Agrivirology Laboratory, Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama, Japan.
Instituto de Agricultura Sostenible C.S.I.C., Alameda del Obispo, Córdoba, Spain.
mBio. 2022 Oct 26;13(5):e0168522. doi: 10.1128/mbio.01685-22. Epub 2022 Aug 30.
We have previously discovered a virus neo-lifestyle exhibited by a capsidless positive-sense (+), single-stranded (ss) RNA virus YkV1 (family ) and an unrelated double-stranded (ds) RNA virus YnV1 (proposed family "") in a phytopathogenic ascomycete, . YkV1 has been proposed to replicate in the capsid provided by YnV1 as if it were a dsRNA virus and enhance YnV1 replication in return. Recently, viruses related to YkV1 (yadokariviruses) have been isolated from diverse ascomycetous fungi. However, it remains obscure whether such viruses generally show the YkV1-like lifestyle. Here, we identified partner viruses for three distinct yadokariviruses, YkV3, YkV4a, and YkV4b, isolated from that were coinfected with multiple dsRNA viruses phylogenetically distantly related to YnV1. We first established transformants of carrying single yadokarivirus cDNAs and fused them with infectants by single partner candidate dsRNA viruses. Consequently, YkV3 and YkV4s replicated only in the presence of RnMBV3 (family ) and RnMTV1 (proposed family ""), respectively. The partners were mutually interchangeable between the two YkV4 strains and three RnMTV1 strains but not between other combinations involving YkV1 or YkV3. In contrast to YkV1 enhancing YnV1 accumulation, YkV4s reduced RnMTV1 accumulation to different degrees according to strains. Interestingly, YkV4 rescued the host from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3) or host fungus. Overall, we revealed that while yadokariviruses generally require partner dsRNA viruses for replication, each yadokarivirus partners with a different dsRNA virus species in the three diverse families and shows a distinct symbiotic relation in a fungus. A capsidless (+)ssRNA virus YkV1 (family ) highjacks the capsid of an unrelated dsRNA virus YnV1 (proposed family "") in a phytopathogenic ascomycete, while YkV1 -enhances YnV1 replication. Herein, we identified the dsRNA virus partners of three yadokariviruses (YkV3, YkV4a, and YkV4b) with genome organization different from YkV1 as being different from YnV1 at the suborder level. Their partners were mutually interchangeable between the two YkV4 strains and three strains of the partner virus RnMTV1 (proposed family "") but not between other combinations involving YkV1 or YkV3. Unlike YkV1, YkV4s reduced RnMTV1 accumulation and rescued the host fungus from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3, family ) or host fungus. These revealed that while each yadokarivirus has a species-specific partnership with a dsRNA virus, yadokariviruses collectively partner extremely diverse dsRNA viruses and show three-layered complex mutualistic/antagonistic interactions in a fungus.
我们之前在一种植物病原子囊菌中发现了一种无衣壳正链（+）单链（ss）RNA 病毒 YkV1（科）和一种与它无关的双链（ds）RNA 病毒 YnV1（提议的科）所表现出的病毒新生活方式。YkV1 被提议在 YnV1 提供的衣壳内复制，就像它是一种 dsRNA 病毒一样，并且反过来增强 YnV1 的复制。最近，与 YkV1 相关的病毒（yadokariviruses）已从各种子囊菌真菌中分离出来。然而，仍然不清楚这种病毒是否普遍表现出 YkV1 样的生活方式。在这里，我们鉴定了三个不同的 yadokariviruses（YkV3、YkV4a 和 YkV4b）的伙伴病毒，这些病毒来自与 YnV1 在系统发育上亲缘关系较远的多种 dsRNA 病毒感染的。我们首先建立了携带单个 yadokarivirus cDNA 的转化体，并通过单一候选 dsRNA 病毒将它们与感染体融合。因此，YkV3 和 YkV4s 仅在 RnMBV3（科）和 RnMTV1（提议的科）存在的情况下复制。这些伙伴在两个 YkV4 株和三个 RnMTV1 株之间是相互可互换的，但在涉及 YkV1 或 YkV3 的其他组合之间则不可互换。与 YkV1 增强 YnV1 积累相反，YkV4s 根据菌株的不同程度降低了 RnMTV1 的积累。有趣的是，YkV4 挽救了宿主真菌免受 RnMTV1 诱导的生长受损。YkV3 对其伙伴（RnMBV3）或宿主真菌没有明显影响。总的来说，我们揭示了尽管 yadokariviruses 通常需要伙伴 dsRNA 病毒进行复制，但每个 yadokarivirus 与三种不同科中的不同 dsRNA 病毒物种伙伴关系，并在真菌中表现出不同的共生关系。一种无衣壳（+）ssRNA 病毒 YkV1（科）劫持了一种与它无关的 dsRNA 病毒 YnV1（提议的科）的衣壳，而 YkV1 增强了 YnV1 的复制。在这里，我们鉴定了三个 yadokariviruses（YkV3、YkV4a 和 YkV4b）的 dsRNA 病毒伙伴，它们的基因组组织与 YkV1 不同，在亚目水平上与 YnV1 不同。它们的伙伴在两个 YkV4 株和三个 RnMTV1 株（提议的科）之间是相互可互换的，但在涉及 YkV1 或 YkV3 的其他组合之间则不可互换。与 YkV1 不同，YkV4s 降低了 RnMTV1 的积累，并挽救了宿主真菌免受 RnMTV1 诱导的生长受损。YkV3 对其伙伴（RnMBV3，科）或宿主真菌没有明显影响。这些揭示了虽然每个 yadokarivirus 都与一种 dsRNA 病毒具有特定的伙伴关系，但 yadokariviruses 共同与极其多样化的 dsRNA 病毒伙伴关系，并在真菌中表现出三层复杂的互利/拮抗相互作用。
