Global phylogeny of the Shiitake mushroom and related Lentinula species uncovers novel diversity and suggests an origin in the Neotropics

Lentinula (Basidiomycota, Agaricales) includes the most widely cultivated mushroom in the world, Lentinula edodes, also known as shiitake (Japanese) or xiang-gu (Chinese). At present, nine species are recognized in the genus, based on morphology, mating criteria, and geographic distribution. However, analyses of internal transcribed spacers (ITS) of ribosomal RNA genes have suggested that there are cryptic lineages. We analyzed a global-scale phylogenetic dataset from 325 Lentinula individuals from 24 countries in Asia-Australasia and the Americas plus Madagascar, with 325 sequences of ITS, 80 LSU sequences, and 111 sequences of translation elongation factor (tef1-α) genes. We recovered 15 independent lineages (Groups 1–15) that may correspond to species. Lineages in Asia-Australasia (Groups 1–5) and the Americas plus Madagascar (Groups 6–15) formed sister clades. Four lineages are represented only by sequences from single individuals and require further molecular sampling, including L. aff. raphanica (Group 7), L. ixodes (Group 8), L. boryana (Group 12), and L. aff. aciculospora (Group 14). Groups 1 and 5 are here referred to L. edodes and L. aff. edodes, respectively. However, these groups most likely represent the same species and are only recognized as (unsupported) monophyletic lineages by maximum likelihood analyses of ITS alone. Other putative species resolved here include L. lateritia (Group 2), L. novae-zelandieae (Group 3), L. aff. lateritia (Group 4), L. raphanica (Group 6), L. aff. detonsa (Group 9), L. detonsa (Group 10), L. guzmanii sp. nov. (Group 11), L. aciculospora (Group 13), and L. madagasikarensis (Group 15). Groups 9–12 represent the “L. boryana complex”. Molecular clock and historical biogeographic analyses suggest that the most recent common ancestor (MRCA) of Lentinula can be placed in the middle Oligocene, ca. 30 million years ago (Ma), and had a likely presence in neotropical America. The MRCA of Lentinula in the Americas and Madagascar lived ca. 22 Ma in the Neotropics and the MRCA of Lentinula in Asia-Australasia lived ca. 6 Ma in Oceania. Given the current knowledge about plate tectonics and paleoclimatic models of the last 30 Myr, our phylogenetic hypothesis suggests that the extant distribution of Lentinula is likely to have arisen, in large part, due to long-distance dispersal. Lentinula collections include at least four dubious taxa that need further taxonomic studies: L. reticeps from the USA (Ohio); L. guarapiensis from Paraguay; Lentinus puiggarii from Brazil (São Paulo); and “L. platinedodes” from Vietnam. Approximately ten of the fifteen Groups are reported on Fagaceae, which appears to be the ancestral substrate of Lentinula.