TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.
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DOI：
10.1371/journal.pgen.1007338
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发表时间：
2018-04
期刊：
影响因子：
4.5
通讯作者：
Maekawa K
中科院分区：
文献类型：
--
作者：
Masuoka Y;Yaguchi H;Toga K;Shigenobu S;Maekawa K
对不育等级分化的内在近似因素的工作知识对于理解真社会性昆虫的进化是必要的。对群居膜翅目昆虫的基因组学和转录组学分析得出了一种假设，即不育种姓是由独居祖先中发现的共同基因网络的新功能产生的。然而，种姓分化过程中的转录组分析尚未在白蚁中进行测试，与获得种姓相关的进化过程仍然未知。白蚁拥有士兵等级，这被认为是该分类单元中第一个获得的永久不育等级。本研究以湿木白蚁（zotermopsis nevadensis）为研究对象，在自然条件下，对工蚁、士兵和士兵蜕皮3个蜕皮过程中的白蚁头部进行了转录组比较分析。虽然在每个蜕皮过程中观察到相似的表达模式，但在军人蜕皮前（军人的中间阶段），有50多个基因被证明是高表达的。然后，我们对候选的13个基因进行了RNA干扰（RNAi），包括转录因子和未表征的蛋白质基因，在幼年激素（JH）类似物治疗诱导的军人分化过程中。两种与tgf - β（转化生长因子β）信号相关的基因被RNAi后诱导的前生士兵非常不寻常，具有士兵样表型。这些个体在面对作为假想敌的蚁群时，也表现出与天然士兵相似的攻击行为。这些前军人从未蜕皮到下一龄，可能是由于蜕皮激素（20-羟基蜕皮激素；20E）信号基因的表达水平降低。这些结果表明，在白蚁士兵分化过程中，TGFβ信号通路在JH和20E信号通路之间具有调节的新功能。不育种姓的获得是动物社会进化的关键一步。士兵是白蚁中第一个获得的永久不育种姓，白蚁与膜翅目的真社会昆虫（蜜蜂、蚂蚁和黄蜂）有远亲关系。然而，获得士兵种姓的进化背景在很大程度上仍然不清楚。在这里，我们进行了转录组分析，在自然条件下的工人和士兵阶层分化的头，其中全基因组序列是可用的。士兵通过两次蜕皮过程与工蚁区别开来，中间阶段被称为士兵。通过对不同蜕皮期的比较，鉴定出一些前体特异性高表达基因，包括转录因子和一些未表征的蛋白基因。两种可能参与TGFβ信号传导的基因的RNAi导致具有士兵样表型（例如，良好的角质层）的前士兵的形成，而不会进一步蜕皮为士兵。20E信号基因的表达水平受到RNAi处理的负面影响。本研究为白蚁等级分化的激素调控提供了新的视角。
A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites. The acquisition of a sterile caste is a key step in animal eusocial evolution. The soldier is the first acquired permanently sterile caste in termites, which are distantly related to hymenopteran eusocial insects (bees, ants and wasps). However, the evolutionary background to acquiring the soldier caste is still largely unclear. Here we performed transcriptome analysis of heads during worker and soldier caste differentiation under natural conditions in Zootermopsis nevadensis, for which the whole-genome sequence is available. Soldiers differentiate from workers via a double molting processes, and the intermediate stage is called a presoldier. Based on the comparison among molting stages, some presoldier-specific highly expressed genes, including transcription factors and several uncharacterized protein genes, were identified. RNAi of two genes presumably involved in the TGFβ signaling resulted in the formation of presoldiers possessing soldier-like phenotypes (e.g. well-tunned cuticle) without further molting into soldiers. Expression levels of 20E signaling genes were negatively affected by the RNAi treatment of these genes. This study provides a novel insight into the hormonal control for termite caste differentiation.
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