Lorchel taxonomy overhauled: Synopsis of our Discinaceae phylogenomics publication

In investigating the genetics and evolution of gyromitrin, I sequenced 75 Discinaceae genomes representing all the known species-group clades in the family and conducted phylogenomic analyses. This means that instead of using a few genes to infer a phylogenetic tree, thousands of conserved genes are used to infer evolutionary relatedness. Why are more data better? A few genes may conflict with each other in the story they tell, but thousands of genes typically result in a much more robust inference of evolutionary history. It's basically statistical — the bigger the sample size the greater your power to infer the truth (up to a point). Indeed, our large dataset allowed us to resolve the ancestral relationships of the lorchel family, and the results were published in the journal Molecular Phylogenetics and Evolution (PDF). The lorchels are an amazing and diverse group of mushrooms whose taxonomy has been debated for centuries. With these genomes, we were able to not only infer a robust phylogenetic tree and make informed taxonomic revisions but also better understand lorchel ecology and reproduction based on their genomic properties.  

Figure 1. Morphological diversity of Discinaceae and related taxa. A–M. Species belonging to Discinaceae arranged according to their top-to-bottom order in Figure 2. N–O. Species belonging to familia incertae sedis. Tribe Discineae: A) Discina ancilis; B) Discina mcknightii; C) Neogyromitra brunnea; D) Neogyromitra martinii; E) Maublancomyces korfii; F) Maublancomyces sp. 2; G) Piscidiscina leucoxantha; H) Pseudodiscina melaleucoides. Tribe Gyromitreae: I) Hydnotrya sp. 3; J) Paragyromitra infula; K) Gyromitra venenata; L) Pseudorhizina californica; M) Pseudoverpa anthracobia. Familia incertae sedis: N) Marcelleina donadinii; O) Paradiscina melaleuca. Photo credits: Alden Dirks (A, C, K), Bernd Fellmann (D), Brittany Marcotte (M), Drew Henderson (B), Eric 175 Chandler (J), Garrett Taylor (E, G), Jacques Guinberteau (O), Jen Chandler (J), Matthew E. Smith (I), 176 Rubén Martínez Gil (N), Steve Ness (L), Vail Paterson (F), and Yi-Min Wang (H).

Taxonomic revisions

For most people, the greatest interest and biggest consequence of this work are the substantial taxonomic revisions facilitated by our robust phylogenomic tree. 

As can be seen in Figure 2, the phylogenomic tree shows an early bifurcation resulting in two major clades that I am calling tribe Discineae and tribe Gyromitreae (tribe is a taxonomic rank below family and above genus). Each tribe consists of five genera. Of these twelve names (two tribes and ten genera), only one of them is newly erected: Piscidiscina, which means "fish cup", in reference to the scooped out, fishtail-like ascospore apiculi of the species in this genus (e.g., Piscidiscina leucoxantha and Piscidiscina persicula). Our taxonomic system aligns pretty well with ones proposed by some earlier mycologists based solely on morphology, which is why these names were already in existence. Each genus has a distinct combination of macro- and micromorphological traits that should allow for any mature specimen to be readily identified to genus with a microscope.  

Taxonomic change is jarring for users, especially when we have grown accustomed to calling everything Gyromitra. In the first iteration of this work, I did call everything in the family Gyromitra (including the Hydnotrya truffles). While this approach was an elegant act of lumping that satisfied many field mycologists, in the end it was not the best approach. I encourage you to check out the publication, which includes a lengthy discussion on the pros and cons of various taxonomic proposals. I hope that the one presented here will result in a stable and useful system for communicating and classifying lorchel biodiversity for a long time to come.

Tribe Discineae

1. Discina - cup or discoid fungi with prominent pointed apiculi on their ascospores (Discina ancilis, Discina perlata, and related species); 8 species, a substantial number of undescribed species, and lots of old names that require revisionary taxonomic treatment
2. Neogyromitra - discoid or stipitate fungi with multiple apiculi on each end of their ascospores (Neogyromitra brunnea and Neogyromitra caroliniana are the most well known species); 6 species, perhaps one more undescribed species (see Miller et al. 2025)
3. Maublancomyces - discoid or stipitate fungi with single rounded apiculi on their ascospores (including Maublancomyces gigas, Maublancomyces korfii, and Maublancomyces montanus, among others); 13 species, some undescribed species still in the Maublancomyces gigas group, the discoid Maublancomyces are in need of taxonomic revision (see Miller et al. 2020 and Miller et al. 2022)
4. Piscidiscina - discoid fungi with fishtail-like apiculi on their ascospores (Piscidiscina leucoxantha and related species); 3 species, at least on undescribed species known to occur in China
5. Pseudodiscina - cup fungi with no apiculi (Pseudodiscina melaleucoides); 2 species

Tribe Gyromitreae

1. Hydnotrya - truffles; 17 species, many undescribed species
2. Paragyromitra - Paragyromitra infula and related species recognizable by macromorphology; 8 species, a few undescribed species
3. Gyromitra - Gyromitra esculenta and related species recognizable by macromorphology; 7 species, perhaps no more undescribed species but in need of taxonomic revision
4. Pseudorhizina - Pseudorhizina californica and Pseudorhizina sphaerospora recognizable by macromorphology; 4 species, in need of taxonomic revision to resolve potential synonymy
5. Pseudoverpa - the Verpa-like Pseudoverpa anthracobia; 1 species, a potentially undescribed species occurs in the Pacific Northwest of North America

Finally, we found that the species Paradiscina melaleuca, previously thought to be in Discinaceae, belongs to a separate, undescribed family-level lineage along with the species Marcelleina donadinii. This group requires more sampling and further study. 

Figure 2. Phylogenomic tree of the lorchel family Discinaceae and closely related Pezizales families. The phylogenomic tree was inferred with 1542 concatenated BUSCO genes that were analyzed using an edge-linked proportional partition model and 1000 ultrafast bootstrap replicates in IQ-TREE2. Bootstrap support (not shown) was 100% across all branches, except for the shortest branch within the Gyromitra venenata clade (70%). Gene concordance factors (gCF) are listed on the branches, and values less than 50% are indicated in red. Families are colored according to the legend. Discinaceae tribes and genera are labeled, and the diversity of macromorphology present in each genus or outgroup family is represented by icons. Sequences derived from type specimens are in bold. The scale bar indicates the number of nucleotide substitutions per site.

Ecological assesments

Genomes can provide insight not only into evolutionary relatedness but also other properties of an organism such as trophic mode (ecological means of nutrient acquisition). A good indicator of a fungus's ecology is its enzymatic toolkit for carbohydrate degradation, deemed CAZymes (Carbohydrate-Active enZymes). Saprotrophic species (ones that eat dead organic matter) need lots of CAZymes to break down complex substrates like wood and leaves. On the other hand, mycorrhizal species tend to possess fewer CAZymes because they acquire most of their sugars from a living plant host in exchange for soilbound nutrients. I found that all Discinaceae genera possess enzymatic signatures of saprotrophy except for the genus Hydnotrya, the only truffle-producing clade in the family (Fig. 3). Hydnotrya has already been confirmed to be ectomycorrhizal in previous studies, and this is evident in their CAZyme repertoire, which is significantly reduced in lignocellulose-degrading enzymes. Interestingly, mycorrhizal truffles have evolved independently numerous times in the Pezizales. The reason for this "covariance" (the property of both being mycorrhizal and producing truffles) is a fascinating evolutionary question that requires further study. 

By plotting gyromitrin production on the phylogenomic tree, I was also able to better understand its likely evolutionary history. Figure 3 shows that gyromitrin is absent from all genera except Gyromitra and Piscidiscina, distantly related genera in different tribes. It's feasible that gyromitrin evolved in the last common ancestor of Discinaceae and was then lost multiple times, resulting in this phylogenetically discontinuous distribution. However, more likely, gyromitrin was horizontally transferred between the two genera (the direction of transfer being unknown) or that gyromitrin production convergently evolved in Gyromitra and Piscidiscina. Research is ongoing to identify the genes responsible for gyromitrin biosynthesis, which will hopefully elucidate the reasons why gyromitrin has this peculiar distribution. 

Figure 3. Discinaceae time divergence estimation, modeling of AA9 CAZyme family evolutionary history, gyromitrin status, and genome traits. Branches are colored according to the AA9 CAZyme family count inferred through time with CAFE5. The background color of the tips of the tree indicates gyromitrin status (red: tested positive; blue: gyromitrin not detected; no background color: not tested). Genome size, average GC content, total number of genes sized by number of transposable elements, number of CAZyme genes per class, and number of biosynthesis gene clusters predicted by antiSMASH are shown for each sample. The dotted vertical lines indicate mean values.

So what do we call them? 

With these taxonomic changes, we are well positioned to articulate what to call Discinaceae fungi in terms of common names. Are "false morels" any Discinaceae species, just the toxic Gyromitra genus, or is this name broadly applied to any stipitate Pezizales fungus and thus of no use? Do we refer to Discinaceae species collectively as "lorchels"? Maybe the nontoxic, edible Discinacaeae species such as Neogyromitra brunnea, Neogyromitra caroliniana, Maublancomyces montanus, and Maublancomyces korfii should be called "lorchels" and the toxic Gyromitra species "false morels"? What do you think? Let me know in the comments!

References

Dirks AC, Methven AS, Miller AN, Orozco-Quime M, Maurice S, Bonito G, Wyk J, Ahrendt S, Kuo A, Andreopoulos W, Riley R, Lipzen A, Chovatia M, Savage E, Barry K, Grigoriev I, Bradshaw A, Martin F, Arnold A, James TY. 2025. Phylogenomic insights into the taxonomy, ecology, and mating systems of the lorchel family Discinaceae (Pezizales, Ascomycota). Molecular Phylogenetics and Evolution. In press. 

Miller AN, Yoon A, Gulden G, Stensholt Ø, Van Vooren N, Ohenoja E, Methven AS. 2020. Studies in Gyromitra I: the Gyromitra gigas species complex. Mycol Progress 19:1459–1473.

Miller AN, Dirks AC, Filippova N, Popov E, Methven AS. 2022. Studies in Gyromitra II: cryptic speciation in the Gyromitra gigas species complex; rediscovery of G. ussuriensis and G. americanigigas sp. nov. Mycol Progress 21:81.

Miller AN, Dirks AC, Van Vooren N, Methven AS. 2025. Studies in Gyromitra III: the Gyromitra brunnea lineage including G. japonica sp. nov. Mycol Progress​. In press.