Identification of crucial genes and metabolites regulating the eggshell brownness in chicken

Abstract Background Protoporphyrin IX (Pp IX) is the primary pigment for brown eggshells. However, the regulatory mechanisms directing Pp IX synthesis, transport, and genetic regulation during eggshell calcification in chickens remain obscure. In this study, we investigated the mechanism of brown eg...

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Main Authors: Jing Yang, Zhiqiong Mao, Xiqiong Wang, Jingjie Zhuang, Sijia Gong, Zhouyang Gao, Guiyun Xu, Ning Yang, Congjiao Sun
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-022-08987-7
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author Jing Yang
Zhiqiong Mao
Xiqiong Wang
Jingjie Zhuang
Sijia Gong
Zhouyang Gao
Guiyun Xu
Ning Yang
Congjiao Sun
author_facet Jing Yang
Zhiqiong Mao
Xiqiong Wang
Jingjie Zhuang
Sijia Gong
Zhouyang Gao
Guiyun Xu
Ning Yang
Congjiao Sun
author_sort Jing Yang
collection DOAJ
description Abstract Background Protoporphyrin IX (Pp IX) is the primary pigment for brown eggshells. However, the regulatory mechanisms directing Pp IX synthesis, transport, and genetic regulation during eggshell calcification in chickens remain obscure. In this study, we investigated the mechanism of brown eggshell formation at different times following oviposition, using White Leghorn hens (WS group), Rhode Island Red light brown eggshell line hens (LBS group) and Rhode Island Red dark brown eggshell line hens (DBS group). Results At 4, 16 and 22 h following oviposition, Pp IX concentrations in LBS and DBS groups were significantly higher in shell glands than in liver (P < 0.05). Pp IX concentrations in shell glands of LBS and DBS groups at 16 and 22 h following oviposition were significantly higher than WS group (P < 0.05). In comparative transcriptome analysis, δ-aminolevulinate synthase 1 (ALAS1), solute carrier family 25 member 38 (SLC25A38), ATP binding cassette subfamily G member 2 (ABCG2) and feline leukemia virus subgroup C cellular receptor 1 (FLVCR1), which were associated with Pp IX synthesis, were identified as differentially expressed genes (DEGs). RT-qPCR results showed that the expression level of ALAS1 in shell glands was significantly higher in DBS group than in WS group at 16 and 22 h following oviposition (P < 0.05). In addition, four single nucleotide polymorphisms (SNPs) in ALAS1 gene that were significantly associated with eggshell brownness were identified. By identifying the differential metabolites in LBS and DBS groups, we found 11-hydroxy-E4-neuroprostane in shell glands and 15-dehydro-prostaglandin E1(1-) and prostaglandin G2 2-glyceryl ester in uterine fluid were related to eggshell pigment secretion. Conclusions In this study, the regulatory mechanisms of eggshell brownness were studied comprehensively by different eggshell color and time following oviposition. Results show that Pp IX is synthesized de novo and stored in shell gland, and ALAS1 is a key gene regulating Pp IX synthesis in the shell gland. We found three transporters in Pp IX pathway and three metabolites in shell glands and uterine fluid that may influence eggshell browning.
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spelling doaj.art-9de81dad7ca34330807edc65c92991e62022-12-22T02:55:06ZengBMCBMC Genomics1471-21642022-11-0123111510.1186/s12864-022-08987-7Identification of crucial genes and metabolites regulating the eggshell brownness in chickenJing Yang0Zhiqiong Mao1Xiqiong Wang2Jingjie Zhuang3Sijia Gong4Zhouyang Gao5Guiyun Xu6Ning Yang7Congjiao Sun8National Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityBeinongda Technology Co,.LtdNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityNational Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, China Agricultural UniversityAbstract Background Protoporphyrin IX (Pp IX) is the primary pigment for brown eggshells. However, the regulatory mechanisms directing Pp IX synthesis, transport, and genetic regulation during eggshell calcification in chickens remain obscure. In this study, we investigated the mechanism of brown eggshell formation at different times following oviposition, using White Leghorn hens (WS group), Rhode Island Red light brown eggshell line hens (LBS group) and Rhode Island Red dark brown eggshell line hens (DBS group). Results At 4, 16 and 22 h following oviposition, Pp IX concentrations in LBS and DBS groups were significantly higher in shell glands than in liver (P < 0.05). Pp IX concentrations in shell glands of LBS and DBS groups at 16 and 22 h following oviposition were significantly higher than WS group (P < 0.05). In comparative transcriptome analysis, δ-aminolevulinate synthase 1 (ALAS1), solute carrier family 25 member 38 (SLC25A38), ATP binding cassette subfamily G member 2 (ABCG2) and feline leukemia virus subgroup C cellular receptor 1 (FLVCR1), which were associated with Pp IX synthesis, were identified as differentially expressed genes (DEGs). RT-qPCR results showed that the expression level of ALAS1 in shell glands was significantly higher in DBS group than in WS group at 16 and 22 h following oviposition (P < 0.05). In addition, four single nucleotide polymorphisms (SNPs) in ALAS1 gene that were significantly associated with eggshell brownness were identified. By identifying the differential metabolites in LBS and DBS groups, we found 11-hydroxy-E4-neuroprostane in shell glands and 15-dehydro-prostaglandin E1(1-) and prostaglandin G2 2-glyceryl ester in uterine fluid were related to eggshell pigment secretion. Conclusions In this study, the regulatory mechanisms of eggshell brownness were studied comprehensively by different eggshell color and time following oviposition. Results show that Pp IX is synthesized de novo and stored in shell gland, and ALAS1 is a key gene regulating Pp IX synthesis in the shell gland. We found three transporters in Pp IX pathway and three metabolites in shell glands and uterine fluid that may influence eggshell browning.https://doi.org/10.1186/s12864-022-08987-7Protoporphyrin IXBrown eggshellδ-aminolevulinate synthase 1Shell glandOviposition
spellingShingle Jing Yang
Zhiqiong Mao
Xiqiong Wang
Jingjie Zhuang
Sijia Gong
Zhouyang Gao
Guiyun Xu
Ning Yang
Congjiao Sun
Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
BMC Genomics
Protoporphyrin IX
Brown eggshell
δ-aminolevulinate synthase 1
Shell gland
Oviposition
title Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
title_full Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
title_fullStr Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
title_full_unstemmed Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
title_short Identification of crucial genes and metabolites regulating the eggshell brownness in chicken
title_sort identification of crucial genes and metabolites regulating the eggshell brownness in chicken
topic Protoporphyrin IX
Brown eggshell
δ-aminolevulinate synthase 1
Shell gland
Oviposition
url https://doi.org/10.1186/s12864-022-08987-7
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