Genome sequencing and comparison of five Tilletia species to identify candidate genes for the detection of regulated species infecting wheat

IMA Fungus - 2019
Hai D. T. Nguyen1, Tahera Sultana1, Prasad Kesanakurti1, Sarah Hambleton1
1Biodiversity and Bioresources, Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, 960 Carling Ave, Ottawa, Ontario, K1A 0C6, Canada

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Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

Bao X (2010) Host specificity and phylogenetic relationships among Tilletia species infecting wheat and other cool season grasses. In: PhD thesis, Department of Plant Pathology, Washington State University, USA

Boetzer M, Pirovano W (2012) Toward almost closed genomes with GapFiller. Genome Biol 13:R56

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

Bonde MR, Peterson GL, Schaad NW, Smilanick JL (1997) Karnal bunt of wheat. Plant Dis 81:1370–1377

Borgen A, Davanlou M (2001) Biological control of common bunt (Tilletia tritici). J Crop Production 3:157–171

Borodovsky M, Lomsadze A (2011) Gene identification in prokaryotic genomes, phages, metagenomes, and EST sequences with GeneMarkS suite. Curr Protoc Bioinformatics 35:4.5.1–4.5.17

Borowiec ML (2016) AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4:e1660

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X et al (2011) Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One 6:e24230

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

Carris L, Gray P (1994) The ability of Tilletia fusca to hybridize with the wheat bunt species under axenic conditions. Mycologia 86:157–163

Carris LM, Castlebury LA, Goates BJ (2006) Nonsystemic bunt Fungi - Tilletia indica and T. horrida: a review of history, systematics, and biology. Annu Rev Phytopathol 44:113–133

Carris LM, Castlebury LA, Huang G, Alderman SC, Luo J et al (2007) Tilletia vankyi, a new species of reticulate-spored bunt fungus with non-conjugating basidiospores infecting species of Festuca and Lolium. Mycol Res 111:1386–1398

Castlebury LA, Carris LM (1999) Tilletia walkeri, a new species on Lolium multiflorun and L. perenne. Mycologia 91:121–131

Castlebury LA, Carris LM, Vánky K (2005) Phylogenetic analysis of Tilletia and allied genera in order Tilletiales (Ustilaginomycetes; Exobasidiomycetidae) based on large subunit nuclear rDNA sequences. Mycologia 97:888–900

Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C et al (2015) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7:1590–1601

Corrochano LM, Kuo A, Marcet-Houben M, Polaino S, Salamov A et al (2016) Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr Biol 26:1577–1584

Cunfer B, Castlebury LA (1999) Tilletia walkeri on annual ryegrass in wheat fields in the southeastern United States. Plant Dis 83:685–689

Eddy SR (2009) A new generation of homology search tools based on probabilistic inference. In: Morishita S, Lee SY, Sakakibara Y (eds) Genome informatics 2009, proceedings of the 20th international conference. Imperial College Press, Singapore, pp 205–211

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157

Enright A, Van Dongen S, Ouzounis C (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30:1575–1584

Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P et al (2017) InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res 45:D190–D199

Floudas D, Binder M, Riley R, Barry K, Blanchette RA et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

Frederick RD, Snyder KE, Tooley PW, Berthier-Schaad Y, Peterson GL et al (2000) Identification and differentiation of Tilletia indica and I using the polymerase chain reaction. Phytopathology 90:951–960

Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND et al (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868

Gao L, Yu H, Han W, Gao F, Liu T et al (2014) Development of a SCAR marker for molecular detection and diagnosis of Tilletia controversa Kühn, the causal fungus of wheat dwarf bunt. World J Microbiol Biotechnol 30:3185–3195

Gao Y, Tan MK, Zhu YG (2016) Rapid and specific detection of Tilletia indica using loop-mediated isothermal DNA amplification. Aust Plant Pathol 45:361–367

García-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Götz S et al (2012) Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28:2678–2679

Geiser E, Ludwig F, Zambanini T, Wierckx N, Blank LM (2016) Draft genome sequences of itaconate-producing ustilaginaceae. Genome Announc 4:e01291–e01216

Gioti A, Nystedt B, Li W, Xu J, Andersson A et al (2013) Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. MBio 4:e00572–e00512

Goffeau A, Barrell BG, Bussey H, Davis R, Dujon B et al (1996) Life with 6000 genes. Science 274:546–567

Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R et al (2014) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42:D699–D704

Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075

Gurjar S, Aggarwal R, Jogawat A, Sharma S, Kulshreshtha D et al (2017) Development of real time PCR assay for detection and quantification of teliospores of Tilletia indica in soil. Indian J Exp Biol 55:549–554

Haitjema CH, Gilmore SP, Henske JK, Solomon KV, de Groot R et al (2017) A parts list for fungal cellulosomes revealed by comparative genomics. Nat Microbiol 2:17087

Hall B, DeRego T, Geib S (2014) GAG: the genome annotation generator (version 1.0). Available from http://genomeannotation.github.io/GAG

Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16:169

Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M (2016) BRAKER1: unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32:767–769

IPPC (2016) ISPM 27 diagnostic protocols for regulated pests. Annex DP4: Tilletia indica Mitra. International Plant Protection Convention, Food and Agriculture Organization of the United Nations, Italy

Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications 9: 5114

James TY, Pelin A, Bonen L, Ahrendt S, Sain D et al (2013) Shared signatures of parasitism and phylogenomics unite cryptomycota and microsporidia. Curr Biol 23:1548–1553

Josefsen L, Christiansen SK (2002) PCR as a tool for the early detection and diagnosis of common bunt in wheat, caused by Tilletia tritici. Mycol Res 106:1287–1292

Kämper J, Kahmann R, Bölker M, Ma L-J, Brefort T et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

Kijpornyongpan T, Mondo SJ, Barry K, Sandor L, Lee J et al (2018) Broad genomic sampling reveals a smut pathogenic ancestry of the fungal clade Ustilaginomycotina. Mol Biol Evol 35:1840–1854

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R et al (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

Kochanová M, Zouhar M, Prokinová E, Rysanek P (2004) Detection of Tilletia controversa and Tilletia caries in wheat by PCR method. Plant Soil Environ 50:75–77

Konishi M, Hatada Y, Horiuchi J-i (2013) Draft genome sequence of the basidiomycetous yeast-like fungus Pseudozyma hubeiensis SY62, which produces an abundant amount of the biosurfactant mannosylerythritol lipids. Genome Announc 1:e00409–e00413

Kumar A, Mishra P, Maurya R, Mishra AK, Gupta VK et al (2018) Improved draft genome sequence of a monoteliosporic culture of the Karnal bunt (Tilletia indica) pathogen of wheat. Genome Announc 6:e00015–e00018

Kumar A, Pandey V, Singh M, Pandey D, Saharan M et al (2017) Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus. PLoS One 12:e0171323

Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12

Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

Lastovetsky OA, Gaspar ML, Mondo SJ, LaButti KM, Sandor L et al (2016) Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria. Proc Natl Acad Sci USA 113:15102–15107

Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P et al (2012) Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24:1733–1745

Levy L, Castlebury LA, Carris LM, Meyer RJ, Pimentel G (2001) Internal transcribed spacer sequence-based phylogeny and polymerase chain reaction-restriction fragment length polymorphism differentiation of Tilletia walkeri and T. indica. Phytopathology 91:935–940

Liu JH, Gao L, Liu TG, Chen WQ (2009) Development of a sequence-characterized amplified region marker for diagnosis of dwarf bunt of wheat and detection of Tilletia controversa Kuhn. Lett Appl Microbiol 49:235–240

Lorenz S, Guenther M, Grumaz C, Rupp S, Zibek S et al (2014) Genome sequence of the basidiomycetous fungus Pseudozyma aphidis DSM70725, an efficient producer of biosurfactant mannosylerythritol lipids. Genome Announc 2:e00053–e00014

Ma L-J, Ibrahim AS, Skory C, Grabherr MG, Burger G et al (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5:e1000549

Matanguihan JB, Murphy KM, Jones SS (2011) Control of common bunt in organic wheat. Plant Dis 95:92–103

McDonald J, Wong E, White G (2000) Differentiation of Tilletia species by rep-PCR genomic fingerprinting. Plant Dis 84:1121–1125

McNeil M, Roberts A, Cockerell V, Mulholland V (2004) Real-time PCR assay for quantification of Tilletia caries contamination of UK wheat seed. Plant Pathol 53:741–750

Mirarab S, Warnow T (2015) ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31:i44–i52

Mondo SJ, Dannebaum RO, Kuo RC, Louie KB, Bewick AJ et al (2017) Widespread adenine N6-methylation of active genes in fungi. Nat Genet 49:964–968

Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V et al (2012) Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci USA 109:17501–17506

Nikolenko SI, Korobeynikov AI, Alekseyev MA (2013) BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics 14(Suppl 1):S7

Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A et al (2013) The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res 42(D1):D26–D31

OEPP/EPPO (2016) PM 3/78 (1) consignment inspection of seed and grain of cereals. Bull OEPP/EPPO Bull 46:49–57

Petre B, Kamoun S (2014) How do filamentous pathogens deliver effector proteins into plant cells. PLoS Biol 12:e1001801

Pimentel G, Carris LM, Levy L, Meyer RJ (1998) Genetic variability among isolates of Tilletia barclayana, T. indica and allied species. Mycologia 90:1017–1027

Pimentel G, Carris LM, Peever TL (2000) Characterization of interspecific hybrids between Tilletia controversa and T. bromi. Mycologia 92:411–420

Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

Russell BW, Mills D (1994) Morphological, physiological, and genetic evidence in support of a conspecific status for Tilletia caries, T. controversa, and T. foetida. Phytopathology 84:576–582

Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and Indoor Fungi. CBS Laboratory Manual Series 2. CBS-KNAW Fungal Biodiversity Centre, Utrecht

Schirawski J, Mannhaupt G, Münch K, Brefort T, Schipper K et al (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–1548

Sharma P, Tiwari R, Saharan M, Sharma I, Kumar J et al (2016) Draft genome sequence of two monosporidial lines of the Karnal bunt fungus Tilletia indica Mitra (PSWKBGH-1 and PSWKBGH-2). Genome Announc 4:e00928–e00916

Shi Y, Loomis P, Christian D, Carris L, Leung H (1996) Analysis of the genetic relationships among the wheat bunt fungi using RAPD and ribosomal DNA markers. Phytopathology 86:311–318

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212

Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

Sperschneider J, Dodds PN, Gardiner DM, Singh KB, Taylor JM (2018) Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Mol Plant Pathol 19:2094–2110

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

Tan M-K, Ghalayini A, Sharma I, Yi J, Shivas R et al (2009) A one-tube fluorescent assay for the quarantine detection and identification of Tilletia indica and other grass bunts in wheat. Aust Plant Pathol 38:101–109

Tan M-K, Murray GM (2006) A molecular protocol using quenched FRET probes for the quarantine surveillance of Tilletia indica, the causal agent of Karnal bunt of wheat. Mycol Res 110:203–210

Tan M-K, Raman H, Chambers G, Sharma I, Chen Z et al (2016) Characterization of SNP and structural variations in the mitochondrial genomes of Tilletia indica and its closely related species formed basis for a simple diagnostic assay. PLoS One 11:e0166086

Taniguti LM, Schaker PD, Benevenuto J, Peters LP, Carvalho G et al (2015) Complete genome sequence of Sporisorium scitamineum and biotrophic interaction transcriptome with sugarcane. PLoS One 10:e0129318

Thirumalaisamy P, Singh D, Aggrawal R, Gogoi R, Gupta P et al (2011) Development of species-specific primers for detection of Karnal bunt pathogen of wheat. Indian Phytopathol 64:164–172

Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110:20117–20122

Toome M, Kuo A, Henrissat B, Lipzen A, Tritt A et al (2014a) Draft genome sequence of a rare smut relative, Tilletiaria anomala UBC 951. Genome Announc 2:e00539–e00514

Toome M, Ohm RA, Riley RW, James TY, Lazarus KL et al (2014b) Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae. New Phytol 202:554–564

Trail F, Mills D (1990) Growth of haploid Tilletia strains in planta and genetic analysis of a cross of Tilletia caries X T. controversa. Phytopathology 80:367–370

Treangen TJ, Ondov BD, Koren S, Phillippy AM (2014) The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15:524

Trione EJ (1964) Isolation and in vitro culture of wheta bunt fungi, Tilletia caries and Tilletia controversa. Phytopathology 54:592–596

Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal P et al (2017) Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol 19:2964–2983

Wang N, Ai P, Tang Y, Zhang J, Dai X et al (2015) Draft genome sequence of the rice kernel smut Tilletia horrida strain QB-1. Genome Announc 3:e00621–e00615

Wilcoxson RD, Saari EE (1996) Bunt and Smut diseases of wheat: concepts and methods of disease management, vol 4. CIMMYT, Mexico

Wood V, Gwilliam R, Rajandream M-A, Lyne M, Lyne R et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880

Xu J, Saunders CW, Hu P, Grant RA, Boekhout T et al (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735

Zajc J, Liu Y, Dai W, Yang Z, Hu J et al (2013) Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 14:617

Zouhar M, Mazáková J, Prokinová E, Vánová M, Ryšánek P (2010) Quantification of Tilletia caries and Tilletia controversa mycelium in wheat apical meristem by real-time PCR. Plant Protect Sci 46:107–115

Župunski V, Jevtić R, Ignjatović-Micić D, Stanković S, Lević J et al (2012) Incidence of Tilletia species in non-processed seed of Triticum aestivum in Vojvodina. Serbia Seed Sci Technol 40:320–332