Genome assembly of the fungus Cochliobolus miyabeanus, and transcriptome analysis during early stages of infection on American wildrice (Zizania palustris L.)

Castell-Miller, Claudia V.; Gutierrez-Gonzalez, Juan J.; Tu, Zheng Jin; Bushley, Kathryn E.; Hainaut, Matthieu; Henrissat, Bernard; Samac, Deborah A.

doi:10.1371/journal.pone.0154122

Title: Genome assembly of the fungus Cochliobolus miyabeanus, and transcriptome analysis during early stages of infection on American wildrice (Zizania palustris L.)

Journal Article · Thu Jun 02 00:00:00 EDT 2016 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0154122· OSTI ID:1287181

Castell-Miller, Claudia V. ^[1]; Gutierrez-Gonzalez, Juan J. ^[2]; Tu, Zheng Jin ^[3]; Bushley, Kathryn E. ^[4]; Hainaut, Matthieu ^[5]; Henrissat, Bernard ^[6]; Samac, Deborah A. ^[7]

Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Pathology
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Agronomy and Plant Genetics; USDA-ARS-Plant Science Research Unit, St. Paul, MN (United States)
Mayo Clinic, Div. of Biomedical Statistics and Informatics, Rochester, MN (United States)
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Biology
Aix-Marseille Univ., Marseille (France). CNRS UMR 7257
Aix-Marseille Univ., Marseille (France). CNRS UMR 7257; King Abdulaziz Univ., Jeddah (Saudi Arabia). Dept. of Biological Sciences
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Pathology; USDA-ARS-Plant Science Research Unit, St. Paul, MN (United States)

Here, the fungus Cochliobolus miyabeanus causes severe leaf spot disease on rice (Oryza sativa) and two North American specialty crops, American wildrice (Zizania palustris) and switchgrass (Panicum virgatu). Despite the importance of C. miyabeanus as a disease-causing agent in wildrice, little is known about either the mechanisms of pathogenicity or host defense responses. To start bridging these gaps, the genome of C. miyabeanus strain TG12bL2 was shotgun sequenced using Illumina technology. The genome assembly consists of 31.79 Mbp in 2,378 scaffolds with an N₅₀ = 74,921. It contains 11,000 predicted genes of which 94.5% were annotated. Approximately 10% of total gene number is expected to be secreted. The C. miyabeanus genome is rich in carbohydrate active enzymes, and harbors 187 small secreted peptides (SSPs) and some fungal effector homologs. Detoxification systems were represented by a variety of enzymes that could offer protection against plant defense compounds. The non-ribosomal peptide synthetases and polyketide synthases (PKS) present were common to other Cochliobolus species. Additionally, the fungal transcriptome was analyzed at 48 hours after inoculation in planta. A total of 10,674 genes were found to be expressed, some of which are known to be involved in pathogenicity or response to host defenses including hydrophobins, cutinase, cell wall degrading enzymes, enzymes related to reactive oxygen species scavenging, PKS, detoxification systems, SSPs, and a known fungal effector. This work will facilitate future research on C. miyabeanus pathogen-associated molecular patterns and effectors, and in the identification of their corresponding wildrice defense mechanisms.

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Research Organization:: Univ. of Minnesota, St. Paul, MN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1287181

Journal Information:: PLoS ONE, Vol. 11, Issue 6; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 9 works

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References (106)

Improved Prediction of Signal Peptides: SignalP 3.0 Dyrløv Bendtsen, Jannick; Nielsen, Henrik; von Heijne, Gunnar Journal of Molecular Biology, Vol. 340, Issue 4, p. 783-795 https://doi.org/10.1016/j.jmb.2004.05.028	journal	July 2004
Purification, Characterization, and Amino Acid Sequence of Cerato-platanin, a New Phytotoxic Protein from Ceratocystis fimbriata f. sp. platani Pazzagli, Luigia; Cappugi, Gianni; Manao, Giampaolo Journal of Biological Chemistry, Vol. 274, Issue 35 https://doi.org/10.1074/jbc.274.35.24959	journal	August 1999
Conserved Fungal LysM Effector Ecp6 Prevents Chitin-Triggered Immunity in Plants de Jonge, R.; Peter van Esse, H.; Kombrink, A. Science, Vol. 329, Issue 5994 https://doi.org/10.1126/science.1190859	journal	August 2010
TopHat: discovering splice junctions with RNA-Seq Trapnell, Cole; Pachter, Lior; Salzberg, Steven L. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp120	journal	March 2009
Activation of an AP1-Like Transcription Factor of the Maize Pathogen Cochliobolus heterostrophus in Response to Oxidative Stress and Plant Signals Lev, Sophie; Hadar, Ruthi; Amedeo, Paolo Eukaryotic Cell, Vol. 4, Issue 2 https://doi.org/10.1128/ec.4.2.443-454.2005	journal	February 2005
Isolation of the Carbon Catabolite Repressor ( CREA ) Gene from the Plant-pathogenic Fungus Cochliobolus carbonum Tonukari, Nyerhovwo J.; Scott-Craig, John S.; Walton, Jonathan D. DNA Sequence, Vol. 14, Issue 2 https://doi.org/10.1080/1042517031000073727	journal	January 2003
A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Yang, G.; Rose, M. S.; Turgeon, B. G. The Plant Cell, Vol. 8, Issue 11 https://doi.org/10.1105/tpc.8.11.2139	journal	November 1996
Cytochrome P450 enzymes in the fungal kingdom Črešnar, B.; Petrič, Š. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1814, Issue 1 https://doi.org/10.1016/j.bbapap.2010.06.020	journal	January 2011
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
Three Extracellular Proteases from Cochliobolus carbonum: Cloning and Targeted Disruption of ALP1 Murphy, Jenifer M. Molecular Plant-Microbe Interactions, Vol. 9, Issue 4 https://doi.org/10.1094/mpmi-9-0290	journal	January 1996
Symbol Nomenclature for Graphical Representations of Glycans Varki, Ajit; Cummings, Richard D.; Aebi, Markus Glycobiology, Vol. 25, Issue 12 https://doi.org/10.1093/glycob/cwv091	journal	November 2015
Fungal enzyme sets for plant polysaccharide degradation van den Brink, Joost; de Vries, Ronald P. Applied Microbiology and Biotechnology, Vol. 91, Issue 6, p. 1477-1492 https://doi.org/10.1007/s00253-011-3473-2	journal	July 2011
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Leaf spot on switch grass ( Panicum virgatum ), symptoms of a new disease caused by Bipolaris oryzae Krupinsky, J. M.; Berdahl, J. D.; Schoch, C. L. Canadian Journal of Plant Pathology, Vol. 26, Issue 3 https://doi.org/10.1080/07060660409507155	journal	September 2004
Tricking the Guard: Exploiting Plant Defense for Disease Susceptibility Lorang, J.; Kidarsa, T.; Bradford, C. S. Science, Vol. 338, Issue 6107 https://doi.org/10.1126/science.1226743	journal	October 2012
Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi Ohm, Robin A.; Feau, Nicolas; Henrissat, Bernard PLoS Pathogens, Vol. 8, Issue 12 https://doi.org/10.1371/journal.ppat.1003037	journal	December 2012
CYP53A15 of Cochliobolus lunatus, a Target for Natural Antifungal Compounds ^† Podobnik, Barbara; Stojan, Jure; Lah, Ljerka Journal of Medicinal Chemistry, Vol. 51, Issue 12 https://doi.org/10.1021/jm800030e	journal	June 2008
Two glucose/xylose transporter genes from the yeast Candida intermedia: first molecular characterization of a yeast xylose–H⁺ symporter Leandro, Maria José; Gonçalves, Paula; Spencer-Martins, Isabel Biochemical Journal, Vol. 395, Issue 3, p. 543-549 https://doi.org/10.1042/BJ20051465	journal	May 2006
Cloning, purification and characterisation of brassinin glucosyltransferase, a phytoalexin-detoxifying enzyme from the plant pathogen Sclerotinia sclerotiorum Sexton, Adrienne C.; Minic, Zoran; Cozijnsen, Anton J. Fungal Genetics and Biology, Vol. 46, Issue 2 https://doi.org/10.1016/j.fgb.2008.10.014	journal	February 2009
The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species Bolton, Melvin D.; van Esse, H. Peter; Vossen, Jack H. Molecular Microbiology, Vol. 69, Issue 1 https://doi.org/10.1111/j.1365-2958.2008.06270.x	journal	July 2008
Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes Kroken, S.; Glass, N. L.; Taylor, J. W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2532165100	journal	December 2003
Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea Cuesta Arenas, Yaite; Kalkman, Eric R. I. C.; Schouten, Alexander Physiological and Molecular Plant Pathology, Vol. 74, Issue 5-6 https://doi.org/10.1016/j.pmpp.2010.06.003	journal	September 2010
Simultaneous Transcriptome Analysis of Sorghum and Bipolaris sorghicola by Using RNA-seq in Combination with De Novo Transcriptome Assembly Yazawa, Takayuki; Kawahigashi, Hiroyuki; Matsumoto, Takashi PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0062460	journal	April 2013
Fungal Transporters Involved in Efflux of Natural Toxic Compounds and Fungicides Del Sorbo, Giovanni; Schoonbeek, Henk-jan; De Waard, Maarten A. Fungal Genetics and Biology, Vol. 30, Issue 1 https://doi.org/10.1006/fgbi.2000.1206	journal	June 2000
Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence de Waard, Maarten A.; Andrade, Alan C.; Hayashi, Keisuke Pest Management Science, Vol. 62, Issue 3 https://doi.org/10.1002/ps.1150	journal	January 2006
NPS6 , Encoding a Nonribosomal Peptide Synthetase Involved in Siderophore-Mediated Iron Metabolism, Is a Conserved Virulence Determinant of Plant Pathogenic Ascomycetes Oide, Shinichi; Moeder, Wolfgang; Krasnoff, Stuart The Plant Cell, Vol. 18, Issue 10 https://doi.org/10.1105/tpc.106.045633	journal	October 2006
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Histone deacetylases in fungi: novel members, new facts Trojer, P. Nucleic Acids Research, Vol. 31, Issue 14 https://doi.org/10.1093/nar/gkg473	journal	July 2003
Molecular Cloning and Characterization of cel2 from the Fungus Cochlibolus carbonum Ahn, Joong-Hoon; Sposato, Paola; Kim, Su-Il Bioscience, Biotechnology, and Biochemistry, Vol. 65, Issue 6, p. 1406-1411 https://doi.org/10.1271/bbb.65.1406	journal	January 2001
Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T‐toxin Turgeon, B. Gillian; Baker, Scott E. Advances in Genetics, Vol. 57 https://doi.org/10.1016/S0065-2660(06)57006-3	book	January 2007
β-Glucan biosynthesis inhibitors isolated from fungi as hyphal malformation inducer Fukushima, Yoshito; Sakagami, Youji; Marumo, Shingo Bioorganic & Medicinal Chemistry Letters, Vol. 3, Issue 6 https://doi.org/10.1016/s0960-894x(00)80319-4	journal	June 1993
Gene Expression Modulation of Two Biosynthesis Pathways via Signal Transduction in Cochliobolus heterostrophus Degani, Ofir Advances in Bioscience and Biotechnology, Vol. 05, Issue 04 https://doi.org/10.4236/abb.2014.54042	journal	January 2014
Molecular Characterization and Functional Analysis of MgNLP , the Sole NPP1 Domain–Containing Protein, from the Fungal Wheat Leaf Pathogen Mycosphaerella graminicola Motteram, Juliet; Küfner, Isabell; Deller, Siân Molecular Plant-Microbe Interactions®, Vol. 22, Issue 7 https://doi.org/10.1094/mpmi-22-7-0790	journal	July 2009
Disruption of phacA , an Aspergillus nidulans Gene Encoding a Novel Cytochrome P450 Monooxygenase Catalyzing Phenylacetate 2-Hydroxylation, Results in Penicillin Overproduction Mingot, José Manuel; Peñalva, Miguel Angel; Fernández-Cañón, José Manuel Journal of Biological Chemistry, Vol. 274, Issue 21 https://doi.org/10.1074/jbc.274.21.14545	journal	May 1999
Creating and screening Cochliobolus heterostrophus non-ribosomal peptide synthetase mutants Gillian Turgeon, B.; Oide, Shinichi; Bushley, Kathryn Mycological Research, Vol. 112, Issue 2 https://doi.org/10.1016/j.mycres.2007.10.012	journal	February 2008
Wild Rice Domestication, Fungal Brown Spot Disease, and the Future of Commercial Production in Minnesota Johnson, David R. Plant Disease, Vol. 76, Issue 12 https://doi.org/10.1094/pd-76-1193	journal	January 1992
Transcription of the yeast TNA1 gene is not only regulated by nicotinate but also by p -aminobenzoate Klebl, F.; Zillig, M.; Sauer, N. FEBS Letters, Vol. 481, Issue 1 https://doi.org/10.1016/s0014-5793(00)01959-1	journal	September 2000
Two Polyketide Synthase-Encoding Genes Are Required for Biosynthesis of the Polyketide Virulence Factor, T-toxin, by Cochliobolus heterostrophus Baker, Scott E.; Kroken, Scott; Inderbitzin, Patrik Molecular Plant-Microbe Interactions, Vol. 19, Issue 2 https://doi.org/10.1094/mpmi-19-0139	journal	February 2006
Cochliobolus Heterostrophus. Cause of Southern Corn Leaf Blight Yoder, O. C. Genetics of Plant Pathogenic Fungi https://doi.org/10.1016/B978-0-12-033706-4.50009-8	book	January 1988
(1,3;1,4)-β-D-Glucans in Cell Walls of the Poaceae, Lower Plants, and Fungi: A Tale of Two Linkages Burton, Rachel A.; Fincher, Geoffrey B. Molecular Plant, Vol. 2, Issue 5 https://doi.org/10.1093/mp/ssp063	journal	September 2009
Phylogeny and biogeography of the eastern Asian–North American disjunct wild-rice genus (Zizania L., Poaceae) Xu, Xinwei; Walters, Christina; Antolin, Michael F. Molecular Phylogenetics and Evolution, Vol. 55, Issue 3 https://doi.org/10.1016/j.ympev.2009.11.018	journal	June 2010
Development of Fungal Brown Spot and Spot Blotch on Cultivated Wild Rice in Minnesota Nyvall, R. F.; Percich, J. A. Plant Disease, Vol. 83, Issue 10 https://doi.org/10.1094/pdis.1999.83.10.936	journal	October 1999
Fungal LysM effectors: extinguishers of host immunity? de Jonge, Ronnie; Thomma, Bart P. H. J. Trends in Microbiology, Vol. 17, Issue 4 https://doi.org/10.1016/j.tim.2009.01.002	journal	April 2009
Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions Seidl, Verena Fungal Biology Reviews, Vol. 22, Issue 1 https://doi.org/10.1016/j.fbr.2008.03.002	journal	February 2008
CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes Parra, G.; Bradnam, K.; Korf, I. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm071	journal	March 2007
A Gene Related to Yeast HOS2 Histone Deacetylase Affects Extracellular Depolymerase Expression and Virulence in a Plant Pathogenic Fungus Baidyaroy, Dipnath; Brosch, Gerald; Ahn, Joong-hoon The Plant Cell, Vol. 13, Issue 7 https://doi.org/10.2307/3871389	journal	July 2001
Phytotoxins Produced by Germinating Spores of Bipolaris oryzae Xiao, J. Z. Phytopathology, Vol. 81, Issue 1 https://doi.org/10.1094/Phyto-81-58	journal	January 1991
The Cochliobolus carbonum SNF1 Gene Is Required for Cell Wall–Degrading Enzyme Expression and Virulence on Maize Tonukari, Nyerhovwo J.; Scott-Craig, John S.; Waltonb, Jonathan D. The Plant Cell, Vol. 12, Issue 2 https://doi.org/10.1105/tpc.12.2.237	journal	February 2000
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training Ter-Hovhannisyan, V.; Lomsadze, A.; Chernoff, Y. O. Genome Research, Vol. 18, Issue 12 https://doi.org/10.1101/gr.081612.108	journal	October 2008
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
A Eukaryotic Alanine Racemase Gene Involved in Cyclic Peptide Biosynthesis Cheng, Yi-Qiang; Walton, Jonathan D. Journal of Biological Chemistry, Vol. 275, Issue 7 https://doi.org/10.1074/jbc.275.7.4906	journal	February 2000
A MAP kinase gene, BMK1, is required for conidiation and pathogenicity in the rice leaf spot pathogen Bipolaris oryzae Moriwaki, Akihiro; Kihara, Junichi; Mori, Chie Microbiological Research, Vol. 162, Issue 2 https://doi.org/10.1016/j.micres.2006.01.014	journal	April 2007
An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins Kulkarni, Resham D.; Kelkar, Hemant S.; Dean, Ralph A. Trends in Biochemical Sciences, Vol. 28, Issue 3 https://doi.org/10.1016/s0968-0004(03)00025-2	journal	March 2003
Glucose uptake and growth of glucose-limited chemostat cultures of Aspergillus niger and a disruptant lacking MstA, a high-affinity glucose transporter Jorgensen, T. R.; vanKuyk, P. A.; Poulsen, B. R. Microbiology, Vol. 153, Issue 6 https://doi.org/10.1099/mic.0.2006/005090-0	journal	June 2007
Structure of victorin C, the major host-selective toxin fromCochliobolus victoriae Wolpert, T. J.; Macko, V.; Acklin, W. Experientia, Vol. 41, Issue 12 https://doi.org/10.1007/BF01964789	journal	December 1985
Endopolygalacturonase is not required for pathogenicity of Cochliobolus carbonum on maize. Scott-Craig, J. S.; Panaccione, D. G.; Cervone, F. The Plant Cell, Vol. 2, Issue 12 https://doi.org/10.1105/tpc.2.12.1191	journal	December 1990
A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum Pitkin, J. W.; Panaccione, D. G.; Walton, J. D. Microbiology, Vol. 142, Issue 6 https://doi.org/10.1099/13500872-142-6-1557	journal	June 1996
Cloning, disruption, and expression of two endo-beta 1, 4-xylanase genes, XYL2 and XYL3, from Cochliobolus carbonum Apel-Birkhold, P. C.; Walton, J. D. Applied and Environmental Microbiology, Vol. 62, Issue 11 https://doi.org/10.1128/aem.62.11.4129-4135.1996	journal	November 1996
Analysis and annotation of the hexaploid oat seed transcriptome Gutierrez-Gonzalez, Juan J.; Tu, Zheng; Garvin, David F. BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-471	journal	January 2013
Hydrophobins—Unique Fungal Proteins Bayry, Jagadeesh; Aimanianda, Vishukumar; Guijarro, J. Iñaki PLoS Pathogens, Vol. 8, Issue 5 https://doi.org/10.1371/journal.ppat.1002700	journal	May 2012
Endopolygalacturonase Is Not Required for Pathogenicity of Cochliobolus carbonum on Maize Scott-Craig, John S.; Panaccione, Daniel G.; Cervone, Felice The Plant Cell, Vol. 2, Issue 12 https://doi.org/10.2307/3869339	journal	December 1990
Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes Moktali, Venkatesh; Park, Jongsun; Fedorova-Abrams, Natalie D. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-525	journal	January 2012
Intracellular Siderophores Are Essential for Ascomycete Sexual Development in Heterothallic Cochliobolus heterostrophus and Homothallic Gibberella zeae Oide, Shinichi; Krasnoff, Stuart B.; Gibson, Donna M. Eukaryotic Cell, Vol. 6, Issue 8 https://doi.org/10.1128/ec.00111-07	journal	June 2007
AP1-mediated Multidrug Resistance in Saccharomyces cerevisiae Requires FLR1 Encoding a Transporter of the Major Facilitator Superfamily Alarco, Anne-Marie; Balan, Inga; Talibi, Driss Journal of Biological Chemistry, Vol. 272, Issue 31 https://doi.org/10.1074/jbc.272.31.19304	journal	August 1997
Efflux in Fungi: La Pièce de Résistance Coleman, Jeffrey J.; Mylonakis, Eleftherios PLoS Pathogens, Vol. 5, Issue 6 https://doi.org/10.1371/journal.ppat.1000486	journal	June 2009
FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes Al-Shahrour, F.; Diaz-Uriarte, R.; Dopazo, J. Bioinformatics, Vol. 20, Issue 4 https://doi.org/10.1093/bioinformatics/btg455	journal	January 2004
Nonribosomal peptides: from genes to products Schwarzer, Dirk; Finking, Robert; Marahiel, Mohamed A. Natural Product Reports, Vol. 20, Issue 3 https://doi.org/10.1039/b111145k	journal	January 2003
Gepard: a rapid and sensitive tool for creating dotplots on genome scale Krumsiek, J.; Arnold, R.; Rattei, T. Bioinformatics, Vol. 23, Issue 8 https://doi.org/10.1093/bioinformatics/btm039	journal	February 2007
Cloning and characterization of the PDA6-1 gene encoding a fungal cytochrome P-450 which detoxifies the phytoalexin pisatin from garden pea Reimmann, Cornelia; VanEtten, Hans D. Gene, Vol. 146, Issue 2 https://doi.org/10.1016/0378-1119(94)90296-8	journal	September 1994
Helminthosporium oryzae toxin suppresses phenol metabolism in rice plants and aids pathogen colonization Vidhyasekaran, P.; Borromeo, E. S.; Mew, T. W. Physiological and Molecular Plant Pathology, Vol. 41, Issue 5 https://doi.org/10.1016/0885-5765(92)90018-Q	journal	November 1992
Functional analysis of the Alternaria brassicicola non-ribosomal peptide synthetase gene AbNPS2 reveals a role in conidial cell wall construction Kim, Kwang-Hyung; Cho, Yangrae; La Rota, Mauricio Molecular Plant Pathology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1364-3703.2006.00366.x	journal	January 2007
Correction: Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum Kleemann, Jochen; Rincon-Rivera, Linda J.; Takahara, Hiroyuki PLoS Pathogens, Vol. 8, Issue 8 https://doi.org/10.1371/annotation/0f398a0c-dfda-4277-b172-4ff9cb31aec3	journal	August 2012
Transcriptional regulation of the Saccharomyces cerevisiae DAL5 gene family and identification of the high affinity nicotinic acid permease TNA1 ( YGR260w ) Llorente, Bertrand; Dujon, Bernard FEBS Letters, Vol. 475, Issue 3 https://doi.org/10.1016/s0014-5793(00)01698-7	journal	June 2000
Glycosyltransferases and their products: cryptococcal variations on fungal themes Klutts, James Stacey; Yoneda, Aki; Reilly, Morgann C. FEMS Yeast Research, Vol. 6, Issue 4 https://doi.org/10.1111/j.1567-1364.2006.00054.x	journal	June 2006
Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships Bushley, Kathryn E.; Turgeon, B. Gillian BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-26	journal	January 2010
Analysis of Two in Planta Expressed LysM Effector Homologs from the Fungus Mycosphaerella graminicola Reveals Novel Functional Properties and Varying Contributions to Virulence on Wheat Marshall, Rosalind; Kombrink, Anja; Motteram, Juliet Plant Physiology, Vol. 156, Issue 2 https://doi.org/10.1104/pp.111.176347	journal	April 2011
Proteomics of rice and Cochliobolus miyabeanus fungal interaction: Insight into proteins at intracellular and extracellular spaces Kim, Jin Yeong; Wu, Jingni; Kwon, Soon Jae PROTEOMICS, Vol. 14, Issue 20 https://doi.org/10.1002/pmic.201400066	journal	August 2014
A Decarboxylase Encoded at the Cochliobolus heterostrophus Translocation-Associated Tox1B Locus Is Required for Polyketide (T-toxin) Biosynthesis and High Virulence on T-cytoplasm Maize Rose, Mark S.; Yun, Sung-Hwan; Asvarak, Thipa Molecular Plant-Microbe Interactions®, Vol. 15, Issue 9 https://doi.org/10.1094/MPMI.2002.15.9.883	journal	September 2002
Wild Rice Yield Losses Associated with Growth-Stage-Specific Fungal Brown Spot Epidemics Kohls, C. L. Plant Disease, Vol. 71, Issue 5 https://doi.org/10.1094/PD-71-0419	journal	January 1987
The biology of ophiobolins Au, T. K.; Chick, Wallace S. H.; Leung, P. C. Life Sciences, Vol. 67, Issue 7 https://doi.org/10.1016/s0024-3205(00)00668-8	journal	July 2000
Cerato-platanin protein is located in the cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani Boddi, Silvia; Comparini, Cecilia; Calamassi, Roberto FEMS Microbiology Letters, Vol. 233, Issue 2 https://doi.org/10.1111/j.1574-6968.2004.tb09501.x	journal	April 2004
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
EST mining identifies proteins putatively secreted by the anthracnose pathogen Colletotrichum truncatum Bhadauria, Vijai; Banniza, Sabine; Vandenberg, Albert BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-327	journal	June 2011
Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor Kaku, H.; Nishizawa, Y.; Ishii-Minami, N. Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0508882103	journal	July 2006
Cerato-platanins: Elicitors and effectors Pazzagli, Luigia; Seidl-Seiboth, Verena; Barsottini, Mario Plant Science, Vol. 228 https://doi.org/10.1016/j.plantsci.2014.02.009	journal	November 2014
Effect of Calcium Silicate on Blast and Brown Spot Intensities and Yields of Rice Datnoff, L. E. Plant Disease, Vol. 75, Issue 7 https://doi.org/10.1094/PD-75-0729	journal	January 1991
Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots Stergiopoulos, I.; van den Burg, H. A.; Okmen, B. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.1002910107	journal	April 2010
A novel class of gene controlling virulence in plant pathogenic ascomycete fungi Lu, S. -W.; Kroken, S.; Lee, B. -N. Proceedings of the National Academy of Sciences, Vol. 100, Issue 10 https://doi.org/10.1073/pnas.0931375100	journal	May 2003
LysM receptors recognize friend and foe Knogge, Wolfgang; Scheel, Dierk Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0604601103	journal	July 2006
Rapid preparation of DNA from filamentous fungi Raeder, U.; Broda, P. Letters in Applied Microbiology, Vol. 1, Issue 1 https://doi.org/10.1111/j.1472-765X.1985.tb01479.x	journal	January 1985
Fungal chitinases: diversity, mechanistic properties and biotechnological potential Hartl, Lukas; Zach, Simone; Seidl-Seiboth, Verena Applied Microbiology and Biotechnology, Vol. 93, Issue 2 https://doi.org/10.1007/s00253-011-3723-3	journal	December 2011
Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies Zerbino, Daniel R. Current Protocols in Bioinformatics, Vol. 31, Issue 1 https://doi.org/10.1002/0471250953.bi1105s31	journal	September 2010
Targeted Mutants of Cochliobolus carbonum Lacking the Two Major Extracellular Polygalacturonases Scott-Craig, John S.; Cheng, Yi-Qiang; Cervone, Felice Applied and Environmental Microbiology, Vol. 64, Issue 4 https://doi.org/10.1128/aem.64.4.1497-1503.1998	journal	April 1998
G-Protein β Subunit of Cochliobolus heterostrophus Involved in Virulence, Asexual and Sexual Reproductive Ability, and Morphogenesis Ganem, Sherif; Lu, Shun-Wen; Lee, Bee-Na Eukaryotic Cell, Vol. 3, Issue 6 https://doi.org/10.1128/ec.3.6.1653-1663.2004	journal	December 2004
Novel phacB-Encoded Cytochrome P450 Monooxygenase from Aspergillus nidulans with 3-Hydroxyphenylacetate 6-Hydroxylase and 3,4-Dihydroxyphenylacetate 6-Hydroxylase Activities Ferrer-Sevillano, Francisco; Fernández-Cañón, José M. Eukaryotic Cell, Vol. 6, Issue 3 https://doi.org/10.1128/ec.00226-06	journal	December 2006
Carbohydrate-binding modules: fine-tuning polysaccharide recognition Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J. Biochemical Journal, Vol. 382, Issue 3 https://doi.org/10.1042/BJ20040892	journal	September 2004
A putative branched-chain-amino-acid transaminase gene required for HC-toxin biosynthesis and pathogenicity in Cochliobolus carbonum The GenBank accession number for the nucleotide sequence reported in this paper is AF157629. Cheng, Yi-Qiang; Ahn, Joong-Hoon; Walton, Jonathan D. Microbiology, Vol. 145, Issue 12 https://doi.org/10.1099/00221287-145-12-3539	journal	December 1999
Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice: LysM receptors for rice chitin signaling Shimizu, Takeo; Nakano, Takuto; Takamizawa, Daisuke The Plant Journal, Vol. 64, Issue 2 https://doi.org/10.1111/j.1365-313X.2010.04324.x	journal	September 2010
The Cochliobolus Carbonum SNF1 Gene Is Required for Cell Wall-Degrading Enzyme Expression and Virulence on Maize Tonukari, Nyerhovwo J.; Scott-Craig, John S.; Walton, Jonathan D. The Plant Cell, Vol. 12, Issue 2 https://doi.org/10.2307/3870925	journal	February 2000
Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy Qutob, Dinah; Kamoun, Sophien; Gijzen, Mark The Plant Journal, Vol. 32, Issue 3 https://doi.org/10.1046/j.1365-313x.2002.01439.x	journal	November 2002
The In Planta-Produced Extracellular Proteins ECP1 and ECP2 of Cladosporium fulvum Are Virulence Factors Laugé, Richard; Joosten, Matthieu H. A. J.; Van den Ackerveken, Guido F. J. M. Molecular Plant-Microbe Interactions®, Vol. 10, Issue 6 https://doi.org/10.1094/MPMI.1997.10.6.725	journal	August 1997
A Gene Related to Yeast HOS2 Histone Deacetylase Affects Extracellular Depolymerase Expression and Virulence in a Plant Pathogenic Fungus Baidyaroy, D. THE PLANT CELL ONLINE, Vol. 13, Issue 7 https://doi.org/10.1105/tpc.13.7.1609	journal	July 2001
CCL5 derived from tumor-associated macrophages promotes prostate cancer stem cells and metastasis via activating β-catenin/STAT3 signaling Huang, Renlun; Wang, Shengqi; Wang, Neng Cell Death & Disease, Vol. 11, Issue 4 https://doi.org/10.1038/s41419-020-2435-y	journal	April 2020
Functional Analysis of All Nonribosomal Peptide Synthetases in Cochliobolus heterostrophus Reveals a Factor, NPS6, Involved in Virulence and Resistance to Oxidative Stress Lee, Bee-Na; Kroken, Scott; Chou, David Y. T. Eukaryotic Cell, Vol. 4, Issue 3 https://doi.org/10.1128/ec.4.3.545-555.2005	journal	March 2005
The cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungus Cochliobolus carbonum is encoded by a 15.7-kilobase open reading frame. Scott-Craig, J. S.; Panaccione, D. G.; Pocard, J. A. Journal of Biological Chemistry, Vol. 267, Issue 36 https://doi.org/10.1016/S0021-9258(18)35714-4	journal	December 1992

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Genome sequence and spore germination-associated transcriptome analysis of Corynespora cassiicola from cucumber Gao, Shigang; Zeng, Rong; Xu, Lihui BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-01873-w	journal	July 2020

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
plant-pathogenic fungus
cyclic peptide biosynthesis
polyketide virulence factor
f-sp platani
functional-analysis
brown spot
t-toxin
hc-toxin
rna-seq
cytochrome-p450 monooxygenase
fungal genomics
protein domains
fungal genetics
transcriptome analysis
pathogenesis
genomic databases
plant genomics
fungi