Transcriptome analysis reveals the molecular mechanisms of heterosis on thermal resistance in hybrid abalone

Abstract

Background Heterosis has been exploited for decades in different animals and crops due to it resulting in dramatic increases in yield and adaptability. Hybridization is a classical breeding method that can effectively improve the genetic characteristics of organisms through heterosis. Abalone has become an increasingly economically important aquaculture resource with high commercial value. However, due to changing climate, abalone is now facing serious threats of high temperature in summer. Interspecific hybrid abalone (Haliotis gigantea ♀ × H. discus hannai ♂, SD) has been cultured at large scale in southern China and has been shown high survival rates under heat stress in summer. Therefore, SD has become a good model material for heterosis research, but the molecular basis of heterosis remains elusive. Results Heterosis in thermal tolerance of SD was verified through Arrhenius break temperatures (ABT) of cardiac performance in this study. Then RNA-Sequencing was conducted to obtain gene expression patterns and alternative splicing events at control temperature (20 °C) and heat stress temperature (30 °C). A total of 356 (317 genes), 476 (435genes), and 876 (726 genes) significantly diverged alternative splicing events were identified in H. discus hannai (DD), H. gigantea (SS), and SD in response to heat stress, respectively. In the heat stress groups, 93.37% (20,512 of 21,969) of the expressed genes showed non-additive expression patterns, and over-dominance expression patterns of genes account for the highest proportion (40.15%). KEGG pathway enrichment analysis showed that the overlapping genes among common DEGs and NAGs were significantly enriched in protein processing in the endoplasmic reticulum, mitophagy, and NF-κB signaling pathway. In addition, we found that among these overlap genes, 39 genes had undergone alternative splicing events in SD. These pathways and genes may play an important role in the thermal resistance of hybrid abalone. Conclusion More alternative splicing events and non-additive expressed genes were detected in hybrid under heat stress and this may contribute to its thermal heterosis. These results might provide clues as to how hybrid abalone has a better physiological regulation ability than its parents under heat stress, to increase our understanding of heterosis in abalone.

Full-Length Transcriptome Reconstruction Reveals the Genetic Mechanisms of Eyestalk Displacement and Its Potential Implications on the Interspecific Hybrid Crab (Scylla serrata ♀ × S. paramamosain ♂)

“…Another study reported that the high degree of transcriptome complexity was the genetic basis of yield heterosis [ 70 ]. However, more abundant isoforms in hybrid crabs did not result in more alternative splicing events ( Figure 3 B), which contradicted a recent study that more alternative splicing events were detected in hybrids under heat stress and may contribute to heterosis in abalone [ 71 ]. These findings suggested that, in our study, hybridization might increase the isoforms of certain genes, while decreasing the isoforms of others.…”

Transcriptome Profiling Revealed Basis for Growth Heterosis in Hybrid Tilapia (Oreochromis niloticus ♀ × O. aureus ♂)

“…Studies in transcriptomics, proteomics, metabolism, and epigenomics have provided new insights into parental genomic interactions, leading to regulatory and network changes and heterosis [1,8,9]. Recently, the differentially expressed genes (DEGs) and pathways related to heterosis have been identified through the transcriptome profiles analysis in aquatic species, such as hybrid grouper (Epinephelus fuscogutatus ♀× E. lanceolatus ♂) [10,11], hybrid pufferfish (Takifugu obscurus ♀× T. rubripes ♂) [12], hybrid tambacu (Colossoma macropomum ♀× Piaractus mesopotamicus ♂) [13], hybrid tilapia (Oreochromis niloticus ♀× O. aureus ♂) [14,15], hybrid carp (Hypophthalmichthys nobilis ♀× H. molitrix ♂) [16], hybrid seabream (Acanthopagrus schlegelii ♂× Pagrus major ♀) [17], hybrid cypriniformes [Megalobrama amblycephala ♀× (M. amblycephala ♀× Culter alburnus ♂) ♂] [18], hybrid Chinese soft-shelled turtle (Pelodiscus sinensis Japanese strain ♀× P.sinensis Qingxi black turtle ♂) [19], sea cucumber (Chinese Apostichopus japonicus ♀× Russian A. japonicus ♂) [20], and hybrid abalone (Haliotis gigantea ♀× H. discus hannai ♂) [21]. These works could help us to further understand the molecular mechanism of the heterosis in various aquatic species.…”

Transcriptomic responses to thermal stress in hybrid abalone (Haliotis discus hannai ♀ × H. fulgens ♂)

“…So far, some positive progress has been recorded ( He et al, 2017 ; Zhang et al, 2019 ; Zhang et al, 2020 ). Many metabolism- and immune-related pathways like “the protein processing in endoplasmic reticulum (ER)” ( Chen et al, 2019 ), “PI3K-AKT signaling pathway” ( Sun et al, 2016 ), “NF-κB signaling pathway” ( Zhang et al, 2014 ; Zhang et al, 2019 ; Xiao et al, 2021 ) and “nucleotide binding and oligomerization domain (NOD) like receptor signaling” ( Chen et al, 2019 ) were suggested to be involved in thermal stress in abalone ( De Zoysa et al, 2009 ; Zhang et al, 2014 ; Morash and Alter, 2015 ). It is noteworthy that the heat shock response (HSR) is one of the most common responses to thermal stress.…”

“…Hybridization is an effective way of genetic improvement in aquaculture, which can introduce improved traits to the hybrids ( Liang et al, 2014 ). And the commercial implementation of crossbreeding technology has greatly improved the thermotolerance in abalone ( Alter et al, 2017 ; Xiao et al, 2021 ). New abalone species that can withstand high temperature were introduced to China.…”