Expanding genomics of mycorrhizal symbiosis

Abstract

The mycorrhizal symbiosis between soil fungi and plant roots is a ubiquitous mutualism that plays key roles in plant nutrition, soil health, and carbon cycling. The symbiosis evolved repeatedly and independently as multiple morphotypes [e.g., arbuscular mycorrhizae (AM), ectomycorrhizal (ECM)] in multiple fungal clades (e.g., phyla Glomeromycota, Ascomycota, Basidiomycota). The accessibility and cultivability of many mycorrhizal partners make them ideal models for symbiosis studies. Alongside molecular, physiological, and ecological investigations, sequencing led to the first three mycorrhizal fungal genomes, representing two morphotypes and three phyla. The genome of the ECM basidiomycete Laccaria bicolor showed that the mycorrhizal lifestyle can evolve through loss of plant cell wall-degrading enzymes (PCWDEs) and expansion of lineage-specific gene families such as short secreted protein (SSP) effectors. The genome of the ECM ascomycete Tuber melanosporum showed that the ECM type can evolve without expansion of families as in Laccaria, and thus a different set of symbiosis genes. The genome of the AM glomeromycete Rhizophagus irregularis showed that despite enormous phylogenetic distance and morphological difference from the other two fungi, symbiosis can involve similar solutions as symbiosis-induced SSPs and loss of PCWDEs. The three genomes provide a solid base for addressing fundamental questions about the nature and role of a vital mutualism.

Fungal Traits That Drive Ecosystem Dynamics on Land

“…To date, their defining characteristic-symbioses with plant roots-is not associated with known universal genes (245). In addition, only three published genomes of mycorrhizal fungi were available when we conducted our analyses, which limited our ability to detect phylogenetically independent differences between mycorrhizal fungi and other groups.…”

Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis?

“…2). In particular, they show a significant expansion of gene families potentially involved in the symbiotic interaction with the host plant (Kuo et al, 2014;Van der Heijden et al, 2015), such as taxon-specific mycorrhiza-induced small secreted proteins (MiSSPs; Pellegrin et al, 2015). Some MiSSPs were demonstrated to act as effector proteins, playing crucial roles in symbiosis formation in the ECM fungus Laccaria bicolor (Plett et al, 2014;Pellegrin et al, 2017) and in the AM fungus Rhizophagus irregularis (Kloppholz et al, 2011).…”

“…Other distinct endomycorrhizal types, both characterized by intracellular fungal pelotons, occur in specific plant lineages, such as orchid mycorrhiza (ORM) in the Orchidaceae and ericoid mycorrhiza (ERM) in the youngest subfamilies of Ericaceae (Martin et al, 2016). Mycorrhizal fungi provide fundamental ecosystem services and the last decade has witnessed great efforts to sequence the genomes of phylogenetically and ecologically diverse mycorrhizal taxa, thus providing new insights into the evolution of the mycorrhizal lifestyle and the diversity of mycorrhizal fungi-plant interaction mechanisms (Kuo et al, 2014). Here, we discuss some key similarities and differences between ERM fungi and other kinds of mycorrhizal fungi, as revealed by the genomes of four ERM fungal species in the Ascomycetes (Kohler et al, 2015;Martino et al, 2018), and suggest possible explanations for their distinctive features.…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…The genetic bases of mycorrhiza formation comprise complex pathways of secreted proteins, effectors, regulators, PCWDEs, and several hitherto unknown components. Small secreted proteins are particularly abundant in ECM species and are upregulated during mycorrhiza formation in high numbers (176). These might be involved in controlling host defense mechanisms during the establishment of the mycorrhizal interaction.…”