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DNA hypomethylation of the host tree impairs interaction with mutualistic ectomycorrhizal fungus

Publicated to:New Phytologist. 238 (6): 2561-2577 - 2023-06-01 238(6), DOI: 10.1111/nph.18734

Authors: Vigneaud, J; Kohler, A; Sow, MD; Delaunay, A; Fauchery, L; Guinet, F; Daviaud, C; Barry, KW; Keymanesh, K; Johnson, J; Singan, V; Grigoriev, I; Fichot, R; Conde, D; Perales, M; Tost, J; Martin, FM; Allona, I; Strauss, SH; Veneault-Fourrey, C; Maury, S

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Abstract

Ectomycorrhizas are an intrinsic component of tree nutrition and responses to environmental variations. How epigenetic mechanisms might regulate these mutualistic interactions is unknown. By manipulating the level of expression of the chromatin remodeler DECREASE IN DNA METHYLATION 1 (DDM1) and two demethylases DEMETER-LIKE (DML) in Populus tremula × Populus alba lines, we examined how host DNA methylation modulates multiple parameters of the responses to root colonization with the mutualistic fungus Laccaria bicolor. We compared the ectomycorrhizas formed between transgenic and wild-type (WT) trees and analyzed their methylomes and transcriptomes. The poplar lines displaying lower mycorrhiza formation rate corresponded to hypomethylated overexpressing DML or RNAi-ddm1 lines. We found 86 genes and 288 transposable elements (TEs) differentially methylated between WT and hypomethylated lines (common to both OX-dml and RNAi-ddm1) and 120 genes/1441 TEs in the fungal genome suggesting a host-induced remodeling of the fungal methylome. Hypomethylated poplar lines displayed 205 differentially expressed genes (cis and trans effects) in common with 17 being differentially methylated (cis). Our findings suggest a central role of host and fungal DNA methylation in the ability to form ectomycorrhizas including not only poplar genes involved in root initiation, ethylene and jasmonate-mediated pathways, and immune response but also terpenoid metabolism.

Keywords

cellschromatindemeterdna demethylationeepigenomeexpressionlaccaria bicolorlaccaria-bicolormethylationmethylomemycorrhizaspigeneticpoplarDemeterDnaDna demethylationeDna methylationDna methylation 1LaccariaLaccaria bicolorMycorrhizaeMycorrhizasPigeneticPlant rootsPoplarPopulusPopulus-trichocarpaTrees

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal New Phytologist due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2023, it was in position 11/265, thus managing to position itself as a Q1 (Primer Cuartil), in the category Plant Sciences. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 2.49. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Weighted Average of Normalized Impact by the Scopus agency: 2.31 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 7.18 (source consulted: Dimensions Jun 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-06-01, the following number of citations:

  • WoS: 12
  • Scopus: 12
  • Google Scholar: 7
  • OpenCitations: 12

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-06-01:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 27.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 25 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 29.05.
  • The number of mentions on the social network Facebook: 1 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 25 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: France; United States of America.