{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,18]],"date-time":"2026-01-18T01:50:28Z","timestamp":1768701028960,"version":"3.49.0"},"reference-count":59,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T00:00:00Z","timestamp":1672790400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008862","name":"China National Tobacco Corporation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100008862","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p><jats:italic>Rhizopus oryzae<\/jats:italic> is a destructive pathogen that frequently causes tobacco pole rot in curing chambers. Phenotypic characterization of the pathogen was conducted to provide basic biological and pathological information using Biolog Phenotype MicroArray (PM). In addition, the Y5 strain of <jats:italic>R. oryzae<\/jats:italic> was sequenced using Illumina HiSeq and Pacific Biosciences (PacBio) technologies. Using PM plates 1\u20138, 758 growth conditions were tested. Results indicated that <jats:italic>R. oryzae<\/jats:italic> could metabolize 54.21% of tested carbon sources, 86.84% of nitrogen sources, 100% of sulfur sources, and 98.31% of phosphorus sources. About 37 carbon compounds, including D-xylose, N-acetyl-D-glucosamine, D-sorbitol, \u03b2-methyl-D-glucoside, D-galactose, L-arabinose, and D-cellobiose, significantly supported the growth of the pathogen. PM 3 indicated the active nitrogen sources, including Gly-Asn, Ala-Asp., Ala-Gln, and uric acid. PM 6\u20138 showed 285 different nitrogen pathways, indicating that different combinations of different amino acids support the growth of the pathogen. Genome sequencing results showed that the <jats:italic>R. oryzae<\/jats:italic> Y5 strain had raw data assembled into 2,271 Mbp with an N50 value of 10,563\u2009bp. A genome sequence of 50.3\u2009Mb was polished and assembled into 53 contigs with an N50 length of 1,785,794\u2009bp, maximum contig length of 3,223,184\u2009bp, and a sum of contig lengths of 51,182,778\u2009bp. A total of 12,680 protein-coding genes were predicted using the Nonredundant, Gene Ontology, Clusters of Orthologous Groups, Kyoto Encyclopedia of Genes and Genomes, and SWISS-PROT databases. The genome sequence and annotation resources of <jats:italic>R. oryzae<\/jats:italic> provided a reference for studying its biological characteristics, trait-specific genes, pathogen-host interaction, pathogen evolution, and population genetic diversity. The phenomics and genome of <jats:italic>R. oryzae<\/jats:italic> will provide insights into microfungal biology, pathogen evolution, and the genetic diversity of epidemics.<\/jats:p>","DOI":"10.3389\/fmicb.2022.1031023","type":"journal-article","created":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T20:22:15Z","timestamp":1672863735000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Phenotypic analysis and genome sequence of Rhizopus oryzae strain Y5, the causal agent of tobacco pole rot"],"prefix":"10.3389","volume":"13","author":[{"given":"Zhen","family":"Li","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cai-hua","family":"Shi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yang","family":"Huang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Han-cheng","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wen-hong","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liu-ti","family":"Cai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,1,4]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"795","DOI":"10.3390\/ijms12010795","article-title":"Development of proteomics-based fungicides: new strategies for environmentally friendly control of fungal plant diseases","volume":"12","author":"Acero","year":"2011","journal-title":"Int. J. Mol. Sci."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1186\/s12864-015-1474-8","article-title":"Comparative genomic analysis of Ralstonia solanacearum reveals candidate genes for host specificity","volume":"16","author":"Ailloud","year":"2015","journal-title":"BMC Genomics"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1093\/nar\/28.1.45","article-title":"The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000","volume":"28","author":"Amos","year":"2000","journal-title":"NAR."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"2159","DOI":"10.1093\/nar\/gky066","article-title":"Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics","volume":"46","author":"Ardui","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1038\/75556","article-title":"Gene ontology: tool for the unification of biology","volume":"25","author":"Ashburner","year":"2000","journal-title":"Nat. Genet."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1093\/nar\/27.2.573","article-title":"Tandem repeats finder: a program to analyze DNA sequences","volume":"27","author":"Benson","year":"1999","journal-title":"NAR."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1246","DOI":"10.1101\/gr.186501","article-title":"Phenotype microarrays for high-throughput phenotypictesting and assay of gene function","volume":"11","author":"Bochner","year":"2001","journal-title":"Genome Res."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"D233","DOI":"10.1093\/nar\/gkn663","article-title":"The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics","volume":"37","author":"Cantarel","year":"2009","journal-title":"NAR"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"2136","DOI":"10.3389\/fmicb.2020.554051","article-title":"Fungal composition and diversity of the tobacco leaf phyllosphere during curing of leaves","volume":"11","author":"Chen","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"16","DOI":"10.16135\/j.issn1002-0861.2021.0081","article-title":"Pathogenicity and metabolic phenotypic characteristics of Rhizopus oryzae in tobacco under different osmotic pressure and pH environments","volume":"2022","author":"Chen","year":"2021","journal-title":"Tobacco Science & Technology."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1111\/mpp.12001","article-title":"Exploitation of genomics in fungicide research: current status and future perspectives","volume":"14","author":"Cools","year":"2013","journal-title":"Mol. Plant Pathol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.bbapap.2010.06.020","article-title":"Cytochrome P450 enzymes in the fungal kingdom","volume":"1814","author":"Cre\u0161nar","year":"2011","journal-title":"Biochim. Biophys. Acta"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1126\/science.1162986","article-title":"Real-timeDNA sequencing from single polymerase molecules","volume":"323","author":"Eid","year":"2009","journal-title":"Science"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1080\/00275514.1985.12025091","article-title":"Species and varieties in the Rhizopus arrhizus-Rhizopus oryzae group as indicated by their dna complementarity","volume":"77","author":"Ellis","year":"1985","journal-title":"Mycologia"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1111\/j.1558-5646.1985.tb00420.x","article-title":"Confidence limits on phylogenies: an approach using the bootstrap","volume":"39","author":"Felsenstein","year":"1985","journal-title":"Evolution"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"D136","DOI":"10.1093\/nar\/gkn766","article-title":"Rfam: updates to the RNA families database","volume":"37","author":"Gardner","year":"2009","journal-title":"NAR."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"103","DOI":"10.4141\/cjps72-013","article-title":"Rhizopus arrhizus causing pole rot of flue-cured tobacco in Ontario","volume":"52","author":"Gayed","year":"1972","journal-title":"Can. J. Plant Sci."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1094\/PDIS.2002.86.4.345","article-title":"Influence of wound type and storage duration on susceptibility of sweet potatoes to Rhizopus soft rot","volume":"86","author":"Holmes","year":"2002","journal-title":"Plant Dis."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"e63769","DOI":"10.1371\/journal.pone.0063769","article-title":"Aspergillus luchuensis, an industrially important black Aspergillus in East Asia","volume":"8","author":"Hong","year":"2013","journal-title":"PLoS One"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-05478-8","article-title":"Draft whole genome sequence of groundnut stem rot fungus Athelia rolfsii revealing genetic architect of its pathogenicity and virulence","volume":"7","author":"Iquebal","year":"2017","journal-title":"Sci. Rep."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e1000211","DOI":"10.1371\/journal.pgen.1000211","article-title":"High-throughput phenotypic characterization of Pseudomonas aeruginosa membrane transport genes","volume":"4","author":"Johnson","year":"2008","journal-title":"PLoS Genet."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"D354","DOI":"10.1093\/nar\/gkj102","article-title":"From genomics to chemical genomics: new developments in KEGG","volume":"34","author":"Kanehisa","year":"2006","journal-title":"NAR."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"277D","DOI":"10.1093\/nar\/gkh063","article-title":"The KEGG resource for deciphering the genome","volume":"32","author":"Kanehisa","year":"2004","journal-title":"NAR."},{"key":"ref25","first-page":"535","article-title":"Infection and decay of tobacco caused by Rhizopus oryzae\/die Infektion und F\u00e4ulnis von Tabak verursacht durch Rhizopus oryzae","volume":"110","author":"Kortekamp","year":"2003","journal-title":"J. Plant. Dis. Protect."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"3100","DOI":"10.1093\/nar\/gkm160","article-title":"RNAmmer: consistent and rapid annotation of ribosomal RNA genes","volume":"35","author":"Lagesen","year":"2007","journal-title":"NAR."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1093\/bioinformatics\/18.1.77","article-title":"Tolerating some redundancy significantly speeds up clustering of large protein databases","volume":"18","author":"Li","year":"2002","journal-title":"CCF TCBI."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1111\/jam.13011","article-title":"Portable lysis apparatus for rapid single-step DNA extraction of Bacillus subtilis","volume":"120","author":"Lim","year":"2016","journal-title":"J. Appl. Microbiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1038\/nature02651","article-title":"Role of transposable elements in heterochromatin and epigenetic control","volume":"430","author":"Lippman","year":"2004","journal-title":"Nature"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"1678","DOI":"10.1590\/1678-4324-2017160474","article-title":"Genome-wide identification, classification and expression analysis of the mildew resistance locus o (MLO) gene family in sweet orange (Citrus sinensis)","volume":"60","author":"Liu","year":"2017","journal-title":"Braz. Arch. Biol.Technol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"5114","DOI":"10.1073\/pnas.0600521103","article-title":"A previously undescribed pathway for pyrimidine catabolism","volume":"103","author":"Loh","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.ijfoodmicro.2017.06.012","article-title":"Rhizopus oryzae\u2013ancient microbial resource with importance in modern food industry","volume":"257","author":"Londo\u00f1o-Hern\u00e1ndez","year":"2017","journal-title":"Int. J. Food Microbiol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"955","DOI":"10.1093\/nar\/25.5.955","article-title":"tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence","volume":"25","author":"Lowe","year":"1997","journal-title":"NAR."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"e1000549","DOI":"10.1371\/journal.pgen.1000549","article-title":"Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication","volume":"5","author":"Ma","year":"2009","journal-title":"PLoS Genet."},{"key":"ref36","article-title":"The pathogen-host interactions database (phi-base): additions and future developments","volume-title":"Nucleic Acids Research (NAR)","author":"Martin","year":"2015"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"W339","DOI":"10.1093\/nar\/gkr466","article-title":"antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences","volume":"39","author":"Medema","year":"2011","journal-title":"NAR."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1016\/S0092-8674(00)80126-9","article-title":"The role of the genome project in determining gene function: insights from model organisms","volume":"86","author":"Miklos","year":"1996","journal-title":"Cells"},{"key":"ref39","article-title":"The transporter classification database","volume-title":"Nucleic Acids Research (NAR)","author":"Milton","year":"2014"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1093\/bioinformatics\/btp157","article-title":"Eddy SR: infernal 1.0: inference of RNA alignments","volume":"25","author":"Nawrocki","year":"2009","journal-title":"CCF TCBI."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"e000473","DOI":"10.1099\/mgen.0.000473","article-title":"Genetic diversity of clinical and environmental Mucorales isolates obtained from an investigation of mucormycosis cases among solid organ transplant recipients","volume":"6","author":"Nguyen","year":"2020","journal-title":"Microb. Genomics."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1038\/nmeth.1701","article-title":"SignalP 4.0: discriminating signal peptides from transmembrane regions","volume":"8","author":"Petersen","year":"2011","journal-title":"Nat. Methods"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41525-017-0042-3","article-title":"Cytogenomic identification and long-read single molecule real-time (SMRT) sequencing of aBardet\u2013Biedl syndrome 9(BBS9)","volume":"3","author":"Reiner","year":"2018","journal-title":"NPJ Genom. Med."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"2284","DOI":"10.1093\/nar\/gkn064","article-title":"Empirical comparison of ab initio repeat finding programs","volume":"36","author":"Saha","year":"2008","journal-title":"NAR"},{"key":"ref45","first-page":"406","article-title":"The neighbor-joining method: a new method for reconstructing phylogenetic trees","volume":"4","author":"Saitou","year":"1987","journal-title":"Mol. Biol. Evol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"1126","DOI":"10.1101\/gr.5144106","article-title":"Predicting essential genes in fungal genomes","volume":"16","author":"Seringhaus","year":"2006","journal-title":"Genome Res."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1093\/bioinformatics\/btn013","article-title":"Using native and syntenically mapped cDNA alignments to improve de novo gene finding","volume":"24","author":"Stanke","year":"2008","journal-title":"CCF TCBI."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"51","DOI":"10.3969\/j.issn.1006\u20136500.2018.02.013","article-title":"Effects of different curing process on tobacco mildew disease","volume":"24","author":"Su","year":"2018","journal-title":"Tianjin Agricultural Sciences."},{"key":"ref49","article-title":"Quicksand: hydrogel, granular matter, mercury (element), water circulation, non-newtonian fluid, viscosity","author":"Surhone","year":"2010"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"11030","DOI":"10.1073\/pnas.0404206101","article-title":"Prospects for inferring very large phylogenies by using the neighbor-joining method","volume":"101","author":"Tamura","year":"2004","journal-title":"PNAS"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1128\/JB.188.2.687-693.2006","article-title":"Phenotype microarray profiling of Staphylococcus aureus menD and hemB mutants with the small-colony-variant phenotype","volume":"188","author":"Von Eiff","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1094\/PDIS-08-15-0935-PDN","article-title":"Leaf and stem rot of tobacco (Nicotiana tabacum) caused by Rhizopus oryzae in closed curing barns in Guizhou Province of China","volume":"100","author":"Wang","year":"2016","journal-title":"Plant Dis."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"79","DOI":"10.3923\/ppj.2015.79.85","article-title":"Phenotypic analysis of Alternaria alternata, the causal agent of tobacco Brown spot","volume":"14","author":"Wang","year":"2015","journal-title":"Plant Pathology J."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"9","DOI":"10.3389\/fmicb.2018.00470","article-title":"Metabolic phenotype characterization of Botrytis cinerea, the causal agent of Gray Mold","volume":"13","author":"Wang","year":"","journal-title":"Front. Microbiol."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.13343\/j.cnki.wsxb.20150036","article-title":"Phenotypic analysis of Phytophthora parasitica by using high throughput phenotypic microarray","volume":"55","author":"Wang","year":"2015","journal-title":"Acta Microbiol Sin."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"743","DOI":"10.16801\/j.issn.1008-7303.2018.0095","article-title":"Pathogen detection, carbon metabolic phenotype analysis of Rhizopus oryzae from tobacco and its sensitivity to seven fungicides","volume":"20","author":"Wang","year":"","journal-title":"J. Pestic. Sci."},{"key":"ref59","doi-asserted-by":"crossref","DOI":"10.1201\/9781420040821","volume-title":"Pictorial atlas of soil and seed fungi: Morphologies of cultured fungi and key to species","author":"Watanabe","year":"2002"},{"key":"ref60","first-page":"95","article-title":"Host range of the lily pathogen Rhizopus oryzae","volume":"42","author":"Xu","year":"2020","journal-title":"J. yi chun University."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"62","DOI":"10.16213\/j.cnki.scjas.2018.1.011","article-title":"Study on color parameters and curing characteristics of flue-cured tobacco leaves in process ofmaturity","volume":"31","author":"Zhang","year":"2018","journal-title":"Southwest China J Agric Sci."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"4956","DOI":"10.1128\/JB.185.16.4956-4972.2003","article-title":"Phenotype microarray analysis of Escherichia coli K-12mutants with deletions of all two-component systems","volume":"185","author":"Zhou","year":"2003","journal-title":"J. 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