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Background  Small RNAs (sRNAs) are short non-coding RNA molecules (20–30 nt) that regulate gene expression at transcriptional or post-transcriptional levels in many eukaryotic organisms, through a mechanism known as RNA interference (RNAi). Recent studies have highlighted that they are also involved in cross-kingdom communication: sRNAs can move across the contact surfaces from “donor” to “receiver” organisms and, once in the host cells of the receiver, they can target specific mRNAs, leading to a modulation of host metabolic pathways and defense responses. Very little is known about RNAi mechanism and sRNAs occurrence in Arbuscular Mycorrhizal Fungi (AMF), an important component of the plant root microbiota that provide several benefits to host plants, such as improved mineral uptake and tolerance to biotic and abiotic stress.    Results  Taking advantage of the available genomic resources for the AMF  Rhizophagus irregularis  we described its putative RNAi machinery, which is characterized by a single  Dicer -like ( DCL ) gene and an unusual expansion of  Argonaute -like ( AGO -like) and  RNA-dependent RNA polymerase  ( RdRp ) gene families. In silico investigations of previously published transcriptomic data and experimental assays carried out in this work provided evidence of gene expression for most of the identified sequences. Focusing on the symbiosis between  R. irregularis  and the model plant  Medicago truncatula , we characterized the fungal sRNA population, highlighting the occurrence of an active sRNA-generating pathway and the presence of microRNA-like sequences. In silico analyses, supported by host plant degradome data, revealed that several fungal sRNAs have the potential to target  M. truncatula  transcripts, including some specific mRNA already shown to be modulated in roots upon AMF colonization.    Conclusions  The identification of RNAi-related genes, together with the characterization of the sRNAs population, suggest that  R. irregularis  is equipped with a functional sRNA-generating pathway. Moreover, the in silico analysis predicted 237 plant transcripts as putative targets of specific fungal sRNAs suggesting that cross-kingdom post-transcriptional gene silencing may occur during AMF colonization.    Electronic supplementary material  The online version of this article (10.1186/s12864-019-5561-0) contains supplementary material, which is available to authorized users.

bmc genomics

In silico analysis of fungal small RNA accumulation reveals putative plant mRNA targets in the symbiosis between an arbuscular mycorrhizal fungus and its host plant