Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree

Abstract

Mycorrhizas are known to have a positive impact on plant growth and ability to resist major biotic and abiotic stresses. However, the metabolic alterations underlying mycorrhizal symbiosis are still understudied. By using metabolomics and transcriptomics approaches, cork oak roots colonized by the ectomycorrhizal fungus Pisolithus tinctorius were compared with non-colonized roots. Results show that compounds putatively corresponding to carbohydrates, organic acids, tannins, long-chain fatty acids and monoacylglycerols, were depleted in ectomycorrhizal cork oak colonized roots. Conversely, non-proteogenic amino acids, such as gamma-aminobutyric acid (GABA), and several putative defense-related compounds, including oxylipin-family compounds, terpenoids and B6 vitamers were induced in mycorrhizal roots. Transcriptomic analysis suggests the involvement of GABA in ectomycorrhizal symbiosis through increased synthesis and inhibition of degradation in mycorrhizal roots. Results from this global metabolomics analysis suggest decreases in root metabolites which are common components of exudates, and in compounds related to root external protective layers which could facilitate plant-fungal contact and enhance symbiosis. Root metabolic pathways involved in defense against stress were induced in ectomycorrhizal roots that could be involved in a plant mechanism to avoid uncontrolled growth of the fungal symbiont in the root apoplast. Several of the identified symbiosis-specific metabolites, such as GABA, may help to understand how ectomycorrhizal fungi such as P. tinctorius benefit their host plants.

Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions

“…This is supported by observations that the established mycorrhizal roots were associated with decreased or unaffected levels of protective compounds (e.g. cell‐wall bound ferulic acids, tannins, Münzenberger et al, 1995; Solaiman & Senoo, 2018; Sebastiana et al, 2021) and lack of additional lignin deposition (Chen et al, 2021). However, mycorrhizas were shown to accumulate defence compounds in the endodermis/exodermis of roots (e.g.…”

Applying molecular and genetic methods to trees and their fungal communities

“…Supportive activity tests in environmental samples or their extracts are feasible for a few more persistent types of enzymes, for instance, laccases and peroxidases. Backing for actual physiological activities through meta-proteomics and metabolomics is desired (Sebastiana et al 2021 ), but also still goes beyond the current technical feasibilities of routine (Baldrian 2019 ).…”

Application of Metabolomics in Fungal Research

“…When Pisolithus tinctorius was parasitized on cork oak roots, the contents of root exudates such as carbohydrates, organic acids, tannins, long-chain fatty acids, and monoacylglycerols were significantly decreased. In contrast, root defense substances such as γ-aminobutyric acid (GABA), a terpenoid, guarantee that the cork oak roots can control the proliferative range of Pisolithus tinctorius while symbiosing with Pisolithus tinctorius [ 55 ]. Phytohormones such as salicylic acid (SA) and jasmonic acid (JA) are endogenous regulators used by higher plants to defend against foreign pathogens [ 135 , 136 ].…”