The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.

The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression.
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DOI:
10.1371/journal.pgen.1002596
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发表时间:
2012
期刊:
影响因子:
4.5
通讯作者:
Robinson GE
Robinson GE
中科院分区:
生物学2区
文献类型:
--
作者:
Ament SA;Wang Y;Chen CC;Blatti CA;Hong F;Liang ZS;Negre N;White KP;Rodriguez-Zas SL;Mizzen CA;Sinha S;Zhong S;Robinson GE

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行为是最动态的动物表型之一,由各种内部和外部刺激调节。行为差异与基因表达的大规模变化有关,但人们对这些变化是如何调节的知之甚少。在这里,我们展示了一种转录因子(TF),类视黄醇X受体的昆虫同源物,如何在复杂的转录网络中工作,可以调节行为可塑性和基因表达的相关变化。我们首先表明,RNAi敲低蜜蜂腹部脂肪体中的USP延迟了蜜蜂从在蜂巢内工作(主要是“护理”幼虫)到在室外觅食的转变。然后,我们通过转录组学实验证明,USP通过介导对幼年激素的转录反应,在脂肪体中诱导了许多与成熟相关的转录变化。ChIP-chip显示,这些与USP成熟相关的转录反应发生在USP基因组结合位点没有变化的情况下。相反,行为相关的基因表达可能是由USP和其他tf之间的组合相互作用决定的,这些tf的顺式调控基序在USP的结合位点富集。JH -和成熟相关基因的许多模块在脂肪体和大脑中都被共同调控,这预示着usp和辅助因子会影响这两个成熟相关组织中的共享转录网络。我们的研究结果表明,“单基因效应”对行为可塑性的影响可能涉及大脑和外周组织中复杂的转录网络。动物将行为作为满足其基本需求和灵活应对环境变化的主要手段之一。一种新兴的见解是,行为的改变与大脑中基因表达的巨大变化有关,但我们对这些变化是如何被调节的知之甚少。一类重要的基因调节因子是转录因子(TF),它是一种协调数万个基因表达的蛋白质。我们发现,以前主要以其在发育中的作用而为人所知的一种TF——超囊泡(USP),调节了蜜蜂的行为变化;我们表明,USP通过介导对内分泌调节剂,青少年激素的反应,导致基因表达的行为相关变化。我们提供的证据表明,这些对基因表达的影响是通过USP和其他tf之间的组合相互作用发生的,并且这些激素相关的转录网络在两个组织之间保存,这些组织在行为可塑性中起因果作用:大脑和脂肪体,一个外周营养感知器官。这些结果表明,行为是由基因和基因网络之间复杂的相互作用所决定的,这种相互作用既发生在大脑中,也发生在周围组织中。更一般地说,我们的结果表明,分子系统生物学是一个很有前途的范例,通过它来理解行为的机制基础。
Behavior is among the most dynamic animal phenotypes, modulated by a variety of internal and external stimuli. Behavioral differences are associated with large-scale changes in gene expression, but little is known about how these changes are regulated. Here we show how a transcription factor (TF), ultraspiracle (usp; the insect homolog of the Retinoid X Receptor), working in complex transcriptional networks, can regulate behavioral plasticity and associated changes in gene expression. We first show that RNAi knockdown of USP in honey bee abdominal fat bodies delayed the transition from working in the hive (primarily “nursing” brood) to foraging outside. We then demonstrate through transcriptomics experiments that USP induced many maturation-related transcriptional changes in the fat bodies by mediating transcriptional responses to juvenile hormone. These maturation-related transcriptional responses to USP occurred without changes in USP's genomic binding sites, as revealed by ChIP–chip. Instead, behaviorally related gene expression is likely determined by combinatorial interactions between USP and other TFs whose cis-regulatory motifs were enriched at USP's binding sites. Many modules of JH– and maturation-related genes were co-regulated in both the fat body and brain, predicting that usp and cofactors influence shared transcriptional networks in both of these maturation-related tissues. Our findings demonstrate how “single gene effects” on behavioral plasticity can involve complex transcriptional networks, in both brain and peripheral tissues. Animals use behavior as one of the principal means of meeting their basic needs and responding flexibly to changes in their environment. An emerging insight is that changes in behavior are associated with massive changes in gene expression in the brain, but we know relatively little about how these changes are regulated. One important class of gene regulators are transcription factors (TF), proteins that orchestrate the expression of tens to thousands of genes. We discovered that ultraspiracle (USP), a TF previously known primarily for its role in development, regulates behavioral change in the honey bee; and we show that USP causes behaviorally related changes in gene expression by mediating responses to an endocrine regulator, juvenile hormone. We present evidence that these effects on gene expression occur through combinatorial interactions between USP and other TFs, and that these hormonally related transcriptional networks are preserved between two tissues with causal roles in behavioral plasticity: the brain and the fat body, a peripheral nutrient-sensing organ. These results suggest that behavior is subserved by complex interactions between genes and gene networks, occurring both in the brain and in peripheral tissues. More generally our results suggest that molecular systems biology is a promising paradigm by which to understand the mechanistic basis for behavior.
高度社会性蜜蜂意大利蜜蜂种姓分化的分子决定因素。
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