Dual RNA-Seq Analysis of the Interaction Between Edible Fungus Morchella sextelata and Its Pathogenic Fungus Paecilomyces penicillatus Uncovers the Candidate Defense and Pathogenic Factors

Abstract

Morels (Morchella spp.) are economically important mushrooms cultivated in many countries. However, their production and quality are hindered by white mold disease because of Paecilomyces penicillatus infection. In this study, we aimed to understand the genetic mechanisms of interactions between P. penicillatus and Morchella. M. sextelata, the most prevalent species of Morchella in China, was inoculated with P. penicillatus; then, the expression profiles of both fungi were determined simultaneously at 3 and 6 days post-inoculation (dpi) using a dual RNA-Seq approach. A total of 460 and 313 differentially expressed genes (DEGs) were identified in P. penicillatus and M. sextelata, respectively. The CAZymes of β-glucanases and mannanases, as well as subtilase family, were upregulated in P. penicillatus, which might be involved in the degradation of M. sextelata cell walls. Chitin recognition protein, caffeine-induced death protein, and putative apoptosis-inducing protein were upregulated, while cyclin was downregulated in infected M. sextelata. This indicates that P. penicillatus could trigger programmed cell death in M. sextelata after infection. Laccase-2, tyrosinases, and cytochrome P450s were also upregulated in M. sextelata. The increased expression levels of these genes suggest that M. sextelata could detoxify the P. penicillatus toxins and also form a melanin barrier against P. penicillatus invasion. The potential pathogenic mechanisms of P. penicillatus on M. sextelata and the defense mechanisms of M. sextelata against P. penicillatus were well described.

Transcriptomic and Metabolomic Profiles Provide Insights into the Red-Stipe Symptom of Morel Fruiting Bodies

“…A gene ( TRINITY_DN14093_c0_g1 ) encoding for programmed cell death protein 6 was upregulated in the R group (log2 FC = 1.53; Supplementary Table S3 ). This was consistent with previous findings suggesting that P. penicillatus was suppressed by M. sextelata via programmed cell death [ 40 ]. At the same time, the GO term “oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen (GO:0016705)” was significantly enriched by the DEGs ( Supplementary Table S4 ).…”

“…Overall, 257 out of 748 DEGs and 175 out of 189 DAMs were enriched in the combined transcriptome and metabolome analysis ( Supplementary Tables S16 and S17 ). Compared to Morchella response to P. penicillatus , similarly determined using a dual RNA-Seq approach [ 40 ], “tryptophan metabolism (map00380)” and “pantothenate and CoA biosynthesis (map00770)” were also identified in our study. When compared to the Morchella fruiting bodies and mycelium metabolites based on widely targeted metabolomic analyses [ 29 ], only “glycerophospholipid metabolism (map00564)” was common in our study.…”

“…However, the function of this gene is unknown. Interestingly, genes encoding chitin recognition protein ( TRINITY_DN5661_c0_g1 ), an allergen Asp f 15 precursor ( TRINITY_DN13718_c0_g4 ), and cyclin-dependent protein kinase ( TRINITY_DN14130_c2_g15 ) were among the DEGs ( Supplementary Table S7 ), and they have been previously reported to be involved in immune responses of mushrooms to pathogenic fungi [ 40 ].…”

“…Lecanicillium aphanocladii [ 36 ] and Clonostachys rosea [ 61 ] are the causal agents of rot disease M. sextelata , and P. penicillatus causes the white mold disease [ 35 ]. M. sextelata defense mechanisms against P. penicillatus were studied by dual host-pathogen RNA-Seq analysis, and 313 DEGs were identified [ 40 ]. The results revealed that programmed cell death in M. sextelata was triggered by P. penicillatus infection via the upregulation of a chitin recognition protein, a caffeine-induced death protein, a putative apoptosis-inducing protein, and cyclin downregulation.…”

“…The genomic regions associated with dry-bubble resistance in A. bisporus were determined by quantitative trait loci (QTL) analysis of four traits related to resistance [ 39 ]. The genetic mechanisms of the interactions between M. sextelata and P. penicillatus, responsible for white mold disease in Morchella were studied using a dual RNA-Seq approach in both the host and the pathogen [ 40 ]. In infected M. sextelata , genes encoding for a chitin recognition protein, tyrosinases, a caffeine-induced death protein, Laccase-2, cytochrome P450s, and putative apoptosis-inducing proteins were upregulated, whereas cyclin was downregulated.…”