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

Abstract

Summary 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.

A perspective on cross‐kingdom RNA interference in mutualistic symbioses

“…Tantalising results from studies of pathogen-plant ckRNAi also open many avenues for future research; for instance, the loading of endosymbiont sRNAs into host AGO4 proteins opens the prospect of these driving transcriptional gene silencing, possibly allowing long-term regulation of gene expression in the host through methylation of target genes. Such regulation would have considerable benefits in a mutualism, potentially adapting one or both partners to increase the stability of the interaction; indeed, the importance of DNA methylation in symbiosis has been recently (Vigneaud et al, 2023). Determining whether this is observed in the AM symbiosis will be an important avenue for research, especially given that this could be modified to increase the stability of symbioses in key crops.…”

“…Such regulation would have considerable benefits in a mutualism, potentially adapting one or both partners to increase the stability of the interaction; indeed, the importance of DNA methylation in symbiosis has been recently demonstrated in ectomycorrhizal symbiosis, with hypomethylation in the Populus sp. host associated with decreased association with the Laccaria bicolor mycorrhizal fungus (Vigneaud et al ., 2023 ). Determining whether this is observed in the AM symbiosis will be an important avenue for research, especially given that this could be modified to increase the stability of symbioses in key crops.…”

Epigenetic Variation in Tree Evolution: a case study in black poplar (Populus nigra)

“…Poplars are characterized by a high genetic diversity, fast juvenile growth, vegetative propagation capacity, and the genome of several species has been sequenced (Tuskan et al 2006;Mader et al 2016). Over the past decade, poplar has been widely used to investigate the role of DNA methylation in phenotypic plasticity and adaptation to environmental changes (Brautigam et al 2013;Lafon-Placette et al 2013Zhu et al 2013;Plomion et al 2016;Conde et al 2017;Le Gac et al 2018, 2019Sow et al 2018aSow et al , 2018bSow et al , 2021Vigneaud et al 2023). However, several open questions remain to be addressed, such as (i) does epigenetics play a role in genome reprogramming in response to polyploidization events?…”

Epigenetic control is involved in molecular dialogue in plant–microbe symbiosis

“…In the case of arbuscular mycorrhizal (AM) symbiosis, studies have shown that epigenetic modifications occur in the seeds of Geranium sylvaticum, and the roots and leaves of Geranium robertianum, in symbiosis with the AM fungus Funneliformis mosseae (Varga & Soulsbury, 2017. In this issue of New Phytologist, Vigneaud et al (2023Vigneaud et al ( , pp. 2561Vigneaud et al ( -2577 analyzed gene regulation at the epigenetic level interfering with plant ectomycorrhizal (ECM) interactions.…”

“…In this issue of New Phytologist , Vigneaud et al . (2023, pp. 2561–2577) analyzed gene regulation at the epigenetic level interfering with plant ectomycorrhizal (ECM) interactions.…”