Defective RNA of a Novel Mycovirus with High Transmissibility Detrimental to Biocontrol Properties of Trichoderma spp.

You, Jiaqi; Zhou, Kang; Liu, Xiaolin; Wu, Mingde; Yang, Long; Zhang, Jing; Chen, Weidong; Li, Guoqing

doi:10.3390/microorganisms7110507

Cited by 22 publications

(26 citation statements)

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“…Furthermore, mycoviruses can participate in some complex mutualistic symbiosis, enhancing the survival of host fungi and plants under extreme conditions [ 24 ]. In addition, mycoviruses may also be involved in the interaction between biocontrol agents and target phytopathogenic fungi [ 25 ]. Although mycoviruses having biological effects are frequently observed and widely investigated, most mycoviral infections are asymptomatic or cryptic, and this may be related to their lifestyle.…”

Section: Introductionmentioning

confidence: 99%

Viral cross-class transmission results in disease of a phytopathogenic fungus

Deng

Zhou

et al. 2022

The ISME Journal

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Interspecies transmission of viruses is a well-known phenomenon in animals and plants whether via contacts or vectors. In fungi, interspecies transmission between distantly related fungi is often suspected but rarely experimentally documented and may have practical implications. A newly described double-strand RNA (dsRNA) virus found asymptomatic in the phytopathogenic fungus Leptosphaeria biglobosa of cruciferous crops was successfully transmitted to an evolutionarily distant, broad-host range pathogen Botrytis cinerea. Leptosphaeria biglobosa botybirnavirus 1 (LbBV1) was characterized in L. biglobosa strain GZJS-19. Its infection in L. biglobosa was asymptomatic, as no significant differences in radial mycelial growth and pathogenicity were observed between LbBV1-infected and LbBV1-free strains. However, cross-species transmission of LbBV1 from L. biglobosa to infection in B. cinerea resulted in the hypovirulence of the recipient B. cinerea strain t-459-V. The cross-species transmission was succeeded only by inoculation of mixed spores of L. biglobosa and B. cinerea on PDA or on stems of oilseed rape with the efficiency of 4.6% and 18.8%, respectively. To investigate viral cross-species transmission between L. biglobosa and B. cinerea in nature, RNA sequencing was carried out on L. biglobosa and B. cinerea isolates obtained from Brassica samples co-infected by these two pathogens and showed that at least two mycoviruses were detected in both fungal groups. These results indicate that cross-species transmission of mycoviruses may occur frequently in nature and result in the phenotypical changes of newly invaded phytopathogenic fungi. This study also provides new insights for using asymptomatic mycoviruses as biocontrol agent.

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Section: Introductionmentioning

confidence: 99%

Viral cross-class transmission results in disease of a phytopathogenic fungus

Deng

Zhou

et al. 2022

The ISME Journal

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“…The inducible genome deletions of MyRV1 dsRNA S4 and S10 are related to changes in vertical transmission efficiency and host colony morphology, but not to viral replication (Sun and Suzuki, 2008;Eusebio-Cope et al, 2010;Kanematsu et al, 2014). Several other findings of RNA genome deletions in the hypoviruses also demonstrated their encoded in-frame fusion proteins affecting host growth negatively (Hillman et al, 2000;Xie et al, 2011;You et al, 2019).…”

Section: Discussionmentioning

confidence: 92%

Unique Terminal Regions and Specific Deletions of the Segmented Double-Stranded RNA Genome of Alternaria Alternata Virus 1, in the Proposed Family Alternaviridae

Aoki

Takeshita

et al. 2021

Front. Microbiol.

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Alternaria alternata virus 1 (AaV1) has been identified in the saprophytic fungus Alternaria alternata strain EGS 35–193. AaV1 has four genomic double-stranded (ds)RNA segments (dsRNA1–4) packaged in isometric particles. The 3' end of each coding strand is polyadenylated (36–50nt), but the presence of a cap structure at each 5' end has not previously been investigated. Here, we have characterized the AaV1 genome and found that it has unique features among the mycoviruses. We confirmed the existence of cap structures on the 5' ends of the AaV1 genomic dsRNAs using RNA dot blots with anti-cap antibodies and the oligo-capping method. Polyclonal antibodies against purified AaV1 particles specifically bound to an 82kDa protein, suggesting that this protein is the major capsid component. Subsequent Edman degradation indicated that the AaV1 dsRNA3 segment encodes the major coat protein. Two kinds of defective AaV1 dsRNA2, which is 2,794bp (844 aa) in length when intact, appeared in EGS 35–193 during subculturing, as confirmed by RT-PCR and northern hybridization. Sequence analysis revealed that one of the two defective dsRNA2s contained a 231bp deletion, while the other carried both the 231bp deletion and an additional 465bp deletion in the open reading frame. Both deletions occurred in-frame, resulting in predicted proteins of 767 aa and 612 aa. The fungal isolates carrying virions with the defective dsRNA2s showed impaired growth and abnormal pigmentation. To our best knowledge, AaV1 is the first dsRNA virus to be identified with both 5' cap and 3'poly(A) structures on its genomic segments, as well as the specific deletions of dsRNA2.

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“…It effectively controlled tomato gray mold disease (caused by B. cinerea ) and watermelon fusarium wilt (caused by Fusarium oxysporum ) and exhibited plant-growth-promoting ability in tomato and watermelon. In our previous study, we reported a mycovirus from T. harzianum (ThHV1) and its defective RNA (ThHV1-S), and demonstrated that ThHV1-S decreased mycoparasitism and increased the antifungal activity of the culture filtrate (CF) of the host [ 19 ]. A derivative strain 51-13 was obtained by transmission of ThHV-1 and ThHV1-S into the wild-type strain of T. koningiopsis T-51.…”

Section: Introductionmentioning

confidence: 99%

“…A derivative strain 51-13 was obtained by transmission of ThHV-1 and ThHV1-S into the wild-type strain of T. koningiopsis T-51. The derivative strain showed increased antifungal activity against B. cinerea [ 19 ]. In this study, the antifungal activity of CF and VOCs produced by strain 51-13 were evaluated against several pathogenic fungi of plants and the mechanism underlying the effect of ThHV1-S on the host’s antifungal activity was explored.…”

Section: Introductionmentioning

confidence: 99%

The Effect of Trichoderma harzianum Hypovirus 1 (ThHV1) and Its Defective RNA ThHV1-S on the Antifungal Activity and Metabolome of Trichoderma koningiopsis T-51

You

Yang

et al. 2023

JoF

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Mycoviruses widely exist in filamentous fungi and sometimes cause phenotypic changes in hosts. Trichoderma harzianum hypovirus 1 (ThHV1) and its defective RNA ThHV1-S were found in T. harzianum and exhibited high transmissibility. In our previous study, ThHV1 and ThHV1-S were transferred to an excellent biological control agent T. koningiopsis T-51 to form a derivative strain 51-13. In this study, we assessed the metabolic changes in strain 51-13 and antifungal activity of its culture filtrate (CF) and volatile organic compounds (VOCs). The antifungal activity of CF and VOCs of T-51 and 51-13 was different. Compared with the CF of T-51, that of 51-13 exhibited high inhibitory activity against B. cinerea, Sclerotinia sclerotiorum, and Stagonosporopsis cucurbitacearum but low inhibitory activity against Leptosphaeria biglobosa and Villosiclava virens. The VOCs of 51-13 exhibited high inhibitory activity against F. oxysporum but low inhibitory activity against B. cinerea. The transcriptomes of T-51 and 51-13 were compared; 5531 differentially expressed genes (DEGs) were identified in 51-13 with 2904 up- and 2627 downregulated genes. In KEGG enrichment analysis, 1127 DEGs related to metabolic pathways (57.53%) and 396 DEGs related to biosynthesis of secondary metabolites (20.21%) were clearly enriched. From the CF of T-51 and 51-13, 134 differential secondary metabolites (DSMs) were detected between T-51 and 51-13 with 39 up- and 95 downregulated metabolites. From these, 13 upregulated metabolites were selected to test their antifungal activity against B. cinerea. Among them, indole-3-lactic acid and p-coumaric acid methyl ester (MeCA) exhibited strong antifungal activity. The IC50 of MeCA was 657.35 μM and four genes possibly related to the synthesis of MeCA exhibited higher expression in 51-13 than in T-51. This study revealed the mechanism underlying the increase in antifungal activity of T-51 because of the mycovirus and provided novel insights in fungal engineering to obtain bioactive metabolites via mycoviruses.

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Defective RNA of a Novel Mycovirus with High Transmissibility Detrimental to Biocontrol Properties of Trichoderma spp.

Cited by 22 publications

References 50 publications

Viral cross-class transmission results in disease of a phytopathogenic fungus

Viral cross-class transmission results in disease of a phytopathogenic fungus

Unique Terminal Regions and Specific Deletions of the Segmented Double-Stranded RNA Genome of Alternaria Alternata Virus 1, in the Proposed Family Alternaviridae

The Effect of Trichoderma harzianum Hypovirus 1 (ThHV1) and Its Defective RNA ThHV1-S on the Antifungal Activity and Metabolome of Trichoderma koningiopsis T-51

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