High serum reproductive hormone levels at mid-pregnancy support Meishan pig prolificacy

doi:10.1016/j.jia.2023.05.014

Journal of Integrative Agriculture

2023, Vol. 22

Issue (11): 3489-3499 DOI: 10.1016/j.jia.2023.05.014

Animal Science · Veterinary Medicine

Advanced Online Publication | Current Issue | Archive | Adv Search

High serum reproductive hormone levels at mid-pregnancy support Meishan pig prolificacy

ZHOU Rong^{1, 2*}, YANG Ya-lan^{3, 4*}, LIU Ying¹, CHEN Jie⁵, YANG Bing¹, TANG Zhong-lin^{3, 4#}

¹ MOE Laboratory of Biosystem Homeostasis and Protection, Life Sciences Institute, Zhejiang University, Hangzhou 310058, P.R.China
² State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
³ Kunpeng Institute of Modern Agriculture at Foshan, Institute of Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences Foshan 528226, P.R.China
⁴ Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Shenzhen 518000, P.R.China
⁵ Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, P.R.China

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

提高我国种猪生产效率是当务之急，尽管与母猪总产仔数性状相关的候选位点已逐步被揭示，但其分子机制尚不清晰。梅山猪是享誉世界的高产猪种，其繁殖力高于瘦肉型的大白猪等西方引进猪种。卵巢合成和分泌雌二醇、孕酮等类固醇激素，指导着猪卵母细胞发育、妊娠建立和维持、泌乳等生殖过程，是决定妊娠期生殖特征的关键器官。本研究关注妊娠中期第二个胎儿丢失的关键时期，妊娠第49天的卵巢生理过程，通过转录组、蛋白质组和代谢组的多组学比较研究，旨在确定梅山猪和大白郡猪卵巢黄体的基因组、蛋白质组学和代谢组学差异，以揭示母猪高繁殖力的潜在分子遗传机制。结果显示：梅山猪在妊娠中期的转录组和蛋白质组水平上都表现出卵巢类固醇生物合成和丁酸代谢的普遍下调，但血清胆固醇、雌二醇和孕酮水平均高于大白猪；鉴定出类固醇激素途径基因中与猪总产仔数、猪初生窝重和胎重相关的位点；揭示了梅山猪的高繁殖力性状形成的关键因素之一：调控妊娠中期较低的类固醇物质生物合成效率和较高的生殖激素血清水平的平衡，减少妊娠期的胎儿丢失。

Abstract Increasing prolificacy is an important aim in the pig industry. Regions associated with litter size have been revealed, but detailed molecular mechanisms are unclear. The Meishan pig is one of the most prolific breeds, with higher prolificacy than the Yorkshire pig, which exhibits high feeding efficiency and lean meat yield. The ovary is the key organ determining reproductive traits during pregnancy by synthesizing and secreting reproductive hormones essential for conceptus maintenance. In this comparative multi-omics study of the ovary transcriptome, proteome, and metabolome on day 49 of pregnancy, we aimed to identify genomic, proteomic, and metabolomic differences between the ovaries of Meishan and Yorkshire pigs to reveal potential molecular mechanisms conferring high prolificacy. Meishan pigs demonstrated general downregulation of steroid biosynthesis and butanoate metabolism in the ovary during mid-pregnancy at both transcriptome and proteome levels but exhibited higher serum cholesterol, estradiol, and progesterone levels than Yorkshire pigs. We also identified several single-nucleotide polymorphisms in the genes of the steroid hormone pathway associated with litter number, average birth weight, and total litter weight. Lower biosynthesis rates but elevated serum levels of reproductive hormones during mid- and late pregnancy are essential for the greater prolificacy of Meishan pigs.

Keywords: ovary progesterone Meishan steroid biosynthesis multi-omics

Received: 09 September 2022 Accepted: 09 October 2022

Fund: This work was supported by the National Natural Science Foundation of China (31972541 and 31830090), the Central Public-interest Scientific Institution Basal Research Fund, China (Y2021XK20), the Special Construction Project Fund for Shandong Province Taishan Scholars, China and the Agricultural Science and Technology Innovation Program, China (ASTIP-IAS05).

About author: ZHOU Rong, E-mail: zhourong03@caas.cn; #Correspondence TANG Zhong-lin, E-mail: tangzhonglin@caas.cn * These authors contributed equally to this study.

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors
	ZHOU Rong
	YANG Yalan
	LIU Ying
	CHEN Jie
	YANG Bing
	TANG Zhong-lin

Cite this article:

ZHOU Rong, YANG Yalan, LIU Ying, CHEN Jie, YANG Bing, TANG Zhong-lin. 2023. High serum reproductive hormone levels at mid-pregnancy support Meishan pig prolificacy. Journal of Integrative Agriculture, 22(11): 3489-3499.

Anders S, Pyl P T, Huber W. 2015. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166–169.

Corbin C J, Moran F M, Vidal J D, Ford J J, Wise T, Mapes S M, Njar V C, Brodie A M, Conley A J. 2003. Biochemical assessment of limits to estrogen synthesis in porcine follicles. Biology of Reproduction, 69, 390–397.

Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26, 1367–1372.

DeBose-Boyd R A. 2008. Feedback regulation of cholesterol synthesis: Sterol-accelerated ubiquitination and degradation of HMG CoA reductase. Cell Research, 18, 609–621.

Fernandez-Rodriguez A, Munoz M, Fernandez A, Pena R N, Tomas A, Noguera J L, Ovilo C, Fernandez A I. 2011. Differential gene expression in ovaries of pregnant pigs with high and low prolificacy levels and identification of candidate genes for litter size. Biology of Reproduction, 84, 299–307.

Frantz L A, Schraiber J, Madsen O, Megens H J, Cagan A, Bosse M, Paudel Y, Crooijmans R P, Larson G, Groenen M A. 2015. Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nature Genetics, 47, 1141–1148.

Gao X, Pujos-Guillot E, Sébédio J L. 2010. Development of a quantitative metabolomic approach to study clinical human fecal water metabolome based on trimethylsilylation derivatization and GC/MS analysis. Analytical Chemistry, 82, 6447–6456.

Groenen M A, Archibald A L, Uenishi H, Tuggle C K, Takeuchi Y, Rothschild M F, Rogel-Gaillard C, Park C, Milan D, Megens H J. 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491, 393–398.

Gu T, Zhu M J, Schroyen M, Qu L, Nettleton D, Kuhar D, Lunney J K, Ross J W, Zhao S H, Tuggle C K. 2014. Endometrial gene expression profiling in pregnant Meishan and Yorkshire pigs on day 12 of gestation. BMC Genomics, 15, 156.

Haley C, Lee G, Ritchie M. 1995. Comparative reproductive performance in Meishan and Large White pigs and their crosses. Animal Science, 60, 259–267.

Hernandez S C, Finlayson H A, Ashworth C J, Haley C S, Archibald A L. 2014. A genome-wide linkage analysis for reproductive traits in F2 Large White×Meishan cross gilts. Animal Genetics, 45, 191–197.

Huang J, Liu R, Su L, Xiao Q, Yu M. 2015. Transcriptome analysis revealed the embryo-induced gene expression patterns in the endometrium from meishan and yorkshire pigs. International Journal of Molecular Sciences, 16, 22692–22710.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.

Liu L Q, Li F E, Deng C Y, Zuo B, Zheng R, Xiong Y Z. 2009. Polymorphism of the pig 17beta-hydroxysteroid dehydrogenase type1 (HSD17B1) gene and its association with reproductive traits. Animal Reproduction Science, 114, 318–323.

Liu Y, Fu Y, Yang Y, Yi G, Lian J, Xie B, Yao Y, Chen M, Niu Y, Liu L, Wang L, Zhang Y, Fan X, Tang Y, Yuan P, Zhu M, Li Q, Zhang S, Chen Y, Wang B, et al. 2022. Integration of multi-omics data reveals cis-regulatory variants that are associated with phenotypic differentiation of eastern from western pigs. Genetics Selection Evolution, 54, 62.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Lu N, Li M, Lei H, Jiang X, Tu W, Lu Y, Xia D. 2017. Butyric acid regulates progesterone and estradiol secretion via cAMP signaling pathway in porcine granulosa cells. Journal of Steroid Biochemistry and Molecular Biology, 172, 89–97.

Noguera J L, Rodriguez C, Varona L, Tomas A, Munoz G, Ramirez O, Barragan C, Arque M, Bidanel J P, Amills M, Ovilo C, Sanchez A. 2009. A bi-dimensional genome scan for prolificacy traits in pigs shows the existence of multiple epistatic QTL. BMC Genomics, 10, 636.

Zhou R, Yang Y L, Liu Y, Chen Q M, Chen J, Li K. 2017. Association of CYP19A1 gene polymorphisms with reproductive traits in pigs. Journal of Integrative Agriculture, 16, 1558–1565.

Ross J W, Ashworth M D, Stein D R, Couture O P, Tuggle C K, Geisert R D. 2009. Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium. Physiological Genomics, 36, 140–148.

Spotter A, Distl O. 2006. Genetic approaches to the improvement of fertility traits in the pig. Veterinary Journal, 172, 234–247.

Wang Z, Yang Y, Li S, Li K, Tang Z. 2019. Analysis and comparison of long non-coding RNAs expressed in the ovaries of Meishan and Yorkshire pigs. Animal Genetics, 50, 660–669.

Yu G, Wang L G, Han Y, He Q Y. 2012. clusterProfiler: An R package for comparing biological themes among gene clusters. Omics: A Journal of Integrative Biology, 16, 284–287.

Zhang X, Huang L, Wu T, Feng Y, Ding Y, Ye P, Yin Z. 2015. Transcriptomic analysis of ovaries from pigs with high and low litter size. PLoS ONE, 10, e0139514.

Zhou R, Li S T, Yao W Y, Xie C D, Chen Z, Zeng Z J, Wang D, Xu K, Shen Z J, Mu Y, Bao W, Jiang W, Li R, Liang Q, Li K. 2021. The Meishan pig genome reveals structural variation-mediated gene expression and phenotypic divergence underlying Asian pig domestication. Molecular Ecology Resources, 21, 2077–2092.

[1]	YANG Ya-lan, ZHOU Rong, LI Kui. Future livestock breeding: Precision breeding based on multi-omics information and population personalization[J]. >Journal of Integrative Agriculture, 2017, 16(12): 2784-2791.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors