Interannual dynamics, diversity and evolution of the virome in Sclerotinia sclerotiorum from a single crop field

Abstract

Mycovirus diversity is generally analyzed from isolates of fungal culture isolates at a single point in time as a snapshot. The stability of mycovirus composition within the same geographical location over time remains unclear. Not knowing how the population fluctuates in the field can be a source of unpredictability in the successful application of virocontrol. To better understand the changes over time, we monitored the interannual dynamics and abundance of mycoviruses infecting Sclerotinia sclerotiorum at a rapeseed-growing field for three years. We found that the virome in S. sclerotiorum harbors unique mycovirus compositions each year. In total, 68 mycoviruses were identified, among which 24 were detected in all three successive years. These 24 mycoviruses can be classified as the members of the core virome in this S. sclerotiorum population, which show persistence and relatively high transmissibility under field conditions. Nearly two-thirds of the mycoviruses have positive-sense, single-stranded RNA genomes and were found consistently across all three years. Moreover, 28 mycoviruses are newly described, including four novel, multi-segmented narnaviruses, and four unique bunyaviruses. Overall, the newly discovered mycoviruses in this study belong to as many as 20 families, into which eight were first identified in S. sclerotiorum, demonstrating evolutionarily diverse viromes. Our findings not only shed light on the annual variation of mycovirus diversity, but also provide important virus evolutionary clues.

Nine viruses from eight lineages exhibiting new evolutionary modes that co-infect a hypovirulent phytopathogenic fungus

“…However, jingmenviruses are phylogenetically clustered in a separate group that is distinctive from the genera of Flavivirus [49]. Recently, the novel narna-like viruses and virga-like mycovirus with segmented genomes have been found in Aspergillus species, S. sclerotiorum, and endomycorrhizal fungi, suggesting that mycovirus genome segmentation are more complex [5][6][7]. From PLOS PATHOGENS our present study, SsDFV3 has a tripartite genome, and was phylogenetically positioned into previously characterized unsegmented deltaflexiviruses group based on conserved RdRp domain.…”

“…Three RNA segments (SsDFV3S1-S3) were recently detected in a previously characterized S. sclerotiorum strain SCH941 and its single protoplast isolate (S2B Fig). Moreover, seven of hundred S. sclerotiorum isolates isolated from a single crop field were also infected with this virus with the three fragments (S2C and S2D Fig) [5], which suggested that SsDFV3 could be widespread in S.…”

“…S. sclerotiorum harbors rich diverse mycoviruses including dsRNA, ssRNA, and DNA mycoviruses, of which ssRNA mycoviruses are dominant [25,26]. Some of those identified mycoviruses were positioned in a critical evolutionary node, contributing to knowledge on viral evolutionary history [5,[27][28][29]. Some mycoviruses associated with hypovirulence have been demonstrated to be resources for Sclerotinia disease management [30,31].…”

“…org/ictv-reports/ictv_online_report/). Recently, an increasing number of mycoviruses representing novel viruses with unique genomes or evolutionary positions, but broadly referred to as unclassified, have been discovered and characterized [2][3][4][5][6][7][8]. The discovery of more mycoviruses will expand our knowledge regarding virus diversity, classification, and evolution.…”

Direct Metatranscriptomic Survey of the Sunflower Microbiome and Virome

“…A study to include multiple sites can be advantageous, especially if the disease in question is widespread and the pathogen is cosmopolitan. It would be interesting to monitor whether there is a correlation between the mycoviral read counts and the disease severities and yield intra-annually [ 30 ], since yield enhancement has been reported in a mycovirus that presents in fields of brassica spp. [ 16 ].…”