Candidate gene screen in the red flour beetle Tribolium reveals six3 as ancient regulator of anterior median head and central complex development.

Candidate gene screen in the red flour beetle Tribolium reveals six3 as ancient regulator of anterior median head and central complex development.
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DOI:
10.1371/journal.pgen.1002416
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发表时间:
2011-12
期刊:
影响因子:
4.5
通讯作者:
Bucher G
Bucher G
中科院分区:
生物学2区
文献类型:
--
作者:
Posnien N;Koniszewski ND;Hein HJ;Bucher G

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一些高度保守的基因在脊椎动物的前神经板图案化和昆虫的头部和大脑图案化中起作用。然而,果蝇头部退化阻碍了昆虫头部形成所需基因的系统鉴定。因此,我们使用赤拟谷盗Tribolium castaneum来全面测试脊椎动物神经板图案形成基因的直系同源物在昆虫头部发育中的功能。RNAi分析表明,这些基因中的大多数确实是昆虫头囊图案化所必需的,我们还确定了几个以前没有参与这一过程的基因。此外,我们发现,TC-six 3/optix行为的TC-wingless,TC-orthodenticle 1,和TC-eyeless上游控制前正中的发展。最后,我们证明,Tc-six 3/Optix是已知的第一个基因所需的胚胎形成的中央复合体,中线跨越大脑部分连接到神经内分泌部intercerebralis。这些功能很可能在两侧对称动物中是保守的,因为脊椎动物six 3是神经内分泌和中脑发育所必需的,某些突变导致前脑无裂畸形。所有的两侧对称动物都是从一个共同的祖先进化而来的。先前的基因功能分析已经揭示了几个基因在所有两侧对称动物的前部区域的图案化中起作用,这表明人类前部神经系统形成的机制与昆虫头部和大脑的图案化相似。为了鉴定昆虫前部发育所需的新基因,我们系统地测试了已知在脊椎动物(例如小鼠和人类)的早期神经系统发育中至关重要的基因在红粉甲虫Tribolium casteneum头部的活性。事实上,除了一个基因之外,所有这些基因都是头部发育所必需的。有趣的是,我们发现six 3是昆虫大脑前正中结构所必需的,就像脊椎动物一样,six 3突变导致前脑无裂畸形。
Several highly conserved genes play a role in anterior neural plate patterning of vertebrates and in head and brain patterning of insects. However, head involution in Drosophila has impeded a systematic identification of genes required for insect head formation. Therefore, we use the red flour beetle Tribolium castaneum in order to comprehensively test the function of orthologs of vertebrate neural plate patterning genes for a function in insect head development. RNAi analysis reveals that most of these genes are indeed required for insect head capsule patterning, and we also identified several genes that had not been implicated in this process before. Furthermore, we show that Tc-six3/optix acts upstream of Tc-wingless, Tc-orthodenticle1, and Tc-eyeless to control anterior median development. Finally, we demonstrate that Tc-six3/optix is the first gene known to be required for the embryonic formation of the central complex, a midline-spanning brain part connected to the neuroendocrine pars intercerebralis. These functions are very likely conserved among bilaterians since vertebrate six3 is required for neuroendocrine and median brain development with certain mutations leading to holoprosencephaly. All bilaterian animals evolved from one common ancestor. Previous gene function analyses have revealed that several genes play a role in the patterning of anterior regions in all bilaterian animals, suggesting similar mechanisms underlying anterior nervous system formation in humans and the patterning of the insect head and brain. In order to identify novel genes required for anterior development in insects, we have systematically tested genes known to be crucially involved in early nervous system development in vertebrates (e.g. mice and humans) for their activity in the head of the red flour beetle Tribolium casteneum. Indeed, all but one of these genes are required for head development. Intriguingly, we find that six3 is required for anterior median brain structures in insects just as it is in vertebrates, where six3 mutations lead to holoprosencephaly.
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