Ectomycorrhizal symbiosis evolved independently and by convergent gene duplication in rosid lineages

Abstract

Many land plants rely on mutualistic symbiotic associations to thrive, starting with their common ancestor associating with arbuscular mycorrhizal (AM) fungi (Rich et al., 2021). Similar to AM symbiosis, multiple other intracellular symbiotic interactions have evolved in land plants, such as ericoid symbiosis in the Ericaceae and root nodule symbiosis with nitrogen-fixing bacteria in the legumes and their relatives (Strullu-Derrien et al., 2018; Radhakrishnan et al., 2020). Ectomycorrhizal (ECM) symbiosis contrasts with these relationships, as there is no intracellular accommodation of the symbiont inside the plant cell, but only intercellular colonization (Brundrett & Tedersoo, 2018). This symbiotic relationship is common in seed plants, mostly trees and shrubs, such as the gymnosperm pines, dicot willows and oaks (Cairney, 2000; Wang & Qiu, 2006; Tedersoo & Brundrett, 2017). The fungal partners are primarily of the Ascomycete, Basidiomycete and sporadically Zygomycota clades and evolved from a saprotrophic to a symbiotic lifestyle (Cairney, 2000; Martin et al., 2016), with varying degrees of plant host specificity (Bakker et al., 2004; Plett et al., 2015; Lofgren et al., 2021).

Efforts have been made to uncover the fungal side of this symbiotic relationship (Martin et al., 2008, 2016; Kohler et al., 2015; Liao et al., 2016; Zhang et al., 2018, 2022; Chowdhury et al., 2022), but the plant side remains more elusive. Although the plant lineages involved in ECM symbiosis are known (Tedersoo & Brundrett, 2017), there has been little investigation into the evolutionary origin of ECM symbiosis in these lineages. The current hypothesis is that plants evolved the ability to engage in ECM symbiosis repeatedly and independently as a response to environmental change, but genetic evidence for this is lacking (Cairney, 2000; Wang & Qiu, 2006; Brundrett & Tedersoo, 2018). Furthermore, the genetic innovations and transcriptomic response related to this symbiosis have been studied largely in a genus or species-specific context (Liao et al., 2016; Bouffaud et al., 2020; Chowdhury et al., 2022; Hill et al., 2022), which hinders the study of their evolutionary origins. It has been proposed that most ECM plants have evolved from AM plants, potentially by repurposing genes involved in AM symbiosis for ECM symbiosis (Brundrett & Tedersoo, 2018; Li et al., 2024).

In this study, we reconstruct the origin of ECM symbiosis in the rosid clade, showing at least 16 independent origins, resulting in the 17 known extant ECM rosid lineages. Moreover, comparative genomics of these lineages highlight genes involved in cell wall remodeling, which underwent duplications in a convergent manner across ECM lineages.

None declared.

PMD conceived and coordinated the project. FvB, YB, CP, MEB and CL carried out the bioinformatic analyses. MB, JK and PMD coordinated the analyses. FvB, YB and PMD wrote the manuscript with input from all authors. FvB and YB contributed equally to this work.

Code used for this work is available on GitLab (https://gitlab.com/fabianvanbeveren/ecm/) and phylogenies and alignments can be found on Figshare (doi: 10.6084/m9.figshare.27241689). Genome data used is listed in Table S3 and sources for the RbcL and MatK sequences in Table S1.

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