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Genomics

journal homepage: www.elsevier.com/locate/ygeno

Whole genome sequence of Auricularia heimuer (Basidiomycota, Fungi), thethird most important cultivated mushroom worldwide

Yuan Yuana,b, Fang Wub, Jing Sib, Yi-Fan Zhaoc, Yu-Cheng Daia,b,⁎

a Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, Chinab Institute of Microbiology, Beijing Forestry University, Beijing 100083, Chinac Beijing Genomics Institute, Shenzhen 518083, China

A R T I C L E I N F O

Keywords:Whole genome sequencingAuricularia heimuerEdible-medicinal fungusSecondary metabolism

A B S T R A C T

Heimuer, Auricularia heimuer, is one of the most famous traditional Chinese foods and medicines, and it is thethird most important cultivated mushroom worldwide. The aim of this study is to develop genomic resources forA. heimuer to furnish tools that can be used to study its secondary metabolite production capability, wooddegradation ability and biosynthesis of polysaccharides. The genome was obtained from single spore mycelia ofthe strain Dai 13782 by using combined high-throughput Illumina HiSeq 4000 system with the PacBio RSII long-read sequencing platform. Functional annotation was accomplished by blasting protein sequences with differentpublic available databases to obtain their corresponding annotations. It is 49.76 Mb in size with a N50 scaffoldsize of 1,350,668 bp and encodes 16,244 putative predicted genes. This is the first genome-scale assembly andannotation for A. heimuer, which is the third sequenced species in Auricularia.

1. Introduction

Auricularia is a very important genus of wood-decaying fungi, andseveral species are widely cultivated as edible and medicinal mush-rooms in China and some other Asian countries. Among them, Heimuer,previously identified as Auricularia auricula (L.) Underw or A. auricula-judae (Bull.) Quél. but currently as A. heimuer F. Wu, B.K. Cui & Y.C. Dai[1], is the most common and popular species of the genus, and is thethird most important cultivated mushrooms worldwide (Fig. 1; [2]). Ithas good taste and a wide spectrum of health-associated properties,including antitumor, cholesterol-lowering, anticoagulant, antioxidant,immunomodulatory, anti-inflammatory, and antimicrobial activities[3]. The earliest report about its medicinal value appeared in the fa-mous Chinese medicinal monograph Compendium of Materia Medicaby Shi-Zhen Li in the Ming Dynasty [4,5]. Since the simple log culti-vation method was recorded in Tang Materia Medica by Gong Su, thecultivation of Heimuer could be traced back to 1300 years ago [6].

The availability of the genome sequences of fungi, which has in-creased tremendously in recent years, has facilitated the research ofgene diversity and the identification of genes involved in the bio-synthesis of secondary metabolites by genome mining [7]. Recent ex-amples of medicinal mushroom genomes studied are Ganoderma lu-cidum [8,9], Wolfiporia cocos [10] and Daedalea quercina [11]. Othergenomes of edible mushrooms analyzed include Volvariella volvacea

[12], Pleurotus ostreatus [13], Flammulina velutipes [14], Agaricus bis-porus [15,16], and others.

In this paper, we present the genome sequence of A. heimuer Dai13782. We have also identified putative genes that may be involved inthe biosynthesis of bioactive proteins and polysaccharides. And for allwe know, this whole genome assembly and annotation data representsthe first genome-scale assembly for this species. The aim of this study isto develop foundational genomic resources for this species that can beused in further researches.

2. Methods and materials

2.1. Fungal material, sequencing, and assembly

Fruiting bodies of A. heimuer were collected by Yu-Cheng Dai onQuercus in Ning'an County, Heilongjiang Province, northeastern China.The specimen (Dai 13782) was deposited in the herbarium of theInstitute of Microbiology, Beijing Forestry University (BJFC), with theaccession number BJFC017513. A single spore strain was obtained fromthe specimen following the methods of Choi et al. [17]. Genomic DNAwas extracted from the single spore mycelia by using CetyltrimethylAmmonium Bromide (CTAB) method [18].

We sequenced the genome of A. heimuer strain Dai 13782 using awhole-genome shotgun strategy by high-throughput Illumina HiSeq

https://doi.org/10.1016/j.ygeno.2017.12.013Received 25 September 2017; Received in revised form 18 December 2017; Accepted 22 December 2017

⁎ Corresponding author at: Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, China.E-mail address: yuchengdai@bjfu.edu.cn (Y.-C. Dai).

Genomics xxx (xxxx) xxx–xxx

0888-7543/ © 2017 Published by Elsevier Inc.

Please cite this article as: Yuan, Y., Genomics (2017), https://doi.org/10.1016/j.ygeno.2017.12.013

4000 sequencing and the PacBio RSII long-read sequencing platform atBGI-Shenzhen, China. Paired-end reads were generated by sequencingof insert libraries of 350 bp and 10 kb using Illumina HiSeq4000system. For PacBio RSII platform, a 20 kb library was built and se-quenced.

In order to ensure the accuracy of the follow-up analyses, reads oflow complexity, low quality with adapter and duplication contamina-tion were removed from the raw data. Several steps were performed.

For filtering the raw data of 350 bp library: Read 1 and read 2 were

cut by 1–100 bp; reads with a certain proportion of low quality (ReadQuality ≤ 20) bases (40% as default, parameter setting at 40 bp) wereremoved; reads with a certain proportion of Ns' base or low complexityreads (10% as default, parameter setting at 10 bp) were removed;adapter contaminations (15 bp overlap between adapter and reads asdefault, parameter setting at 15 bp) were removed; duplication con-taminations were removed.

For filtering the raw data of 10 kb library: Read 1 and read 2 werecut by 1–49 bp; reads with a certain proportion of low quality (ReadQuality ≤ 20) bases (40% as default, parameter setting at 20 bp) wereremoved; reads with a certain proportion of Ns' base or low complexityreads (10% as default, parameter setting at 5 bp) were removed;adapter contaminations (15 bp overlap between adapter and reads asdefault, parameter setting at 15 bp) were removed; duplication con-taminations were removed.

The above processes are applied to filter read 1 and read 2 based onconventional BGI pipelines. After that, 10%–20% of the data is elimi-nated generally (For small insert size reads). Because large insert sizereads have high duplication, the data eliminated is more but there is nocertain proportion.

Reads of PacBio RSII were filtered using custom BGI pipelines withfollowing methods: polymerase reads with length < 100 bp were fil-tered out; polymerase reads with quality score < 0.8 were filtered out;adapter sequences were filtered out and then subreads were produced;subreads with length < 1000 bp were filtered out; subreads withquality score < 0.8 were filtered out for further analysis.

PacBio data were assembled using the SMRT Analysis v2.3.0workflow into contigs. GATK 3.4.0, SOAPsnp and SOAPindel were usedto correct single bases from the assembly results. The parameters ofGATK were: -cluster 2 -window 5 -stand_call_conf 50 -stand_emit_conf10.0 -dcov 200 MQ0 ≥ 4. The parameters of SOAPsnp and SOAPindelwere the default. After that, SSPACE_Basic_v2.0 [19] was used to con-struct the scaffold by using HiSeq long-insert-size data (default para-meters). For the PacBio data, Pbsuite 14.9.9 was used to fill gaps bydefault parameters.

BUSCO (Benchmarking Universal Single-Copy Orthologs) softwarewas used to assess the completeness of genome assembly and annota-tion with single-copy orthologs [20]. BUSCO v2.0 was run on thescaffolded genome assembly (using “-m genome”). The lineage datasetof BUSCO was fungi_odb9 (Creation date: 2016-10-21, number of spe-cies: 85, number of BUSCOs: 290). In addition, assembly of A. heimuerwas compared with A. auricula-judae, A. subglabra and E. glandulosa.

2.2. Genome annotation methods

Protein-encoding genes were predicted applying the ab initio genepredictors SNAP [21], Augustus [22], and GeneMark-ES [23]. The re-sulting gene sets were integrated to obtain the most comprehensive andnon-redundant reference genes.

Transposon sequence analysis of A. heimuer was carried out for theassembled gene sequences with the transposon Repbase database

Fig. 1. Fruiting bodies of Auricularia heimuer. Scale bar: 2.5 cm.

Table 1Illumina HiSeq 4000 data statistics of Auricularia heimuer.

Insert size(bp)

Reads length(bp)

Raw data(Mb)

Filtered reads(%)

Clean data(Mb)

350 2 × 100 5223 9.44 473010,000 2 × 49 6390 70.51 1884

Table 2PacBio RSII data statistics of Auricularia heimuer.

Library (kb) Bases of polymerasereads (bp)

Bases of subreads(bp)

Utilization ratio(%)

20 3,118,289,335 2,835,110,054 90.9

Table 3Gene annotation summary statistics of Auricularia heimuer.

Scaffold characteristicsTotal number 103Total length (bp) 49,761,846Total gap bases (bp) 33,403Gap number 11N50 (bp) 1,350,668N90 (bp) 235,572Max length (bp) 2,880,034Min length (bp) 33,191GC content (%) 56.98

Genome characteristicsGenome assembly (Mb) 49.76Number of coding sequence genes 16,244Number of exons 87,130Number of introns 70,886Average length of coding sequence genes (bp) 1355.30Average exon length (bp) 252.67Average intron length (bp) 98.18Average number of exons per genes 5.36

Table 4Assembly summary statistics compared to other Auriculariales genomes.

Species NCBIBioProject(PRJNA#)

Contigcount(N50 kb)

Scaffoldcount(N50 Mb)

Totallength(Mb)

GC (%)

A. heimuer 382,748 114(1006.44)

103 (1.35) 49.76 57.0

A. auricula-judae 382,471 1071(121.22)

534 (0.27) 43.57 56.6

A. subglabra 242,540 4688(36.02)

1531 (0.49) 74.92 58.6

E. glandulosa 196,053 4019(40.34)

1723 (0.12) 78.16 56.7

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[24–26], using RepeatMasker software (version 3.3.0) at http://www.repeatmasker.org/ and RepeatProteinMasker software (using thetransposon protein library that comes with RepeatMasker). Tandemrepeat sequences were searched in the DNA sequence with TandemRepeat Finder (TRF version 4.04, [24]).

rRNA sequences were predicted by RNAmmer (version 1.2) pre-diction software with the whole genome sequence [27]. tRNA genesand tRNA secondary structure were identified by tRNAscan-SE software(version 1.23, [28]). Other non-coding RNAs, such as miRNA, sRNA andsnRNA, were predicted by Rfam (version 9.1, [29]).

The functional annotations of predicted genes were mainly based onhomology to known annotated genes within different databases usingBLAST as the main tool. For the purpose of achieving their corre-sponding annotation, we aligned protein models in SwissProt [30],TrEMBL, the National Center for Biotechnology Information (NCBI)non-redundant (nr) database, InterPro, GO [31,32], NCBI Clusters ofOrthologous Groups of proteins (COG) [33,34], and Kyoto En-cyclopedia of Genes and Genomes (KEGG) [35,36].

Annotations of carbohydrate-active enzymes (CAZymes) in the A.heimuer genome were actualized with the CAZy database by BLASTP athttp://www.cazy.org/ [37]. The reference P450 sequences weredownloaded from http://drnelson.uthsc.edu/CytochromeP450.html.Auricularia heimuer gene models were aligned to search the referenceP450 data set using the BLASTP program with a cut off e-value≤1e−10 [38].

AntiSMASH fungal 4.0.0, a web-based analysis platform, was em-ployed to predict the gene clusters of secondary metabolites [39]. Theparameter settings were maintained as the default parameter values. Tovalidate the predicted results, the obtained gene clusters were checkedmanually. BLAST analysis and gene annotation were carried out withina software platform provided by the JGI genome portal [40]. TheBLASTP and TBLASTN algorithms were used to search all hypotheticalgene models present in the database.

The sequence data of other taxa used in the present paper weredownloaded from the US Department of Energy Joint Genome Institutewebsite at http://genome.jgi.doe.gov/ and the National Center for

Table 5BUSCO analysis on assembly and annotation.

Species GCAa BUSCO mode Completeb Fragmented Missing

A. heimuer 002287115.1 Genome 268 (92.4%) 16 (5.5%) 6 (2.1%)A. auricula-judae 002092955.1 Genome 280 (96.5%) 4 (1.4%) 6 (2.1%)A. subglabra 000265015.1 Genome 274 (94.5%) 8 (2.8%) 8 (2.7%)E. glandulosa 001632375.1 Genome 273 (94.1%) 6 (2.1%) 11 (3.8%)

a This is the number of GenBank assembly accession.b Number of BUSCO proteins (percent of total BUSCOs).

Fig. 2. The Clusters of Orthologous Groups of proteins (COG) function classification of proteins in Auricularia heimuer.

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Biotechnology Information https://www.ncbi.nlm.nih.gov/genome(Table S1, [10][12][13][16][59–63]).

3. Results and discussion

3.1. The data of sequencing and assembly

Auricularia heimuer generated 6614 Mb HiSeq-data and 2835 MbPacBio-data. The details of data generation are listed in Tables 1 and 2,respectively.

3.2. Genome features

The details of gene annotation summary statistics of Auriculariaheimuer are shown in Table 3.

Currently, three genomes of Auriculariales species (Auriculariasubglabra, Auricularia auricula-judae and Exidia glandulosa) are availablein the NCBI WGS database. Assembly statistics of A. heimuer are com-pared to other three species in Table 4, showing similar GC content butsignificant different genome sizes with A. subglabra and E. glandulosa.

The completeness of genome assembly and annotation with single-copy orthologs test results suggested a well complete annotation set,with 92.4% of the Fungi BUSCOs being present within the RefSeq

annotation set, and 5.5% of those fragmented. Details of BUSCO ana-lysis are presented in Table 5.

3.3. Repeat sequences

The total length of repeat sequences was 3,429,083 bp, covering6.89% of the genomic length. Of the repeat elements, tandem repeatsequences account for 2.32% and transposable elements (TEs) wereabout 4.57% of the assembled genome. Among the TEs, the proportionof long terminal repeats (LTRs) and non-LTR transposons were 2.96%and 0.99% of the genome, respectively.

3.4. Gene annotation

The annotations of 16,244 protein-encoding genes were supportedusing publicly available databases. All the protein-encoding genes to-gether had a total sequence length of 28,840,601 bp, including exonsareas of 22,015,521 bp, and intron areas of 6,825,080 bp. The protein-encoding region accounted for 44.24% of the genome. On average, eachpredicted gene contained 5.36 exons. Genes typically contained smallexons (average 252.67 bp) and introns (average 98.18 bp), which issimilar to other basidiomycetes.

For RNA, 150 tRNAs, 34 snRNAs, and 11 rRNAs were predicted. The

Fig. 3. The Gene Ontology (GO) function annotation of Auricularia heimuer.

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gene density was 5.63 genes/10 kb, and the average size of protein-encoding genes was 1355.30 bp. Among the tRNAs, 12 were possiblepseudogenes and the remaining 138 anti-codon tRNAs corresponded tothe 20 common amino acid codons. In addition, 79 tRNAs were absenceof intron sequences.

A total of 1109 predicted genes encoding hypothetical proteinswithout apparent homologs to currently available sequences werefound in the A. heimuer genome. The annotations with NCBI nr, GO,NCBI COG, KEGG, CAZy, SwissProt, PHI, InterPro and TrEMBL proteindatabases are shown in Tables S2 and S3. These homologous proteingenes represent 93.17% of the assembled genome.

By NCBI COG mapping, 1801 proteins (11.08%) were assigned to

COG categories (Fig. 2). “General functional prediction only” had thehighest number of genes (408); these proteins were not unambiguouslyassigned to a particular group. This was followed by “Translation, ri-bosomal structure and biogenesis”, “Posttranslational modification,protein turnover, chaperones”, “Transcription”, “Replication, re-combination and repair”, and “Energy production and conversion” asthe most gene-rich classes in the COG groupings. These findings weresuggestive of the presence of an enriched and varied array of proteinmetabolism and energy metabolism functions that enable better ab-sorption and transformation of nutrients from substrates.

According to GO database, 7056 predicted proteins that accountedfor 43.43% of the entire genome were mainly distributed in five func-tional entries, “Binding”, “Catalytic activity”, “Cellular process”,“Metabolic process”, and “Single-organism process” (Fig. 3).

To further understand the gene functions in A. heimuer, we suc-cessfully assigned 5676 (34.94%) putative proteins to their orthologs inthe KEGG database. The KEGG function classification is shown in Fig. 4.Similar with the COG annotation, some metabolism and biosynthesiscategories in KEGG were highly enriched.

3.5. The CAZyme

We mapped our fungal genomes with CAZy to study the presence ofCAZymes. A total of 336 genes could be assigned to carbohydrate-activeenzyme (CAZymes) families as defined in CAZy database (Table 6). Thenumber of GHs was remarkably larger than GTs, which could be due tothe lifestyle, in which its survival is dependent on lignocellulose de-composition. It is concluded that the polysaccharides decomposition ismore important than their construction for growth and metabolism ofA. heimuer. The number of CBMs in A. heimuer is more than average,while CEs, GTs, GHs and PLs were less than the basidiomycetes average(Table S4).

3.6. The CYPs family

It is worth to note that A. heimuer has 72 genes distributed in“Metabolism of xenobiotics by cytochrome P450” and 60 in “Drugmetabolism – cytochrome P450” KEGG sub-pathways.

Auricularia heimuer had a total of 83 CYP genes, which could be

Fig. 4. The Kyoto Encyclopedia of Genes and Genomes(KEGG) function annotation of Auricularia heimuer.

Table 6Carbohydrate-active enzyme annotation results.

Classification Number Superfamily number

Carbohydrate-Binding Modules (CBMs) 103 18Carbohydrate Esterases (CEs) 22 4Glycoside Hydrolases (GHs) 106 52Glycosyl Transferases (GTs) 29 22Polysaccharide Lyases (PLs) 14 4Auxiliary activities (AAs) 62 9

Table 7P450 genes and subfamilies in Auricularia heimuer.

Family Subfamily Gene number Total gene number

CYP64 A 26 26CYP2 B; J; U 1; 1; 8 10CYP4 A; F; V; – 2; 2; 1; 4 9CYP5076 C 6 6CYP97 A 5 5CYP102 A 3 3CYP1 A; B 1; 2 3CYP3 A 3 3CYP5067 A 3 3CYP6 – 3 3CYP9 – 2 2Others – – 10

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Fig. 5. “Terpenoid backbone biosynthesis” pathway of Auricularia heimuer. The red box indicates existing homologous genes of the enzyme, while white box means not. The photo wasdone by KEGG mapper. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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classified into 21 families according to Nelson's nomenclature (Table 7)[38]. The CYP64 family was found to have the highest number of genes(26 genes), followed by the CYP2 (10 genes), and CYP4 (9 genes) fa-milies (Table 5).

The CYP64 family is involved in “Metabolism – Biosynthesis ofother secondary metabolites”, while genes from the CYP73, CYP76 andCYP97 families are necessary in “Metabolism – Metabolism of terpe-noids and polyketides”. The CYP2 and CYP4 families play a role in“Lipid metabolism”. However, these predicted CYP genes still need tobe validated in further studies.

3.7. Secondary metabolisms

For modern pharmacology and therapeutics fields, deep interest hasbeen generated in medicinal fungi due to their diverse and significantsecondary metabolites, which have been proved to possess pharmaco-logical properties, such as immunomodulatory, anti-inflammatory, an-tiviral, antioxidant, antitumor, and antimicrobial activities [41,42].

The biosynthesis genes of secondary metabolites are often in con-tiguous gene clusters [43]. We searched for genes that may be involvedin biosynthesis of secondary metabolite through genome mining basedon the previous studies such as terpene synthases (TS), non-ribosomalpeptide synthetases (NRPS), and polyketide synthases (PKS) [44–49].One NRPS gene clusters were identified in the A. heimuer genome. Thedetails of secondary metabolite gene clusters are listed in Table S5.

The potential PKS genes were aligned to Genebank with blastp andtheir function information were manual checked. The results demon-strate that A. heimuer has no PKS gene. The reason for this phenomenonstill needs further research. One lineage of NPRS gene clusters of A.heimuer may be responsible for intracellular siderophore biosynthesisthat encodes a single copy gene for siderophore synthetase(Dai13782_GLEAN_10006893). Ferrichrome siderophores perform keyfunctions in fungal cells, which have main role in sexual spore devel-opment or asexual development [50,51]. All known fungal side-rophores are synthesized by NRPSs [52].

In fungi, one of the largest groups of bioactive natural products thathave been identified is the terpenoids, which is derived from the simplefive carbon precursor molecules dimethylallyl diphosphate (DMAPP)and isopentenyl diphosphate (IPP) produced from acetyl-CoA via themevalonate pathway [47,53]. There are 5 gene clusters encoding TS,which are key enzyme for the biosynthesis of terpene. We checked theA. heimuer genes in the “Terpenoid backbone biosynthesis (map00900)”pathway and identified 15 key enzymes distributed in the MVApathway (Fig. 5). All the core enzymes involved in the MVA pathwayare summarized in Table 8. The enzymes protein-S-isoprenylcysteine O-

methyltransferase, farnesyl diphosphate synthase, and dipho-sphomevalonate decarboxylase are each encoded by two copies of thegenes, whereas the remaining 12 enzymes are encoded by single-copyof genes.

The search of potential triterpenoid biosynthesis genes in A. heimuergenome resulted in an ORF (Dai13782_GLEAN_10010970) that encodesa single copy gene for lanosterol synthase (LSS) (ERG7; K01852;EC5.4.99.7).

LSS is an oxidosqualene cyclase family enzyme that catalyzes thecyclization of the triterpenes squalene or 2–3-oxidosqualene to a pro-tosterol cation and finally to lanosterol, the precursor of all steroids[54]. Lanosterol is a key four-ringed intermediate in cholesterol bio-synthesis [55]. The CYP73, CYP76, and CYP97 families of P450 geneshave been predicted to participate in “Metabolism – Metabolism ofterpenoids and polyketides”.

3.8. Biosynthesis of polysaccharides in A. heimuer

Polysaccharides that are accounted for the pharmaceutical potentialof A. heimuer are another kind of extensively bioactive compounds.

Among the polysaccharides, water soluble β-1,3-glucan with sidechain β-1,6-glucose has the most active immunomodulating and anti-tumor compounds [56]. Table S6 lists 33 enzymes that may be involvedin the biosynthesis of uridine diphosphate glucose (UDP-glucose, pre-cursor of glucans) in A. heimuer. These enzymes include 1,3-beta-glucansynthasem, hexokinase, phosphoglucomutase, GTPase-activating pro-tein, and UTP-glucose-1-phosphate uridylyltransferase.

4. Conclusion

In summary, the exposition of the A. heimuer genome has allowed usto predict gene function and study the biosynthesis of active com-pounds. A research of the secondary metabolite biosynthesis genes inthe A. heimuer genome shows that it is particularly enriched with ter-pene biosynthesis genes. Hence, the future study of bioactive moleculescan be concentrated in this class of metabolites. Although not complete,the elucidation of A. heimuer genome in this study provides founda-tional information for studying the biosynthesis of the pharmacologi-cally active compounds and functional food applications in the future.

4.1. Data availability

This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession NEKD00000000. The version de-scribed in this paper is version NEKD01000000. The genome raw

Table 8Putative genes involved in terpenoid backbone biosynthesis.

Gene name and definition KO term EC no. Gene ID

HMGCR; hydroxymethylglutaryl-CoA reductase (NADPH) K00021 1.1.1.34 Dai13782_GLEAN_10005490ICMT, STE14; protein-S-isoprenylcysteine O-methyltransferase K00587 2.1.1.100 Dai13782_GLEAN_10009478

Dai13782_GLEAN_10009757FDPS; farnesyl diphosphate synthase K00787 2.5.1.10; 2.5.1.1 Dai13782_GLEAN_10004067

Dai13782_GLEAN_10010441GGPS1; geranylgeranyl diphosphate synthase, type III K00804 2.5.1.29; 2.5.1.10; 2.5.1.1 Dai13782_GLEAN_10004161E2.7.4.2, mvaK2; phosphomevalonate kinase K00938 2.7.4.2 Dai13782_GLEAN_10003335MVD, mvaD; diphosphomevalonate decarboxylase K01597 4.1.1.33 Dai13782_GLEAN_10014658

Dai13782_GLEAN_10012162E2.3.3.10; hydroxymethylglutaryl-CoA synthase K01641 2.3.3.10 Dai13782_GLEAN_10012746hexPS, COQ1; hexaprenyl-diphosphate synthase K05355 2.5.1.82; 2.5.1.83 Dai13782_GLEAN_10003540PCYOX1, FCLY; prenylcysteine oxidase/farnesylcysteine lyase K05906 1.8.3.6; 1.8.3.5 Dai13782_GLEAN_10012594FNTB; protein farnesyltransferase subunit beta K05954 2.5.1.58 Dai13782_GLEAN_10007998FNTA; protein farnesyltransferase/geranylgeranyltransferase type-1 subunit alpha K05955 2.5.1.59; 2.5.1.58 Dai13782_GLEAN_10002446STE24; STE24 endopeptidase K06013 3.4.24.84 Dai13782_GLEAN_10001866RCE1, FACE2; prenyl protein peptidase K08658 3.4.22.- Dai13782_GLEAN_10012075DHDDS, RER2, SRT1; ditrans, polycis-polyprenyl diphosphate synthase K11778 2.5.1.87 Dai13782_GLEAN_10015786E2.5.1.68; short-chain Z-isoprenyl diphosphate synthase K12503 2.5.1.68 Dai13782_GLEAN_10004406

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sequencing data and the assembly reported in this paper is associatedwith NCBI BioProject: PRJNA382748 and BioSample: SAMN06718193within GenBank. The SRA accession number is SRR5889175.

The authors state that all data necessary for confirming the con-clusions presented in the article are represented fully within the articleand supplemental materials.

Acknowledgments

We thank the US Department of Energy Joint Genome Institute(http://www.jgi.doe.gov/) in collaboration with the user communityand the National Center for Biotechnology Information (https://www.ncbi.nlm.nih.gov/genome) for providing most of the sequencing datafor fungi used in this study. The research was supported by the NationalNatural Science Foundation of China (Project No. 31372115).

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ygeno.2017.12.013.

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