A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches

A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches
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DOI:
10.1534/genetics.118.301038
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发表时间:
2018-08-01
期刊:
影响因子:
3.3
通讯作者:
Maekawa, Kiyoto
Maekawa, Kiyoto
中科院分区:
生物学2区
文献类型:
--
作者:
Masuoka, Yudai;Toga, Kouhei;Maekawa, Kiyoto

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不育种姓是社会性的定义标准。研究它们的进化起源可以批判性地推进理论。在白蚁中,士兵种姓被认为是第一个获得的永久不育种姓。以往的研究表明,保幼激素(JH)是诱导士兵分化的主要因素,对工人进行人工JH治疗可以产生士兵前分化。由此可见,在蟑螂进化枝内的白蚁进化过程中,士兵的形成可能需要改变典型的半代谢 JH 反应。为了解决这种可能性,我们在白蚁 Zootermopsis nevadensis 中分析了 JH 的作用及其信号通路,并与木蟑螂 Cryptocercus punculatus(白蚁姐妹群的成员)进行了比较。用 JH 类似物 (JHA) 处理可诱导 C. punctulatus 的若虫蜕皮。然后对JH受体Methoprene耐受(Met)进行RNA干扰(RNAi),它抑制了Z. nevadensis的前蜕皮和C. punctuatus的若虫蜕皮。两个物种中 Met 的敲低都会抑制 20-羟基蜕皮激素(20E;蜕皮激素的活性形式)合成基因的表达。然而,在 Z. nevadensis 中,几个 20E 信号基因被 Met RNAi 特异性抑制。因此,这些基因的 RNAi 在 JHA 处理的白蚁个体中进行。 20E 信号传导和核受体基因激素受体 39 (HR39/FTZ-F1) 的敲除导致新蜕皮的个体具有正常的工蜂表型。这是白蚁和隐尾蚴中 JH-Met 信号传导特征的首次报道。 JH 依赖性蜕皮激活是两个类群共有的,并且 JH 受体和 20E 信号之间的介导对于士兵形态发生是白蚁特有的。
Sterile castes are a defining criterion of eusociality; investigating their evolutionary origins can critically advance theory. In termites, the soldier caste is regarded as the first acquired permanently sterile caste. Previous studies showed that juvenile hormone (JH) is the primary factor inducing soldier differentiation, and treatment of workers with artificial JH can generate presoldier differentiation. It follows that a shift from a typical hemimetabolous JH response might be required for soldier formation during the course of termite evolution within the cockroach clade. To address this possibility, analysis of the role of JH and its signaling pathway was performed in the termite Zootermopsis nevadensis and compared with the wood roach Cryptocercus punctulatus, a member of the sister group of termites. Treatment with a JH analog (JHA) induced a nymphal molt in C. punctulatus. RNA interference (RNAi) of JH receptor Methoprene tolerant (Met) was then performed, and it inhibited the presoldier molt in Z. nevadensis and the nymphal molt in C. punctulatus. Knockdown of Met in both species inhibited expression of 20-hydroxyecdysone (20E; the active form of ecdysone) synthesis genes. However, in Z. nevadensis, several 20E signaling genes were specifically inhibited by Met RNAi. Consequently, RNAi of these genes were performed in JHA-treated termite individuals. Knockdown of 20E signaling and nuclear receptor gene, Hormone receptor 39 (HR39/FTZ-F1) resulted in newly molted individuals with normal worker phenotypes. This is the first report of the JH-Met signaling feature in termites and Cryptocercus. JH-dependent molting activation is shared by both taxa and mediation between JH receptor and 20E signalings for soldier morphogenesis is specific to termites.