Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages

Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages
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DOI:
10.1242/jeb.244063
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发表时间:
2022-06-01
影响因子:
2.8
通讯作者:
Ragland, Gregory J.
Ragland, Gregory J.
中科院分区:
生物学2区
文献类型:
--
作者:
Freda, Philip J.;Toxopeus, Jantina;Ragland, Gregory J.

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具有复杂生命周期的生物体表现出在整个发育过程中改变其表型的非凡能力,可能是对发育可变环境的进化适应。在全变态昆虫中,环境敏感性表现的发育变异,特别是热敏感性,已被很好地证明。例如,成虫和幼虫阶段的热性能表现出很小的遗传相关性(遗传解耦),可以独立进化,导致不同的热反应。然而,我们对这种遗传脱钩是如何发生的知之甚少。我们测试的假设,热生理学的遗传解耦是由生命阶段之间的生理学的根本差异,尽管潜在的保守的细胞应激反应。我们使用RNAseq来比较果蝇幼虫和成虫对冷应激的转录表达,并使用RNA干扰(RNAi)来测试敲除9个靶基因是否会不同地影响幼虫和成虫的耐冷性。整个幼虫和成人的转录组学反应期间和之后暴露于-5摄氏度在很大程度上是独特的响应转录本的身份和时间动态。此外,我们分析了来自FlyAtlas 2数据的差异表达转录物的组织特异性,并得出结论,转录中的阶段特异性差异不仅仅是由组织组成的差异驱动的。此外,靶基因的RNAi对耐冷性的影响主要是阶段特异性的,有时是性别特异性的。综合证据表明,热生理学在很大程度上是阶段特异性的基因表达水平,因此,自然选择可能会在不同的生命阶段的独立热适应过程中作用于不同的位点。
Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation ( genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved cellular stress response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNA interference (RNAi) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to -5 degrees C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we analyzed the tissue-specificity of differentially expressed transcripts from FlyAtlas 2 data, and concluded that stage-specific differences in transcription were not simply driven by differences in tissue composition. In addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages.