Asymmetric expression patterns reveal a strong maternal effect and dosage compensation in polyploid hybrid fish

Abstract

BackgroundHybridization and polyploidization are regarded as the major driving forces in plant speciation, diversification, and ecological adaptation. Our knowledge regarding the mechanisms of duplicated-gene regulation following genomic merging or doubling is primarily derived from plants and is sparse for vertebrates.ResultsWe successfully obtained an F1 generation (including allodiploid hybrids and triploid hybrids) from female Megalobrama amblycephala Yih (BSB, 2n = 48) × male Xenocypri davidi Bleeker (YB, 2n = 48). The duplicated-gene expression patterns of the two types of hybrids were explored using RNA-Seq data. In total, 5.44 × 108 (69.32 GB) clean reads and 499,631 assembled unigenes were obtained from the testis transcriptomes. The sequence similarity analysis of 4265 orthologs revealed that the merged genomes were dominantly expressed in different ploidy hybrids. The differentially expressed genes in the two types of hybrids were asymmetric compared with those in both parents. Furthermore, the genome-wide expression level dominance (ELD) was biased toward the maternal BSB genome in both the allodiploid and triploid hybrids. In addition, the dosage-compensation mechanisms that reduced the triploid expression levels to the diploid state were determined in the triploid hybrids.ConclusionsOur results indicate that divergent genomes undergo strong interactions and domination in allopolyploid offspring. Genomic merger has a greater effect on the gene-expression patterns than genomic doubling. The various expression mechanisms (including maternal effect and dosage compensation) in different ploidy hybrids suggest that the initial genomic merger and doubling play important roles in polyploidy adaptation and evolution.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4883-7) contains supplementary material, which is available to authorized users.

Genotyping of polyploid plants using quantitative PCR: application in the breeding of white-fleshed triploid loquats (Eriobotrya japonica)

“…After WGD occurs in plants, a large number of repetitive genes are produced. These repetitive genes have three different expression patterns, including expression level advantage, homology expression bias, and homology expression silencing [ 52 ]. These phenomena have been reported in species such as cotton [ 53 ], wheat [ 54 ] and Brassica napus [ 55 ].…”

“…WGD changes the regulation of gene expression, which involves complex dose effects and dose compensation effects [ 52 , 58 ]. Plant ploidy does not directly correspond to the change trend of gene expression, which exist a kind of heterosis [ 59 ].…”

Vigour‐related traits and immunity in hybrids of evolutionary divergent cyprinoid species: advantages of hybrid heterosis?

“…Li et al . (2018) analysed testis transcriptomes and showed a strong maternal effect on asymmetrical gene expression in cyprinids. Innate and adaptive immune‐relevant factors are transferred maternally, some of them functioning in the defence of fish larvae against pathogens (reviewed by Zhang et al ., 2013).…”

A New Type of Allodiploid Hybrids Derived From Female Megalobrama amblycephala × Male Gobiocypris rarus

“…Distant hybridization is an important technique and widely used in fish genetic breeding, which can combine whole genomes from parent species and lead to changes in both phenotypes and genotypes in the offspring ( Liu, 2010 ; Zhang et al, 2014 ; Xu et al, 2015a ). For example, in terms of phenotypes, the allodiploid lineage with hybrid traits, high survival rate, good meat quality, and strong stress resistance were established by the distant hybridization of Japanese white crucian carp ( Carassius cuvieri , ♀) and red crucian carp ( Carassius auratus red var., ♂) ( Wang et al, 2015 ; Liu et al, 2017 , 2018 , 2019a , b ); the triploid fish with fast growth were produced by the crossing of diploid fish with allotetraploid fish ( Tiwary et al, 2004 ; Zhong et al, 2012 ; Wang et al, 2020 ); in terms of genotypes, a high proportion of chimeric genes (>9%) have been found among orthologous genes in the transcriptomes of allotetraploid fish ( Liu et al, 2016 ); many different expressed genes associated with sperm flagellar assembly and motility were found in testis transcriptomes from diploid fish and triploid fish ( Xu et al, 2015b ; Li et al, 2018a ). These phenotypes and genotypes are very important for breeding applications and scientific research.…”