Plants are a difficult food resource to use, and herbivorous insects have evolved a variety of mechanisms that allow them to fully exploit this poor nutritional resource. One such mechanism is the maintenance of bacterial symbionts that aid in host plant feeding and development. The majority of these intracellular symbionts have highly eroded genomes that lack many key regulatory genes; consequently, it is unclear if these symbionts can respond to changes in the insect's diet to facilitate host plant use. There is emerging evidence that symbionts with highly eroded genomes express small RNAs (sRNAs), some of which potentially regulate gene expression. In this study, we sought to determine if the reduced genome of the nutritional symbiont (Buchnera) in the pea aphid responds to changes in the aphid's host plant diet. Using transcriptome sequencing (RNA-seq), Buchnera sRNA expression profiles were characterized within two Buchnera life stages when pea aphids fed on either alfalfa or fava bean. Overall, this study demonstrates that Buchnera sRNA expression changes not only with life stage but also with changes in aphid host plant diet. Of the 321 sRNAs characterized in this study, 47% were previously identified and 22% showed evidence of conservation in two or more Buchnera taxa. Functionally, 13 differentially expressed sRNAs were predicted to target genes related to pathways involved in essential amino acid biosynthesis. Overall, results from this study reveal that host plant diet influences the expression of conserved and lineage-specific sRNAs in Buchnera and that these sRNAs display distinct host plant-specific expression profiles among biological replicates.IMPORTANCE In general, the genomes of intracellular bacterial symbionts are reduced compared to those of free-living relatives and lack many key regulatory genes. Many of these reduced genomes belong to obligate mutualists of insects that feed on a diet that is deficient in essential nutrients, such as essential amino acids. It is unclear if these symbionts respond with their host to changes in insect diet, because of their reduced regulatory capacity. Emerging evidence suggests that these symbionts express small RNAs (sRNAs) that regulate gene expression at the posttranscriptional level. Therefore, in this study, we sought to determine if the reduced genome of the nutritional symbiont Buchnera in the pea aphid responds to changes in the aphid's host plant diet. This study demonstrates for the first time that Buchnera sRNAs, some conserved in two or more Buchnera lineages, are differentially expressed when aphids feed on different plant species and potentially target genes within essential amino acid biosynthesis pathways.

中文翻译：

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蚜虫寄主植物饮食的变化影响其专性营养共生体 Buchnera 的小 RNA 表达谱。

植物是一种难以利用的食物资源，草食性昆虫已经进化出多种机制，使它们能够充分利用这种贫乏的营养资源。其中一种机制是维持有助于宿主植物进食和发育的细菌共生体。这些细胞内共生体中的大多数都具有高度侵蚀的基因组，缺乏许多关键的调控基因；因此，尚不清楚这些共生体是否能够对昆虫饮食的变化做出反应，以促进宿主植物的利用。越来越多的证据表明，基因组高度受损的共生体表达小RNA (sRNA)，其中一些可能调节基因表达。在这项研究中，我们试图确定豌豆蚜中营养共生体（Buchnera）基因组的减少是否会对蚜虫寄主植物饮食的变化做出反应。使用转录组测序 (RNA-seq)，对豌豆蚜取食苜蓿或蚕豆时的两个 Buchnera 生命阶段内的 Buchnera sRNA 表达谱进行了表征。总的来说，这项研究表明，Buchnera sRNA 表达不仅随着生命阶段的变化而变化，而且还随着蚜虫寄主植物饮食的变化而变化。在本研究中鉴定的 321 种 sRNA 中，47% 是先前鉴定的，22% 显示出在两个或更多 Buchnera 类群中保守的证据。从功能上来说，13 个差异表达的 sRNA 预计会靶向与必需氨基酸生物合成途径相关的基因。总体而言，这项研究的结果表明，宿主植物饮食影响 Buchnera 中保守和谱系特异性 sRNA 的表达，并且这些 sRNA 在生物复制中表现出不同的宿主植物特异性表达谱。 重要性 一般来说，细胞内细菌共生体的基因组是与自由生活的亲属相比，这些基因的数量有所减少，并且缺乏许多关键的调控基因。许多这些减少的基因组属于专性共生昆虫，它们以缺乏必需营养素（例如必需氨基酸）的饮食为食。目前尚不清楚这些共生体是否会与宿主一起对昆虫饮食的变化做出反应，因为它们的调节能力下降。新出现的证据表明，这些共生体表达小RNA (sRNA)，在转录后水平调节基因表达。因此，在这项研究中，我们试图确定豌豆蚜中营养共生体 Buchnera 基因组的减少是否会对蚜虫寄主植物饮食的变化做出反应。这项研究首次证明，当蚜虫取食不同植物物种和必需氨基酸生物合成途径中的潜在目标基因时，Buchnera sRNA（其中一些在两个或多个 Buchnera 谱系中保守）存在差异表达。