874f2024-03-24T12:11:28ZengBMCBMC Genomics1471-21642024-03-0125112110.1186/s12864-024-10144-1Sex and fetal genome influence gene expression in pig endometrium at the end of gestationAgnes Bonnet0Lisa Bluy1Laure Gress2Laurianne Canario3Laure Ravon4Aurelie Sécula5Yvon Billon6Laurence Liaubet7GenPhySE, Université de Toulouse, INRAE, INPT, ENVTGenPhySE, Université de Toulouse, INRAE, INPT, ENVTGenPhySE, Université de Toulouse, INRAE, INPT, ENVTGenPhySE, Université de Toulouse, INRAE, INPT, ENVTGenESI, INRAEGenPhySE, Université de Toulouse, INRAE, INPT, ENVTGenESI, INRAEGenPhySE, Université de Toulouse, INRAE, INPT, ENVTAbstract Background A fine balance of feto-maternal resource allocation is required to support pregnancy, which depends on interactions between maternal and fetal genetic potential, maternal nutrition and environment, endometrial and placental functions. In particular, some imprinted genes have a role in regulating maternal-fetal nutrient exchange, but few have been documented in the endometrium. The aim of this study is to describe the expression of 42 genes, with parental expression, in the endometrium comparing two extreme breeds: Large White (LW); Meishan (MS) with contrasting neonatal mortality and maturity at two days of gestation (D90-D110). We investigated their potential contribution to fetal maturation exploring genes-fetal phenotypes relationships. Last, we hypothesized that the fetal genome and sex influence their endometrial expression. For this purpose, pure and reciprocally crossbred fetuses were produced using LW and MS breeds. Thus, in the same uterus, endometrial samples were associated with its purebred or crossbred fetuses. Results Among the 22 differentially expressed genes (DEGs), 14 DEGs were differentially regulated between the two days of gestation. More gestational changes were described in LW (11 DEGs) than in MS (2 DEGs). Nine DEGs were differentially regulated between the two extreme breeds, highlighting differences in the regulation of endometrial angiogenesis, nutrient transport and energy metabolism. We identified DEGs that showed high correlations with indicators of fetal maturation, such as ponderal index at D90 and fetal blood fructose level and placental weight at D110. We pointed out for the first time the influence of fetal sex and genome on endometrial expression at D90, highlighting AMPD3, CITED1 and H19 genes. We demonstrated that fetal sex affects the expression of five imprinted genes in LW endometrium. Fetal genome influenced the expression of four genes in LW endometrium but not in MS endometrium. Interestingly, both fetal sex and fetal genome interact to influence endometrial gene expression. Conclusions These data provide evidence for some sexual dimorphism in the pregnant endometrium and for the contribution of the fetal genome to feto-maternal interactions at the end of gestation. They suggest that the paternal genome may contribute significantly to piglet survival, especially in crossbreeding production systems.https://doi.org/10.1186/s12864-024-10144-1Perinatal survivalFeto-maternal interfaceEndometriumFetal genomeFetal sexPiglets
spellingShingle Agnes Bonnet
Lisa Bluy
Laure Gress
Laurianne Canario
Laure Ravon
Aurelie Sécula
Yvon Billon
Laurence Liaubet
Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
BMC Genomics
Perinatal survival
Feto-maternal interface
Endometrium
Fetal genome
Fetal sex
Piglets
title Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
title_full Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
title_fullStr Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
title_full_unstemmed Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
title_short Sex and fetal genome influence gene expression in pig endometrium at the end of gestation
title_sort sex and fetal genome influence gene expression in pig endometrium at the end of gestation
topic Perinatal survival
Feto-maternal interface
Endometrium
Fetal genome
Fetal sex
Piglets
url https://doi.org/10.1186/s12864-024-10144-1
work_keys_str_mv AT agnesbonnet sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT lisabluy sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT lauregress sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT lauriannecanario sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT laureravon sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT aureliesecula sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT yvonbillon sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation
AT laurenceliaubet sexandfetalgenomeinfluencegeneexpressioninpigendometriumattheendofgestation