Armillaria mellea Symbiosis Drives Metabolomic and Transcriptomic Changes in Polyporus umbellatus Sclerotia

Abstract

Sclerotia, the medicinal part of Polyporus umbellatus, play important roles in diuresis and renal protection, with steroids and polysaccharides as the main active ingredients. The sclerotia grow and develop only after symbiosis with Armillaria sp. In this study, a systematic metabolomics based on non-targeted UPLC-MS method was carried out between the infected part of the separated cavity wall of the sclerotia (QR) and the uninfected part (the control group, CK) to find and identify differential metabolites. The biosynthetic pathway of characteristic steroids in sclerotia of P. umbellatus was deduced and the content of ergosterol, polyporusterone A and B in the QR and CK groups were detected with the High Performance Liquid Chromatography (HPLC). Furthermore, the expression patterns of putative genes associated with steroid biosynthesis pathway were also performed with quantitative real-time PCR. The results showed that a total of 258 metabolites originated from fungi with the fragmentation score more than 45 and high resolution mass were identified, based on UPLC-MS metabolomic analysis, and there were 118 differentially expressed metabolites (DEMs) between both groups. The metabolic pathways indicated that steroids, fatty acid and carbohydrate were active and enriched during P. umbellatus sclerotia infected by A. mellea. The content of ergosterol, polyporusterone A and B in the QR group increased by 32.2, 75.0, and 20.0%, in comparison to that of the control group. The qRT-PCR analysis showed that series of enzymes including C-8 sterol isomerase (ERG2), sterol C-24 methyltransferase (ERG6) and sterol 22-desaturase (ERG5), which played important roles in the final steps of ergosterol biosynthesis, all presented up-regulated patterns in the QR group in P. umbellatus. The comprehensive metabolomic and transcriptomic information will contribute to further study concerning the mechanisms of P. umbellatus sclerotial formation infected by A. mellea in the future.

An exploration of mechanism of high quality and yield of Gastrodia elata Bl. f. glauca by the isolation, identification and evaluation of Armillaria

“…At present, over 40 species of Armillaria have been described in the world, some of which are serious tree pathogens, some have medicinal value, and some can coexist with G. elata Bl. for its cultivation and production [18][19][20]. There are 15 Armillaria species in China, of which eight are endemic to China [21].…”

Hallmarks of Comparative Transcriptome between Rhizomorphs and Hyphae of Armillaria sp. 541 Participating in Fungal Symbiosis with Emphasis on LysM Domains

“…As parasitic fungi, Armillaria can parasitize more than 500 tree species causing root rot, leading to potentially substantial economic losses [ 2 ]. Interestingly, Armillaria mellea , one of these fungi, has also been observed to establish a symbiotic relationship with the original plant of traditional Chinese medicine (TCM), such as Gastrodia elata (an orchid) and the fungus Polyporus umbellatus (sclerotia) [ 3 , 4 ]. Without Armillaria , G. elata could not grow at all [ 5 ], which would lead to over ten billion economic losses, as was the case with P. umbellatus.…”

“…In addition, rhizomorphs spread throughout the soil in search of nutrients derived from both decaying wood and living tree roots [ 11 , 12 ]. Importantly, the rhizomorphs of Armillaria have similarly been characterized as functional structures during the colonization of G. elata (Orchid) protocorm and P. umbellatus sclerotia [ 3 , 4 ]. Our previous studies indicated that metabolic pathways involved in steroids, etc., were active and enriched during the infection of P. umbellatus sclerotia by A. mellea by metabolic and transcriptomic analysis.…”

“…Our previous studies indicated that metabolic pathways involved in steroids, etc., were active and enriched during the infection of P. umbellatus sclerotia by A. mellea by metabolic and transcriptomic analysis. In comparison with the control group, the content of polyporusterone A, polyporusterone B and ergosterol in the infected sclerotia increased by 75.0%, 20.0% and 32.2%, respectively [ 4 ]. If the rhizomorph network of Armillaria linked with P. umbellatus is cut, the sclerotia will stop growing and developing [ 13 ].…”

Transcriptome analysis reveals the regulatory mode by which NAA promotes the growth of Armillaria gallica

“…elata digests the symbiotic Armillaria mellea ( A . mellea ) to provide its nutrition [ 1 – 3 ]. A .…”