Title: The ectomycorrhizal fungus Pisolithus microcarpus encodes a microRNA involved in cross-kingdom gene silencing during symbiosis

Abstract

Small 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.

Authors:

Wong-Bajracharya, Johanna  ^[1];

• Search DOE PAGES for author "Wong-Bajracharya, Johanna"
• Search DOE PAGES for ORCID "0000-0001-6119-8645"

Singan, Vasanth R. ^[2]; Monti, Remo ^[2]; Plett, Krista L. ^[1]; Ng, Vivian ^[2]; Grigoriev, Igor V.  ^[3];

• Search DOE PAGES for author "Grigoriev, Igor V."
• Search DOE PAGES for ORCID "0000-0002-3136-8903"

Martin, Francis M. ^[4]; Anderson, Ian C. ^[5]; Plett, Jonathan M.  ^[5]

• Search DOE PAGES for author "Plett, Jonathan M."
• Search DOE PAGES for ORCID "0000-0003-0514-8146"

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+ Show Author Affiliations

1. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2753, Australia, NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, NSW 2568, Australia
2. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
3. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, Plant and Microbial Biology Department, University of California Berkeley, Berkeley, CA 94720
4. French National Research Institute for Agriculture, Food and Environment (INRAE), Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, 54280 Champenoux, France
5. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2753, Australia

Publication Date:

Mon Jan 10 00:00:00 EST 2022

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1839163

Alternate Identifier(s):

OSTI ID: 1855359

Grant/Contract Number:  

AC02-05CH11231

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 119 Journal Issue: 3; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; effector; small RNA; symbiosis; mycorrhizae; plant defense