The evolution and pathogenic mechanisms of the rice sheath blight pathogen

Rhizoctonia solani is a major fungal pathogen of rice (Oryza sativa L.) that causes great yield losses in all rice-growing regions of the world. Here we report the draft genome sequence of the rice sheath blight disease pathogen, R. solani AG1 IA, assembled using next-generation Illumina Genome Analyser sequencing technologies. The genome encodes a large and diverse set of secreted proteins, enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, which probably reflect an exclusive necrotrophic lifestyle. We find few repetitive elements, a closer relationship to Agaricomycotina among Basidiomycetes, and expand protein domains and families. Among the 25 candidate pathogen effectors identified according to their functionality and evolution, we validate 3 that trigger crop defence responses; hence we reveal the exclusive expression patterns of the pathogenic determinants during host infection.

[1]  A. Ogoshi,et al.  Ecology and Pathogenicity of Anastomosis and Intraspecific Groups of Rhizoctonia Solani Kuhn , 1987 .

[2]  M. Borodovsky,et al.  Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. , 2008, Genome research.

[3]  H. Kanuka,et al.  Legionella Metaeffector Exploits Host Proteasome to Temporally Regulate Cognate Effector , 2010, PLoS pathogens.

[4]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[5]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[6]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[7]  R. Yi,et al.  A-Mating-Type Gene Expression Can Drive Clamp Formation in the Bipolar Mushroom Pholiota microspora (Pholiota nameko) , 2010, Eukaryotic Cell.

[8]  Jameel Akhtar,et al.  Occurrence of banded leaf and sheath blight of maize in Jharkhand with reference to diversity in Rhizoctonia solani. , 2009 .

[9]  P. Solomon,et al.  New developments in pathogenicity and virulence of necrotrophs. , 2010, Current opinion in plant biology.

[10]  Huanming Yang,et al.  De novo assembly of human genomes with massively parallel short read sequencing. , 2010, Genome research.

[11]  D. Nelson,et al.  Progress in tracing the evolutionary paths of cytochrome P450. , 2011, Biochimica et biophysica acta.

[12]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[13]  S. Schornack,et al.  Recent developments in effector biology of filamentous plant pathogens , 2010, Cellular microbiology.

[14]  C. Walsh,et al.  Cytosine methylation and the ecology of intragenomic parasites. , 1997, Trends in genetics : TIG.

[15]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[16]  A. Blinov,et al.  Open Access Research Article Evolutionary Genomics Revealed Interkingdom Distribution of Tcn1-like Chromodomain-containing Gypsy Ltr Retrotransposons among Fungi and Plants , 2022 .

[17]  Pavel A. Pevzner,et al.  De novo identification of repeat families in large genomes , 2005, ISMB.

[18]  K. Korhonen,et al.  An unknown mechanism promotes somatic incompatibility in Ceratobasidium bicorne , 2003, Mycologia.

[19]  J. Bennett,et al.  Fungal secondary metabolism — from biochemistry to genomics , 2005, Nature Reviews Microbiology.

[20]  Anders Gorm Pedersen,et al.  Neural Network Prediction of Translation Initiation Sites in Eukaryotes: Perspectives for EST and Genome Analysis , 1997, ISMB.

[21]  Xiaoying Zhan,et al.  Genome-wide prediction of G protein-coupled receptors in Verticillium spp. , 2010, Fungal biology.

[22]  B. McDonald,et al.  Divergence between sympatric rice- and maize-infecting populations of Rhizoctonia solani AG-1 IA from Latin America. , 2010, Phytopathology.

[23]  Cathryn J. Rehmeyer,et al.  The genome sequence of the rice blast fungus Magnaporthe grisea , 2005, Nature.

[24]  D. E. Groth,et al.  Effects of cultivar resistance and single fungicide application on rice sheath blight, yield, and quality , 2008 .

[25]  S. Brunak,et al.  Locating proteins in the cell using TargetP, SignalP and related tools , 2007, Nature Protocols.

[26]  Ash A. Alizadeh,et al.  Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling , 2000, Nature.

[27]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[28]  A. Driessen,et al.  Phylogenetic analysis of fungal ABC transporters , 2010, BMC Genomics.

[29]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[30]  Anton J. Enright,et al.  An efficient algorithm for large-scale detection of protein families. , 2002, Nucleic acids research.

[31]  *Contributed equally to the work , 2010 .

[32]  S Miyano,et al.  Open source clustering software. , 2004, Bioinformatics.

[33]  Christina A. Cuomo,et al.  Source (or Part of the following Source): Type Article Title Comparative Genomics Reveals Mobile Pathogenicity Chromosomes in Fusarium Author(s) , 2022 .

[34]  S. Schornack,et al.  Recent developments in effector biology of filamentous plant pathogens , 2010, Cellular microbiology.

[35]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  K. Aktories,et al.  Bacterial toxin and effector glycosyltransferases. , 2010, Biochimica et biophysica acta.

[37]  Satoru Miyano,et al.  Open source clustering software , 2004 .

[38]  Tilmann Weber,et al.  Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs) , 2005, Nucleic acids research.

[39]  Sarah Calvo,et al.  Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis , 2006, Nature.

[40]  Thomas Schiex,et al.  EUGÈNE: An Eukaryotic Gene Finder That Combines Several Sources of Evidence , 2000, JOBIM.

[41]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[42]  Bernard Henrissat,et al.  Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis , 2010, Nature.

[43]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[44]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[45]  R. D. de Vries,et al.  The secretome of the maize pathogen Ustilago maydis. , 2008, Fungal genetics and biology : FG & B.

[46]  E. Uberbacher,et al.  CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. , 2010, Glycobiology.

[47]  E. Eichler,et al.  Structural Dynamics of Eukaryotic Chromosome Evolution , 2003, Science.

[48]  R. Vilgalys,et al.  Genetic structure of populations of Rhizoctonia solani AG-3 on potato in eastern North Carolina. , 2002, Mycologia.

[49]  Christian A. Rees,et al.  Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Bölker,et al.  G proteins in Ustilago maydis: transmission of multiple signals? , 1997, The EMBO journal.

[51]  B. McDonald,et al.  Genetic structure of populations of Rhizoctonia solani anastomosis group-1 IA from soybean in Brazil. , 2008, Phytopathology.

[52]  I. Ial,et al.  Nature Communications , 2010, Nature Cell Biology.

[53]  N. Talbot,et al.  Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus , 2004, Molecular microbiology.

[54]  Jonathan D. G. Jones,et al.  Gene Gain and Loss during Evolution of Obligate Parasitism in the White Rust Pathogen of Arabidopsis thaliana , 2011, PLoS biology.

[55]  Costas Tsatsoulis,et al.  Classifying genes to the correct Gene Ontology Slim term in Saccharomyces cerevisiae using neighbouring genes with classification learning , 2010, BMC Genomics.

[56]  B. McDonald,et al.  Genetic structure of populations of the rice-infecting pathogen Rhizoctonia solani AG-1 IA from China. , 2009, Phytopathology.

[57]  R. Oliver,et al.  A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens , 2010, Proceedings of the National Academy of Sciences.

[58]  D. Lakshman,et al.  Characterization of the arom gene in Rhizoctonia solani, and transcription patterns under stable and induced hypovirulence conditions , 2006, Current Genetics.

[59]  Eugene W. Myers,et al.  PILER : identification and classification of genomic repeats , 2005 .

[60]  E. Pérez-Nadales,et al.  Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. , 2009, Fungal genetics and biology : FG & B.

[61]  D. Haft,et al.  SMURF: Genomic mapping of fungal secondary metabolite clusters. , 2010, Fungal genetics and biology : FG & B.

[62]  L. D. Ploper,et al.  Soybean Disease Loss Estimates for the Top 10 Soybean Producing Countries in 1994. , 1997, Plant disease.

[63]  Xiang Jia Min,et al.  FunSecKB: the Fungal Secretome KnowledgeBase , 2011, Database J. Biol. Databases Curation.

[64]  Q. Qian,et al.  [QTL analysis of sheath blight resistance in rice (Oryza sativa L.)]. , 2002, Yi chuan xue bao = Acta genetica Sinica.