Operons are rare in eukaryotes, where they often allow concerted expression of functionally related genes. While a dicistronic transcription unit encoding two unrelated genes, the suppressor of position-effect variegation su(var)3-9 and the gamma subunit of eukaryotic translation initiation factor 2 (eIF2γ) has been found in insecta, and its significance is not well understood. Here, we analyzed the evolutionary history of this transcription unit in arthropods and its functions by using model Coleoptera insect Tribolium castaneum. In T. castaneum, Tcsu(var)3-9 fused into the 80 N-terminal amino acids of TceIF2γ, the transcription of these two genes are resolved by alternative splicing. Phylogenetic analysis supports the natural gene fusion of su(var)3-9 and eIF2γ occurred in the ancestral line of winged insects and silverfish, but with frequent re-fission during the evolution of insects. Functional analysis by using RNAi for these two genes revealed that gene fusion did not invoke novel functions for the gene products. As a histone methyltransferase, Tcsu(var)3-9 is primarily responsible for H3K9 di-, and tri-methylation and plays important roles in metamorphosis and embryogenesis in T. castaneum. While TceIF2γ plays essential roles in T. castaneum by positively regulating protein translation mediated ecdysteroid biosynthesis. The vulnerability of the gene fusion and totally different role of su(var)3-9 and eIF2γ in T. castaneum confirm this gene fusion is a non-selected, constructive neutral evolution event in insect. Moreover, the positive relationship between protein translation and ecdysteroid biosynthesis gives new insights into correlations between translation regulation and hormonal signaling.

中文翻译：

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在Tribolium castaneum中编码组蛋白甲基转移酶su（var）3-9和翻译调节因子eIF2γ的特殊双顺反子转录单位的功能表征。

操纵子在真核生物中很少见，在那里它们通常允许功能相关基因的协调表达。虽然在昆虫中发现了编码两个不相关基因的双顺反子转录单位，但是位置效应杂色su（var）3-9和真核翻译起始因子2（eIF2γ）的γ亚基的抑制因子已经被发现，但其意义尚不清楚。在这里，我们通过使用鞘翅目昆虫Tribolium castaneum模型分析了节肢动物中该转录单位的进化历史及其功能。在T. castaneum中，Tcsu（var）3-9融合到TceIF2γ的80个N末端氨基酸中，这两个基因的转录通过选择性剪接得以解决。系统发育分析支持在有翅昆虫和银鱼的祖先系中发生的su（var）3-9和eIF2γ的自然基因融合，但在昆虫进化过程中经常裂变。通过对这两个基因使用RNAi进行的功能分析表明，基因融合并未为该基因产物调用新功能。作为组蛋白甲基转移酶，Tcsu（var）3-9主要负责H3K9二甲基和三甲基化，并在锥栗木的变态和胚胎发生中起重要作用。TceIF2γ通过积极调节蛋白质翻译介导的蜕皮甾类生物合成而在cast树中起重要作用。基因融合的脆弱性以及粟（T. castaneum）中su（var）3-9和eIF2γ的完全不同的作用证实了这种基因融合是昆虫中非选择性的建设性中性进化事件。此外，