Abstract

Heterosis is a widely distributed phenomenon in mollusks. It is vital in aquaculture by bringing beneficial traits into hybrids. People have utilized the heterosis theory in aquaculture for years. However, the molecular basis of heterosis remains elusive. Evident growth and survival heterosis were shown in the hybrid (“Dongyou-1”) of two Haliotis diversicolor geographic genotypes (Japan and Taiwan). To explore the molecular basis underlying the hybrid abalone’s heterosis, we conducted comparative mRNA and miRNA transcriptional analysis in the hybrid and parental genotypes. Differentially expression analysis identified 5,562 differentially expressed genes (DEGs) and 102 differentially expressed miRNAs (DEMs) between the three genotypes. 1,789 DEGs and 71 DEMs were found to be non-additively expressed in the hybrid. Meanwhile, both the expression level dominance pattern (ELD) and expression level overdominance pattern (ELOD) were found in the DEGs and DEMs, showing the existence of dominance and overdominance models in the hybrid’s transcriptome and post-transcriptional regulation. Functional analysis showed the non-additively expressed genes, ELD genes, and ELOD genes were significantly enriched in growth, immunity, and stress response related pathways, while some of the pathways were regulated by the mRNA-miRNA interactions. The expression levels of FGF, C1Q, HC, CAT, SEGPX, and MGST were significantly up-regulated in the hybrid compared to the middle parent value. In conclusion, we identified the existence of non-additivity, dominance, and overdominance models in the transcriptome and miRNAome of the H. diversicolor hybrid; these models facilitate the advantageous parental alleles’ integration into the hybrid, contributing to the hybrid’s growth and survival heterosis.

Highlights

  • Heterosis, or hybrid vigor, refers to the phenomenon that hybrids often show advantages in growth, fitness, or resistance relative to the parents (Chen, 2013)

  • The number of ELD-T patterns was significantly higher than that of ELD-J patterns in DEGs, while in DEMs the two patterns had similar numbers. These findings indicate the widespread of ELD and ELOD patterns in the hybrid’s transcriptome and miRNAome

  • The ELOD genes were mainly enriched in “transportrelated processes”, “membrane-related components”, and “transmembranerelated functions” (Supplementary Figures 3–6). These results suggest the ELD-J and ELOD genes are more related to cellular interaction and signaling transduction functions, while the ELD-T genes are more related to growth and development functions

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Summary

Introduction

Hybrid vigor, refers to the phenomenon that hybrids often show advantages in growth, fitness, or resistance relative to the parents (Chen, 2013). Heterosis is widespread in plants and animals, such as Arabidopsis, maize, rice, cotton, mice, donkey, chicken, dog, oyster, abalone, and mussel (Chen, 2013; McKeown et al, 2013). H. discus hannai ♀ × H. discus ♂ and H. discus hannai ♀ × H. fulgens were superior in growth or viability than the parents (Inoue et al, 1986; You et al, 2015). The reciprocal hybrids of H. gigantea and H. discus hannai were more resistant to heat and bacteria than the parents (Luo et al, 2010; Liang et al, 2014, 2018). Some abalone hybrids have been successfully applied in abalone aquaculture due to their superior traits (You et al, 2015; Cook, 2019)

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