A Botybirnavirus Isolated from Alternaria tenuissima Confers Hypervirulence and Decreased Sensitivity of Its Host Fungus to Difenoconazole

Abstract

Alternaria alternata botybirnavirus 1 (AaBRV1) was isolated from a strain of Alternaria alternata, causing watermelon leaf blight in our previous research. The effect of AaBRV1 on the phenotype of its host fungus, however, was not determined. In the present study, a novel strain of AaBRV1 was identified in A. tenuissima strain TJ-NH-51S-4, the causal agent of cotton Alternaria leaf spot, and designated as AaBRV1-AT1. A mycovirus AaBRV1-AT1-free strain TJ-NH-51S-4-VF was obtained by protoplast regeneration, which eliminated AaBRV1-AT1 from the mycovirus AaBRV1-AT1-infected strain TJ-NH-51S-4. Colony growth rate, spore production, and virulence of strain TJ-NH-51S-4 were greater than they were in TJ-NH-51S-4-VF, while the sensitivity of strain TJ-NH-51S-4 to difenoconazole, as measured by the EC50, was lower. AaBRV1-AT1 was capable of vertical transmission via asexual spores and horizontal transmission from strain TJ-NH-51S-4 to strain XJ-BZ-5-1hyg (another strain of A. tenuissima) through hyphal contact in pairing cultures. A total of 613 differentially expressed genes (DEGs) were identified in a comparative transcriptome analysis between TJ-NH-51S-4 and TJ-NH-51S-4-VF. Relative to strain TJ-NH-51S-4-VF, the number of up-regulated and down-regulated DEGs in strain TJ-NH-51S-4 was 286 and 327, respectively. Notably, the expression level of one DEG-encoding cytochrome P450 sterol 14α-demethylase and four DEGs encoding siderophore iron transporters were significantly up-regulated. To our knowledge, this is the first documentation of hypervirulence and reduced sensitivity to difenoconazole induced by AaBRV1-AT1 infection in A. tenuissima.

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

“…In our previous study, the sensitivity of Alternaria alternata strain SD-BZF-12 infected by Alternaria alternata chrysovirus 1-AT1 to difenoconazole and tebuconazole reduced [80]. Our recent study demonstrated that Alternaria alternata botybirnavirus 1-AT1 decreased the sensitivity of its host A. tenuissima strain TJ-NH-51S-4 to difenoconazole [81]. In the present study, each of the tested 244 Rhizoctonia isolates presented different sensitivity to the three fungicides (flutolanil, thifluzamide, and pencycuron).…”

Characterization of the First Alternavirus Identified in Fusarium avenaceum, the Causal Agent of Potato Dry Rot

“…Sclerotinia sclerotiorum partitivirus 1 (SsPV1/WF-1), however, was readily transmitted horizontally through hyphal contact between different vegetative compatibility groups in S. sclerotiorum [ 45 ]. Alternaria alternata botybirnavirus 1 (AaBRV1) was transmitted horizontally from the AaBRV1-AT1-infected Alternaria tenuissima strain TJ-NH-51S-4 to the AaBRV1-AT1-free strain XJ-BZ-5-1 (another strain of A. tenuissima ) through hyphal contact in paired cultures [ 60 ]. Interspecies transmission of mycoviruses between closely-related species has also been documented.…”

Greetings from virologists to mycologists: A review outlining viruses that live in fungi

“…In C. higginsianum, infection with Colletotrichum higginsianum non-segmented virus (ChNRV1) results in decreased high-temperature stress tolerance and increased pathogenicity, but no changes in osmotic stress tolerance (Olivé & Campo, 2021). In Alternaria tenuissima, infection with the Alternaria alternata botybirnavirus 1 AT strain (AaBRV1-AT1) enhances growth and increases resistance to difenoconazole, leading to increased pathogenicity in plants; however, these phenotypes are attenuated in non-natural host strains (Liang et al, 2022). Previous analyses of Penicillium crustosum infected with Penicillium crustosum chrysovirus 1 (PcCV1), as well as P. digitatum co-infected with Penicillium digitatum polymycovirus 1 (PdPmV1) and Penicillium digitatum Narna-like virus 1 (PdNLV1) showed decreased resistance to prochloraz, suggesting a common effect among Penicillium species (Niu et al, 2018;Wang et al, 2019).…”