Inheritance patterns of leukocyte gene expression under heat stress in F1 hybrid cattle and their parents

Abstract

Crossbreeding capitalizes on heterosis effects and results in increased performance of crossbred animals. Dominance hypothesis and overdominance hypothesis are 2 common models proposed to explain heterosis. Differential gene expression between parents and hybrids is hypothesized to be responsible for heterosis. This study aimed to investigate the heat tolerance and inheritance patterns of leukocyte transcriptomics in F1 hybrid cattle (Angus males × Droughtmaster females) and their parents Red Angus (AN) and Droughtmaster (DR) under heat stress. According to the respiratory rate and heat tolerance coefficient index, DR was better adapted to heat stress than AN. The physiological responses to heat stress of F1 hybrids were similar to AN. We identified 802 differentially expressed genes in leukocytes between AN and DR under heat stress using mRNA sequencing. Compared with AN, upregulated genes in DR were enriched in biological processes of response to stress, external and chemical stimulus, and cytokine, cell surface receptor signaling pathway, and cardiovascular system development. In contrast, upregulated genes in AN were enriched in B cell activation and regulation of B cell activation. Gene expression levels can be inherited additively or nonadditively and are classified into additive (35%), dominance (44%), and overdominance and underdominance (18%) modes in F1 hybrids and their parents. Inheritance patterns of gene expression showed that 97% (249/255) of the dominant genes were classified as paternal AN dominant in hybrids. The paternal imprinted PEG10 gene and its regulatory transcription factor MYC showed an AN dominant expression pattern. The MYC interacted with most AN dominant genes. These transcriptomic analyses revealed that DR and AN had specific cellular and humoral immunity and cardiovascular systems development function under heat stress. Inheritance pattern analyses from gene expression partly explained phenotypic differences between parents and F1 hybrids. The paternal imprinted PEG10 gene interaction with transcription factor MYC may contribute to explaining paternal dominant gene expression in hybrids.