Apothecial Ancestry, Evolution, and Re-Evolution in Thelebolales (Leotiomycetes, Fungi)

Abstract

Closed cleistothecia-like ascomata have repeatedly evolved in non-related perithecioid and apothecioid lineages of lichenized and non-lichenized Ascomycota. The evolution of a closed, darkly pigmented ascoma that protects asci and ascospores is conceived as either an adaptation to harsh environmental conditions or a specialized dispersal strategy. Species with closed ascomata have mostly lost sterile hymenial elements (paraphyses) and the capacity to actively discharge ascospores. The class Leotiomycetes, one of the most speciose classes of Ascomycota, is mainly apothecioid, paraphysate, and possesses active ascospore discharge. Lineages with closed ascomata, and their morphological variants, have evolved independently in several families, such as Erysiphaceae, Myxotrichaceae, Rutstroemiaceae, etc. Thelebolales is a distinctive order in the Leotiomycetes class. It has two widespread families (Thelebolaceae, Pseudeurotiaceae) with mostly closed ascomata, evanescent asci, and thus passively dispersed ascospores. Within the order, closed ascomata dominate and a great diversity of peridia have evolved as adaptations to different dispersal strategies. The type genus, Thelebolus, is an exceptional case of ascomatal evolution within the order. Its species are the most diverse in functional traits, encompassing species with closed ascomata and evanescent asci, and species with open ascomata, active ascospore discharge, and paraphyses. Open ascomata were previously suggested as the ancestral state in the genus, these ascomata depend on mammals and birds as dispersal agents. In this scheme, species with closed ascomata, a lack of paraphyses, and passive ascospore discharge exhibit derived traits that evolved in adaptation to cold ecosystems. Here, we used morphological and phylogenetic methods, as well as the reconstruction of ancestral traits for ascomatal type, asci dehiscence, the presence or absence of paraphyses, and ascospore features to explore evolution within Thelebolales. We demonstrate the apothecial ancestry in Thelebolales and propose a new hypothesis about the evolution of the open ascomata in Thelebolus, involving a process of re-evolution where the active dispersal of ascospores appears independently twice within the order. We propose a new family, Holwayaceae, within Thelebolales, that retains the phenotypic features exhibited by species of Thelebolus, i.e., pigmented capitate paraphyses and active asci discharge with an opening limitation ring.

Divergent Fungal Community Dynamics of Thuja sutchuenensis in Arid Environments

“…Interestingly, Group A had a relatively lower prevalence of plant pathogens compared to Groups B and C. Our LDA further highlighted the unique fungal assembly in Group A, particularly noting the significance of genera like Russula , Myxotrichaceae , and Sebacina . These findings are crucial as they point towards a specific ecological adaptation of the fungal community in low moisture conditions, which could be instrumental in supporting the resilience and health of plants [ 46 ]. The presence of specific fungal genera such as Myxotrichaceae , Thelephoraceae , and Tomentella in Group A underscores their potential importance in this unique ecological setting.…”

Additions to Thelebolales (Leotiomycetes, Ascomycota): Pseudogeomyces lindneri gen. et sp. nov. and Pseudogymnoascus campensis sp. nov.

“…The classification of Thelebolales remains controversial to date ( Ekanayaka et al 2019 ; Johnston et al 2019 ; Batista et al 2020 ; Quijada et al 2022 ). In contrast, however, the work of Ekanayaka et al (2019) contained more genera in Thelebolales ; therefore, we continued the phylogenetic analysis in Thelebolales , based on this study.…”

“…The order Thelebolales comprises important members of Leotiomycetes due to their diverse functions and potential applications ( Hassan et al 2017 ; Batista et al 2020 ). Thelebolales was established by Haeckel in 1894; however, the classification of this order remains controversial to date ( Ekanayaka et al 2019 ; Johnston et al 2019 ; Batista et al 2020 ; Quijada et al 2022 ). According to Johnston et al (2019) and Batista et al (2020) , Thelebolales comprises Pseudeurotiaceae and Thelebolaceae .…”

“…However, Ekanayaka et al (2019) reported that Pseudeurotiaceae was nested within Thelebolaceae ; thus, the former was regarded as a synonym of the latter. Recently, the work of Quijada et al (2022) showed that Thelebolaceae is monophyletic and valid, whereas Pseudeurotiaceae is polyphyletic and includes multiple clades and established the Holwayaceae (i.e. Alatospora - Miniancora clade, Ekanayaka et al (2019) ).…”

Cultivable fungal diversity in two karstic caves in Italy: under-investigated habitats as source of putative novel taxa

“…Two dataset consisting of nrITS and nrLSU Gelatinodiscaceae and in nrSSU, nrITS and nrLSU for Leotiales/Phacidiales, were assembled on the basis of BLASTn results and of the available phylogenetic studies focused on Leotiomycetes 40 , 41 , 50 , 51 . Reference sequences were obtained from GenBank.…”