Transgenerational transmission of maternal stimulatory experience in domesticated birds

Lei Liu; Ning Yang; Guiyun Xu; Shuli Liu; Di Wang; Jiuzhou Song; Zhongyi Duan; Shuang Yang; Ying Yu

doi:10.1096/fj.201800762RR

Transgenerational transmission of maternal stimulatory experience in domesticated birds

FASEB J. 2018 Sep 27:fj201800762RR. doi: 10.1096/fj.201800762RR. Online ahead of print.

Authors

Lei Liu^{1

2}, Ning Yang^{1

2}, Guiyun Xu^{1

2}, Shuli Liu^{1

2}, Di Wang^{1

2}, Jiuzhou Song³, Zhongyi Duan^{1

2}, Shuang Yang^{1

2}, Ying Yu^{1

2}

Affiliations

¹ National Engineering Laboratory for Animal Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University, Beijing, China.
² Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University, Beijing, China; and.
³ Department of Animal and Avian Sciences, University of Maryland, College Park, Maryland, USA.

PMID: 30260701
DOI: 10.1096/fj.201800762RR

Abstract

The environmental stimuli experienced by a female can influence phenotypes and gene expression in the subsequent generations. We used a specifically designed domesticated-bird model to examine the transgenerational transmission of maternal stimulus exposure, a phenomenon that has been observed but has not been understood in noninbred animals. We subjected parental generation [filial (F)₀] hens to viral- or bacterial-like stimulation after artificial insemination. Subsequent filial generations F₁ and F₂ transmitted growth or fertility variations without further stimulation in contrast to the controls. The whole-genome bisulfite sequence and next-generation mRNA sequencing of peripheral blood lymphocytes (PBLs) from the F₁ generation revealed DNA methylome and transcriptome differences in the F₁ polyriboinosinic:polyribocytidylic [poly(I:C)] acid or LPS offspring, compared with the F₁ controls. In the F₁ offspring, DNA methylation changes induced by maternal immune stimulation may have contributed to transcriptional variation. Pathways analysis indicated that the metabolic processes of xenobiotics and drug metabolism pathways, as well as reproduction-related pathways, were involved in the transgenerational transmission of maternal stimulatory experience. Furthermore, LPS-induced transcriptional transmission may have contributed to subfertility, as indicated by the results of comparative analysis between the transcriptomes of spleen tissues across the F₀ and F₁ generations, as well as the correlative analysis between the transcriptome and reproductive phenotypes. Our findings provide a framework for determining the mechanisms by which maternal stimulatory factors can be inherited transgenerationally with respect to growth, fertility, DNA methylation, and transcriptional levels in outbred animals.-Liu, L., Yang, N., Xu, G., Liu, S., Wang, D., Song, J., Duan, Z., Yang, S., Yu, Y. Transgenerational transmission of maternal stimulatory experience in domesticated birds.

Keywords: chicken; epigenetic regulation; transcriptome.