Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken

ABSTRACT: Egg production, regulated by multiple tissues, is among the most important economic traits in poultry. However, current research only focuses on the hypothalamic-pituitary-ovarian axis, ignoring the most important organ for substance metabolism in the body, the liver. Eggs are rich in lipi...

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Main Authors: Jun’an Shi, Hanlin Xiong, Junchao Su, Qigui Wang, Haiwei Wang, Chaowu Yang, Chenming Hu, Zhifu Cui, Lingbin Liu
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579124008551
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author Jun’an Shi
Hanlin Xiong
Junchao Su
Qigui Wang
Haiwei Wang
Chaowu Yang
Chenming Hu
Zhifu Cui
Lingbin Liu
author_facet Jun’an Shi
Hanlin Xiong
Junchao Su
Qigui Wang
Haiwei Wang
Chaowu Yang
Chenming Hu
Zhifu Cui
Lingbin Liu
author_sort Jun’an Shi
collection DOAJ
description ABSTRACT: Egg production, regulated by multiple tissues, is among the most important economic traits in poultry. However, current research only focuses on the hypothalamic-pituitary-ovarian axis, ignoring the most important organ for substance metabolism in the body, the liver. Eggs are rich in lipids, proteins, and other nutrients, which are biosynthesized in the liver. Therefore, here the liver was included in the study of the hypothalamic-pituitary axis. This study used hypothalamus (HH_vs_LH), pituitary (HP_vs_LP), liver (HL_vs_LL), and ovary (HO_vs_LO) tissue samples from high- and low-laying Chengkou mountain chickens (CMC) for epihistological, transcriptome and metabolomic analyses aimed at improving the reproductive performance of CMC. The results showed that the liver of the high-laying group was yellowish, the cell boundary was clear, and the lipid droplets were evenly distributed. The ovaries of the high-laying group had a complete sequence of hierarchical follicles, which were rich in yolk. In contrast, the ovaries of the low-laying group were atrophic, except for a few small yellow follicles, and numerous primordial follicles that remained. The transcriptome sequences yielded 167.11 Gb of clean data, containing 28,715 genes. Furthermore, 285, 822, 787, and 1,183 differentially expressed genes (DEG) were identified in HH_vs_LH, HP_vs_LP, HL_vs_LL and HO_vs_LO and the DEGs significantly enriched 77, 163, 170, 171 pathways, respectively. Metabolome sequencing yielded 21,808 peaks containing 4,006 metabolites. The differential metabolite analysis yielded 343 and 682 significantly different metabolites (SDM) that significantly enriched 136 and 87 pathways in the liver and ovaries, respectively. A combined analysis of the transcriptome and metabolome of the liver and ovaries identified “CYP51A1-4α-carboxy-stigmasta7, 24(24(1))-dien-3β-ol” and “ACSS1B-estrone 3-sulfate” and other multiple gene-metabolite pairs. The DEGs in the hypothalamus and pituitary mainly enriched signaling transduction. In contrast, the DEGs and SDMs in the liver and ovaries mainly enriched the substance metabolism pathways: “gap junction”, “extracellular matrix (ECM)-receptor interaction”, “Steroid biosynthesis”, and “Steroid hormone biosynthesis”. These results suggest that the hypothalamic-pituitary axis may affect egg production mainly by regulating lipid metabolism in the liver and ovaries.
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spelling doaj-art-d145b44d09bc4e6eae398b027329ba782025-08-20T02:39:29ZengElsevierPoultry Science0032-57912024-12-011031210427610.1016/j.psj.2024.104276Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chickenJun’an Shi0Hanlin Xiong1Junchao Su2Qigui Wang3Haiwei Wang4Chaowu Yang5Chenming Hu6Zhifu Cui7Lingbin Liu8College of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University, Beibei, 400700, Chongqing, ChinaCollege of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University, Beibei, 400700, Chongqing, ChinaCollege of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University, Beibei, 400700, Chongqing, ChinaChongQing Academy of Animal Sciences, Rongchang, Chongqing 402460, ChinaChongQing Academy of Animal Sciences, Rongchang, Chongqing 402460, ChinaSichuan Animal Science Academy, Animal Breeding and Genetics Key Laboratory of Sichuan Province, Chengdu 610066, ChinaSichuan Animal Science Academy, Animal Breeding and Genetics Key Laboratory of Sichuan Province, Chengdu 610066, ChinaCollege of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University, Beibei, 400700, Chongqing, ChinaCollege of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University, Beibei, 400700, Chongqing, China; Corresponding author:ABSTRACT: Egg production, regulated by multiple tissues, is among the most important economic traits in poultry. However, current research only focuses on the hypothalamic-pituitary-ovarian axis, ignoring the most important organ for substance metabolism in the body, the liver. Eggs are rich in lipids, proteins, and other nutrients, which are biosynthesized in the liver. Therefore, here the liver was included in the study of the hypothalamic-pituitary axis. This study used hypothalamus (HH_vs_LH), pituitary (HP_vs_LP), liver (HL_vs_LL), and ovary (HO_vs_LO) tissue samples from high- and low-laying Chengkou mountain chickens (CMC) for epihistological, transcriptome and metabolomic analyses aimed at improving the reproductive performance of CMC. The results showed that the liver of the high-laying group was yellowish, the cell boundary was clear, and the lipid droplets were evenly distributed. The ovaries of the high-laying group had a complete sequence of hierarchical follicles, which were rich in yolk. In contrast, the ovaries of the low-laying group were atrophic, except for a few small yellow follicles, and numerous primordial follicles that remained. The transcriptome sequences yielded 167.11 Gb of clean data, containing 28,715 genes. Furthermore, 285, 822, 787, and 1,183 differentially expressed genes (DEG) were identified in HH_vs_LH, HP_vs_LP, HL_vs_LL and HO_vs_LO and the DEGs significantly enriched 77, 163, 170, 171 pathways, respectively. Metabolome sequencing yielded 21,808 peaks containing 4,006 metabolites. The differential metabolite analysis yielded 343 and 682 significantly different metabolites (SDM) that significantly enriched 136 and 87 pathways in the liver and ovaries, respectively. A combined analysis of the transcriptome and metabolome of the liver and ovaries identified “CYP51A1-4α-carboxy-stigmasta7, 24(24(1))-dien-3β-ol” and “ACSS1B-estrone 3-sulfate” and other multiple gene-metabolite pairs. The DEGs in the hypothalamus and pituitary mainly enriched signaling transduction. In contrast, the DEGs and SDMs in the liver and ovaries mainly enriched the substance metabolism pathways: “gap junction”, “extracellular matrix (ECM)-receptor interaction”, “Steroid biosynthesis”, and “Steroid hormone biosynthesis”. These results suggest that the hypothalamic-pituitary axis may affect egg production mainly by regulating lipid metabolism in the liver and ovaries.http://www.sciencedirect.com/science/article/pii/S0032579124008551hypothalamic-pituitary axisliver-ovarian axistranscriptomemetabolomeegg production
spellingShingle Jun’an Shi
Hanlin Xiong
Junchao Su
Qigui Wang
Haiwei Wang
Chaowu Yang
Chenming Hu
Zhifu Cui
Lingbin Liu
Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
Poultry Science
hypothalamic-pituitary axis
liver-ovarian axis
transcriptome
metabolome
egg production
title Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
title_full Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
title_fullStr Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
title_full_unstemmed Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
title_short Multiomics analyses reveal high yield-related genes in the hypothalamic-pituitary-ovarian/liver axis of chicken
title_sort multiomics analyses reveal high yield related genes in the hypothalamic pituitary ovarian liver axis of chicken
topic hypothalamic-pituitary axis
liver-ovarian axis
transcriptome
metabolome
egg production
url http://www.sciencedirect.com/science/article/pii/S0032579124008551
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