Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria

Abstract

Summary A systematic and evolutionary ecology study of the model ectomycorrhizal (ECM) genus Laccaria was performed using herbarium material and field collections from over 30 countries covering its known geographic range.A four‐gene (nrITS, 28S, RPB2, EF1α) nucleotide sequence dataset consisting of 232 Laccaria specimens was analyzed phylogenetically. The resulting Global Laccaria dataset was used for molecular dating and estimating diversification rates in the genus. Stable isotope analysis of carbon and nitrogen was used to evaluate the origin of Laccaria's ECM ecology.In all, 116 Laccaria molecular species were identified, resulting in a near 50% increase in its known diversity, including the new species described herein: Laccaria ambigua. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Paleocene (56–66 million yr ago), probably in Australasia. At this time, Laccaria split into two lineages: one represented by the new species L. ambigua, and the other reflecting a large shift in diversification that resulted in the remainder of Laccaria. L. ambigua shows a different isotopic profile than all other Laccaria species.Isotopes and diversification results suggest that the evolution of the ECM ecology was a key innovation in the evolution of Laccaria. Diversification shifts associated with Laccaria's dispersal to the northern hemisphere are attributed to adaptations to new ecological niches.

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

“…However, the ECM symbiosis has evolved independently several times from ancestral saprotrophs (Tedersoo & Smith, 2013) and some ECM lineages originated fairly recently. For example, Wilson et al (2017) reconstructed the evolution of the ECM habit in the genus Laccaria. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Palaeocene (56-66 Ma), and accumulating data point to a later evolution and unique origin of the Laccaria ECM habit from a saprotrophic progenitor (Wilson et al, 2017).…”

“…For example, Wilson et al (2017) reconstructed the evolution of the ECM habit in the genus Laccaria. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Palaeocene (56-66 Ma), and accumulating data point to a later evolution and unique origin of the Laccaria ECM habit from a saprotrophic progenitor (Wilson et al, 2017). Although the rate of genome evolution may not be the same, the evolutionary timeframe is comparable for ERM and recent ECM taxa such as L. bicolor, which lost most of its decay apparatus (Martin et al, 2016).…”

A new species and a new record of Laccaria (Fungi, Basidiomycota) found in a relict forest of the endangered Fagus grandifolia var. mexicana

“…In the phylogeny presented here that is based on sequences used in the worldwide survey of Laccaria by Wilson et al (2017) and complemented with some from GenBank (Fig. 1) and sequences of L. squarrosa , described here, this new taxon is clearly shown to be phylogenetically isolated from other Laccaria species.…”

“…The phylogenetic analysis was performed with the sequences obtained in this study, as well as some retrieved from GenBank (http://www.ncbi.nlm.nih.gov/) derived from the Blast analysis (only those that best match), and complemented with related sequences used by Osmundson et al (2005), Montoya et al (2015) and Wilson et al (2017) (Table 1). For this purpose, we constructed a dataset (ITS+LSU) using PhyDE v.0.9971 (Müller et al 2010), also with MEGA 6.06 (Tamura et al 2013) calculated the best evolutionary model and constructed the phylogenetic tree under the method of Maximum Likelihood (ML) with 500 bootstrap replications, and finally with MrBayes v 3.2.6 (Ronquist et al 2012) constructed the phylogenetic tree (as Montoya et al 2014) under the method of Bayesian Inference (BI).…”

“…New or potential undescribed species from different regions, based on morphological and molecular characteristics of fructifications, or on DNA identifications of environmental samples, have been discovered recently (Wang et al 2004, Osmundson et al 2005, Sheedy et al 2013, Wilson et al 2013, 2017, Montoya et al 2015, Luo et al 2016, Popa et al 2014, 2016). Nowadays, MycoBank recognizes 112 records in this group of fungi, and additionally, Wilson et al (2017) inferred 116 phylogenetic species from 30 countries covering the known geographic range of Laccaria . During the advances on the systematics of the group, a small number of morphological (macro- and microscopic) features had been found taxonomically informative (McNabb 1972, Mueller 1992), which may be the cause of false interpretations, leading to conceptual misunderstandings.…”