De novo genome sequencing and secretome analysis of Tilletia indica inciting Karnal bunt of wheat provides pathogenesis-related genes

Agarwal VK, Verma HS (1983) A simple technique for the detection of karnal bunt infection in wheat seed samples. Seed Res 11(1):100–102

Agarwal VK, Verma HS, Khetarpal RK (1977) Occurrence of partial bunt on triticale. FAO Plant Prot Bull 25:210–211

Aggarwal R, Tripathi A, Yadav A (2010) Pathogenic and genetic variability in Tilletia indica monosporidial culture lines using universal rice primer-PCR. Eur J Plant Pathol 128:333–342. https://doi.org/10.1007/s10658-010-9655-4

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

Anonymous (2017–2018) Production of major crops. Econ Surv 2:A35. ( http://mofapp.nic.in:8080/economicsurvey/appendixPDF/tab1.12.pdf )

Bankevich A, Nurk S, Antipov D (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021

Bansal R, Singh DV, Joshi LM (1983) Germination of teliospores of Karnal bunt of wheat. Seed Res 11:258–261

Basse CW, Steinberg G (2004) Ustilago maydis, model system for analysis of the molecular basis of fungal pathogenicity. Mol Plant Pathol 5(2):83–92

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170

Bonde MR, Nester SE, Olsen MW, Berner DK (2004) Survival of teliospores of Tilletia indica in Arizona field soils. Plant Dis 88:804–810. https://doi.org/10.1094/PDIS.2004.88.8.804

Brar GS, Fuentes-Dávila G, He Xinyao, Sansaloni CP, Singh RP, Singh PK (2018) Genetic mapping of resistance in hexaploid wheat for a quarantine disease: Karnal bunt. Front Plant Sci 9:1497. https://doi.org/10.3389/fpls.2018.01497

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. https://doi.org/10.1146/annurev.phyto.44.070505.143402

Castanera R, López-Varas L, Borgognone A, LaButti K, Lapidus A, Schmutz J et al (2016) Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genet 12(6):e1006108. https://doi.org/10.1371/journal.pgen.1006108

Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2018:619832. https://doi.org/10.1155/2008/619832

Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14(7):1394–1403. https://doi.org/10.1101/gr.2289704

Dhaliwal HS, Singh DV (1989) Production and inter-relationship of two types of secondary sporidia of Neovossia indica. Curr Sci 58:614–618

Duran R, Cromarty R (1977) Tilletia indica: a heterothallic wheat bunt fungus with multiple alleles controlling incompatibility. Phytopathology 67:812–815

Gill KS, Sharma I, Aujla SS (1993) Karnal and wheat production. Punjab Agriculture University, Ludhiana, p 153

Gupta AK, Joshi GK, Seneviratne JM, Pandey D, Kumar A (2013) Cloning, in silico characterization and induction of TiKpp2 MAP kinase in Tilletia indica under the influence of host factor (s) from wheat spikes. Mol Biol Rep 40(8):4967–4978. https://doi.org/10.1007/s11033-013-2597-0

Gurjar MS, Jogawat A, Kulshreshtha D, Sharma S, Gogoi R, Aggarwal R (2016) Intraspecific variation of Tilletia indica isolates causing Karnal bunt of Wheat in India. Indian Phytopath 69:352–356

Gurjar MS, Aggarwal R, Sharma S, Kulshreshtha D, Gupta A, Gogoi R, Thirumalaisamy PP, Saini A (2017) Development of real time PCR assay for the detection and quantification of teliospores of Tilletia indica causing Wheat Karnal bunt in soil. Indian J Exp Biol 55(6):549–554. http://nopr.niscair.res.in/handle/123456789/42556

Gurjar MS, Jogawat A, Saharan MS, Aggarwal R (2018) Response of putative pathogenicity-related genes in Tilletia indica inciting Karnal bunt of wheat. Cereal Res Commun 46(1):89–103. https://doi.org/10.1556/0806.45.2017.067

Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101. https://doi.org/10.1038/nature05248

Kumar J, Shoran J, Sharma I, Aggarwal R, Saharan MS, Sharma AK (2009) Distribution of heterothallic alleles of Tilletia indica in India. Indian Phytopath 62(3):285–294

Kumar A, Pandey V, Singh M, Pandey D, Saharan MS, Marla SS (2017) Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus. PLoS One 12(2):e0171323. https://doi.org/10.1371/journal.pone.0171323

Kumar A, Mishra P, Maurya R, Mishra AK, Gupta VK, Ramteke PW, Marla SS (2018) Improved draft genome sequence of a monoteliosporic culture of the Karnal bunt (Tilletia indica) pathogen of wheat. Genome Announc 6(20):e0001518. https://doi.org/10.1128/genomeA.00015-18

Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P, Guldener U 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(5):1733–1745. https://doi.org/10.1105/tpc.112.097261

Mitra M (1931) A new bunt on wheat in India. Ann App Biol 18(2):178–179. https://doi.org/10.1111/j.1744-7348.1931.tb02294.x

Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185. https://doi.org/10.1093/nar/gkm321

Nagarajan S, Aujla SS, Nanda GS, Sharma I, Goel LB, Kumar J, Singh DV (1997) Karnal bunt (Tilletia indica) of wheat—a review. Rev Plant Pathol 76(12):1207–1214

Ospina-Giraldo MD, Griffith JG, Laird EW, Mingora C (2010) The CAZyome of Phytophthora spp: a comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genomics 11:525–541. https://doi.org/10.1186/1471-2164-11-525

Pandey V, Singh M, Pandey D, Kumar A (2018) Integrated proteomics, genomics, metabolomics approaches reveal oxalic acid as pathogenicity factor in Tilletia indica inciting Karnal bunt disease of wheat. Sci Rep 8(1):7826. https://doi.org/10.1038/s41598-018-26257-z

Pandey V, Gupta AK, Singh M, Pandey D, Kumar A (2019) Complementary Proteomics, Genomics approaches identifies potential pathogenicity/virulence factors in Tilletia indica induced under the influence of host factor. Sci Rep 9(1):553. https://doi.org/10.1038/s41598-018-37810-1

Petersen TN, Brunak S, von Gunnar H, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions Thomas Nordahl. Nature Methods 8(10):785–786. https://doi.org/10.1038/nmeth.1701

Prescott JM (1984) Overview of CIMMYT’s Karnal bunt programme, Proceedings of the conference on Karnal bunt, 1984, Obregon, Sonora, Mexico, p 24

Schirawski J, Mannhaupt G, Munch K, Brefort T, Schipper K, Doehlemann G et al (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 12(330):1546–1548. https://doi.org/10.1126/science.1195330

Singh DV, Gogoi R (2011) Karnal bunt of wheat (Triticum sp.): a global scenario. Indian J Agril Sci 81:3–14

Singh DV, Srivastava KD, Joshi LM, Verma BR (1985) Evaluation of some fungicides for control of Karnal bunt of wheat. Indian Phytopath 38:571–573

Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32(2):W309–W312. https://doi.org/10.1093/nar/gkh379

Tan MK, Brennan JP, Wright D, Murray GM (2013) A review of the methodology to detect and identify Karnal bunt—a serious biosecurity threat. Austr Plant Pathol 42:95–102. https://doi.org/10.1007/s13313-012-0176-9

Thirumalaisamy PP, Singh DV (2012) Variability of Indian isolates of Tilletia indica assessed by pathogenicity and molecular markers. J Phytopathol 160:525–531. https://doi.org/10.1111/j.1439-0434.2012.01940.x

Tripathi A, Aggarwal R, Yadav A (2011) Determination of variability in monosporidial lines of Tilletia indica by RAPD analysis. Arch Phytopathol Plant Protect 44:1312–1321. https://doi.org/10.1080/03235408.2010.496560

Tripathi A, Aggarwal R, Yadav A (2013) Differential expression analysis of defense related genes responsive to Tilletia indica infection in wheat. Turk J Biol 37:606–613. https://doi.org/10.3906/biy-1301-16

Verma S, Gazara RK, Nizam S, Parween S, Chattopadhyay D, Verma PK (2016) Draft genome sequencing and secretome analysis of fungal phytopathogen Ascochyta rabiei provides insight into the necrotrophic effector repertoire. Sci Rep 6:24638. https://doi.org/10.1038/srep24638

Wang Y, Coleman-Derr D, Chen G, Gu YQ (2015) OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 43:W78–W84. https://doi.org/10.1093/nar/gkv487

Warham EJ (1986) Karnal bunt disease of wheat: a literature review. Trop Pest Manag 32(3):229–242

Winnenburg R, Baldwin TK, Urban M, Rawlings C, Kohler J, Hammond-Kosack KE (2006) PHI-base: a new database for pathogen-host interactions. Nucleic Acids Res 34:D459–D464. https://doi.org/10.1093/nar/gkj047

Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451. https://doi.org/10.1093/nar/gks479

Zhao Z, Liu H, Wang C, Xu J (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 23(14):274–289. https://doi.org/10.1186/1471-2164-14-274