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Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Genomics, Genetics and Molecular Biology".

Deadline for manuscript submissions: closed (31 May 2023) | Viewed by 19399

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Prof. Dr. Robert H. A. Coutts

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Department of Clinical, Pharmaceutical and Biological Science, University of Hertfordshire, Hatfield AL10 9AB, UK
Interests: mycoviruses; sequencing; sequence analysis; gene function
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Prof. Dr. Ioly Kotta-Loizou

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1. Department of Life Sciences, Faculty of Natural Sciences, Imperial College London, London, UK
2. Department of Clinical, Pharmaceutical and Biological Science, University of Hertfordshire, Hatfield AL10 9AB, UK
Interests: mycoviruses; mycovirus infection; mycovirus population studies; mycovirus evolution; mycovirus–fungus interactions; bacterial gene expression; RNA damage and repair; oxidative stress; antibiotics resistance; CRISPR-Cas
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

We are honoured to act as Guest Editors for a Special Issue dedicated to mycoviruses, to be published in Journal of Fungi. Mycovirus infection may manifest itself via phenotypic effects on the fungal host, influencing among other traits morphology, growth, sporulation, metabolism, toxin production, pathogenicity, virulence, susceptibility to antifungals and interactions with biotic and abiotic factors. The molecular mechanisms underpinning these phenotypes are not always well characterised. Additionally, we believe that the full range of potential mycovirus-mediated phenotypes is yet to be revealed. We would like to invite you to contribute to this Special Issue by submitting your recent work for publication, as an original research article, a short communication or a review. Investigations on mycovirus-mediated phenotypes, mycovirus–fungal host interactions and the role of RNA silencing in infection are most welcome. We are looking forward to hearing from you.

Dr. Robert H. A. Coutts
Dr. Ioly Kotta-Loizou
Guest Editors

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Keywords

mycoviruses
mycovirus infection
mycovirus-mediated phenotypes
mycovirus–fungal host interactions
mycovirus RNA silencing

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Related Special Issue

Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction, 2nd Edition in Journal of Fungi

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Research

15 pages, 4661 KiB

Open AccessArticle

The Effects of Mycovirus BmPV36 on the Cell Structure and Transcription of Bipolaris maydis

by Yajiao Wang, Qiusheng Li, Yuxing Wu, Sen Han, Ying Xiao and Lingxiao Kong

J. Fungi 2024, 10(2), 133; https://doi.org/10.3390/jof10020133 - 6 Feb 2024

Viewed by 1318

Abstract

Bipolaris maydis partitivirus 36 (BmPV36) is a mycovirus that can significantly reduce the virulence of the host Bipolaris maydis, but its hypovirulence mechanism is not clear. To investigate the response of B. maydis to BmPV36, the effects of BmPV36 on host cell structure and gene expression were studied via transmission electron microscopy and transcriptome sequencing using BmPV36-carrying and virus-free mycelium on the second and fifth culture. The results of transmission electron microscopy showed that the cell wall microfibrils of B. maydis were shortened, the cell membrane was broken, and membrane-bound vesicles and vacuoles appeared in the cells after carrying BmPV36. Transcriptome sequencing results showed that after carrying BmPV36, B. maydis membrane-related genes were significantly up-regulated, but membrane transport-related genes were significantly down-regulated. Genes related to carbohydrate macromolecule polysaccharide metabolic and catabolic processes were significantly down-regulated, as were genes related to the synthesis of toxins and cell wall degrading enzymes. Therefore, we speculated that BmPV36 reduces the virulence of B. maydis by destroying the host’s cell structure, inhibiting the synthesis of toxins and cell wall degrading enzymes, and reducing cell metabolism. Gaining insights into the hypovirulence mechanism of mycoviruses will provide environmentally friendly strategies for the control of fungal diseases. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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17 pages, 2219 KiB

Open AccessArticle

AfuPmV-1-Infected Aspergillus fumigatus Is More Susceptible to Stress Than Virus-Free Fungus

by Gabriele Sass, Marife Martinez, Ioly Kotta-Loizou and David Stevens

J. Fungi 2023, 9(7), 750; https://doi.org/10.3390/jof9070750 - 15 Jul 2023

Cited by 2 | Viewed by 1293

Abstract

Infection with Aspergillus fumigatus polymycovirus 1 (AfuPmV-1) affects Aspergillus fumigatus Af293’s growth in vitro, iron metabolism, resistance in intermicrobial competition with Pseudomonas aeruginosa, resistance to osmotic stress, and resistance to the chitin synthase inhibitor nikkomycin Z. Here, we show that response to high temperature, Congo Red-induced stress, and hydrogen peroxide are also dependent on the viral infection status of A. fumigatus. AfuPmV-1- infected Af293 was more susceptible than virus-free Af293 to growth inhibition by high temperature, hydrogen peroxide, Congo Red exposure, and nutrient restriction. Increased resistance of virus-free fungus was observed when cultures were started from conidia but, in the case of high temperature and hydrogen peroxide, not when cultures were started from hyphae. This indicates that the virus impairs the stress response during the growth phase of germination of conidia and development into hyphae. In conclusion, our work indicates that AfuPmV-1 infection in A. fumigatus impairs host responses to stress, as shown by exposure to high temperature, oxidative stress such as hydrogen peroxide, and some cell wall stresses, as shown by exposure to Congo Red (in agreement with our previous observations using nikkomycin Z) and nutrient restriction. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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23 pages, 8109 KiB

Open AccessArticle

Anastomosis Groups and Mycovirome of Rhizoctonia Isolates Causing Sugar Beet Root and Crown Rot and Their Sensitivity to Flutolanil, Thifluzamide, and Pencycuron

by Can Zhao, Siwei Li, Zhihao Ma, Wenjun Wang, Lihong Gao, Chenggui Han, Anpei Yang and Xuehong Wu

J. Fungi 2023, 9(5), 545; https://doi.org/10.3390/jof9050545 - 9 May 2023

Cited by 6 | Viewed by 1770

Abstract

Anastomosis groups (AGs) or subgroups of 244 Rhizoctonia isolates recovered from sugar beet roots with symptoms of root and crown rot were characterized to be AG-A, AG-K, AG-2-2IIIB, AG-2-2IV, AG-3 PT, AG-4HGI, AG-4HGII, and AG-4HGIII, with AG-4HGI (108 isolates, 44.26%) and AG-2-2IIIB (107 isolates, 43.85%) being predominate. Four unclassified mycoviruses and one hundred and one putative mycoviruses belonging to six families, namely Mitoviridae (60.00%), Narnaviridae (18.10%), Partitiviridae (7.62%), Benyviridae (4.76%), Hypoviridae (3.81%), and Botourmiaviridae (1.90%), were found to be present in these 244 Rhizoctonia isolates, most of which (88.57%) contained positive single-stranded RNA genome. The 244 Rhizoctonia isolates were all sensitive to flutolanil and thifluzamide, with average median effective concentration (EC₅₀) value of 0.3199 ± 0.0149 μg·mL⁻¹ and 0.1081 ± 0.0044 μg·mL⁻¹, respectively. Among the 244 isolates, except for 20 Rhizoctonia isolates (seven isolates of AG-A and AG-K, one isolate of AG-4HGI, and 12 isolates of AG-4HGII), 117 isolates of AG-2-2IIIB, AG-2-2IV, AG-3 PT, and AG-4HGIII, 107 isolates of AG-4HGI, and six isolates of AG-4HGII were sensitive to pencycuron, with average EC₅₀ value of 0.0339 ± 0.0012 μg·mL⁻¹. Correlation index (ρ) of cross-resistance level between flutolanil and thifluzamide, flutolanil and pencycuron, and thifluzamide and pencycuron was 0.398, 0.315, and 0.125, respectively. This is the first detailed study on AG identification, mycovirome analysis, and sensitivity to flutolanil, thifluzamide, and pencycuron of Rhizoctonia isolates associated with sugar beet root and crown rot. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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17 pages, 383 KiB

Open AccessArticle

Mycoviruses in Fungi: Carcinogenesis of Fungal Agents May Not Always Be Mycotoxin Related

by Cameron K. Tebbi

J. Fungi 2023, 9(3), 368; https://doi.org/10.3390/jof9030368 - 17 Mar 2023

Cited by 8 | Viewed by 2810

Abstract

Certain viruses have been found to induce diverse biological pathways to carcinogenesis, evidenced by the presence of viral gene products in some tumors. Despite the fact that many fungal agents contain mycoviruses, until recently, their possible direct effects on human health, including carcinogenesis and leukemogenesis, had not been explored. In this regard, most studies of fungal agents have rightly concentrated on their mycotoxin formation and effects. Recently, the direct role of yeasts and fungi in the etiology of cancers, including leukemia, have been investigated. While greater attention has been placed on the carcinogenic effects of Candida, the role of filamentous fungi in carcinogenesis has also been explored. Recent findings from studies using the enzyme-linked immunosorbent assay (ELISA) technique indicate that the plasma of patients with acute lymphoblastic leukemia (ALL) uniformly contains antibodies for a certain mycovirus-containing Aspergillus flavus, while controls are negative. The exposure of mononuclear leukocytes from patients with ALL in full remission, and long-term survivors, to the product of this organism was reported to result in the re-development of typical genetics and cell surface phenotypes characteristic of active ALL. Mycoviruses are known to be able to significantly alter the biological characteristics and functions of their host. The possible carcinogenic and leukemogenic role of mycoviruses, with and without their host, needs to be further investigated. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

19 pages, 3153 KiB

Open AccessArticle

Diversity of Mycoviruses Present in Strains of Binucleate Rhizoctonia and Multinucleate Rhizoctonia, Causal Agents for Potato Stem Canker or Black Scurf

by Yuting Li, Naibo Yang, Tongyu Mu, Xuehong Wu and Can Zhao

J. Fungi 2023, 9(2), 214; https://doi.org/10.3390/jof9020214 - 6 Feb 2023

Cited by 6 | Viewed by 1573

Abstract

In this study, the diversity of putative mycoviruses present in 66 strains of binucleate Rhizoctonia (BNR, including anastomosis group (AG)-A, AG-Fa, AG-K, and AG-W) and 192 strains of multinucleate Rhizoctonia (MNR, including AG-1-IA, AG-2-1, AG-3 PT, AG-4HGI, AG-4HGII, AG-4HGIII, and AG-5), which are the causal agents of potato stem canker or black scurf, was studied using metatranscriptome sequencing. The number of contigs related to mycoviruses identified from BNR and MNR was 173 and 485, respectively. On average, each strain of BNR accommodated 2.62 putative mycoviruses, while each strain of MNR accommodated 2.53 putative mycoviruses. Putative mycoviruses detected in both BNR and MNR contained positive single-stranded RNA (+ssRNA), double-stranded RNA (dsRNA), and negative single-stranded RNA (-ssRNA) genomes, with +ssRNA genome being the prevalent nucleic acid type (82.08% in BNR and 75.46% in MNR). Except for 3 unclassified, 170 putative mycoviruses found in BNR belonged to 13 families; excluding 33 unclassified, 452 putative mycoviruses found in MNR belonged to 19 families. Through genome organization, multiple alignments, and phylogenetic analyses, 4 new parititviruses, 39 novel mitoviruses, and 4 new hypoviruses with nearly whole genome were detected in the 258 strains of BNR and MNR. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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12 pages, 2117 KiB

Open AccessArticle

A Novel Gammapartitivirus That Causes Changes in Fungal Development and Multi-Stress Tolerance to Important Medicinal Fungus Cordyceps chanhua

by Qiuyan Zhu, Najie Shi, Ping Wang, Yuxiang Zhang, Fan Peng, Guogen Yang and Bo Huang

J. Fungi 2022, 8(12), 1309; https://doi.org/10.3390/jof8121309 - 16 Dec 2022

Cited by 5 | Viewed by 1517

Abstract

Cicada flower, scientifically named Cordyceps chanhua, is an important and well-known Chinese cordycipitoid medicinal mushroom. Although most mycoviruses seem to induce latent infections, some mycoviruses cause host effects. However, the effects of mycovirus on the fungal development and stress tolerance of C. chanhua remain unknown. In this study, we report a novel mycovirus designated Cordyceps chanhua partitivirus 1 (CchPV1) from C. chanhua isolate RCEF5997. The CchPV1 genome comprises dsRNA 1 and dsRNA 2, 1784 and 1563 bp in length, respectively. Phylogenetic analysis using the aa sequences of RdRp revealed that CchPV1 grouped with members of the genus Gammapartitivirus in the family Partitiviridae. We further co-cultivated on PDA donor strain RCEF5997 and recipient C. chanhua strain RCEF5833 (Vf) for 7 days, and we successfully obtained an isogenic line of strain RCEF5833 with CchPV1 (Vi) through single-spore isolation, along with ISSR marker and dsRNA extraction. The biological comparison revealed that CchPV1 infection slows the growth rate of the host, but increases the conidiation and formation of fruiting bodies of the host. Furthermore, the assessment of fungal tolerance demonstrated that CchPV1 weakens the multi-stress tolerance of the host. Thus, CchPV1 infection cause changes in fungal development and multi-stress tolerance of the host C. chanhua. The findings of this study elucidate the effects of gammapartitivirus on host entomogenous fungi and provide a novel strategy for producing high-quality fruiting bodies of C. chanhua. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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12 pages, 3296 KiB

Open AccessArticle

Interference of Small RNAs in Fusarium graminearum through FgGMTV1 Infection

by Shuangchao Wang, Shaojian Ruan, Mingming Zhang, Jianhua Nie, Clement Nzabanita and Lihua Guo

J. Fungi 2022, 8(12), 1237; https://doi.org/10.3390/jof8121237 - 22 Nov 2022

Cited by 3 | Viewed by 1554

Abstract

Small RNA (sRNA) plays a central role in RNA silencing in fungi. The genome of Fusarium graminearum gemytripvirus 1 (FgGMTV1) is comprised of three DNA segments: DNA-A, DNA-B, and DNA-C. DNA-A and DNA-B are associated with fungal growth and virulence reduction. To elucidate the role of RNA silencing during the interactions of fungi and viruses, the sRNA profiles of F. graminearum in association with FgGMTV1 were established, using an FgGMTV1-free library (S-S), a library for infection with the DNA-A and DNA-B segments (S-AB), and a library for infection with the DNA-A, DNA-B, and DNA-C segments (S-ABC). A large amount of virus-derived sRNA (vsiRNA) was detected in the S-AB and S-ABC libraries, accounting for 9.9% and 13.8% of the total sRNA, respectively, indicating that FgGMTV1 triggers host RNA silencing. The total numbers of sRNA reads differed among the three libraries, suggesting that FgGMTV1 infection interferes with host RNA silencing. In addition, the relative proportions of the different sRNA lengths were altered in the S-AB and S-ABC libraries. The genome distribution patterns of the mapping of vsiRNA to DNA-A and DNA-B in the S-AB and S-ABC libraries were also different. These results suggest the influence of DNA-C on host RNA silencing. Transcripts targeted by vsiRNAs were enriched in pathways that included flavin adenine dinucleotide binding, protein folding, and filamentous growth. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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11 pages, 1574 KiB

Open AccessArticle

Fungal Virus, FgHV1-Encoded p20 Suppresses RNA Silencing through Single-Strand Small RNA Binding

by Shuangchao Wang, Jingze Zhang, Clement Nzabanita, Mingming Zhang, Jianhua Nie and Lihua Guo

J. Fungi 2022, 8(11), 1171; https://doi.org/10.3390/jof8111171 - 7 Nov 2022

Cited by 6 | Viewed by 1747

Abstract

Fungal viruses are widespread in fungi infecting plants, insects and animals. High-throughput sequencing has rapidly led to the discovery of fungal viruses. However, the interactive exploration between fungi and viruses is relatively limited. RNA silencing is the fundamental antivirus pathway in fungi. Fusarium graminearum small RNA (sRNA) pattern was regulated by Fusarium graminearum hypovirus 1 (FgHV1) infection, indicating the activation of RNA silencing in virus defense. In this study, we focused on the function of an uncharacterized protein sized at 20 kD (p20) encoded by FgHV1. In the agro-infiltration assay, p20 was identified as a novel fungal RNA silencing suppressor. p20 can block systemic RNA silencing signals besides local RNA silencing suppression. We further elucidated the RNA silencing suppression mechanism of p20. The single-strand sRNA, instead of double-strand sRNA, can be incorporated by p20 in electrophoretic mobility shift assay. p20 binds sRNA originating from virus and non-virus sources in a non-sequence-specific manner. In addition, The F. graminearum 22 and 23-nt sRNA abundance and pathways related to RNA processing and redox regulation were regulated by p20. Our study revealed the first fungal virus-encoded RNA silencing suppressor with sRNA binding capability. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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14 pages, 3469 KiB

Open AccessArticle

Mycoviromic Analysis Unveils Complex Virus Composition in a Hypovirulent Strain of Sclerotinia sclerotiorum

by Yong Wang, Zhiyong Xu, Du Hai, Huang Huang, Jiasen Cheng, Yanping Fu, Yang Lin, Daohong Jiang and Jiatao Xie

J. Fungi 2022, 8(7), 649; https://doi.org/10.3390/jof8070649 - 21 Jun 2022

Cited by 5 | Viewed by 1967

Abstract

Mycoviruses are ubiquitous in pathogenic fungi including Sclerotinia sclerotiorum. Using RNA sequencing, more mycoviruses have been identified in individual strains, which were previously reported to be infected by a single mycovirus. A hypovirulent strain of S. sclerotiorum, HC025, was previously thought to harbor a single mitovirus, Sclerotinia sclerotiorum mitovirus 1 (SsMV1), based on the analysis of the conventional dsRNA extraction method. We found HC025 to be co-infected by five mycoviruses. In addition to SsMV1, four mycoviruses were identified: Sclerotinia sclerotiorum narnavirus 4 (SsNV4), Sclerotinia sclerotiorum negative-stranded RNA virus 1 (SsNSRV1), Sclerotinia sclerotiorum ourmia-like virus 14 (SsOLV14), and SsOLV22. Three mycoviruses including SsNV4, SsNSRV1, and SsOLV14 share high replicase identities (more than 95%) with the previously reported corresponding mycoviruses, and SsOLV22 shows lower identity to the known viruses. The complete genome of SsOLV22 is 3987 nt long and contains a single ORF-encoded RdRp, which shares 24.84% identity with the RNA-dependent RNA polymerase (RdRp) of Hubei narna-like virus 10 (query coverage: 26%; e-value: 8 × 10⁻¹⁹). The phylogenetic tree of RdRp suggests that SsOLV22 is a new member within the family Botourmiaviridae. All of the mycoviruses except for SsNSRV1 could horizontally co-transfer from HC025 to the virulent strain Ep-1PNA367 with hypovirulent phenotypes, and converted a later strain into a hypovirulent strain. In summary, we molecularly characterized the hypovirulent strain HC025 and identified five RNA mycoviruses including a new member within Botourmiaviridae. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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24 pages, 3910 KiB

Open AccessArticle

Adaptive Response of Saccharomyces Hosts to Totiviridae L-A dsRNA Viruses Is Achieved through Intrinsically Balanced Action of Targeted Transcription Factors

by Bazilė Ravoitytė, Juliana Lukša, Ralf Erik Wellinger, Saulius Serva and Elena Servienė

J. Fungi 2022, 8(4), 381; https://doi.org/10.3390/jof8040381 - 9 Apr 2022

Cited by 3 | Viewed by 2536

Abstract

Totiviridae L-A virus is a widespread yeast dsRNA virus. The persistence of the L-A virus alone appears to be symptomless, but the concomitant presence of a satellite M virus provides a killer trait for the host cell. The presence of L-A dsRNA is common in laboratory, industrial, and wild yeasts, but little is known about the impact of the L-A virus on the host’s gene expression. In this work, based on high-throughput RNA sequencing data analysis, the impact of the L-A virus on whole-genome expression in three different Saccharomyces paradoxus and S. cerevisiae host strains was analyzed. In the presence of the L-A virus, moderate alterations in gene expression were detected, with the least impact on respiration-deficient cells. Remarkably, the transcriptional adaptation of essential genes was limited to genes involved in ribosome biogenesis. Transcriptional responses to L-A maintenance were, nevertheless, similar to those induced upon stress or nutrient availability. Based on these data, we further dissected yeast transcriptional regulators that, in turn, modulate the cellular L-A dsRNA levels. Our findings point to totivirus-driven fine-tuning of the transcriptional landscape in yeasts and uncover signaling pathways employed by dsRNA viruses to establish the stable, yet allegedly profitless, viral infection of fungi. Full article

(This article belongs to the Special Issue Mycoviruses: Emerging Investigations on Virus-Fungal Host Interaction)

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