Genome assembly of M. spongiola and comparative genomics of the genus Morchella provide initial insights into taxonomy and adaptive evolution.

Morchella spongiola is a highly prized mushroom for its delicious flavor and medical value and is one of the most flourishing, representative, and dominant macrofungi in the Qilian Mountains of the Qinghai-Tibet Plateau subkingdoms (QTPs). However, the understanding of M. spongiola remains largely unknown, and its taxonomy is ambiguous. In this study, we redescribed a unique species of M. spongiola, i.e., micromorphology, molecular data, genomics, and comparative genomics, and the historical biogeography of M. spongiola were estimated for 182 single-copy homologous genes. A high-quality chromosome-level reference genome of M. spongiola M12-10 was obtained by combining PacBio HiFi data and Illumina sequencing technologies; it was approximately 57.1 Mb (contig N50 of 18.14 Mb) and contained 9775 protein-coding genes. Comparative genome analysis revealed considerable conservation and unique characteristics between M. spongiola M12-10 and 32 other Morchella species. Molecular phylogenetic analysis indicated that M. spongiola M12-10 is similar to the M. prava/Mes-7 present in sandy soil near rivers, differentiating from black morels ~ 43.06 Mya (million years ago), and diverged from M. parva/Mes-7 at approximately 12.85 Mya (in the Miocene epoch), which is closely related to the geological activities in the QTPs (in the Neogene). Therefore, M. spongiola is a unique species rather than a synonym of M. vulgaris/Mes-5, which has a distinctive grey-brown sponge-like ascomata. This genome of M. spongiola M12-10 is the first published genome sequence of the species in the genus Morchella from the QTPs, which could aid future studies on functional gene identification, germplasm resource management, and molecular breeding efforts, as well as evolutionary studies on the Morchella taxon in the QTPs.

Distribution of rhizosphere fungi of Kobresia humilis on the Qinghai-Tibet Plateau.

Kobresia humilis is a major species in the alpine meadow communities of the Qinghai-Tibet Plateau (QTP); it plays a crucial role in maintaining the ecological balance of these meadows. Nevertheless, little is known about the rhizosphere fungi associated with K. humilis on the Qinghai Tibet Plateau. In this study, we used Illumina Miseq to investigate the fungal diversity, community structure, and ecological types in the root and rhizosphere soil of K. humilis across eight areas on the QTP and analyzed the correlation between rhizosphere fungi of K. humilis and environmental factors. A total of 19,423 and 25,101 operational taxonomic units (OTUs) were obtained from the roots and rhizosphere soil of K. humilis. These were classified into seven phyla, 25 classes, 68 orders, 138 families, and 316 genera in the roots, and nine phyla, 31 classes, 76 orders, 152 families, and 407 genera in the rhizosphere soil. There were 435 and 415 core OTUs identified in root and rhizosphere soil, respectively, which were categorized into 68 and 59 genera, respectively, with 25 shared genera. Among them, the genera with a relative abundance >1% included Mortierella, Microscypha, Floccularia, Cistella, Gibberella, and Pilidium. Compared with the rhizosphere soil, the roots showed five differing fungal community characteristics, as well as differences in ecological type, and in the main influencing environmental factors. First, the diversity, abundance, and total number of OTUs in the rhizosphere soil of K. humilis were higher than for the endophytic fungi in the roots by 11.85%, 9.85%, and 22.62%, respectively. The composition and diversity of fungal communities also differed between the eight areas. Second, although saprotroph-symbiotrophs were the main ecological types in both roots and rhizosphere soil; there were 62.62% fewer pathotrophs in roots compared to the rhizosphere soil. Thirdly, at the higher altitude sites (3,900-4,410 m), the proportion of pathotroph fungi in K. humilis was found to be lower than at the lower altitude sites (3,200-3,690 m). Fourthly, metacommunity-scale network analysis showed that during the long-term evolutionary process, ZK (EICZK = 1) and HY (EICHY = 1) were critical sites for development of the fungal community structure in the roots and rhizosphere soil of K. humilis, respectively. Fifthly, canonical correspondence analysis (CCA) showed that key driving factors in relation to the fungal community were longitude (R2 = 0.5410) for the root community and pH (R2 = 0.5226) for the rhizosphere soil community. In summary, these results show that K. humilis fungal communities are significantly different in the root and rhizosphere soil and at the eight areas investigated, indicating that roots select for specific microorganisms in the soil. This is the first time that the fungal distribution of K. humilis on the QTP in relation to long-term evolutionary processes has been investigated. These findings are critical for determining the effects of environmental variables on K. humilis fungal communities and could be valuable when developing guidance for ecological restoration and sustainable utilization of the biological resources of the QTP.

Corrigendum: Out of the Qinghai-Tibetan plateau: origin, evolution and historical biogeography of Morchella (both Elata and Esculenta clades).

[This corrects the article DOI: 10.3389/fmicb.2022.1078663.].

Out of the Qinghai-Tibetan plateau: Origin, evolution and historical biogeography of Morchella (both Elata and Esculenta clades).

Introduction: Morchella has become a research hotspot because of its wide distribution, delicious taste, and phenotypic plasticity. The Qinghai-Tibet Plateau subkingdoms (QTPs) are known as the cradle of Ice age biodiversity. However, the diversity of Morchella in the QTPs has been poorly investigated, especially in phylogenetic diversity, origin, and biogeography. Methods: The genealogical concordance phylogenetic species recognition (GCPSR, based on Bayesian evolutionary analysis using sequences from the internal transcribed spacer (ITS), nuclear large subunit rDNA (nrLSU), translation elongation factor 1-α (EF1-α), and the largest and second largest subunits of RNA polymerase II (RPB1 and RPB2)), differentiation time estimation, and ancestral region reconstruction were used to infer Morchella's phylogenetic relationships and historical biogeography in the QTPs. Results: Firstly, a total of 18 Morchella phylogenetic species are recognized in the QTPs, including 10 Elata clades and 8 Esculenta clades of 216 individuals Secondly, the divergences of the 18 phylogenetic species were 50.24-4.20 Mya (Eocene-Pliocene), which was closely related to the geological activities in the QTPs. Furthermore, the ancestor of Morchella probably originated in the Northern regions (Qilian Shan, Elata cade) and southwestern regions (Shangri-La, Esculenta clade) of QTPs and might have migrated from North America (Rufobrunnea clade) via Beringian Land Bridge (BLB) and Long-Distance Dispersal (LDD) expansions during the Late Cretaceous. Moreover, as the cradle of species origin and diversity, the fungi species in the QTPs have spread out and diffused to Eurasia and South Africa starting in the Paleogene Period. Conclusion: This is the first report that Esculenta and Elata clade of Morchella originated from the QTPs because of orogenic, and rapid differentiation of fungi is strongly linked to geological uplift movement and refuge in marginal areas of the QTPs. Our findings contribute to increasing the diversity of Morchella and offer more evidence for the origin theory of the QTPs.