A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis

Summary Cross‐kingdom RNA interference (ckRNAi) is a mechanism of interspecies communication where small RNAs (sRNAs) are transported from one organism to another; these sRNAs silence target genes in trans by loading into host AGO proteins. In this work, we investigated the occurrence of ckRNAi in A...

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Published in:	The New phytologist Vol. 246; no. 3; pp. 924 - 935
Main Authors:	Silvestri, Alessandro, Ledford, William Conrad, Fiorilli, Valentina, Votta, Cristina, Scerna, Alessia, Tucconi, Jacopo, Mocchetti, Antonio, Grasso, Gianluca, Balestrini, Raffaella, Jin, Hailing, Rubio‐Somoza, Ignacio, Lanfranco, Luisa
Format:	Journal Article
Language:	English
Published:	England Wiley Subscription Services, Inc 01.05.2025 John Wiley and Sons Inc
Subjects:	Alfalfa arbuscular mycorrhizal symbiosis Arbuscular mycorrhizas Argonaute Proteins - metabolism computer simulation cross‐kingdom RNA interference Fungi Gene Expression Regulation, Plant Gene Silencing genes Glomeromycota - genetics Glomeromycota - physiology Host plants Immunoprecipitation Medicago truncatula Medicago truncatula - genetics Medicago truncatula - microbiology Mycorrhizae - genetics Mycorrhizae - physiology mycorrhizal fungi Nicotiana - genetics Nicotiana - microbiology Nicotiana benthamiana Plant Proteins - genetics Plant Proteins - metabolism Plant Roots - microbiology Plants prediction Priority Report Rhizophagus irregularis RNA interference RNA, Fungal - genetics RNA, Fungal - metabolism RNA, Small Untranslated - genetics RNA, Small Untranslated - metabolism RNA-mediated interference Roots small RNA Symbiosis Symbiosis - genetics Transcription factors Transcription Factors - genetics Transcription Factors - metabolism vesicular arbuscular mycorrhizae Medicago truncatula cross‐kingdom RNA interference small RNA arbuscular mycorrhizal symbiosis Rhizophagus irregularis
ISSN:	0028-646X, 1469-8137, 1469-8137
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Summary:	Summary Cross‐kingdom RNA interference (ckRNAi) is a mechanism of interspecies communication where small RNAs (sRNAs) are transported from one organism to another; these sRNAs silence target genes in trans by loading into host AGO proteins. In this work, we investigated the occurrence of ckRNAi in Arbuscular Mycorrhizal Symbiosis (AMS). We used an in silico prediction analysis to identify a sRNA (Rir2216) from the AM fungus Rhizophagus irregularis and its putative plant gene target, the Medicago truncatula MtWRKY69 transcription factor. Heterologous co‐expression assays in Nicotiana benthamiana, 5′ RACE reactions and AGO1‐immunoprecipitation assays from mycorrhizal roots were used to characterize the Rir2216–MtWRKY69 interaction. We further analyzed MtWRKY69 expression profile and the contribution of constitutive and conditional MtWRKY69 expression to AMS. We show that Rir2216 is loaded into an AGO1 silencing complex from the host plant M. truncatula, leading to cleavage of a host target transcript encoding for the MtWRKY69 transcription factor. MtWRKY69 is specifically downregulated in arbusculated cells in mycorrhizal roots and increased levels of MtWRKY69 expression led to a reduced AM colonization level. Our results indicate that MtWRKY69 silencing, mediated by a fungal sRNA, is relevant for AMS; we thus present the first experimental evidence of fungus to plant ckRNAi in AMS. See also the Commentary on this article by Xie & Fan, 246: 814–817.
Bibliography:	These authors contributed equally to this work. 814–817 Xie & Fan 246 See also the Commentary on this article by . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 See also the Commentary on this article by Xie & Fan, 246: 814–817.
ISSN:	0028-646X 1469-8137 1469-8137
DOI:	10.1111/nph.20273