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. 2020 Jan 24;15(1):e0227923.
doi: 10.1371/journal.pone.0227923. eCollection 2020.

Unusual Genome Expansion and Transcription Suppression in Ectomycorrhizal Tricholoma Matsutake by Insertions of Transposable Elements

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Free PMC article

Unusual Genome Expansion and Transcription Suppression in Ectomycorrhizal Tricholoma Matsutake by Insertions of Transposable Elements

Byoungnam Min et al. PLoS One. .
Free PMC article

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Abstract

Genome sequencing of Tricholoma matsutake revealed its unusually large size as 189.0 Mbp, which is a consequence of extraordinarily high transposable element (TE) content. We identified that 702 genes were surrounded by TEs, and 83.2% of these genes were not transcribed at any developmental stage. This observation indicated that the insertion of TEs alters the transcription of the genes neighboring these TEs. Repeat-induced point mutation, such as C to T hypermutation with a bias over "CpG" dinucleotides, was also recognized in this genome, representing a typical defense mechanism against TEs during evolution. Many transcription factor genes were activated in both the primordia and fruiting body stages, which indicates that many regulatory processes are shared during the developmental stages. Small secreted protein genes (<300 aa) were dominantly transcribed in the hyphae, where symbiotic interactions occur with the hosts. Comparative analysis with 37 Agaricomycetes genomes revealed that IstB-like domains (PF01695) were conserved across taxonomically diverse mycorrhizal genomes, where the T. matsutake genome contained four copies of this domain. Three of the IstB-like genes were overexpressed in the hyphae. Similar to other ectomycorrhizal genomes, the CAZyme gene set was reduced in T. matsutake, including losses in the glycoside hydrolase genes. The T. matsutake genome sequence provides insight into the causes and consequences of genome size inflation.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The genome sequencing of Tricholoma matsutake.
a. Genome size vs. gene number of all available fungal genomes in the NCBI. As of September 2019, 5,415 fungal genome assemblies had been deposited, and 1,618 had gene predictions. We used one genome per genus to draw the plot. Tricholoma matsutake is indicated by the arrow. b. Species tree of Tricholoma matsutake and 37 Agaricomycetes genomes. Only bootstrap values less than 100 are marked. The scale bar that represents the mean number of amino acid substitutions per site is shown. The Aspergillus nidulans genome (GenBank: GCF_000149205.2) was used as an outgroup. The branch to the outgroup was shortened for visualization purposes.
Fig 2
Fig 2. Repeat content in the Tricholoma matsutake and the 37 Agaricomycetes genomes.
RepeatModeler and RepeatMasker (http://www.repeatmasker.org) were used sequentially to predict repeat elements in the genomes.
Fig 3
Fig 3. Transposable-element-silencing genes over diverse fungal genomes.
The orthologs were inferred using OrthoFinder 1.0.6. Dim-2 and Masc2, Sms-3 and Dcl2, and Sms-2 and Qde2 were further differentiated from the gene trees because they belonged to the same gene families. Reference genes are listed in Table A in S2 File.
Fig 4
Fig 4. Three developmental stages of Tricholoma matsutake: Hyphae, primordia, and fruiting body.
a. The Venn diagram depicts the number of expressed genes (>1 FPKM) across the three developmental stages. b. Upregulated and downregulated genes during development. Gene functional categorization was carried out using Gene Ontology Slim http://www.geneontology.org.
Fig 5
Fig 5. Transcription factor expressions at the three developmental stages.
Differentially expressed genes were determined based on logFC (>1 or <−1), calculated by IsoEM2 and IsoDE2. When two conditions were more expressed than the other but there was no difference between them (−1 < logFC < 1), we assigned this gene as being co-overexpressed in these two conditions. Row-wise Z-scores of fragments per kilobase of transcript per million mapped reads were used.
Fig 6
Fig 6. CAZyme genes in Tricholoma matsutake and 37 Agaricomycetes.
All available CAZyme modules were counted. Scaled values based on row Z-scores were used to fill each cell.
Fig 7
Fig 7. Differentially expressed CAZymes at each of the developmental stages.
The pie graphs depict the number of CAZyme families for each specific expression type. Abbreviations for CAZyme families are as follows: glycoside hydrolase (GH), carbohydrate-binding module (CBM), glycosyl transferase (GT), polysaccharide lyase (PL), carbohydrate esterase (CE), and auxiliary activity (AA). Row-wise Z-scores of fragments per kilobase of transcript per million mapped reads were used.

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Grant support

BM, JP, YO and IC were supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (No. NRF-2019R1A2C1089704) and New and Renewable Energy Core Technology Program of the Korea Institute of Energy Technology Evaluation and Planning (KETEP) grants from the Ministry of Trade, Industry and Energy (No. 20173010092460). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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