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Phytopathogenic Fungus Hosts a Plant Virus: a Naturally Occurring Cross-Kingdom Viral Infection

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Phytopathogenic Fungus Hosts a Plant Virus: a Naturally Occurring Cross-Kingdom Viral Infection Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection Ida Bagus Andikaa,b, Shuang Weia, Chunmei Caoc, Lakha Salaipetha,d, Hideki Kondob, and Liying Suna,1 aState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China; bInstitute of Plant Science and Resources, Okayama University, Kurashiki, 710-0046, Japan; cPotato Research Center, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Hohhot, China; and dSchool of Bioresources and Technology, King Mongkut’s University of Technology Thonburi, Bangkok, Thailand Edited by James L. Van Etten, University of Nebraska–Lincoln, Lincoln, NE, and approved October 6, 2017 (received for review August 23, 2017) The transmission of viral infections between plant and fungal hosts usually in the form of micro-RNAs or small interfering RNAs, from has been suspected to occur, based on phylogenetic and other fungi and also other microbes to plants, and vice versa (25–27), findings, but has not been directly observed in nature. Here, we showing that the infecting fungus and plant could exchange their report the discovery of a natural infection of the phytopathogenic genetic materials. Fungal virus (mycovirus) infections widely occur in fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus fungi, including in plant pathogenic fungi. Several mycoviruses have (CMV). The CMV-infected R. solani strain was obtained from a potato been characterized to reduce the virulence of their fungal hosts (28). plant growing in Inner Mongolia Province of China, and CMV infec- Notably, some mycoviruses have relatively close sequence identities to tion was stable when this fungal strain was cultured in the labora- plant viruses (29–32). These observations give rise to speculation tory. CMV was horizontally transmitted through hyphal anastomosis about the transmission of viruses between plant and fungi in the not but not vertically through basidiospores. By inoculation via protoplast so distant past. Nevertheless, no contemporary cross-infection of a transfection with virions, a reference isolate of CMV replicated in plant virus to a phytopathogenic fungal host has been described. R. solani and another phytopathogenic fungus, suggesting that some Rhizoctonia solani Kühn [teleomorph: Thanatephorus cucumeris fungi can serve as alternative hosts to CMV. Importantly, in fungal (Frank) Donk] is a soil-borne plant pathogenic fungus that has a inoculation experiments under laboratory conditions, R. solani could wide host range, including field crops, vegetables, ornamental acquire CMV from an infected plant, as well as transmit the virus to plants, alfalfa, shrubs, and fruit trees, and spreads throughout the an uninfected plant. This study presents evidence of the transfer of a world (33). The disease symptoms may vary depending on the host virus between plant and fungus, and it further expands our under- plants, but the most common symptoms are root or stem rot, stem standing of plant–fungus interactions and the spread of plant viruses. canker, and damping-off of seedlings (34). R. solani is a basidio- mycete fungus that does not produce asexual spores (conidia) and plant virus | fungus | transmission | cross-kingdom exists primarily as vegetative mycelium and/or sclerotia (resting bodies) in nature (35). Several studies have shown that R. solani iruses, as obligate parasites that infect cellular organisms, hosts diverse mycoviruses, including some of the novel viruses that – Vstrictly depend on compatibility with the cellular compo- do not belong to any established virus families or genera (36 41). nents for viral multiplication in the host (1–3). Viruses usually In this study, we discovered an infection of a plant virus, cu- spread from one host to another in the environment but, depending cumber mosaic virus (CMV), in an R. solani strain isolated from potato plants (Solanum tuberosum L.) in the field. CMV is a on the host range and transmission pathways, certain viruses may be + limited to a few or only specific host species, while other viruses positive single-stranded RNA [( )ssRNA] virus belonging to the could infect various organisms belonging to the same biological genus Cucumovirus in the family Bromoviridae (42). CMV is known class/phylum (4). In fact, a number of viruses are known to infect to have the largest host range of any plant virus and is vectored organisms from different taxonomic kingdoms, usually involving an insect as one of the host species. This is exemplified by some plant Significance viruses belonging to the families Bunyaviridae, Rhabdoviridae, Reo- viridae, and genus Tenuivirus that infect and propagate in their in- Virus cross-infection is an important topic in understanding the sect vectors (5, 6), as well as a recent report on a fungal virus that course of virus dissemination and evolution. Viruses may spread infects an insect and uses it as a transmission vector (7). Further- between the same host species or into taxonomically distinct or- more, cross-kingdom infections can be experimentally established ganisms. The occurrences of cross-kingdom viral infection for for some virus–host systems in the laboratory (8–13), suggesting that certain virus groups are suggested by the current virus taxonomic more viruses may cross the kingdom barrier in nature if the ap- data. In particular, several plants and fungal viruses show close MICROBIOLOGY propriate conditions, such as close association/contact and com- phylogenetic relationships, but productive transmission of virus patibility with the potential novel host, are available to facilitate between plant and fungal hosts in nature has not been directly demonstrated. Here, we describe the natural infection of Rhizoc- such an event. Indeed, the occurrence of horizontal virus transfers tonia solani across kingdoms is one of the theories suggested to account for the fungus by a plant virus, cucumber mosaic virus (CMV). We further demonstrate that R. solani canacquireandtransmit presence of many viruses that are taxonomically related but exist in CMV during plant infection. Our findings are evidence of cross- organisms belonging to different taxonomic kingdoms (14–16). kingdom virus transmission from the plant to fungus. Virtually all flowering plants are exposed to attack by pathogenic fungi (17). Necrotrophic fungal pathogens kill host tissue and ab- Author contributions: I.B.A. and L. Sun designed research; I.B.A., S.W., C.C., L. Salaipeth, sorb nutrients from the dead host cells, while biotrophic and hem- and L. Sun performed research; I.B.A., H.K., and L. Sun analyzed data; and I.B.A., H.K., and ibiotrophic fungal plant pathogens colonize the living host, and L. Sun wrote the paper. some commonly develop a specialized organ for uptake of sugars The authors declare no conflict of interest. and other nutrients (18–21). To promote infection and disease This article is a PNAS Direct Submission. development, fungal pathogens secrete or inject effector proteins Published under the PNAS license. that interfere with the host immunity and other physiological pro- 1To whom correspondence should be addressed. Email: [email protected]. – cesses (22 24). Interestingly, numerous studies recently reported This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the occurrences of horizontal transfer of small RNAs, which are 1073/pnas.1714916114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1714916114 PNAS | November 14, 2017 | vol. 114 | no. 46 | 12267–12272 Downloaded by guest on September 29, 2021 mainly by aphid insects in a nonpropagative manner (43, 44). CMV has a tripartite genome composed of RNA1, RNA2, and RNA3, each encapsidated within isometric virus particles (44). Further- more, we were able to demonstrate the transmission of CMV from plant to R. solani, as well as the opposite direction from R. solani to plant under laboratory conditions. We discuss the significance of our findings in the context of understanding the host range ex- pansion, spread, and evolution of plant viruses in nature. Results Discovery of a CMV Isolate Infecting an R. solani Strain. To investigate the occurrence of mycoviruses in R. solani,wescreened29R. solani strains isolated from potato plants grown in several fields in Inner Mongolia Province of China for the presence of double-stranded RNA (dsRNA), which is a molecular marker for RNA virus in- fection. Eleven strains were foundtocontaindsRNAswithdiverse sizes, and seven fungal strains representing each distinct dsRNA pattern were selected for further analysis (SI Appendix,Fig.S1A). Those dsRNA-containing strains showed similar colony morphology (SI Appendix,Fig.S1B). Sequence analysis of the intergenic spacer region (ITS) of rRNA indicated that those R. solani strains belong to the hyphal anastomosis group (AG)-3 (45). The dsRNAs extracted from those seven strains were pooled and then subjected to next-generation sequencing (NGS). BLASTp searches using the contig sequences assembled from the NGS reads revealed a number of mycovirus-related sequences. Surprisingly, in addition to these, three contigs (DN711_c0_gl–DN711_c0_g3) showed high sequence identity with RNA1, 2, 3 of CMV (SI Appendix,TableS1). The CMV sequences identified in R. solani (hereafter referred to as CMV-Rs) show a typical CMV genome organization in which RNA1 encodes 1a (replicase component), RNA2 encodes 2a (replicase component) and 2b (RNA-silencing suppressor),
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