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View ORCID ProfileJohanna Wong-Bajracharya, Vasanth R. Singan, Remo Monti, Krista L. Plett, Vivian Ng, View ORCID ProfileIgor V. Grigoriev, Francis M. Martin, Ian C. Anderson, and View ORCID ProfileJonathan M. PlettaHawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2753, Australia;bNSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, NSW 2568, Australia;cUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;dPlant and Microbial Biology Department, University of California Berkeley, Berkeley, CA 94720;eFrench National Research Institute for Agriculture, Food and Environment (INRAE), Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, 54280 Champenoux, France
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Edited by Giles Oldroyd, Crops Science Centre, University of Cambridge, Cambridge, United Kingdom; received February 22, 2021; accepted November 17, 2021
SignificancePlant genomes encode hundreds of genes controlling the detection, signaling pathways, and immune responses necessary to defend against pathogens. Pathogens, in turn, continually evolve to evade these defenses. Small RNAs, such as microRNAs (miRNAs), are one mechanism used by pathogens to overcome plant defenses and facilitate plant colonization. Mounting evidence would suggest that beneficial microbes, likewise, use miRNAs to facilitate symbiosis. Here, we demonstrate that the beneficial fungus Pisolithus microcarpus encodes a miRNA that enters plant cells and stabilizes the symbiotic interaction. These results demonstrate that beneficial fungi may regulate host gene expression through the use of miRNAs and sheds light on how beneficial microbes have evolved mechanisms to colonize plant tissues.AbstractSmall RNAs (sRNAs) are known to regulate pathogenic plant–microbe interactions. Emerging evidence from the study of these model systems suggests that microRNAs (miRNAs) can be translocated between microbes and plants to facilitate symbiosis. The roles of sRNAs in mutualistic mycorrhizal fungal interactions, however, are largely unknown. In this study, we characterized miRNAs encoded by the ectomycorrhizal fungus Pisolithus microcarpus and investigated their expression during mutualistic interaction with Eucalyptus grandis. Using sRNA sequencing data and in situ miRNA detection, a novel fungal miRNA, Pmic_miR-8, was found to be transported into E. grandis roots after interaction with P. microcarpus. Further characterization experiments demonstrate that inhibition of Pmic_miR-8 negatively impacts the maintenance of mycorrhizal roots in E. grandis, while supplementation of Pmic_miR-8 led to deeper integration of the fungus into plant tissues. Target prediction and experimental testing suggest that Pmic_miR-8 may target the host NB-ARC domain containing transcripts, suggesting a potential role for this miRNA in subverting host signaling to stabilize the symbiotic interaction. Altogether, we provide evidence of previously undescribed cross-kingdom sRNA transfer from ectomycorrhizal fungi to plant roots, shedding light onto the involvement of miRNAs during the developmental process of mutualistic symbioses.effectorsmall RNAsymbiosismycorrhizaeplant defenseFootnotesAccepted November 17, 2021.Author contributions: J.W.-B., K.L.P., I.C.A., and J.M.P. designed research; J.W.-B., V.R.S., R.M., K.L.P., F.M.M., and J.M.P. performed research; V.N., I.V.G., I.C.A., and J.M.P. contributed new reagents/analytic tools; J.W.-B., V.R.S., R.M., K.L.P., V.N., I.V.G., F.M.M., I.C.A., and J.M.P. analyzed data; and J.W.-B., V.R.S., K.L.P., I.V.G., F.M.M., I.C.A., and J.M.P. wrote the paper.The authors declare no competing interest.This article is a PNAS Direct Submission.This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi: 10.1073/pnas.2103527119/-/DCSupplemental.Copyright © 2022 the Author(s). Published by PNAS.View Full Text
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