The taste of ribonucleosides: Novel macronutrients essential for larval growth are sensed by Drosophila gustatory receptor proteins.

The taste of ribonucleosides: Novel macronutrients essential for larval growth are sensed by Drosophila gustatory receptor proteins.
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DOI:
10.1371/journal.pbio.2005570
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发表时间:
2018-08
期刊:
影响因子:
9.8
通讯作者:
Amrein H
Amrein H
中科院分区:
生物学1区
文献类型:
--
作者:
Mishra D;Thorne N;Miyamoto C;Jagge C;Amrein H

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动物利用不同类型的味觉感受器来识别和区分不同的营养食品化学物质。这些常量营养素被认为分为三大类:碳水化合物/糖、蛋白质/氨基酸和脂肪。在这里,我们报告了果蝇幼虫对核糖、核糖核苷和RNA的一种新的食欲行为。我们鉴定了味觉受体(Gr)亚家族28(Gr28)的成员,它表达在外部和内部化学感觉神经元中,是细胞和食欲行为对核糖核苷和RNA反应所必需的分子受体。具体地说,行为偏好分析表明,幼虫以依赖于Gr28的方式强烈地被含有核糖或RNA的琼脂糖吸引。此外,钙离子成像实验表明,表达Gr28a的味觉神经元被核糖、RNA和一些核糖核苷激活,这些反应可以通过表达Gr28基因家族的单个成员传递到Gr43aGAL4果糖敏感神经元。最后,我们通过证明Gr28突变幼虫在被要求在食物中发现核糖核苷时显示出低存活率,从而确立了Gr28基因在行为适合性中的关键作用。总之,我们的工作确定了一种新的味觉模式,专门用于检测RNA和核糖核苷,这是果蝇幼虫加速生长阶段生存所必需的营养物质。经历完全变态的昆虫只在幼虫发育阶段生长。在许多物种中,这一时期被限制在几天内,在此期间,幼虫的体重可能会增加数百倍。例如,黑腹果蝇在短短4.5d的时间里从大约10μg的一龄幼虫成长为重约2毫克的游荡的三龄幼虫。已知的对这一快速增长期至关重要的主要常量营养素是氨基酸和糖。在这项研究中,我们确定核糖核苷和RNA是一种新的额外类型的营养物质,对幼虫的快速生长和生存是必要的。我们发现,幼虫体内有味觉神经元,这些神经元表达感知核糖核苷和RNA所必需的味觉受体。缺乏这些味觉感受器的幼虫在暴露在复杂的食物环境中时显示出高死亡率,这种食物环境需要含有核糖核苷的食物的位置。我们假设,在经历快速生长期的昆虫幼虫中,品尝RNA的能力是一种新的味觉方式,因为摄取核糖核苷,而不是从头合成,在极端生长期提供了一种生存优势。
Animals employ various types of taste receptors to identify and discriminate between different nutritious food chemicals. These macronutrients are thought to fall into 3 major groups: carbohydrates/sugars, proteins/amino acids, and fats. Here, we report that Drosophila larvae exhibit a novel appetitive feeding behavior towards ribose, ribonucleosides, and RNA. We identified members of the gustatory receptor (Gr) subfamily 28 (Gr28), expressed in both external and internal chemosensory neurons as molecular receptors necessary for cellular and appetitive behavioral responses to ribonucleosides and RNA. Specifically, behavioral preference assays show that larvae are strongly attracted to ribose- or RNA-containing agarose in a Gr28-dependent manner. Moreover, Ca2+ imaging experiments reveal that Gr28a-expressing taste neurons are activated by ribose, RNA and some ribonucleosides and that these responses can be conveyed to Gr43aGAL4 fructose-sensing neurons by expressing single members of the Gr28 gene family. Lastly, we establish a critical role in behavioral fitness for the Gr28 genes by showing that Gr28 mutant larvae exhibit low survival rates when challenged to find ribonucleosides in food. Together, our work identifies a novel taste modality dedicated to the detection of RNA and ribonucleosides, nutrients that are essential for survival during the accelerated growth phase of Drosophila larvae. Insects that undergo complete metamorphosis grow only during the larval stage of development. In many species, this period is restricted to a few days, during which larvae might increase their weight up to several hundred-fold. Drosophila melanogaster, for example, grow from a tiny first-instar larva of about 10 μg to a wandering third-instar larva weighing about 2 mg over a period of only 4.5 days. The main macronutrients known to be critical for this period of rapid growth are amino acids and sugars. In this study, we identify ribonucleosides and RNA as a new, additional type of nutrient necessary for rapid larval growth and survival. We show that larvae harbor taste neurons that express taste receptors necessary for sensing ribonucleosides and RNA. Larvae lacking these taste receptors show high mortality rates when exposed to a complex food environment that requires the location of ribonucleoside-containing food. We hypothesize that the ability to taste RNA evolved as a new taste modality in larvae of insects that go through a rapid growth period because ingestion of ribonucleosides, as opposed to de novo synthesis, provides a survival advantage during a period of extreme growth.
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