An Improved Genome Sequence Resource of Bipolaris maydis, Causal Agent of Southern Corn Leaf Blight.

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HomePhytopathology®Vol. 112, No. 6An Improved Genome Sequence Resource of Bipolaris maydis, Causal Agent of Southern Corn Leaf Blight PreviousNext Resource Announcement OPENOpen Access licenseAn Improved Genome Sequence Resource of Bipolaris maydis, Causal Agent of Southern Corn Leaf BlightYafei Wang, Houxiang Kang, Jinai Yao, Zhiqiang Li, Xinyao Xia, Shaoqun Zhou, and Wende LiuYafei WangState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, 440307, Shenzhen, ChinaSearch for more papers by this author, Houxiang KangState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaSearch for more papers by this author, Jinai YaoState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaFujian Key Laboratory for Monitoring and Integrated Management of Crop Pests/Institute of Plant Protection, Fujian Academy of Agricultural Sciences, 350013, Fuzhou, ChinaSearch for more papers by this author, Zhiqiang LiState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaSearch for more papers by this author, Xinyao Xiahttps://orcid.org/0000-0001-6547-4993State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaSearch for more papers by this author, Shaoqun ZhouShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, 440307, Shenzhen, ChinaSearch for more papers by this author, and Wende Liu†Corresponding author: W Liu; E-mail Address: [email protected]https://orcid.org/0000-0002-5570-1395State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, ChinaSearch for more papers by this authorAffiliationsAuthors and Affiliations Yafei Wang1 2 Houxiang Kang1 Jinai Yao1 3 Zhiqiang Li1 Xinyao Xia1 Shaoqun Zhou2 Wende Liu1 † 1State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100193, Beijing, China 2Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, 440307, Shenzhen, China 3Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests/Institute of Plant Protection, Fujian Academy of Agricultural Sciences, 350013, Fuzhou, China Published Online:29 Apr 2022https://doi.org/10.1094/PHYTO-11-21-0490-AAboutSectionsView articlePDFSupplemental ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat View articleGenome AnnouncementSouthern corn leaf blight (SCLB), caused by Bipolaris maydis (teleomorph: Cochliobolus heterostrophus), is one of the important leaf diseases on maize and reduces both crop yield and grain quality. This disease is most prevalent in tropical and subtropical maize-growing areas such as the southeastern United States and parts of Asia and Africa, where it could cause nearly 70% of production losses under favorable environmental conditions (Bhandari et al. 2017; Carson et al. 2004; Fisher et al. 1976; Kumar et al. 2016; Singh and Srivastava 2012; Tatum 1971; Ullstrup 1972). B. maydis infection can lead to severe leaf chlorosis by producing some toxins such as T-toxin that attack mitochondria, affecting photosynthesis (Hussain et al. 2016; Singh and Srivastava 2012). The published haploid B. maydis genomes included C5 (number of contigs = 88 and genome assembly size = 36.46 M) and ATCC 48331 (number of contigs = 903 and genome assembly size = 32.93 M) (Condon et al. 2013; Kodama et al. 1999; Ohm et al. 2012). Both strains were collected in North America and sequenced using the Sanger or Illumina short-read platform. In this study, we present an improved genome assembly of B. maydis based on a strain from northeastern China. By combining PacBio Sequel and Illumina HiSeq sequencing technologies, we assembled a more continuous B. maydis genome, which will be helpful for understanding the molecular mechanisms of the fungal pathogenesis.B. maydis field strain BM1 was isolated in 2019 from leaf lesions of maize plants grown in Heilongjiang Province, China. After culturing the strain on potato dextrose agar, a single conidiospore was isolated. The freshly purified hyphae were cultured for 2 days in potato dextrose broth and then collected for genomic DNA extraction using the Omega Fungal DNA Kit D3390-02 following the manufacturer’s protocols. Genome sequencing of BM1 was performed by a combination of PacBio single molecule real-time (SMRT) sequencing and Illumina paired-end sequencing technologies. For PacBio sequencing, the Eppendorf 5424 centrifuge (Eppendorf, NY, U.S.A.) was used to break the genomic DNA into small fragments in the Covaris g-TUBE (Covaris, MA, U.S.A.) and the average fragment size was estimated using the Agilent 2100 Bioanalyzer (Agilent, Santa Clara, CA, U.S.A.). The SMRTbell library was prepared using the sheared genomic DNA with the SMRTbell sequencing adapter (Pacific Biosciences, Menlo Park, CA, U.S.A.), and the approximately 10-kb insert library was sequenced using PacBio Sequel II platform (Frasergen Bioinformatics Co., Ltd., Wuhan, China). After quality control, 887,707 PacBio subreads were used to assemble the genome with the nextDenovo v2.0-beta.1 software (https://github.com/Nextomics/NextDenovo). For Illumina sequencing, the TruSeq PE Cluster Kit was used to construct a DNA library with an average insert length of 490 bp. The library was sequenced using the Illumina HiSeq platform (150-bp paired-end reads), to yield a total of 40,347,732 clean reads. The genome assembled from PacBio data were further polished by Pilon v1.23 software using Illumina short reads (Walker et al. 2014). The program MAKER2 v2.31.9 was used to predict protein-coding genes from the assembled genome (Holt and Yandell 2011). The benchmarking universal single-copy orthologs (BUSCO) datasets (fungi_odb9) were used to assess the completeness of the assembled BM1 genome (Simão et al. 2015). Functional annotation for the predicted genes was completed through homology inference with the Non-Redundant Protein Database (Pruitt et al. 2005), Swiss-Prot (Boutet et al. 2007), Pfam (El-Gebali et al. 2019), Clusters of Orthologous Groups of Proteins (Tatusov et al. 2000), Gene Ontology (Ashburner et al. 2000), and Kyoto Encyclopedia of Genes and Genomes (Kanehisa and Goto 2000).In total, 9,127,866,600 bp of raw data (sequencing depth 251×) was obtained by PacBio sequencing, and 6,302,131,470 bp (sequencing depth of 173×) of raw data were obtained by Illumina sequencing. The final assembled haploid genome was 36,230,517 bp, and its GC content was 49.1% (Table 1). In total, 27 contigs were assembled in BM1, of which the N50 contig length and the maximum contig length were 1,859,413 and 5,449,695 bp, respectively. This represents a significant improvement from the existing B. maydis genomes assemblies (903 contigs in ATCC 48331 and 88 contigs in C5) (Table 1). Among them, the contig 26 (JAHUAA010000026.1) with a length of 104,099 bp was considered to be the mitochondrial genome of BM1 after BLASTn search against the NCBI database. In total, 11,197 protein-coding genes were predicted in the BM1 genome, with an average length of 2,054.25 bp. BUSCO (v4) analysis results showed that the estimated completeness of the assembled BM1 genome is 97.6%, by comparison with the fungi_obd9 database (https://zenodo.org/record/6339882). In addition, 110 transfer RNAs were predicted with the software tRNAscan-SE v1.3.1 and 37 ribosomal RNAs were identified with the software Barrnap 0.4.2. Through metabolic system analysis, 535 genes encoding carbohydrate-active enzymes (CAZymes) and 355 genes belonging to the cytochrome P450 family were identified in the BM1 genome. The identified CAZymes in the BM1 genome included 226 glycoside hydrolases, 141 enzymes involved in auxiliary activities, 82 carbohydrate esterases, 68 glycosyltransferases, 15 polysaccharide lyases, and 3 enzymes related to carbohydrate-binding modules (Cantarel et al. 2009). Through pathogenic system analysis, 1,216 virulence genes were predicted in the assembled genome. There were 1,839 genes in the assembled genome that were related to pathogen–host interactions, 22 of which were genes encoding putative effectors (Winnenburg et al. 2006). In the assembled BM1 genome, 1,116 genes encoding secreted proteins, 1,553 genes encoding transport proteins, and 1,267 genes encoding transmembrane proteins were also identified (Krogh et al. 2001; Petersen et al. 2011; Saier et al. 2006). In addition, nine secondary metabolite gene clusters, including seven polyketides and one nonribosomal peptide synthetase, were annotated in the BM1 genome with the antiSMASH tool (Supplementary Table S1) (Medema et al. 2011). We searched the BM1 genome for the eight key T-toxin biosynthetic genes (including PKS1, PKS2, LAM1, TOX9, OXI1, RED1, RED2, and RED3) (Condon et al. 2013; Kodama et al. 1999). It was found that these genes were absent, suggesting that BM1 does not produce T-toxin and other virulence factors may be involved. The annotation of the BM1 genome will accelerate our research into the virulence mechanisms of BM1.Table 1. Genome assembly statistics of Bipolaris maydis field strain BM1 and other available B. maydis strainsStrainGenomic featuresBM1ATCC 48331C5Genome assembly size (bp)36,230,51732,929,16736,456,735Number of scaffolds−20768Scaffold N50 (bp)−964,0891,842,487Number of contigs2790388Contig N50 (bp)1,859,41383,6841,168,586GC content (%)49.150.749.8Number of coding genes predicted by MAKER211,19710,49710,970Sequencing technologyPacBio + IlluminaIlluminaSangerGenome coverage251×67×36×GenBank numberGCA_019454015.1GCA_000354255.1GCA_000338975.1ReferenceThis studyOhm et al. 2012Ohm et al. 2012Table 1. Genome assembly statistics of Bipolaris maydis field strain BM1 and other available B. maydis strainsView as image HTML The total length of repetitive sequences identified by RepeatMasker v4.0.6 was 3,661,508 bp, which accounted for 10.1% of the BM1 genome sequence (Chen 2004). Transposons (or transposable elements) in the fungal genome are usually closely related to fungal pathogenic variants (Faino et al. 2016; Raffaele and Kamoun 2012). The transposons identified in the BM1 genome included 94 long interspersed retrotransposable element retrotransposons, 31 DNA transposons, 17 short interspersed nuclear element retrotransposons, and 14 long terminal repeat retrotransposons. It is worth mentioning that the telomere repeats CCCTAA were detected at the 5′ end of contigs 5 (JAHUAA010000005.1), 8 (JAHUAA010000008.1), 11 (JAHUAA010000011.1), 18 (JAHUAA010000018.1), and 19 (JAHUAA010000019.1), and were detected at the 3′ end of contigs 4 (JAHUAA010000004.1), 9 (JAHUAA010000009.1), 15 (JAHUAA010000015.1), and 17 (JAHUAA010000017.1). In comparison, the C5 genome assembly has only five contigs with telomere repeat detection (Condon et al. 2013). This further indicates that the BM1 assembly has captured a more complete genome compared with the C5 assembly.This sequencing project provides the basis for a comprehensive understanding of B. maydis at the high-resolution genome level. The BM1 genome is less fragmented (27 contigs) than previous ATCC 48331 and C5 assemblies, which have 903 and 88 contigs, respectively. The N50 contig length of BM1 was greater than previous ATCC 48331 and C5 assemblies (Table 1). It is worth noting that there are significant differences in the predicted number of protein-coding genes among the three B. maydis genome assemblies (Table 1), which may be caused, in part, by different prediction software and sequencing technologies used. To remove potential artifacts introduced by different gene annotation pipelines, we reannotated the ATCC 48331 and C5 assemblies with MAKER2 (Holt and Yandell 2011). The newly obtained gene prediction result showed that the BM1 assembly contained the largest number of coding genes, further demonstrating that this assembly represented a significant improvement (Table 1). Genome-wide colinearity analysis revealed synteny between BM1 and C5 genomes (Fig. 1A) but a clear difference in the length of the entire genome (Fig. 1B). Comparison with the reference genome C5 revealed abundant large-fragment (>10 kb) deletions and insertions, which may be attributed to the geographic segregation between these two strains or the sequencing insufficiency in C5.Fig. 1. Synteny analysis of the assembled genome of Bipolaris maydis BM1 and reference genome of B. maydis C5. A, Linear alignment of B. maydis BM1 and C5 genome sequences; colored regions represented the high-identity regions (>98.5% sequence identity) between BM1 and C5 genomes. Different colors for the alignment lines were for the convenience of distinguishing the comparison between different blocks. B, Compared with the genome sequences of C5, in the 27 contigs of the BM1 genome, the >10-kb large fragment insertions and deletions were marked with blue (>10-kb large insertions happened in the BM1 genome) and gray arrows (>10-kb large deletions happened in the BM1 genome), respectively.Download as PowerPointIn summary, the B. maydis field strain BM1 genome assembly presented in this study provides a valuable resource for studying the SCLB disease and can help to elucidate the molecular mechanisms of its pathogenicity. Furthermore, the new genomic resources provided in this study will facilitate understanding the genetic diversity of B. maydis and comparative genomic analysis of different fungal pathogens.Raw reads from PacBio and Illumina sequencing have been deposited in the NCBI Sequence Read Archive database and the accession number is PRJNA743729. 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Kang contributed equally to this work.Funding: This work was financially supported by grants from the National Natural Science Foundation of China (grant number 32061143033), the Agricultural Science and Technology Innovation Program (ASTIP), and Shenzhen Science and Technology Program (grant number KQTD20180411143628272).The author(s) declare no conflict of interest.DetailsFiguresLiterature CitedRelated Vol. 112, No. 6 June 2022SubscribeISSN:0031-949Xe-ISSN:1943-7684 DownloadCaptionRT1054 exhibits high resistance to stripe rust, caused by Puccinia striiformis f. sp. tritici in the field under severe natural P. striiformis f. sp. tritici infection at Chengdu Plain, Sichuan, China (Ren et al.). Photo credit: Tianheng Ren Metrics Article History Issue Date: 27 May 2022Published: 29 Apr 2022Accepted: 7 Jan 2022 Pages: 1386-1390 Information© 2022 The American Phytopathological SocietyFundingNational Natural Science Foundation of ChinaGrant/Award Number: 32061143033Agricultural Science and Technology Innovation Program (ASTIP)Shenzhen Science and Technology ProgramGrant/Award Number: KQTD20180411143628272KeywordsBipolaris maydisfood safetyfungal pathogensgenome assemblygenomicsIllumina sequencingmicrobe-genome sequencingPacBio sequencingThe author(s) declare no conflict of interest.PDF downloadCited byT-Toxin Virulence Genes: Unconnected Dots in a Sea of Repeats8 March 2023 | mBio, Vol. 128The First Telomere-to-Telomere Chromosome-Level Genome Assembly of Stagonospora tainanensis Causing Sugarcane Leaf Blight16 October 2022 | Journal of Fungi, Vol. 8, No. 10