A mycovirus modulates the endophytic and pathogenic traits of a plant associated fungus

Abstract

Fungi are generally thought to live in host plants with a single lifestyle, being parasitism, commensalism, or mutualism. The former, known as phytopathogenic fungi, cause various plant diseases that result in significant losses every year; while the latter, such as endophytic fungi, can confer fitness to the host plants. It is unclear whether biological factors can modulate the parasitic and mutualistic traits of a fungus. In this study, we isolated and characterized a mycovirus from an endophytic strain of the fungus Pestalotiopsis theae, a pathogen of tea (Camellia sinensis). Based on molecular analysis, we tentatively designated the mycovirus as Pestalotiopsis theae chrysovirus-1 (PtCV1), a novel member of the family Chrysoviridae, genus Alphachrysovirus. PtCV1 has four double-stranded (ds) RNAs as its genome, ranging from 0.9 to 3.4 kbp in size, encapsidated in isometric particles. PtCV1 significantly reduced the growth rates of its host fungus in vitro (ANOVA; P-value < 0.001) and abolished its virulence in planta (ANOVA; P-value < 0.001), converting its host fungus to a non-pathogenic endophyte on tea leaves, while PtCV1-free isolates were highly virulent. Moreover, the presence of PtCV1 conferred high resistance to the host plants against the virulent P. theae strains. Here we report a mycovirus that modulates endophytic and phytopathogenic fungal traits and provides an alternative approach to biological control of plant diseases caused by fungi.

Characterization of a Novel Mitovirus Infecting Melanconiella theae Isolated From Tea Plants

“…MtMV1 is efficiently transmitted through all conidia of strain WJB-5 (100 conidium-generated colonies were checked) in agreement with those mitoviruses detected in a high percentage of the individual spore isolates, as exemplified by Fusarium circinatum mitovirus 1 (FcMV1) and Fusarium circinatum mitovirus 2-2 (FcMV2-2) that showed vertical transmission rates between 60 and 100% depending on the fungal isolate ( Romeralo et al, 2018 ), however, both Fusarium verticillioides mitovirus 1 (FvMV1) and Fusarium andiyazi mitovirus 1 strain 162 (FaMV1-162) showed 100% vertical transmission rate through fungal conidia ( Jacquat et al, 2020 ). In contrast, some mycoviruses are less efficiently transmitted through conidia, as exemplified by Colletotrichum camelliae filamentous virus 1 (CcFV-1) and Pestalotiopsis theae chrysovirus-1 (PtCV1) ( Jia et al, 2017 ; Zhou et al, 2021 ). Generally, the efficient transmission of mitoviruses through asexual spores and sclerotia has hindered to understand mitovirus biology, partly due to lacking mitovirus-free sub-isolates used for infection, although a protoplast fusion-based protocol for horizontal transmission of a mitovirus has been developed ( Shahi et al, 2019 ).…”

The Mycovirome in a Worldwide Collection of the Brown Rot Fungus Monilinia fructicola

“…Moreover, mycoviruses might play a role in the adaptation of fungi to certain ecological niches. For instance, Pestalotiopsis theae chrysovirus-1 (PtCV1) modulates endophytic and phytopathogenic traits of Pestalotiopsis theae [ 36 ]; Curvularia thermal tolerance virus (CThTV), in a three-way symbiosis, confers heat tolerance to both the endophyte Curvularia protuberata and its host plant, a tropical panic grass, and allows both organisms to grow at high soil temperatures [ 37 ].…”

Transcriptional Responses of Sclerotinia sclerotiorum to the Infection by SsHADV-1

“…Mycovirus-induced hypovirulence could be found in many important plant hemi-biotrophic and necrotrophic pathogenic fungi, including Aspergillus spp., Alternaria alternata , Bipolaris maydis , Botryosphaeria dothidea , Botrytis spp., Cryphonectria parasitica , Colletotrichum spp., Diaporthe spp., Fusarium spp., Helicobasidium mompa , Helminthosporium victoriae , Heterobasidion annosum , Macrophomina phaseolina , Magnaporthe oryzae , Ophiostoma spp., Penicillium digitatum , Pestalotiopsis theae , Rosellinia necatrix , Rhizoctonia solani , Sclerotinia spp. and so on [ 3 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 ], indicating hypovirulence-related mycoviruses as potential resources to control plant fungal diseases [ 4 ].…”