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

Abstract

The fungal lineage is one of the three large eukaryotic lineages that dominate terrestrial ecosystems. They share a common ancestor with animals in the eukaryotic supergroup Opisthokonta and have a deeper common ancestry with plants, yet several phenotypes, such as morphological, physiological, or nutritional traits, make them unique among all living organisms. This article provides an overview of some of the most important fungal traits, how they evolve, and what major genes and gene families contribute to their development. The traits highlighted here represent just a sample of the characteristics that have evolved in fungi, including polarized multicellular growth, fruiting body development, dimorphism, secondary metabolism, wood decay, and mycorrhizae. However, a great number of other important traits also underlie the evolution of the taxonomically and phenotypically hyperdiverse fungal kingdom, which could fill up a volume on its own. After reviewing the evolution of these six well-studied traits in fungi, we discuss how the recurrent evolution of phenotypic similarity, that is, convergent evolution in the broad sense, has shaped their phylogenetic distribution in extant species.

Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi

“…The analysis of trait relationships among fungi can also highlight potential evolutionary or physiological tradeoffs that shape responses of functional guilds to environmental pressures (Treseder, Kivlin, & Hawkes, ; Wallenstein & Hall, ; Crowther et al ., ; Martiny et al ., ; Halbwachs, Heilmann‐Clausen, & Bässler, ). Recent papers focus on traits critical to how fungi make their living, including body/thallus size, growth rate, respiration rate, spore size, stress tolerance (especially via melanin production), demand for nitrogen (N) and phosphorus (P), extracellular enzyme production, and development of hyphae versus budding growth (Wallenstein & Hall, ; Chagnon et al ., ; Aguilar‐Trigueros et al ., ; Crowther et al ., ; Koide, Fernandez, & Malcolm, ; Eichlerová et al ., ; Treseder & Lennon, ; Peay et al ., ; Nagy et al ., ; Siletti, Zeiner, & Bhatnagar, ; Zhang & Elser, ; Calhim et al ., ), They also demonstrate correlations between traits and climate or substrate preference (Kauserud et al ., ; Nordén et al ., ; Heilmann‐Clausen et al ., ; Andrew et al ., ; Abrego, Norberg, & Ovaskainen, ; Halbwachs et al ., ; Krah et al ., ), especially those traits that underpin species' abilities to disperse, colonize, and establish in different environments. For instance, spore size, wall thickness, and ornamentation differ among guilds and clades, and in some cases determine where particular individuals establish (Kauserud et al ., ; Nordén et al ., ; Halbwachs, Brandl, & Bässler, ; Andrew et al ., ; Abrego et al ., ; Halbwachs et al ., ; Calhim et al ., ).…”

“…). Similar carbohydrate‐degrading enzymes are reported in saprotrophs (Nagy et al ., ), which explains in part the extensive species overlap among these groups (Fig. A; Gazis et al ., ).…”

“…They possess a range of enzymes (and non‐enzymatic pathways) making them uniquely capable of degrading all structural components of dead plant material, including lignocellulose (Fig. ; Baldrian et al ., ; Riley et al ., ; Eichlerová et al ., ; Schilling et al ., ; Nagy et al ., ; López‐Mondéjar et al ., ). As wood and leaf litter pools degrade, they vertically stratify in terrestrial and aquatic systems, ultimately segregating saprotrophic communities over progressively decomposed material (Lindahl et al ., ; Lindahl & Boberg, ; Baldrian et al ., ; Richards et al ., ; Taylor et al ., ).…”

“…The analysis of trait relationships among fungi can also highlight potential evolutionary or physiological tradeoffs that shape responses of functional guilds to environmental pressures (Treseder, Kivlin, & Hawkes, 2011;Wallenstein & Hall, 2012;Crowther et al, 2014;Martiny et al, 2015;Halbwachs, Heilmann-Clausen, & Bässler, 2017). Recent papers focus on traits critical to how fungi make their living, including body/thallus size, growth rate, respiration rate, spore size, stress tolerance (especially via melanin production), demand for nitrogen (N) and phosphorus (P), extracellular enzyme production, and development of hyphae versus budding growth (Wallenstein & Hall, 2012;Chagnon et al, 2013;Aguilar-Trigueros et al, 2014;Crowther et al, 2014;Koide, Fernandez, & Malcolm, 2014;Eichlerová et al, 2015;Treseder & Lennon, 2015;Peay et al, 2016;Nagy et al, 2017;Siletti, Zeiner, & Bhatnagar, 2017;Zhang & Elser, 2017;Calhim et al, 2018), They also demonstrate correlations between traits and climate or substrate preference (Kauserud et al, 2011;Nordén et al, 2013;Heilmann-Clausen et al, 2014;Andrew et al, 2016;Abrego, Norberg, & Ovaskainen, 2017; (Nguyen et al, 2016). The total number of taxa included is 7678.…”

“…Additionally, brown rot fungi have evolved multiple times from white rot ancestors in Agaricomycotina in the Basidiomycota, coinciding with profound gene losses and shifts to non-enzymatic mechanisms (i.e. the Fenton reaction) for breaking down complex carbon compounds such as lignin in wood (see Section V.3; Martinez et al, 2009;Eastwood et al, 2011;Floudas et al, 2012;Nagy et al, 2017). Combining efforts from various databases (e.g.…”