Inherent constraints on a polyfunctional tissue lead to a reproduction-immunity tradeoff.
Inherent constraints on a polyfunctional tissue lead to a reproduction-immunity tradeoff.
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DOI：
10.1186/s12915-022-01328-w
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发表时间：
2022-06-02
期刊：
影响因子：
5.4
通讯作者：
Lazzaro, Brian P.
中科院分区：
文献类型：
--
作者：
Gupta, Vanika;Frank, Ashley M.;Matolka, Nick;Lazzaro, Brian P.
关键词：
单个组织可能具有多种功能，这可能导致限制、功能受损和权衡。昆虫脂肪体具有多种功能，包括代谢控制、生殖供应和系统免疫反应。多功能组织如何同时执行多种不同的生理功能通常是未知的。在许多生物体中观察到免疫力和生殖力的权衡，但这种权衡的机制基础通常也是未知的。在这里，我们调查的限制和权衡的多功能昆虫脂肪体。使用单核测序，我们确定了果蝇脂肪体执行不同的基本功能与异源细胞亚群。这些亚群的大小和身份是非常稳定的处女和交配苍蝇之间，以及感染前后。然而，作为一种应急功能，免疫反应涉及整个组织，所有细胞亚群产生诱导防御基因的表达。我们发现，受到细菌感染的生殖活跃女性表现出ER应激的特征，并且合成新蛋白质的能力受损，包括产生抗菌肽的能力降低。在感染前向交配的雌性动物瞬时提供可逆的翻译抑制剂，挽救了一般蛋白质合成、特异性抗菌肽的产生和感染的存活。在D.这是由于脂肪体不能同时处理生殖供应和免疫防御的蛋白质翻译需求。我们认为，在执行多种功能的组织中固有的细胞限制可能为生理和进化权衡的广泛流行提供了一般性解释。在线版本包含补充材料，可通过10.1186/s12915-022-01328-w获得。
Single tissues can have multiple functions, which can result in constraints, impaired function, and tradeoffs. The insect fat body performs remarkably diverse functions including metabolic control, reproductive provisioning, and systemic immune responses. How polyfunctional tissues simultaneously execute multiple distinct physiological functions is generally unknown. Immunity and reproduction are observed to trade off in many organisms but the mechanistic basis for this tradeoff is also typically not known. Here we investigate constraints and trade-offs in the polyfunctional insect fat body. Using single-nucleus sequencing, we determined that the Drosophila melanogaster fat body executes diverse basal functions with heterogenous cellular subpopulations. The size and identity of these subpopulations are remarkably stable between virgin and mated flies, as well as before and after infection. However, as an emergency function, the immune response engages the entire tissue and all cellular subpopulations produce induce expression of defense genes. We found that reproductively active females who were given bacterial infection exhibited signatures of ER stress and impaired capacity to synthesize new protein in response to infection, including decreased capacity to produce antimicrobial peptides. Transient provision of a reversible translation inhibitor to mated females prior to infection rescued general protein synthesis, specific production of antimicrobial peptides, and survival of infection. The commonly observed tradeoff between reproduction and immunity appears to be driven, in D. melanogaster, by a failure of the fat body to be able to handle simultaneous protein translation demands of reproductive provisioning and immune defense. We suggest that inherent cellular limitations in tissues that perform multiple functions may provide a general explanation for the wide prevalence of physiological and evolutionary tradeoffs. The online version contains supplementary material available at 10.1186/s12915-022-01328-w.
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