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Macrosynteny analysis between Lentinula edodes and Lentinula novae-zelandiae reveals signals of domestication in Lentinula edodes.

ABSTRACT: The basidiomycete fungus Lentinula novae-zelandiae is endemic to New Zealand and is a sister taxon to Lentinula edodes, the second most cultivated mushroom in the world. To explore the biology of this organism, a high-quality chromosome level reference genome of L. novae-zelandiae was produced. Macrosyntenic comparisons between the genome assembly of L. novae-zelandiae, L. edodes and a set of three genome assemblies of diverse species from the Agaricomycota reveal a high degree of macrosyntenic restructuring within L. edodes consistent with signal of domestication. These results show L. edodes has undergone significant genomic change during the course of its evolutionary history, likely a result of its cultivation and domestication over the last 1000 years.

SUBMITTER: Smith CA

PROVIDER: S-EPMC8110776 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Lentinula edodes is a popular, cultivated edible and medicinal mushroom. Lentinula edodes is susceptible to postharvest problems, such as gill browning, fruiting body softening, and lentinan degradation. We constructed a de novo assembly draft genome sequence and performed gene prediction for Lentinula edodesDe novo assembly was carried out using short reads from paired-end and mate-paired libraries and by using long reads by PacBio, resulting in a contig number of 1,951 and an N50 of 1 Mb. Furthermore, we predicted genes by Augustus using transcriptome sequencing (RNA-seq) data from the whole life cycle of Lentinula edodes, resulting in 12,959 predicted genes. This analysis revealed that Lentinula edodes lacks lignin peroxidase. To reveal genes involved in the loss of quality of Lentinula edodes postharvest fruiting bodies, transcriptome analysis was carried out using serial analysis of gene expression (SuperSAGE). This analysis revealed that many cell wall-related enzymes are upregulated after harvest, such as ?-1,3-1,6-glucan-degrading enzymes in glycoside hydrolase (GH) families GH5, GH16, GH30, GH55, and GH128, and thaumatin-like proteins. In addition, we found that several chitin-related genes are upregulated, such as putative chitinases in GH family 18, exochitinases in GH20, and a putative chitosanase in GH family 75. The results suggest that cell wall-degrading enzymes synergistically cooperate for rapid fruiting body autolysis. Many putative transcription factor genes were upregulated postharvest, such as genes containing high-mobility-group (HMG) domains and zinc finger domains. Several cell death-related proteins were also upregulated postharvest.IMPORTANCE Our data collectively suggest that there is a rapid fruiting body autolysis system in Lentinula edodes The genes for the loss of postharvest quality newly found in this research will be targets for the future breeding of strains that keep fresh longer than present strains. De novoLentinula edodes genome assembly data will be used for the construction of a complete Lentinula edodes chromosome map for future breeding.

Project description:Lentinula edodes, also known as Xiang'gu, is commonly eaten in cultures around the world. However, L. edodes is particularly susceptible to enrichment with heavy metals, particularly cadmium (Cd), which is toxic to human health. Understanding the molecular mechanism and mining key genes involved in Cd enrichment will facilitate genetic modification of L. edodes strains. Two L. edodes genotypes, Le4625 (with higher Cd enrichment capability) and Le4606 (with lower Cd enrichment capability) were used in this study. The Cd concentrations in the mycelia of the tested genotypes differed significantly after Cd (0.1 mg/L) exposure; and the Cd content in Le4625 (1.390 ± 0.098 mg/kg) was approximately three-fold that in Le4606 (0.440 ± 0.038 mg/kg) after 7 h of Cd exposure. A total of 24,592 transcripts were assessed by RNA-Seq to explore variance in Cd accumulation. Firstly, differentially expressed genes (DEGs) were analyzed separately following Cd exposure. In comparison with Ld4625, Ld4606 showed a greater number of Cd-induced changes in transcription. In Ld4606, DEGs following Cd exposure were associated with transmembrane transport, glutathione transfer and cytochrome P450, indicating that these genes could be involved in Cd resistance in L. edodes. Next, Le4606 and Le4625 were exposed to Cd, after which DEGs were identified to explore genetic factors affecting Cd accumulation. After Cd exposure, DEGs between Le4606 and Le4625 encoded proteins involved in multiple biological pathways, including transporters on the membrane, cell wall modification, oxidative stress response, translation, degradation, and signaling pathways. Cadmium enrichment in cells may activate MAPK signaling and the anti-oxidative stress response, which can subsequently alter signal transduction and the intracellular oxidation/reduction balance. Furthermore, several possible candidate genes involved in the Cd accumulation were identified, including the major facilitator superfamily genes, heat shock proteins, and laccase 11, a multicopper oxidase. This comparison of the transcriptomes of two L. edodes strains with different capacities for Cd accumulation provides valuable insight into the cultivation of mushrooms with less Cd enrichment and also serves as a reference for the construction of engineered strains for environmental pollution control.

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Macrosynteny analysis between Lentinula edodes and Lentinula novae-zelandiae reveals signals of domestication in Lentinula edodes.

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