Combined effects of dosage compensation and incomplete dominance on gene expression in triploid cyprinids

Abstract

Hybridization and polyploidy are pervasive evolutionary features of flowering plants and frequent among some animal groups, such as fish. These processes always lead to novel genotypes and various phenotypes, including growth heterosis. However, its genetic basis in lower vertebrate is still poorly understood. Here, we conducted transcriptome-level analyses of the allopolyploid complex of Carassius auratus red var. (R) (♀) × Cyprinus carpio L. (C) (♂), including the allodiploid and allotetraploid with symmetric subgenomes, and the two allotriploids with asymmetric subgenomes. The gradual changes of gene silencing and novel gene expression suggested the weakening of the constraint of polymorphic expression in genotypic changes. Then, analyses of the direction and magnitude of homoeolog expression exhibited various asymmetric expression patterns, which supported that R incomplete dominance and dosage compensation were co-regulated in the two triploids. Under these effects, various magnitudes of R-homoeolog expression bias were observed in growth-regulated genes, suggesting that they might contribute to growth heterosis in the two triploids. The determination of R incomplete dominance and dosage compensation, which might be led by asymmetric subgenomes and multiple sets of homologous chromosomes, explained why various expression patterns were shaped and their potential contribution to growth heterosis in the two triploids.

Heterosis of growth trait regulated by DNA methylation and miRNA in allotriploid fish

“…Some phenotypic diversities, such as heterosis, provide us with a useful research resource for investigating their potential mechanisms and could improve agricultural production by engineering breeding [ 6 , 7 ]. Some potential molecular regulatory mechanisms involving genomic [ 8 ] and transcriptomic changes [ 9 , 10 ] have been reported as key factors in shaping heterosis. However, studies on epigenetic modification and post-transcriptional modification are very rare in allotriploids.…”

“…Their distinct morphological characteristics, including body color and shape [ 13 , 14 ], contribute to their extensive adaptability to a diversified environment of slow-moving rivers, lakes, and ponds. Heterosis of the growth trait was observed in the allotriploid complex of common carp and crucian carp [ 7 , 9 ]. Among the two triploids, 3nRC 2 had two sets of subgenome C (originating from common carp) and one set of subgenome R (originating from red crucian carp) [ 7 , 9 ], while 3nR 2 C had one set of subgenome C and two sets of subgenome R [ 7 , 9 ].…”

“…Heterosis of the growth trait was observed in the allotriploid complex of common carp and crucian carp [ 7 , 9 ]. Among the two triploids, 3nRC 2 had two sets of subgenome C (originating from common carp) and one set of subgenome R (originating from red crucian carp) [ 7 , 9 ], while 3nR 2 C had one set of subgenome C and two sets of subgenome R [ 7 , 9 ].…”

“…Moreover, some studies have reported dosage compensation in allotriploid animals and plants, reducing transcript levels to the diploid state [ 1 , 16 , 17 ]. Incomplete dosage compensation and maternal effects were predicted in the two triploid fish (3nR 2 C and 3nRC 2 ) based on the gene expression changes between the inbred parents and the two triploids [ 9 ]. This also had various effects on the expression of growth-regulated genes, resulting in heterosis of the growth trait.…”

“…The specific genetic status of the two allotriploids (3nR 2 C and 3nRC 2 ) offers us a new insight into how dosage compensation occurs between two sets of the same chromosomes [ 9 , 16 , 17 ], and helps us further understand the relationship between genetic changes and heterosis of growth traits in allotriploids. Here, we performed DNA methylation sequencing (methyl-seq), miRNA-seq, and mRNA-seq in the muscles of the two triploids and their inbred parents ( C. auratus red var.…”