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. 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. 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.

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全基因组基因表达模式分析揭示了鸡生长特性负杂种优势的遗传基础

杂种优势是一种重要的生物学现象，已广泛用于农业育种中。但是，自然界也普遍观察到负面杂种优势，这可能会对生产性能产生不利影响。与正杂种优势的系统研究相比，在遗传研究和育种程序中负杂种现象已被很大程度上忽略，并且迄今为止尚未彻底阐明这种现象的遗传机制。在这里，我们使用了鸡（全世界最常见的农业动物）来确定负杂种优势的遗传和分子机制。我们对两种不同的鸡系进行了相互交叉实验，发现体重在鸡的早期生长中呈现出广泛的负杂种优势。positive体性状的负杂种优势比阳性杂种优势更为普遍，尤其是胸肌质量，在后代中超过-40％。乳房肌肉组织的全基因组基因表达模式分析表明，包括显性和过度优势在内的非可加性是主要的基因遗传模式。非加性基因，包括大量编码ATPase和NADH脱氢酶的基因，在双向杂交中分别占差异表达基因的68％以上（分别为4257和5617和3617和5243）。此外，非加性基因与氧化磷酸化的生物学过程显着相关，氧化磷酸化是能量释放和动物生长发育的主要代谢途径。对纯种和杂交后代的ATP含量和ATPase活性的检测进一步证实，肌肉产量较低的鸡的ATP浓度较低，但水解活性较高，这支持了氧化磷酸化在鸡生长特性的负杂种优势中的重要作用。这些发现表明，非加性基因及其相关的氧化磷酸化是造成鸡生长负杂种优势的主要遗传和分子因素，这将有利于未来的育种策略。