Mycoviruses are viruses that infect fungi, and hypovirulence-associated mycoviruses have the potential to control fungal diseases. However, it is unclear how mycovirus-mediated hypovirulent strains live and survive in the field, and no mycovirus has been applied for field crop protection. In this study, we found that a previously identified small DNA mycovirus (SsHADV-1) can convert its host, Sclerotinia sclerotiorum, from a typical necrotrophic pathogen to a beneficial endophytic fungus. SsHADV-1 downregulates the expression of key pathogenicity factor genes in S. sclerotiorum during infection. When growing in rapeseed, the SsHADV-1-infected strain DT-8 significantly regulates the expression of rapeseed genes involved in defense, hormone signaling, and circadian rhythm pathways. As a result, plant growth is promoted and disease resistance is enhanced. Field experiments showed that spraying DT-8 at the early flowering stage can reduce the disease severity of rapeseed stem rot by 67.6% and improve yield by 14.9%. Moreover, we discovered that SsHADV-1 could also infect other S. sclerotiorum strains on DT-8-inoculated plants and that DT-8 could be recovered from dead plants. These findings suggest that the mycoviruses may have the ability to shape the origin of endophytism. Our discoveries suggest that mycoviruses may influence the origin of endophytism and may also offer a novel strategy for disease control in which mycovirus-infected strains are used to improve crop health and release mycoviruses into the field.

Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4–18% in the field and consistently reduced Fusarium disease by 40–60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum, destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.

Clubroot caused by Plasmodiophora brassicae, is a severe disease of cruciferous crops that causes large hypertrophic galls in the roots. The plant microbiome is important for growth promotion and disease suppression. In this study, using 16S rRNA and internal transcribed spacer (ITS) sequencing techniques, we compared the endosphere microbiome of symptomatic and asymptomatic B. napus roots infected with P. brassicae collected from the same natural clubroot field. The results showed that the microbial population and its relative abundance in the asymptomatic roots was far higher than that in the symptomatic roots, and that many microorganisms in asymptomatic roots have biological control and plant growth promotion functions that may be related to clubroot symptoms. These results suggest the importance of the endosphere microbiome in clubroot disease and provide potential bio-control resources for its prevention.

The compounds involved in the hydroxycinnamic acid amide (HCAA) pathway are an important class of metabolites in plants. Extensive studies have reported that a variety of plant hydroxycinnamamides exhibit pivotal roles in plant–pathogen interactions, such as p-coumaroylagmatine and ferulic acid. The aim of this review is to discuss the emerging findings on the functions of hydroxycinnamic acid amides (HCAAs) accumulation associated with plant defenses against plant pathologies, antimicrobial activity of HCAAs, and the mechanism of HCAAs involved in plant immune responses (such as reactive oxygen species (ROS), cell wall response, plant defense hormones, and stomatal immunity). However, these advances have also revealed the complexity of HCAAs participation in plant defense reactions, and many mysteries remain to be revealed. This review provides an overview of the mechanistic and conceptual insights obtained so far and highlights areas for future exploration of phytochemical defense metabolites.

Stripe rust is a widespread and harmful wheat disease caused by Puccinia striiformis f. sp. tritici (Pst) worldwide. Targeted metabolome and transcriptomics analyses of CYR23 infected leaves were performed to identify the differential metabolites and differentially expressed genes related to wheat disease resistance. We observed upregulation of 33 metabolites involved in the primary and secondary metabolism, especially for homogentisic acid (HGA), p-coumaroylagmatine, and saccharopine. These three metabolites were mainly involved in the phenylpropanoid metabolic pathway, hydroxycinnamic acid amides pathway, and saccharopine pathway. Combined with transcriptome data on non-compatible interaction, the synthesis-related genes of these three differential metabolites were all upregulated significantly. The gene regulatory network involved in response to Pst infection was constructed, which revealed that several transcription factor families including WRKYs, MYBs, and bZIPs were identified as potentially hubs in wheat resistance response against Pst. An in vitro test showed that HGA effectively inhibited the germination of stripe rust fungus urediniospores and reduced the occurrence of wheat stripe rust. The results of gene silencing and overexpression of HGA synthesis-related gene 4-hydroxyphenylpyruvate dioxygenase proved that HGA was involved in wheat disease resistance. These results provided a further understanding of the disease resistance of wheat and indicated that HGA can be developed as a potential agent against Pst.