Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors.
Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors.
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DOI：
10.1371/journal.ppat.1003348
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发表时间：
2013
期刊：
影响因子：
6.7
通讯作者：
Strand MR
中科院分区：
文献类型：
--
作者：
Burke GR;Thomas SA;Eum JH;Strand MR
病毒通常被认为与宿主形成寄生关系，但多DNA病毒科的所有成员都是被称为寄生蜂的昆虫的专性互惠者。基于病毒基因序列比较的系统发育数据表明，Bracovirus属（BV）的多DNA病毒与致病性裸病毒和杆状病毒密切相关。然而，BV和杆状病毒生物学的显著差异以及许多共享基因的高度分化使得BV同源物是否仍然保留杆状病毒样功能尚不清楚。在这里，我们报告说，病毒粒子从侧沟茧蜂茧病毒（MdBV）含有多个杆状病毒样和裸壳病毒样保守基因产物。我们进一步表明，RNA干扰有效地和特异性地敲低MdBV基因表达。将RNAi敲除方法与功能测定相结合，我们检测了MdBV保守基因组中已知在杆状病毒复制期间的转录（lef-4，lef-9）、衣壳组装（vp39，vlf-1）和包膜形成（p74，pif-1）中具有重要作用的六个基因的活性。我们的研究结果表明，MdBV产生杆状病毒样RNA聚合酶，转录病毒的结构基因。我们的研究结果也支持了保守的作用vp39，vlf-1，p74，和pif-1的MdBV病毒粒子的结构组成部分。另外的实验表明，vlf-1与裸病毒样基因int-1一起在调节MdBV前病毒DNA的切除以包装成病毒体中也具有新的功能。总的来说，这些数据提供了第一个实验的BV基因在病毒体形成的功能的见解。微生物与动物和植物形成共生关系，从寄生（病原体）到有益（互利）。虽然存在许多专性互利细菌、真菌和原生动物的例子，但病毒几乎总是被认为是病原体。一个例外是多脱氧核糖核酸病毒科，它由大型DNA病毒组成，这些病毒是称为寄生蜂的昆虫的专性互惠者。先前的研究表明，Bracovirus属的多DNA病毒大约在1亿年前从一组称为裸病毒的病毒进化而来，裸病毒本身与一个称为杆状病毒的昆虫病原体大家族密切相关。因此，多脱氧核糖核酸病毒是理解病毒可以进化成互利主义者的过程的基本兴趣。在这项研究中，我们的特点是病毒颗粒的组成，从侧沟茧蜂茧状病毒（MdBV），并进行功能实验，以评估是否BV基因具有相似的功能与相关的基本杆状病毒复制基因。我们的研究结果表明，MdBV中的几个基因保留了祖先的功能，但选择其他基因具有杆状病毒未知的新功能。我们的研究结果还提供了关于多DNA病毒复制基因功能的第一个实验数据，并增强了对这些病毒及其致病祖先之间相似性的理解。
Viruses are usually thought to form parasitic associations with hosts, but all members of the family Polydnaviridae are obligate mutualists of insects called parasitoid wasps. Phylogenetic data founded on sequence comparisons of viral genes indicate that polydnaviruses in the genus Bracovirus (BV) are closely related to pathogenic nudiviruses and baculoviruses. However, pronounced differences in the biology of BVs and baculoviruses together with high divergence of many shared genes make it unclear whether BV homologs still retain baculovirus-like functions. Here we report that virions from Microplitis demolitor bracovirus (MdBV) contain multiple baculovirus-like and nudivirus-like conserved gene products. We further show that RNA interference effectively and specifically knocks down MdBV gene expression. Coupling RNAi knockdown methods with functional assays, we examined the activity of six genes in the MdBV conserved gene set that are known to have essential roles in transcription (lef-4, lef-9), capsid assembly (vp39, vlf-1), and envelope formation (p74, pif-1) during baculovirus replication. Our results indicated that MdBV produces a baculovirus-like RNA polymerase that transcribes virus structural genes. Our results also supported a conserved role for vp39, vlf-1, p74, and pif-1 as structural components of MdBV virions. Additional experiments suggested that vlf-1 together with the nudivirus-like gene int-1 also have novel functions in regulating excision of MdBV proviral DNAs for packaging into virions. Overall, these data provide the first experimental insights into the function of BV genes in virion formation. Microorganisms form symbiotic associations with animals and plants that range from parasitic (pathogens) to beneficial (mutualists). Although numerous examples of obligate, mutualistic bacteria, fungi, and protozoans exist, viruses are almost always considered to be pathogens. An exception is the family Polydnaviridae, which consists of large DNA viruses that are obligate mutualists of insects called parasitoid wasps. Prior studies show that polydnaviruses in the genus Bracovirus evolved approximately 100 million years ago from a group of viruses called nudiviruses, which are themselves closely related to a large family of insect pathogens called baculoviruses. Polydnaviruses are thus of fundamental interest for understanding the processes by which viruses can evolve into mutualists. In this study we characterized the composition of virus particles from Microplitis demolitor bracovirus (MdBV) and conducted functional experiments to assess whether BV genes share similar functions with related essential baculovirus replication genes. Our results indicate that several genes in MdBV retain ancestral functions, but select other genes have novel functions unknown from baculoviruses. Our results also provide the first experimental data on the function of polydnavirus replication genes and enhance understanding of the similarities between these viruses and their pathogenic ancestors.
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