Whole-Genome Sequence Resource of Fusarium oxysporum Strain TH15, a Plant Growth Promoting Endophytic Fungus Isolated from Tetrastigma hemsleyanum

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HomePhytoFrontiers™Vol. 2, No. 3Whole-Genome Sequence Resource of Fusarium oxysporum Strain TH15, a Plant Growth Promoting Endophytic Fungus Isolated from Tetrastigma hemsleyanum Previous RESOURCE ANNOUNCEMENT OPENOpen Access licenseWhole-Genome Sequence Resource of Fusarium oxysporum Strain TH15, a Plant Growth Promoting Endophytic Fungus Isolated from Tetrastigma hemsleyanumXiaoping Huang, Zhanghui Zeng, Zhehao Chen, Yanjun Yang, Jiliang Pang, Yongsheng Qian, and Taihe XiangXiaoping HuangCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaZhejiang Provincial Key Laboratory for Genetic Improvement and Quality Control of Medicinal Plants, Hangzhou 311121, ChinaSearch for more papers by this author, Zhanghui ZengCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaSearch for more papers by this author, Zhehao ChenCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaSearch for more papers by this author, Yanjun YangCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaSearch for more papers by this author, Jiliang PangCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaSearch for more papers by this author, Yongsheng QianCollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaSearch for more papers by this author, and Taihe Xiang†Corresponding author: T. Xiang; E-mail Address: xthcn@163.com and E-mail Address: xthcn@hznu.edu.cnhttp://orcid.org/0000-0003-3299-7258College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaZhejiang Provincial Key Laboratory for Genetic Improvement and Quality Control of Medicinal Plants, Hangzhou 311121, ChinaSearch for more papers by this authorAffiliationsAuthors and Affiliations Xiaoping Huang1 2 Zhanghui Zeng1 Zhehao Chen1 Yanjun Yang1 Jiliang Pang1 Yongsheng Qian1 Taihe Xiang1 2 † 1College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, China 2Zhejiang Provincial Key Laboratory for Genetic Improvement and Quality Control of Medicinal Plants, Hangzhou 311121, China Published Online:31 Mar 2022https://doi.org/10.1094/PHYTOFR-12-21-0086-AAboutSectionsView articlePDFSupplemental ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat View articleGenome AnnouncementEndophytes are microbes, including bacteria, fungi, and actinomycetes, that live symbiotically inside tissues of their host plants without substantively harming them (Kaul et al. 2016; Kumar and Dubey 2020). In general, they form an association with their host plant and constitute an important part of a plant's microbiome (Dubey et al. 2020). Among plant microbiota, endophytes can be found in most plant species, and have been recovered from various tissues such as roots, leaves, stems, flowers, fruit, and seeds (Elmagzob et al. 2019). Furthermore, it is increasingly recognized that the symbiotic interaction between host plants and endophytes can promote the growth of plants and improve the endophyte's nutrient acquisition as well as response to stress tolerance (Ek-Ramos et al. 2019; Kaul et al. 2016; Wu et al. 2021).The genus Fusarium is one of the top 10 fungal pathogens in molecular plant pathology, and its members are capable of colonizing a wide range of environments on Earth (Dean et al. 2012). Taxonomically, the genus includes approximately 70 well-known species, identified through using a polyphasic approach, according to phylogenetic species concepts (Munkvold 2017). In general, species of Fusarium could cause several plant diseases. For example, the Fusarium redolens strain YP04 was identified as being responsible for root rot of American Ginseng (Fan et al. 2021). Another member, F. culmorum (a well-known pathogen of wheat crop) was reported to cause both blight and rot from the leaf of a black cottonwood tree (Newcombe et al. 2020). Furthermore, several reviews have paid more attention to Fusarium spp. F. graminearum and F. oxysporum (de Lamo and Takken 2020; Ghimire et al. 2020). The former is considered the predominant causal species of Fusarium head blight, which is a cereal disease resulting in reduced yields and mycotoxin contamination of the grain (Karlsson et al. 2021). Conversely, protection from tomato wilt disease conferred by the nonpathogenic F. oxysporum Fo47 is more effective than that conferred by avirulent strains (de Lamo et al. 2021). Despite much recent work, the isolation and identification of F. oxysporum is still incomplete and ongoing.In our previous study, the endophytic F. oxysporum strain TH15 was isolated from the calabash-shaped root of Tetrastigma hemsleyanum, and its fermentation broth could significantly increase plant growth and expression of expansin gene Th-exp (Song et al. 2017). To the best of our knowledge, the Fusarium genus is capable of producing mycotoxins, including trichothecenes deoxynivalenol, nivalenol, and HT2/T2, and the oestrogenic mycotoxin zearalenone (Karlsson et al. 2021; Munkvold 2017). Nevertheless, certain strains of the Fusarium genus are also evidently beneficial for plant growth (Filek et al. 2019; Lofgren et al. 2018) and the genomes of many Fusarium genus have been sequenced (Cuomo et al. 2007; Ma et al. 2010; Wiemann et al. 2013; Wingfield et al. 2012). However, there is currently no publicly available information concerning the genome of the endophytic fungal F. oxysporum strain TH15. Fortunately, the rapid development of whole-genome sequencing technologies provides a powerful tool for the assembly of high-quality genomes (Huo et al. 2021; Zhu et al. 2019). Here, we used PacBio SMRT sequencing technology to derive and present the sequencing of strain TH15’s genome and analyzed its genomic characteristics. This study should advance our understanding of the mechanism by which this fungus benefits host plants and help in developing integrated approaches to control plant growth development.After extraction of the TH15 genomic DNA, the Quant-iT PicoGreen dsDNA Assay Kit was utilized to evaluate the DNA content, and 1% agarose gel electrophoresis was carried out to test the DNA integrity. Then, a next-generation sequencing library was prepared by using the TruSeq DNA Sample Prep Kit, and a PacBio library with an insert size of 10 kb was prepared by using PacBio Template Prep Kit 1.0. Finally, the two prepared high-quality libraries were sequenced by using the whole-genome shotgun strategy based on the Illumina Hi-Seq paired-end platform (2 × 151 bp) and PacBio platform at Shanghai Personalbio Technology Co., Ltd. (Shanghai, China).The low-quality and short reads were filtered using Adapter Removal (version1.5.4) and SOAPec (v 2.0), and the remaining reads were used for the genome assembly. The genome was de novo assembled using the CANU v.17.0 software (Koren et al. 2017). Due to a high error rate of PacBio reads, the Illumina sequencing data were used to polish the genome assembled with PacBio data through PILON software with default settings (Walker et al. 2014). Completeness of the assembled genome sequence was evaluated using the Benchmarking Universal Single-Copy Ortholog (BUSCO) v3.0 program (Simão et al. 2015). Protein coding genes in the genome were predicted based on two prediction strategies: ab-initio- and homology-based prediction. The ab initio gene predictions were performed using the software programs Augustus v3.03 (Stanke and Waack 2003), glimmerHMM v3.0.1 (Majoros et al. 2004), and SNAP v-2006-07-28 (Korf 2004). For homology-based prediction of related species, the genome of F. oxysporum TH15 was used to predict gene models with the exonerate software tool (Haas et al. 2008; Keilwagen et al. 2016). Finally, ab-initio-based gene models and homology-based gene models were combined using EVidenceModeler (Haas et al. 2008) to integrate and derive a final gene set, and default settings were used for all of the programs. Basic annotations for the predicted genes were made according to five major databases, including Pfam, Swiss-Prot, Gene Ontology, Non-Redundant Protein (NR) Database, and Clusters of Orthologous Groups of Proteins (Ashburner et al. 2000; Boutet et al. 2007; El-Gebali et al. 2019; Pruitt et al. 2005; Tatusov et al. 2000). The Kyoto Encyclopedia of Genes and Genomes (KEGG) database was used to further systematically annotate the predicted genes (Kanehisa and Goto 2000).In this study, PacBio sequencing produced 6.06 GB and Illumina pair-end sequencing generated 6.12 GB of high-quality data (sequencing depth 125×). Prior to being assembled, the genome size was surveyed and evaluated to be 48.74 M. The size of the assembled TH15 genome was 46.85 Mb without gaps, and its GC content amounted to 47.5%. The genome assembled into 34 contigs with an N50 length of 4.56 Mb, ranging in length from 14,909 bp to 6.53 Mb. Among them, contig 19 (JAHREO010000019) was the 40-kb mitochondrial genome. Furthermore, completeness of the TH15 genome assembly was 100% and there were 290 complete BUSCOs, including 288 single-copy BUSCOs (99.3%) and 2 duplicated BUSCOs (0.7%). Other characteristics of the assembled genome are shown in Table 1.Table 1. Genome assembly statistics for the Fusarium oxysporum strain TH15VariablesStatisticsGenome assemble size (bp)46,852,391Sequence coverage125×Number of contigs34Contig N50 (bp)4,569,486GC content (%)47.53Largest contig length (bp)6,530,984Shortest contig length (bp)14,909BUSCO completeness (%)a100Number of predicted genes10,442Number of CAZymes735Genome accessionJAHREO000000000aBenchmarking Universal Single-Copy Ortholog.Table 1. Genome assembly statistics for the Fusarium oxysporum strain TH15View as image HTML Overall, 10,442 protein-coding genes for TH15 were predicted using the ab-initio- and homology-based methods. Transfer RNA (tRNA) and ribosomal RNA (rRNA) genes were predicted using tRNAscan-SE (Lowe and Eddy 1997) and RNAmmer (Lagesen et al. 2007) with default settings. We obtained 66 rRNAs and 317 tRNAs, respectively. Carbohydrate-active enzymes (CAZymes) are usually closely related to fungal pathogenicity and affect the interaction between fungi and their hosts (van den Brink and de Vries 2011). CAZymes were identified in the assembled genome by searching against the CAZy database, and 735 CAZymes were predicted, including 87 glycosyl transferases, 27 polysaccharide lyases, 135 carbohydrate esterases, 114 auxiliary activities, 24 carbohydrate-binding modules, and 348 glycoside hydrolases. We used RepeatMasker v4.0.5 software (Tempel 2012) with its default settings to predict repetitive sequences in the TH15 genome, and further classified these identified repetitive sequences. Interspersed repeats, also known as transposon elements (TEs), usually affect pathogenic variation of various fungi (Faino et al. 2016; Raffaele and Kamoun 2012). The total length of the identified repetitive sequence was 1.18 Mb, which accounted for 2.5% of the assembled whole genome. We identified 54 short interspersed retrotransposable element retrotransposons, 12 long interspersed retrotransposable element retrotransposons, 171 long terminal repeat elements, 19 DNA transposons, and 3,050 unclassified TEs in the TH15 genome. Cytochrome P450 enzymes are a large family of proteins that have heme as a prosthetic group. Here, we identified a total of 10,230 genes in the cytochrome P450 family using BLASTP (2.5.0+) software (Table 1). Furthermore, 10,424 (99.8%) genes were mapped to the NR database and 7,396 (70.8%) genes were mapped to Swiss-Prot database. Overall, 10,076 (96.5%) genes were mapped to the EuKaryotic Orthologous Groups database, and these were further classified into 25 categories (Fig. 1A). In addition, 9,805 (93.9%) genes were mapped to the KEGG database and divided into 48 different categories (Fig. 1B).Fig. 1. Functional classification of the Fusarium oxysporum strain TH15 genome based on the A, EuKaryotic Orthologous Groups (KOB) and B, Kyoto Encyclopedia of Genes and Genomes (KEGG) databases.Download as PowerPointIt was well known that an endophyte is capable of a synergistic interaction with its host plant by participating in three major metabolism processes. In this study, 1,562 genes were found to be involved in cellular nitrogen metabolic, 517 genes in carbohydrate metabolic, 280 genes in lipid metabolic, and 11 genes in nitrogen cycle metabolic. Furthermore, endophytes also can enhance plant growth through the synthesis of plant hormones (Taghavi et al. 2009). In this respect, four genes were annotated to be involved in hormone response (Supplementary Table S1). Endophytes can enter the plant root at sites of tissue damage via a process relying on active breakdown of plant cell walls. Surprisingly, 17 genes were involved in pectin metabolic and catabolic processes. Motility is a key characteristic of endophytes so that they can tend to colonize specific plant parts (Taghavi et al. 2010). In this study, one gene was annotated to be involved in cell motility, which indicated that TH15 might actively move toward plant roots, the preferred site of endophytic colonization. Plants rely on a variety of defense mechanisms against bacterial, viral, and fungal infections, including reactive oxygen species (Hammond-Kosack and Jones 1996). Correspondingly, 61 genes in the genome of TH15 were annotated to be involved in oxidative stress, which is consistent with the fact that this fungal endophyte must survive in an oxidative rhizosphere environment prior to host root colonization (Supplementary Table S1). In sum, the data provided here provide a better understanding of the endophytic F. oxysporum TH15 in plant growth regulation.Collectively, the combination of next- and third-generation sequencing technologies was successfully used here for whole-genome sequencing of F. oxysporum TH15. This newly assembled genome improves our understanding of the genomic characteristics of TH15 and the mechanism by which it might help regulate plant growth. F. oxysporum TH15 sequenced in this study is stored in the China General Microbiological Culture Collection Center, at the Institute of Microbiology, Chinese Academy of Sciences, Beijing, China (strain preservation number CGMCC23264). 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This is an open access article distributed under the CC BY-NC-ND 4.0 International license.DetailsFiguresLiterature CitedRelated Vol. 2, No. 3 2022ISSN:2690-5442 Download Metrics Article History Issue Date: 19 Sep 2022Published: 31 Mar 2022Accepted: 17 Jan 2022 Pages: 314-319 InformationCopyright © 2022 The Author(s).This is an open access article distributed under the CC BY-NC-ND 4.0 International license.Funding National Natural Science Foundation of ChinaGrant/Award Number: 31872181 Hangzhou Normal UniversityGrant/Award Number: 2021QDL062 KeywordsendophyteFusarium oxysporumgenome sequenceTetrastigma hemsleyanumThe author(s) declare no conflict of interest.PDF download