Ascoviruses are large, enveloped DNA viruses that induce remarkable changes in cellular architecture during which the cell is partitioned into numerous vesicles for viral replication. Previous studies have shown that these vesicles arise from a process resembling apoptosis yet which differs after nuclear lysis in that mitochondria are not degraded but are modified by the virus, changing in size, shape, and motility. Moreover, infection does not provoke an obvious innate immune response. Thus, we used in vivo RNA sequencing to determine whether infection by the Spodoptera frugiperda ascovirus 1a (SfAV-1a) modified expression of host mitochondrial, cytoskeletal, and innate immunity genes. We show that transcripts from many mitochondrial genes were similar to those from uninfected controls, whereas others increased slightly during vesicle formation, including those for ATP6, ATP8 synthase, and NADH dehydrogenase subunits, supporting electron microscopy (EM) data that these organelles were conserved for virus replication. Transcripts from 58 of 106 cytoskeletal genes studied increased or decreased more than 2-fold postinfection. More than half coded for mitochondrial motor proteins. Similar increases occurred for innate immunity transcripts and their negative regulators, including those for Toll, melanization, and phagocytosis pathways. However, those for many antimicrobial peptides, such as moricin, increased more than 20-fold. In addition, transcripts for gloverin-3, spod_x_tox, Hdd23, and lebocin, also antimicrobial, increased more than 20-fold. Interestingly, a phenoloxidase inhibitor transcript increased 12-fold, apparently to interfere with melanization. SfAV-1a destroys most fat body cells by 7 days postinfection, so innate immunity gene transcripts apparently occur in remaining cells in this tissue and possibly other major tissues, namely, epidermis and tracheal matrix.IMPORTANCE Ascoviruses are large DNA viruses that infect insects, inducing a cellular pathology that resembles apoptosis but which differs by causing enormous cellular hypertrophy followed by cleavage of the cell into numerous viral vesicles for replication. Previous EM studies suggest that mitochondria are important for vesicle formation. Transcriptome analyses of Spodoptera frugiperda larvae infected with SfAV-1a showed that mitochondrial transcripts were similar to those from uninfected controls or increased slightly during vesicle formation, especially for ATP6, ATP8 synthase, and NADH dehydrogenase subunits. This pattern resembles that for chronic disease-inducing viruses, which conserve mitochondria, differing markedly from viruses causing short-term viral diseases, which degrade mitochondrial DNA. Though mitochondrial transcript increases were low, our results demonstrate that SfAV-1a alters host mitochondrial expression more than any other virus. Regarding innate immunity, although SfAV-1a destroys most fat body cells, certain immunity genes were highly upregulated (greater than 20-fold), suggesting that these transcripts may originate from other tissues.

中文翻译：

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来自节食夜蛾幼虫的线粒体和先天免疫转录组已感染了节食夜蛾Ascovirus。

杆状病毒是大型的，包膜的DNA病毒，可诱导细胞结构发生显着变化，在此过程中，细胞被分成许多小泡以进行病毒复制。先前的研究表明，这些囊泡来自类似凋亡的过程，但在核裂解后有所不同，线粒体不会被病毒降解而是被病毒修饰，大小，形状和运动性都会发生变化。而且，感染不会引起明显的先天免疫反应。因此，我们使用体内RNA测序来确定由节食贪夜蛾Ascovirus 1a（SfAV-1a）感染是否修饰了宿主线粒体，细胞骨架和先天免疫基因的表达。我们显示，许多线粒体基因的转录本与未感染对照的转录本相似，而其他转录本在囊泡形成过程中略有增加，包括用于ATP6，ATP8合酶和NADH脱氢酶亚基的那些，支持电子显微镜（EM）数据，这些细胞器被保留用于病毒复制。研究的106个细胞骨架基因中有58个的转录本增加或减少了感染后2倍以上。一半以上编码线粒体运动蛋白。先天免疫转录物及其负调控因子（包括Toll，黑化和吞噬途径）也有类似的增加。但是，许多抗菌肽（如莫里辛）的肽段增加了20倍以上。此外，gloverin-3，spod_x_tox，Hdd23和Lebocin的转录本（也都具有抗菌作用）增加了20倍以上。有趣的是，酚氧化酶抑制剂的转录物增加了12倍，显然干扰了黑色素化。SfAV-1a在感染后7天会破坏大多数脂肪体细胞，因此先天免疫基因转录物显然出现在该组织以及可能的其他主要组织（如表皮和气管基质）中的其余细胞中。一种类似于细胞凋亡的细胞病理学，但通过引起巨大的细胞肥大，随后将细胞切割成大量病毒小囊进行复制而有所不同。先前的EM研究表明，线粒体对于囊泡形成很重要。感染SfAV-1a的草地贪夜蛾幼虫的转录组分析表明，线粒体转录本与未感染对照相似，或在囊泡形成过程中略有增加，尤其是对于ATP6，ATP8合酶和NADH脱氢酶亚基。这种模式类似于保存线粒体的慢性致病病毒，与引起短期病毒性疾病的病毒明显不同，后者会降解线粒体DNA。尽管线粒体转录本的增加较低，但我们的结果表明SfAV-1a比其他任何病毒更能改变宿主线粒体的表达。关于先天免疫，尽管SfAV-1a破坏了大多数脂肪细胞，但某些免疫基因被高度上调（大于20倍），表明这些转录本可能源自其他组织。我们的结果表明，SfAV-1a比其他任何病毒更能改变宿主线粒体的表达。关于先天免疫，尽管SfAV-1a破坏了大多数脂肪细胞，但某些免疫基因被高度上调（大于20倍），表明这些转录本可能源自其他组织。我们的结果表明，SfAV-1a比其他任何病毒更能改变宿主线粒体的表达。关于先天免疫，尽管SfAV-1a破坏了大多数脂肪细胞，但某些免疫基因被高度上调（大于20倍），表明这些转录本可能源自其他组织。