Transcriptome of different fruiting stages in the cultivated mushroom Cyclocybe aegerita suggests a complex regulation of fruiting and reveals enzymes putatively involved in fungal oxylipin biosynthesis

Abstract

Background Cyclocybe aegerita (syn. Agrocybe aegerita) is a commercially cultivated mushroom. Its archetypal agaric morphology and its ability to undergo its whole life cycle under laboratory conditions makes this fungus a well-suited model for studying fruiting body (basidiome, basidiocarp) development. To elucidate the so far barely understood biosynthesis of fungal volatiles, alterations in the transcriptome during different developmental stages of C. aegerita were analyzed and combined with changes in the volatile profile during its different fruiting stages. Results A transcriptomic study at seven points in time during fruiting body development of C. aegerita with seven mycelial and five fruiting body stages was conducted. Differential gene expression was observed for genes involved in fungal fruiting body formation showing interesting transcriptional patterns and correlations of these fruiting-related genes with the developmental stages. Combining transcriptome and volatilome data, enzymes putatively involved in the biosynthesis of C8 oxylipins in C. aegerita including lipoxygenases (LOXs), dioxygenases (DOXs), hydroperoxide lyases (HPLs), alcohol dehydrogenases (ADHs) and ene-reductases could be identified. Furthermore, we were able to localize the mycelium as the main source for sesquiterpenes predominant during sporulation in the headspace of C. aegerita cultures. In contrast, changes in the C8 profile detected in late stages of development are probably due to the activity of enzymes located in the fruiting bodies. Conclusions In this study, the combination of volatilome and transcriptome data of C. aegerita revealed interesting candidates both for functional genetics-based analysis of fruiting-related genes and for prospective enzyme characterization studies to further elucidate the so far barely understood biosynthesis of fungal C8 oxylipins.

Biotransformation of [U-13C]linoleic acid suggests two independent ketonic- and aldehydic cycles within C8-oxylipin biosynthesis in Cyclocybe aegerita (V. Brig.) Vizzini

“…4). A recently published study by Orban et al, (2021) investigating the transcriptome of different fruiting stages in C. aegerita supports our hypothesis of distinct pathways within the C8-oxylipin biosynthesis. By combining transcriptome and volatilome data, different sets of putative LOX, DOX, ER and ADH genes potentially involved in oct-1-en-3-ol (6) and octan-3-one (8) biosynthesis could be identified.…”

“…However, no coherence between 9-HPOD and certain C8-oxylipins exists, although it is well known that fungi of the phylum Basidiomycota harbour various LOX in their genomes. Additionally, it was shown that gene expression levels highly depend on the developmental stages (Orban et al, 2021;Tasaki et al, 2019). Few of the known LOX genes from P. ostreatus, P. sapidus, P. dryinus, P. sajor-caju and C. aegerita have been cloned, heterologously expressed and tested for their specific activity towards linoleic acid (Karrer & Rühl 2019;Karrer et al, 2021a, b;Kuribayashi et al, 2002;Leonhardt et al, 2013;Plagemann et al, 2013).…”

The Pacific Tree-Parasitic Fungus Cyclocybe parasitica Exhibits Monokaryotic Fruiting, Showing Phenotypes Known from Bracket Fungi and from Cyclocybe aegerita

“…Potentially, this may just relate to phenotypic variability of some extent that such structures can exhibit, which may also be found in C. aegerita. Alternatively, this variability may relate to some deviant morphogenetic signaling exhibited by fruiting-related genes (FRGs) of C. parasitica over the one by the FRGs of C. aegerita, some of which have been annotated in the C. aegerita genome [16,31]. This could be revealed by comparative transcriptomic studies on these specimens in the future.…”

“…This way, one might obtain molecular evidence on the level of FRG expression at least with C. parasitica in how far one should consider such 'stromatic proliferations' as a dead end of multicellular development as proclaimed previously [20,24]. For both monokaryotic fruiting phenotypes, the 'stroma type' one in C. parasitica and the 'elongated' ones by C. aegerita and C. parasitica, a hypothetical lack of Dst1 [31][32][33][34] activity might lead to a block in cap tissue differentiation [16]. Further tissue proliferation, although in a polar way in the elongated types versus a non-directional one in stroma type structures, may then lead to the further increase in size of both types of structures over basidiome initials.…”

Transcriptional response of mushrooms to artificial sun exposure

“…Also, given the differing molecular biology of mushrooms during fructification (Orban et al, 2021), and their more direct exposure to abiotic stress, knowledge based on the mycelium seems of limited significance for understanding how mushrooms would react.…”