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

item DENG, YUE - Huazhong Agricultural University
item ZHOU, KANG - Huazhong Agricultural University
item WU, MINGDE - Huazhong Agricultural University
item ZHANG, JING - Huazhong Agricultural University
item YANG, LONG - Huazhong Agricultural University
item Chen, Weidong
item LI, GUOQING - Huazhong Agricultural University

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/15/2022
Publication Date: 8/31/2022
Citation: Deng, Y., Zhou, K., Wu, M., Zhang, J., Yang, L., Chen, W., Li, G. 2022. Viral cross-class transmission results in disease of a phytopathogenic fungus. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 16:2763-2774.

Interpretive Summary: Fungal viruses (mycoviruses) have been studied in search for biocontrol agents for fungal diseases. Thus, only those mycoviruses that manifest adverse effect like decreased virulence (hypovirulence) on their host have received considerable attention. However, many mycoviruses are benign to their host fungi and are asymptomatic. This research showed that an asymptomatic virus in one fungal species can cause severe disease on another fungal species when passed through inter-species transmission. A newly discovered asymptomatic virus in a Brassica pathogen Leptosphaeria biglobosa was transmitted to another fungus, Botrytis cinerea, which can infect many plant species, and resulted in behavior changes like diminished virulence on the new fungal host. Other evidence showed that such interspecies transmission can occur frequently in nature. This study provides new insights for using asymptomatic and seemingly benign mycoviruses as biocontrol agents of their newly invaded fungal pathogens.

Technical Abstract: 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 ramifications. 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. LbBV1 has two dsRNA segments, namely dsRNA 1 (6,190 bp) and dsRNA 2 (5,900 bp), possessing spherical virions of about 37 nm in diameter. The cDNA sequences of dsRNA 1 and dsRNA 2 show high sequence identity of 78% and 81% to those of Alternaria botybirnavirus 1 (ABV1) at nucleotide level, respectively, and phylogenetic analysis showed that LbBV1 was also closely related to Botrytis cinerea botybirnavirus 1 (BcBV1), indicating LbBV1 belonged to the genus Botybirnavirus. LbBV1 infection in L. biglobosa was asymptomatic, as no significant differences in colony morphology, 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 provides new insights for using asymptomatic mycoviruses as biocontrol agents of their newly invaded fungal pathogens.