oskar acts with the transcription factor Creb to regulate long-term memory in crickets.

oskar acts with the transcription factor Creb to regulate long-term memory in crickets.
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DOI:
10.1073/pnas.2218506120
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发表时间:
2023-05-23
影响因子:
11.1
通讯作者:
Extavour, Cassandra G.
Extavour, Cassandra G.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Kulkarni, Arpita;Ewen-Campen, Ben;Terao, Kanta;Matsumoto, Yukihisa;Li, Yaolong;Watanabe, Takayuki;Kao, Jonchee A.;Parhad, Swapnil S.;Ylla, Guillem;Mizunami, Makoto;Extavour, Cassandra G.

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当新的基因进化时,既然有机体以前不需要它们来生存,为什么不立即从基因组中消除它们呢?在这里,我们检验了一种假说,即新基因可以通过进化与控制基本适应性特征的先前存在的基因的调控相互作用而存活下来。我们提供了独特的昆虫特有的Oskar基因通过在成年神经干细胞中表达而在长期记忆中发挥作用的实验证据。我们发现,Oskar在成年板球大脑的干细胞中表达,并需要它来进行长期记忆。此外,我们提供的证据表明,奥斯卡在长期记忆中的作用涉及转录因子Creb的调节,Creb是长期记忆中的一个保守角色,早在奥斯卡起源于动物之前。新的基因有可能驱动新的生物机制的进化,或者整合到先前存在的调节电路中,并有助于调节较老的、保守的生物功能。其中一个基因,新的昆虫特有基因Oskar,是根据它在建立果蝇黑腹果蝇胚系中的作用首次被识别出来的。我们以前曾证明,该基因可能是通过涉及细菌内共生体的不寻常的结构域转移事件而产生的,并在进化其众所周知的生殖系功能之前发挥了体细胞作用。在这里,我们以奥斯卡扮演神经角色的证据的形式为这一假说提供了经验支持。我们发现Oskar在一种半变态昆虫--蟋蟀Gryllus bimaculatus的成体神经干细胞中表达。在这些被称为神经母细胞的干细胞中,奥斯卡需要和古老的动物转录因子Creb一起来调节长期(但不是短期)的嗅觉记忆。我们提供的证据表明,Oskar积极地调节Creb,它在动物的长期记忆中发挥着保守的作用,而Oskar反过来可能是Creb的直接目标。结合之前关于奥斯卡在蟋蟀和苍蝇神经系统发育和功能中的作用的报道,我们的结果与奥斯卡最初的躯体作用可能是在昆虫神经系统中的假设是一致的。此外,它与神经系统中保守的多能性基因piwi的共定位和功能合作可能促进了Oskar后来在全变态昆虫中选择生殖系。
When new genes evolve, why are they not immediately eliminated from the genome, given that the organism did not previously need them for survival? Here, we examine the hypothesis that novel genes can survive by evolving regulatory interactions with preexisting genes that control essential fitness traits. We provide experimental evidence that the unique insect-specific oskar gene plays a role in long-term memory through expression in adult neural stem cells. We show that oskar is expressed and required in stem cells of the adult cricket brain for long-term memory. Further, we provide evidence that oskar’s role in long-term memory involves regulation by the transcription factor Creb, a conserved player in long-term memory that predates the origin of oskar in animals. Novel genes have the potential to drive the evolution of new biological mechanisms, or to integrate into preexisting regulatory circuits and contribute to the regulation of older, conserved biological functions. One such gene, the novel insect-specific gene oskar, was first identified based on its role in establishing the Drosophila melanogaster germ line. We previously showed that this gene likely arose through an unusual domain transfer event involving bacterial endosymbionts and played a somatic role before evolving its well-known germ line function. Here, we provide empirical support for this hypothesis in the form of evidence for a neural role for oskar. We show that oskar is expressed in the adult neural stem cells of a hemimetabolous insect, the cricket Gryllus bimaculatus. In these stem cells, called neuroblasts, oskar is required together with the ancient animal transcription factor Creb to regulate long-term (but not short-term) olfactory memory. We provide evidence that oskar positively regulates Creb, which plays a conserved role in long-term memory across animals, and that oskar in turn may be a direct target of Creb. Together with previous reports of a role for oskar in nervous system development and function in crickets and flies, our results are consistent with the hypothesis that oskar’s original somatic role may have been in the insect nervous system. Moreover, its colocalization and functional cooperation with the conserved pluripotency gene piwi in the nervous system may have facilitated oskar’s later co-option to the germ line in holometabolous insects.
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