Genetic basis of negative heterosis for growth traits in chickens revealed by genome-wide gene expression pattern analysis

Abstract

Background Heterosis is an important biological phenomenon that has been extensively utilized in agricultural breeding. However, negative heterosis is also pervasively observed in nature, which can cause unfavorable impacts on production performance. Compared with systematic studies of positive heterosis, the phenomenon of negative heterosis has been largely ignored in genetic studies and breeding programs, and the genetic mechanism of this phenomenon has not been thoroughly elucidated to date. Here, we used chickens, the most common agricultural animals worldwide, to determine the genetic and molecular mechanisms of negative heterosis. Results We performed reciprocal crossing experiments with two distinct chicken lines and found that the body weight presented widely negative heterosis in the early growth of chickens. Negative heterosis of carcass traits was more common than positive heterosis, especially breast muscle mass, which was over − 40% in reciprocal progenies. Genome-wide gene expression pattern analyses of breast muscle tissues revealed that nonadditivity, including dominance and overdominace, was the major gene inheritance pattern. Nonadditive genes, including a substantial number of genes encoding ATPase and NADH dehydrogenase, accounted for more than 68% of differentially expressed genes in reciprocal crosses (4257 of 5587 and 3617 of 5243, respectively). Moreover, nonadditive genes were significantly associated with the biological process of oxidative phosphorylation, which is the major metabolic pathway for energy release and animal growth and development. The detection of ATP content and ATPase activity for purebred and crossbred progenies further confirmed that chickens with lower muscle yield had lower ATP concentrations but higher hydrolysis activity, which supported the important role of oxidative phosphorylation in negative heterosis for growth traits in chickens. Conclusions These findings revealed that nonadditive genes and their related oxidative phosphorylation were the major genetic and molecular factors in the negative heterosis of growth in chickens, which would be beneficial to future breeding strategies.

Phenotypic and genetic parameters of productive traits in Rahmani and Romanov sheep and crossbreds

“…On the other hand, Elshennawy et al [ 20 ] analyzed 1693 lambs data and reported that increase of Romanov blood from 25% to 50% had no significant change in mature weight, rate of maturity and instantaneous growth rates at 2, 6 and 12 months of age. Negative heterosis is connected with nonadditive genes and their oxidative phosphorylation [ 21 ] which cause unfavourable impacts on production performance of animals. Heterosis reduces in later generations after F1 due to segregation and recombination losses [ 22 ].…”

Transcriptome-Wide Analyses Identify Dominant as the Predominantly Non-Conservative Alternative Splicing Inheritance Patterns in F1 Chickens

“…In addition, oxidative phosphorylation forms adenosine triphosphate (ATP) as a result of the transfer of electrons from NADH or FADH2 to O 2 by a series of electron carriers related to six genes namely ATP6V1A, UQCRQ, NDUFA8, NDUFV3, NDUFB3, and UQCRC2. This pathway is also correlated with body weight in Drosophila, and is associated with heterosis in plants (Mcdaniel and Grimwood, 1971; Katara (Mai et al, 2021). The liver is the major site of amino acid metabolism and fat deposition in the body, and 37 non-conserved AS genes are significantly enriched in metabolic pathways, amino acid metabolism, and glycerolipid metabolism.…”

“…This pathway is also correlated with body weight in Drosophila, and is associated with heterosis in plants ( Mcdaniel and Grimwood, 1971 ; Katara et al, 2020 ). By detecting ATP content and ATPase activity in reciprocal cross chickens, Mai et al validated that oxidative phosphorylation is the major genetic and molecular factor in growth ( Mai et al, 2021 ). The liver is the major site of amino acid metabolism and fat deposition in the body, and 37 non-conserved AS genes are significantly enriched in metabolic pathways, amino acid metabolism, and glycerolipid metabolism.…”

Genetic Basis of Sexual Maturation Heterosis: Insights From Ovary lncRNA and mRNA Repertoire in Chicken

“…Secondly, transcripts with class code “i”, “u” and “x” were retained. Subsequently, the sequence of known lncRNAs were download from two lncRNA databases, Domestic-Animal LncRNA Database (ALDB) ( 12 ) and NONCODE ( 27 ). We then used BLAST to align the unannotated transcripts to known lncRNAs.…”

“…The transcriptional changes in hybrids generally associated with processes involved in the energy production, metabolic rates, stress response and hormone signaling (10). In chickens, multiple studies illustrated the heterosis mechanism of important traits at different stages through genome-wide expression analysis of brain, liver and muscle (11)(12)(13). Long non-coding RNAs (lncRNAs) are pivotal epigenomic factors, a class of endogenous more than 200 bases in length, and could affect gene expression by acting as cis-or transregulators (14).…”