Evolution of the Mode of Nutrition in Symbiotic and Saprotrophic Fungi in Forest Ecosystems

Abstract

In this review, we highlight the main insights that have been gathered from recent developments using large-scale genomics of fungal saprotrophs and symbiotrophs (including ectomycorrhizal and orchid and ericoid mycorrhizal fungi) inhabiting forest ecosystems. After assessing the goals and motivations underlying our approach, we explore our current understanding of the limits and future potential of using genomics to understand the ecological roles of these forest fungi. Comparative genomics unraveled the molecular machineries involved in lignocellulose decomposition in wood decayers, soil and litter saprotrophs, and mycorrhizal symbionts. They also showed that transitions from saprotrophy to mutualism entailed widespread losses of lignocellulose-degrading enzymes; diversification of novel, lineage-specific symbiosis-induced genes; and convergent evolution of genetic innovations that facilitate the accommodation of mutualistic symbionts within their plant hosts. We also identify the major questions that remain unanswered and propose new avenues of genome-based research to understand the role of soil fungi in sustainable forest ecosystems. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities

“…Conversely, Sebacinales , Helotiales , and Cantharellales are younger clades that have more recently acquired their ability to interact with plants [5]. In addition, many of these lineages are still saprotrophs [12,83,84]: these fungal lineages are therefore less dependent on plants than obligate biotrophic ones [85]. Thus, plant colonization can be more facultative for them and often requires a minimal plant-fungus specificity to be established [3], which could explain the higher specialization we have observed for these lineages.…”

Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

“…Another frequently studied group of proteins involved in the plant–fungal interaction are carbohydrate-active enzymes (CAZymes), many of which act as plant cell wall–degrading enzymes (PCWDEs) ( Kubicek et al 2014 ). CAZymes are often referred to as saprotrophic features ( Lebreton et al 2021 ), but are also abundant in plant pathogens and endophytes (e.g., Zhao et al 2013 ; Knapp et al 2018 ; Mesny et al 2021 ), and, although present in lower numbers in mycorrhizal fungi ( Kohler et al 2015 ; Peter et al 2016 ; Miyauchi et al 2020 ), certain CAZymes play key roles in the establishment and maintenance of the symbiosis ( Veneault-Fourrey et al 2014 ; Doré et al 2017 ; Marqués-Gálvez et al 2021 ). Comparing CSEP and CAZyme repertoires is therefore highly relevant to exploring genetic differences in plant associated lifestyles of fusarioid fungi.…”

Comparative genomics reveals a dynamic genome evolution in the ectomycorrhizal milk‐cap (Lactarius) mushrooms

“…In association with this root diversification, multiple saprophytic fungi in various fungal lineages shifted to an EcM lifestyle (Looney et al ., 2018). As a result of convergent evolution, EcM lineages in most fungal orders share similar genomic features, including a larger genome size resulting from TE proliferation, a restricted set of PCWDEs and a specific suite of effector‐like SSPs (Kohler et al ., 2015; Miyauchi et al ., 2020; Lebreton et al ., 2021b). These convergent sets of genetic traits are the hallmarks of the EcM lifestyle and they are shared by the symbiotic Russulales.…”

“…Soilborne ectomycorrhizal (EcM) fungi establish symbiotic relationships with 60% of tree individuals on Earth, and mediate the exchange of plant carbohydrates for soil minerals (Brundrett & Tedersoo, 2018; Steidinger et al ., 2019). They evolved independently, at least 80 times, from diverse saprotrophic ancestors (Tedersoo et al ., 2010; Martin et al ., 2016; Lebreton et al ., 2021b). These multiple emergences of EcM lineages involved lineage‐specific genomic innovations, such as effector‐like mycorrhiza‐induced small secreted proteins (MiSSPs), but also loss of gene families, such as plant cell wall‐degrading enzymes (PCWDEs).…”