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.
中科院分区:
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.
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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影响因子:
1.9
作者:
HEISENBERG, M;BORST, A;BYERS, D
通讯作者:
BYERS, D
影响因子:
10.5
作者:
Breitwieser, W;Markussen, FH;Ephrussi, A
通讯作者:
Ephrussi, A
影响因子:
14.9
作者:
Bailey TL;Johnson J;Grant CE;Noble WS
通讯作者:
Noble WS
影响因子:
10.7
作者:
Blondel L;Besse S;Rivard EL;Ylla G;Extavour CG
通讯作者:
Extavour CG
影响因子:
56.9
作者:
Chen, Chun-Chao;Wu, Jie-Kai;Chiang, Ann-Shyn
通讯作者:
Chiang, Ann-Shyn