Small RNAs: A new paradigm in fungal-fungal interactions used for biocontrol

Abstract

In many eukaryotes, small RNAs (sRNAs) can mediate gene expression regulation through a mechanism known as RNA silencing. In fungi, RNA silencing plays a crucial role in numerous biological processes, including parasitic and mutualistic fungus-plant interactions. This review summarizes recent findings on the role of RNA silencing in parasitic fungus-fungus and fungus-insect interactions in relation to their use for the biological control (biocontrol) of fungal plant diseases and insect damage. Genes belonging to the RNA silencing machinery are identified in the genomes of almost all known fungal and oomycete biocontrol organisms. However, recent functional genetic studies in Ascomycota species of the Hypocreales order, such as Trichoderma atroviride and Clonostachys rosea, show how RNA silencing can have family-specific effects, as conidiation is affected differently in the two organisms when the same elements of the RNA silencing machinery are deleted. The size of sRNAs regulated by RNA silencing can also vary between organisms. Cross-species RNA silencing represents a new field in the study of antagonistic interactions. For example, a microRNA (miRNA) of another hypocrealean fungus, Beauveria bassiana, was proven to target genes involved in the immune response of mosquitoes, and there are indications that miRNAs from the mycoparasitic C. rosea may target factors of virulence in its plant-pathogenic host fungi. Accumulating evidence from many species shows that the number of endogenous genes affected by the disruption of the RNA silencing mechanism is always much higher than the number of predicted direct target genes. As several putative targets of fungal sRNAs are transcription factors, it is possible that specific sRNAs have a role as master regulators of gene expression, affecting the transcription of a high number of genes through cascading regulating effects. The challenges faced when studying cross-species RNA silencing, including sRNA trafficking during mycoparasitism, are also discussed. This includes the difficulties in separating the extracellular vesicles of mycoparasitic fungi from those of their hosts, the high amount of sequencing reads lost in bioinformatics filtering steps, imprecise target prediction and the lack of a streamlined accepted way of reporting results.