Volume 13 - 2022 - Issue 2 (SI Fungal Evolution)


1. On the evolution of ectomycorrhizal fungi

Authors: Ryberg M, Kalsoom Khan F, Sánchez-García M

Recieved: 04 April 2022, Accepted: 09 June 2022, Published: 29 December 2022

Ectomycorrhiza is a symbiosis between plants and fungi. It is the type of mycorrhiza that involves the highest number of fungal species and it involves many stand forming tree species. As the ectomycorrhizal trees include the majority of all the worlds tree stems, it has a huge impact on the nutrient and carbon cycles. Here, we review the evolution of ectomycorrhiza within fungi. It has evolved many times in different clades. The rate of evolution has not varied much through time, but has varied between clades. Thus, no time period seems to have been more important than others for the evolution of new ectomycorrhizal lineages. It seems like once becoming ectomycorrhizal the probability of becoming saprotrophic again is very low. Despite the large change in nutritional strategy, it does not seem like becoming ectomycorrhizal is a key innovation that by itself gives a high rate of speciation and/or adaptive radiations. Genomic studies have shown little commonality in the evolution of ectomycorrhiza except for the loss of decay genes, expansions of transposable elements, and expansions of Mycorrhiza-induced Small Secreted Proteins. Although this fits with a biotrophic lifestyle and possibly an elevated rate of genome evolution, it does not hint at any other functional similarity. As ectomycorrhizal lineages have evolved many times during the evolutionary history of fungi, and it is not unlikely that there are ectomycorrhizal lineages that have gone extinct, the available functions provided by ectomycorrhiza to plants may have varied over time.

Keywords: Evolutionary analysis – Evolutionary transition – Genome evolution – Key innovation – Symbiosis

 

2. Phylogenetic diversity and affiliation of tropical African ectomycorrhizal fungi

Authors: Houdanon RD, Furneaux B, Yorou NS, Ryberg M

Recieved: 01 April 2022, Accepted: 16 June 2022, Published: 29 December 2022

Ectomycorrhizal fungi form a mutualistic symbiosis with plant roots, and are key for nutrient cycling in many ecosystems. Here we study the ectomycorrhizal fungal communities in the Ouémé Supérieur reserve forest in Benin (West Africa). We use phylogenetic methods to test if the species from the study site are closer to other tropical African species than to species from other regions. The Ouémé Supérieur community was represented by nine Operational Taxonomic Units in Amanitaceae, one in Boletaceae, one in Cantharellaceae, one in Cortinariaceae, two in Inocybaceae, fourteen in Russulaceae and three in Sclerodermataceae. Of these thirty-one Operational Taxonomic Units, twenty had no record in other areas, and unique Operational Taxonomic Units were found in all families except Boletaceae and Sclerodermataceae. The added phylogenetic diversity from these unique Operational Taxonomic Units tended to be higher than expected by chance in all families but Cantharellaceae. The Operational Taxonomic Units are generally fairly distinct and contribute proportionally to the phylogenetic diversity, reflecting that they do not only represent recently diverging species, but also more divergent lineages. Our analyses of the different families show that the communities of Amanitaceae, Inocybaceae, and Russulaceae are more closely related to the general Afrotropic community than expected by chance, at least measured as the nearest taxon distance. The lack of significant patterns in the other families may be due to lack of power, but the wide distribution of many Operational Taxonomic Units suggests that there are not likely to be strong patterns. It is only for Russulaceae that there is a significant pattern in the Ouémé Supérieur ectomycorrhizal fungal communities at a regional scale, with the Operational Taxonomic Units being less closely related than expected. At a global scale the patterns seem to reflect the overall distribution of the Afrotropic ectomycorrhizal fungal community. The phylogenetic patterns in the Afrotropic communities differ between families, from clustered to no clear pattern to over-dispersed measured as mean average phylogenetic distance. Each family seems to have its own biogeographic history, and there is no clear pattern for the ectomycorrhizal fungal community at large. Despite the lack of comprehensive taxonomic work to identify fungi in a region, it is still possible to draw some conclusions on their diversity using molecular phylogenetic methods. However, limited success in getting good sequence data from specimens, probably due to preservation issues in the field, and the lack of well annotated molecular data from many regions limit the power of these inferences.

Keywords: community assemblage – mycorrhizal fungi – Operational Taxonomic Units – phylogeny – west Africa

 

3. Evolutionary relationship and a novel method of efficient identification of Lentinula edodes cultivars in China

Authors: Ling YY, Zhang MZ, Ling ZL, Cao B, Wu XP, Peng H, Wang ZR, Zhao RL

Recieved: 24 February 2022, Accepted: 18 July 2022, Published: 29 December 2022

Lentinula edodes (shiitake in Japanese, xiang-gu in Chinese) is the most productive mushroom in China, and there are more than 500 cultivars names. However, the traditional identification of mushroom cultivars can be challenging due to the problems of the heavy workload, insufficient accuracy and low reproducibility, which greatly affect the industrial development and germplasm innovation process. In this study, we developed and illustrated a methodological and technical system for the identification of L. edodes cultivars and for detecting their evolutionary relationship based on the multiple nucleotide polymorphism marker (MNP) sequences. Specifically, 501 universal MNP markers were screened based on the whole-genome resequencing data of 188 L. edodes strains mainly from China (25 of which were self-tested). The following analysis of detection rate, repeatability rate and accuracy rate showed those MNP markers are satisfactory with 94.4%, 99.92%, and 99.96% respectively. This method of multiplex PCR amplification and high-sequencing resulted in the construction of an MNP sequence library of L. edodes. On this basis, 187 MNP markers were further screened as core MNP markers. An ML phylogenetic tree of 162 wild strains and 78 cultivars was generated by using core MNP sequences, revealing all cultivars can be separated into 24 distinct evolutionary pedigrees. The genetic similarity (GS) value between different pedigrees and all cultivars tested showed that a broad library of pedigrees had GS values less than or equal to 94%, and the different cultivars within the same pedigrees had GS values range of 94-99.5%. The combination of all results indicated that most cultivars of L. edodes were originally from the Northeast Asia except the only cultivar L. edodes from south China, but there has a serious homogenization of L. edodes germplasms in China. In this study, we established a genealogical map of L. edodes cultivars in China, a standard library of MNP markers, and a rapid experimental procedure for genealogical and cultivar identification, which lays out a highly reliable platform for encouraging original innovation and modified cultivar innovation. Finally, a brief prospect for MNP markers identification of mushroom cultivars is addressed.

Keywords: edible mushroom – evolution – molecular marker – multiple nucleotide polymorphism – shiitake

 

4. Large-scale genome investigations reveal insights into domestication of cultivated mushrooms

Authors: Fu YP, Dai YT, Chethana KWT, Li ZH, Sun L, Li CT, Yu HL, Yang RH, Tan Q, Bao DP, Deng YJ, Wang SX, Wang YF, Tian FH, Qi LL, Shu LL, Jia PS, Chen LC, Chen MY, Hu QX, Tan H, Song TT, Zhang ZW, Bonito G, Zervakis GI, Xiao SJ, Hyde KD, Li Y, Yuan XH

Recieved: 22 April 2022, Accepted: 19 August 2022, Published: 29 December 2022

Domestication and cultivation of edible and medicinal mushrooms are ongoing ~1,400-year-old evolutionary experiments. There are roughly 55 commercially cultivated mushrooms worldwide; however, genomes for many species are lacking, as is our understanding of mushroom domestication. In this work, 22 high-quality reference genomes, along with 63 transcriptome and 381 re-sequencing data, were reported for the first time. Combined with public genome resources, an integrated omics database (MushDB, http://mushroomomics.com) were constructed including 50 reference genomes, 265 transcriptome and 621 whole-genome re-sequencing data, covering ~90% of the worldwide commercially cultivated mushroom species. Using multi-omics data in MushDB, whole-genome variations of the representative wild and cultivated populations were used for selective sweep analysis to identify putative functional genes contributing to the mushroom domestication. Key genes in the starch and sucrose metabolism and mitogen-activated protein kinase signaling pathway, such as chb1, cdc24 and hog1, were putatively selected in Auricularia cornea, Lentinula edodes, Pleurotus eryngii and Pleurotus tuoliensis, indicating those genes might play important roles during mushroom domestications. The function of hog1 in the low temperature stimulation adaptation and short growth period in cultivation environment, which could facilitate the successful domestication, was validated using CRISPR/Cas9 system. Our work offers valuable and abundant omics open resource for wide research communities and lays solid foundations for multi-purposes in mushroom evolution, genetics, and breeding studies.

Keywords: database – domestication – genome – multi-omics – mushroom

 

5. Comparative genomics provides new insights into the evolution of Colletotrichum

Authors: Chen YP, Wu T, Tian WH, Ilyukhin E, Hyde KD, Maharachchikumbura SSN

Recieved: 14 July 2022, Accepted: 21 September 2022, Published: 29 December 2022

Colletotrichum is an economically important pathogen with a worldwide distribution associated with a wide range of plant hosts. Characterization of the genomic profiles of Colletotrichum can generate new insights to understand its speciation, diversity, and pathogenicity potential. Although some genomic studies on this genus have been reported, a systematic comparative genomic analysis of the genus has so far been lacking. In this study, we first compared genome completeness generated by second- and third-generation sequencing platforms and confirmed the effectiveness of second-generation sequencing techniques for genomic studies. We then integrated the taxonomic concept of Colletotrichum species complexes into the comparative genomic analysis and depicted the genomic features of 102 Colletotrichum genomes from 39 species across ten species complexes and two singletons. Genome sizes of Colletotrichum species vary tremendously (44.15–109.66 Mb), and the average genome sizes of species complexes are significantly different. Repetitive sequences are the key drivers for genome size and GC content variation. The number of predicted genes of each genome (10,354–17,809) is positively correlated to the size of non-repeat genome sequences. Phylogenetically close strains consist of similar composition of secretomes, however, the number of major components is significantly different between different species complexes. The C. gloeosporioides species complex possessed the most abundant CAZymes, which may be responsible for its diverse distribution and higher pathogenicity. A total of 7,971 putative SMGCs covering 20 types were detected in these genomes, suggesting their immense biosynthetic potential to produce natural products. We further constructed a genome-scale TimeTree of Colletotrichum and investigated the evolution of gene families. The result suggested that gene gain and loss are both important for environmental adaption but less useful in delineating species complexes. Our study characterized the genomes of Colletotrichum species from different perspectives, providing insights into the genomic evolution of Colletotrichum species. 

Keywords: CAZymes – Divergence time – Gene family – Pathogenic fungi – Secondary metabolic gene cluster – Secretome – Sordariomycetes – Species complex

 

6. Fossil Tetraploa redefinition and potential contribution of dark pigments for the preservation of its spores in the fossil record

Authors: Nuñez Otaño NB, Bianchinotti MV, Romero IC, Perez Pincheira E, Saxena RK, Saparrat MCN

Recieved: 18 October 2022, Accepted: 23 December 2022, Published: 29 December 2022

The establishment of affinities of fossil fungal spores with extant fungal taxa based mainly on the detailed analysis of morphological traits is difficult. Thus, it is necessary to use mycological terms to properly describe fossil fungi. In this work, we transfer five species of Frasnacritetrus Taugourd. (1968) to Tetraploa Berk. & Broome (1850) because the spores of the fossil and extant species share the same morphological traits. Here, we also discuss how dark pigments of extant spores of Tetraploa are synthesized to assess their potential contribution to the preservation of these diaspores in the fossil record, including their role in the fossilization process. In this work, we conclude that Frasnacritetrus should be considered a synonym of Tetraploa. Our results also shed light on how melanins have played a role in the preservation of fungal spores and other remains in the fossil record to thus, 1) understand how different burial histories and thermal maturation influenced long-term melanin survival, 2) to study the evolution of fungi lineages such as Tetraploa, and 3) to assess how fungal melanins can be used as biomarkers for palaeoecological purposes.

Keywords: Mycopalynology – Melanins – Nearest-living-relative – Non-pollen palynomorphs – Paleomycology – Post-mortem polymerization

 

7. Evolutionary relationships and allied species of Pyronemataceae, with segregation of the novel family Pyropyxidaceae

Authors: Zeng M, Gentekaki E, Zeng XY, Tian Q, Zhao Q, Hyde KD

Recieved: 20 December 2022, Accepted: 28 December 2022, Published: 29 December 2022

Pyronemataceae is the largest family within Pezizomycetes, members of which are distinguished by the shape and color of apothecia, the shape and ornamentation of ascospores, and the presence of carotenoids. Within Pyronemataceae, the Otidea lineage was previously elevated to the family level based on multiple gene analyses. However, this was controversial as the family was embedded in Pyronemataceae sensu stricto redefined by Hansen et al. Herein, we re-elevate the Otidea lineage to Otideaceae at the family rank level. Meanwhile, using a combination of morphology, phylogeny and divergence times estimates, we propose the new family Pyropyxidaceae to accommodate the Pyropyxis lineage containing Jafnea, Micronematobotrys, Pyropyxis, and Smardaea. The Pyropyxis lineage is phylogenetically distinct and branches off Otideaceae and the rest of Pyronemataceae sensu stricto. The monophyly of Otideaceae and Pyropyxidaceae has maximum statistical support. These two families have specific morphological features that set them apart from the rest of Pyronemataceae sensu stricto. Pyropyxidaceae has short hyphoid or moniliform hairs, while Otideaceae has abundant tomentum on the basal of apothecia. Both families lack true ascomatal hairs and carotenoids. Divergence times estimates place the crown of Pyropyxidaceae split at 141 Mya in the Early Cretaceous. The ancestral character state of ascomata in Pyronemataceae, Pyropyxidaceae and Otideaceae was the apothecium represented by epigeous taxa. Within Pyronemataceae, the hypogeous ascomata independently arose at least twice in distantly related lineages at 99 and 31 Mya. Moreover, cleistothecia and gymnothecia independently arose only once at approximately 38 Mya. Besides, we collected 37 allied collections of Pyronemataceae sensu stricto, including six new species, viz., Melastiza verruculosa, Otidea guttulata, O. macrospora, O. ovalispora, O. subleporina and Scutellinia verruculosa. All new species are introduced based on morphological characters and phylogeny.

Keywords: 6 new species ‒ 1 new family ‒ Pezizales ‒ taxonomy ‒ evolution

 

8. Diversity, molecular dating and ancestral characters state reconstruction of entomopathogenic fungi in Hypocreales

Authors: Wei DP, Gentekaki E, Wanasinghe DN, Tang SM, Hyde KD

Recieved: 22 December 2022, Accepted: 28 December 2022, Published: 29 December 2022

Hypocreales (Sordariomycetes, Ascomycota) is a highly diversified order, with more than 1000 entomopathogenic species being reported in Clavicipitaceae, Cordycipitaceae, Ophiocordycipitaceae and Polycephalomycetaceae. Taxa in these families form intimate associations with members of up to 13 orders of Insecta and other arthropods. Their variable morphological characteristics along with the host affiliations have played important roles in the classification of entomopathogenic species. However, it is still unclear whether these morphological characteristics are informative at the family, genus or species level in a phylogenetic context. This study focuses on entomopathogenic taxa collected from Thailand and Southwest China. Thirty-six species belonging to the above four families were identified using morphology and phylogeny inferred from combined data of LSU-SSU-5.8S-tef1-rpb1-rpb2 sequences. Among them, Pleurocordyceps ophiocordycipiticola is a new species. Divergence time estimates indicated the crown age of Hypocreales at 200 Mya, while that of Clavicipitaceae was at 107 Mya, Cordycipitaceae at 129 Mya, Ophiocordycipitacae at 121 Mya and Polycephalomycetaceae at 74 Mya. Based on ancestral character state reconstruction, the ancestral ecologies of Clavicipitaceae, Ophiocordycipitaceae and Polycephalomycetaceae were animal-based, while that of Cordycipitacae was fungi-based. Multiple interkingdom jumps occurred in all entomopathogenic families. Mapping of morphological characters on the phylogeny identified cases of association of perithecial arrangement and stromal texture. Ascospore and secondary ascospores morphologies were not informative at genus and family level classifications. Expanding collections to additional hosts and environments will assist towards further understanding the diversity and ecology of hypocrealean entomopathogens. 

Keywords: 1 new species – China – Evolution – Phylogeny – Taxonomy – Thailand

 

9. Special Issue: Fungal Evolution, in honour of the Academician Professor Yu Li’s 80th Birthday

Authors: Hyde Kevin David, Tolgor Bau, Yongping Fu, Liangcheng Chen, Shijun Xiao

Recieved: 09 January 2023, Accepted: 12 January 2023, Published: 12 January 2023

Keywords:

 

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Mycosphere publishes reviews, research articles, methodology papers, taxonomic works such as monographs, which are relevant to fungal biology, including lichens. The official journal language is English.

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