An Overview of 24 Years of Molecular Phylogenetic Studies in Phallales (Basidiomycota) With Notes on Systematics, Geographic Distribution, Lifestyle, and Edibility.

Gislaine C S Melanda,María P Martín,Alexandre G S Silva-Filho,Iuri Goulart Baseia,Alexandro De Andrade De Lima,Tiara S Cabral,Alexandre Rafael Lenz,Nathalia Mendonça De Assis,Renato Juciano Ferreira,Nelson Menolli

doi:10.3389/fmicb.2021.689374

Abstract

The order Phallales (Basidiomycota) is represented by gasteroid fungi with expanded and sequestrate basidiomata, known as stinkhorns and false truffles. In phalloids, the first DNA sequence was published in 1997, and after that, some studies aimed to resolve phylogenetic conflicts and propose new species based on DNA markers; however, the number of families and genera in the order still generates controversies among researchers. Thus, this work aims to provide an overview of Phallales diversity represented by selected DNA markers available in public databases. We retrieved Phallales sequences from DNA databases (GenBank and UNITE) of seven markers: ITS (internal transcribed spacer), nuc-LSU (nuclear large subunit rDNA), nuc-SSU (nuclear small subunit rDNA), mt-SSU (mitochondrial small subunit rDNA), ATP6 (ATPase subunit 6), RPB2 (nuclear protein-coding second largest subunit of RNA polymerase), and TEF1-α (translation elongation factor subunit 1α). To compose our final dataset, all ITS sequences retrieved were subjected to BLASTn searches to identify additional ITS sequences not classified as Phallales. Phylogenetic analyses based on Bayesian and maximum likelihood approaches using single and combined markers were conducted. All ITS sequences were clustered with a cutoff of 98% in order to maximize the number of species hypotheses. The geographic origin of sequences was retrieved, as well as additional information on species lifestyle and edibility. We obtained a total of 1,149 sequences, representing 664 individuals. Sequences of 41 individuals were unidentified at genus level and were assigned to five distinct families. We recognize seven families and 22 genera in Phallales, although the delimitation of some genera must be further revisited in order to recognize only monophyletic groups. Many inconsistencies in species identification are discussed, and the positioning of genera in each family is shown. The clustering revealed 118 species hypotheses, meaning that approximately 20% of all described species in Phallales have DNA sequences available. Information related to geographic distribution represents 462 individuals distributed in 46 countries on all continents, except Antarctica. Most genera are saprotrophic with only one putative ectomycorrhizal genus, and 2.1% of the legitimate specific names recognized in Phallales are confirmed edible species. Great progress in the molecular analyses of phalloids has already been made over these years, but it is still necessary to solve some taxonomic inconsistencies, mainly at genus level, and generate new data to expand knowledge of the group.

Highlights

The first molecular analyses including gasteroid fungi (Hibbett et al, 1997) showed that they represent a polyphyletic and artificial grouping of taxa that share a common ancestor with gilled and nongilled mushrooms that have active dispersion of the basidiospores. Hibbett et al (1997) showed the gasteroid–phalloid fungi to group in a clade with other forms of gasteroid fungi, the Geastraceae Corda and Sphaerobolaceae J
To construct the maps based on this global distribution, the locality of each individual identified at genus level was retrieved from the databases (Supplementary Table 4)
The year 2006 can be marked as a huge advance in Phallales taxonomy with the work of Hosaka et al (2006), a study aided by the Deep Hypha initiative (Blackwell et al, 2006)

Summary

Introduction

The first molecular analyses including gasteroid fungi (Hibbett et al, 1997) showed that they represent a polyphyletic and artificial grouping of taxa that share a common ancestor with gilled and nongilled mushrooms that have active dispersion of the basidiospores. Hibbett et al (1997) showed the gasteroid–phalloid fungi to group in a clade with other forms of gasteroid fungi, the Geastraceae Corda (earthstars) and Sphaerobolaceae J. The first molecular analyses including gasteroid fungi (Hibbett et al, 1997) showed that they represent a polyphyletic and artificial grouping of taxa that share a common ancestor with gilled and nongilled mushrooms that have active dispersion of the basidiospores. After that, Pine et al (1999) confirmed the phylogenetic relationship between some cantharelloid, clavarioid, and phalloid fungi, naming all of them the gomphoid–phalloid clade, which was later confirmed as monophyletic (Hibbett and Thorn, 2001; Krüger et al, 2001; Binder and Hibbett, 2002; Hibbett and Binder, 2002) and designated as a subclass of Agaricomycetes: Phallomycetidae K. Fisch (Agaricomycetes, Phallomycetidae) includes representatives of gasteroid fungi with basidiospores that are passively dispersed mainly by insects and commonly named phalloid fungi, alien fungi, stinkhorns, and lattice or cage stinkhorns (Fischer, 1898; Cunningham, 1931; Miller and Miller, 1988; Pegler and Gomez, 1994). The phalloid fungi are mostly saprobic and characterized by hypogeous or epigeous immature basidiomata that are divided into chambers; thick white rhizomorphs are usually present; peridium with two or three layers, one of which is gelatinous; mature basidiomata that are usually epigeous or partially hypogeous, expanded, or sequestrate; pseudostipitate or sessile receptacle; receptacle carrying the green, olive to brown gleba; the usual presence of gelatinous to mucilaginous gleba that may be powdery at maturity, as in Gastrosporium Mattir.; and basidiospores mostly ellipsoid and smooth, with only a few genera with ornamentation on the basidiospore wall, as in Gastrosporium, Kjeldsenia Colgan, Castellano and Bougher, and Phlebogaster Fogel (Hosaka et al, 2006; Trierveiler-Pereira et al, 2014a)

Objectives

Methods

Results

Conclusion