Genome and transcriptome based comparative analysis of Tilletia indica to decipher the causal genes for pathogenicity of Karnal bunt in wheat.
Tilletia indica
Dikaryon
Karnal bunt
Pathogenesis
RNA-seq
Wheat
Whole genome assemblies
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
16 Jul 2024
16 Jul 2024
Historique:
received:
11
09
2023
accepted:
28
03
2024
medline:
16
7
2024
pubmed:
16
7
2024
entrez:
15
7
2024
Statut:
epublish
Résumé
Tilletia indica Mitra causes Karnal bunt (KB) in wheat by pathogenic dikaryophase. The present study is the first to provide the draft genomes of the dikaryon (PSWKBGD-3) and its two monosporidial lines (PSWKBGH-1 and 2) using Illumina and PacBio reads, their annotation and the comparative analyses among the three genomes by extracting polymorphic SSR markers. The trancriptome from infected wheat grains of the susceptible wheat cultivar WL711 at 24 h, 48h, and 7d after inoculation of PSWKBGH-1, 2 and PSWKBGD-3 were also isolated. Further, two transcriptome analyses were performed utilizing T. indica transcriptome to extract dikaryon genes responsible for pathogenesis, and wheat transcriptome to extract wheat genes affected by dikaryon involved in plant-pathogen interaction during progression of KB in wheat. A total of 54, 529, and 87 genes at 24hai, 48hai, and 7dai, respectively were upregulated in dikaryon stage while 21, 35, and 134 genes of T. indica at 24hai, 48hai, and 7dai, respectively, were activated only in dikaryon stage. While, a total of 23, 17, and 52 wheat genes at 24hai, 48hai, and 7dai, respectively were upregulated due to the presence of dikaryon stage only. The results obtained during this study have been compiled in a web resource called TiGeR ( http://backlin.cabgrid.res.in/tiger/ ), which is the first genomic resource for T. indica cataloguing genes, genomic and polymorphic SSRs of the three T. indica lines, wheat and T. indica DEGs as well as wheat genes affected by T. indica dikaryon along with the pathogenecity related proteins of T. indica dikaryon during incidence of KB at different time points. The present study would be helpful to understand the role of dikaryon in plant-pathogen interaction during progression of KB, which would be helpful to manage KB in wheat, and to develop KB-resistant wheat varieties.
Identifiants
pubmed: 39009989
doi: 10.1186/s12870-024-04959-z
pii: 10.1186/s12870-024-04959-z
doi:
Types de publication
Journal Article
Comparative Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
676Subventions
Organisme : Indian Council of Agricultural Research
ID : AMAAS (code no. OXX02744)
Organisme : Indian Council of Agricultural Research
ID : CABin grant (F. no. Agril. Edn.4-1/2013-A&P)
Organisme : Indian Council of Agricultural Research
ID : CABin grant (F. no. Agril. Edn.4-1/2013-A&P)
Organisme : Indian Council of Agricultural Research
ID : AMAAS (code no. OXX02744)
Organisme : Indian Council of Agricultural Research
ID : AMAAS (code no. OXX02744)
Organisme : Indian Council of Agricultural Research
ID : CABin grant (F. no. Agril. Edn.4-1/2013-A&P)
Informations de copyright
© 2024. The Author(s).
Références
Mitra M. A new bunt on wheat in India. Ann Appl Biol. 1931;18:178–9. https://doi.org/10.1111/j.1744-7348.1931.tb02294.x .
doi: 10.1111/j.1744-7348.1931.tb02294.x
Agarwal VK, Verma HS, Khetarpal RK. Occurrence of partial bunt on triticale. Plant Prot Bull. 1977;25:210–1.
Agarwal VK, Agarwal M, Gupta RK, Verma HS. Studies on loose smut of wheat. I. A simplified procedure for the detection of seedborne infection. Seed Res. 1981;9:49–51.
Mundker BB. Karnal bunt, an air-borne disease. Curr Sci. 1943;12:230–1.
Jones DR. A reappraisal of the current status of Tilletia indica as an important quarantine pest for Europe. Eur J Plant Pathol. 2007;118(2):105–13.
Jones DR. Towards a more reasoned assessment of the threat to wheat crops from Tilletia indica, the cause of Karnal bunt disease. Eur J Plant Pathol. 2009;123(3):247–59.
Duran R, Cromarty R. Tilletia indica: a heterothallic wheat bunt fungus with multiple alleles controlling incompatibility. Phytopathology. 1977;76:812–5.
Fuentes-Dávila G, Duran R. Tilletia indica: cytology and teliospore formation in vitro and in immature kernels. Can J Bot. 1986;64:1712–9.
Krishna A, Singh RA. Cytology of teliospore germination and development in Neovossia indica the incident of Karnal bunt of wheat. Indian Phytopathol. 1983;36(1):115–23.
Aggarwal R, Tripathi A, Yadav A. Pathogenic and genetic variability in Tilletia indica monosporidial culture lines using universal rice primer-PCR. Eur J Plant Pathol. 2010;128(3):333–42.
Gurjar MS, Jogawat A, Saharan MS, et al. Response of putative pathogenicity-related genes in Tilletia indica inciting Karnal Bunt of Wheat. Cereal Res Commun. 2018a;46:89–103.
Parveen S, Saharan MS, Verma A, Sharma I. Comparative analysis of RAPD and ISSR marker assays for detecting genetic polymorphism in T. indica. Eur J Plant Pathol. 2013;3:380–7.
Sharma P, Tiwari R, Saharan MS, Sharma I, Kumar J, et al. Draft genome sequence of two monosporidial lines of the Karnal bunt fungus Tilletia indica Mitra (PSWKBGH-1 and PSWKBGH-2). Genome Announc. 2016;4:e00928–00916.
pubmed: 27634992
pmcid: 5026432
Kumar A, Pandey V, Singh M, Pandey D, Saharan MS, Marla SS. Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus. PLoS ONE. 2017;12(2):e0171323.
pubmed: 28152050
pmcid: 5289553
Gurjar MS, Aggarwal R, Jogawat A, Kulshreshtha D, Sharma S, Solanke AU, Dubey H, Jain RK. Genome sequencing and secretome analysis of T. indica inciting Karnal bunt of wheat provides pathogenesis-related genes. 3 Biotech. 2019;9:219.
pubmed: 31114743
pmcid: 6527731
Gurjar MS, Mohan MH, Singh J, Saharan MS, Aggarwal R. Tilletia indica: biology, variability, detection, genomics and future perspective. Indian Phytopathol. 2021;74:21–31.
Gurjar MS, Jain P, Jain S, et al. Identification and validation of simple sequence repeats markers in Tilletia indica and compatibility assay of monosporidial lines. Indian Phytopathol. 2022a;75:357–66.
Mishra P, Maurya R, Gupta VK, et al. Comparative genomic analysis of monosporidial and monoteliosporic cultures for unraveling the complexity of molecular pathogenesis of Tilletia indica pathogen of wheat. Sci Rep. 2019;9:8185.
pubmed: 31160715
pmcid: 6547692
Gurjar MS, Jain S, Aggarwal R, Saharan MS, Tej Pratap JK, Kharbikar L. Transcriptome analysis of wheat–Tilletia indica Interaction provides Defense and Pathogenesis-related genes. Plants. 2022b;11:3061.
pubmed: 36432790
pmcid: 9698794
Kumar J, Saharan MS, Sharma S, Sharma AK, Shoran J. Development of monosporidial lines of Neovossia Indica. Indian Phytopathol. 2006;59(1):108–11.
Aujla SS, Sharma I, Singh BB. Rating scale for identifying wheat varieties resistant to Neovossia indica (Mitra) Mundkur. Indian Phytopath. 1989;42:161–2.
Andrews S, FastQC. A quality control tool for high throughput sequence data. 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc .
Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, James AY. The MaSuRCA genome assembler. Bioinformatics. 2013;29(21):2677.
Bankevich A, Nurk S, Antipov D, et al. SPAdes: a New Genome Assembly Algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77.
pubmed: 22506599
pmcid: 3342519
Boetzer M, Christiaan V, et al. SSPACE: scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2011;27(4):578–5789.
pubmed: 21149342
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–5.
pubmed: 23422339
pmcid: 3624806
Manni M, Matthew RB, Seppey M, Simão FA, Zdobnov EM. BUSCO Update: Novel and Streamlined Workflows along with broader and deeper phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and viral genomes. Mol Biol Evol. 2021;38(10):4647–54.
pubmed: 34320186
pmcid: 8476166
Stanke M, Diekhans M, Baertsch R, Haussler D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008;24(5):637–44.
pubmed: 18218656
Altschul S, Gish W, Miller W, Myers E, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.
pubmed: 2231712
Thiel T, Michalek W, Varshney RK, Graner A. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L). Theor Appl Genet. 2003;106(3):411–22.
pubmed: 12589540
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.
Joshi NA, Fass JN, Sickle. A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software]. 2011. https://github.com/najoshi/sickle .
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–6.
pubmed: 23193283
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9.
pubmed: 22388286
pmcid: 3322381
Kovaka S, Zimin AV, Pertea GM, Razaghi R, Salzberg SL, Pertea M. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 2019;20:278.
pubmed: 31842956
pmcid: 6912988
Grabherr MG, Haas BJ, Yassour M, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644–52.
pubmed: 21572440
pmcid: 3571712
Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658–9.
pubmed: 16731699
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323.
pubmed: 21816040
pmcid: 3163565
Love MI, Huber W, Anders S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
pubmed: 25516281
pmcid: 4302049
Armenteros JJA, Sønderby CK, Sønderby SK, Nielsen H, Winther O. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics. 2017;33(21):3387–95.
Teufel F, Armenteros JJA, Johansen AR, et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol. 2022;40:1023–5.
pubmed: 34980915
pmcid: 9287161
Armenteros JJA, Salvatore M, Emanuelsson O, et al. Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance. 2019;2(5):e201900429.
Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80.
pubmed: 11152613
Sperschneider J, Dodds P. EffectorP 3.0: prediction of apoplastic and cytoplasmic effectors 977 in fungi and oomycetes. MPMI. 2021;35(2):146–56.
Urban M, Pant R, Raghunath A, Irvine AG, Pedro H, Hammond-Kosack KE. The Pathogen-host interactions database (PHI-base): additions and future developments. Nucleic Acids Res. 2015;43:D645–55.
pubmed: 25414340
Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
pubmed: 10592173
pmcid: 102409
Kumar A, Mishra P, Maurya R, et al. Improved draft genome sequence of a Monoteliosporic Culture of the Karnal Bunt (Tilletia indica) Pathogen of Wheat. Genome Announc. 2018;6(20):e00015–18.
pubmed: 29773612
pmcid: 5958260
Thapa S, Bala R, Sharma VK, et al. Basis of Karnal bunt resistance in diploid and tetraploid Triticeae species. Indian Phytopathol. 2022;75:251–7.
Mishra KK, Gahtyari NC, Kant L. Common bunt and Smuts in Wheat and Barley Genetics, breeding, and management: current status and future prospects. New Horizons in Wheat and Barley Research. Singapore: Springer; 2022. https://doi.org/10.1007/978-981-16-4449-8_14 .
doi: 10.1007/978-981-16-4449-8_14
Brar GS, Fuentes-Dávila G, He X, Sansaloni CP, Singh RP, Singh PK. Genetic mapping of resistance in Hexaploid Wheat for a Quarantine Disease: Karnal Bunt. Front Plant Sci. 2018;9:1497.
pubmed: 30386358
pmcid: 6198147
Gurjar MS, Jogawat A, Sharma S, et al. Functional expression of MAP kinase TiHOG1 gene in Tilletia indica inciting Karnal bunt of wheat. Indian Phytopathol. 2018b;71:325–35.
Sun K, Wolters AMA, Vossen JH, et al. Silencing of six susceptibility genes results in potato late blight resistance. Transgenic Res. 2016;25:731–42.
pubmed: 27233778
pmcid: 5023794
Gupta PK. SWEET genes for Disease Resistance in plants. Trends Genet. 2020;36(12):901–4.
pubmed: 32896434
Prasad P, Savadi S, Bhardwaj S, Gangwar O, Kumar S. Rust pathogen effectors: perspectives in resistance breeding. Planta. 2019;250:1–22.
pubmed: 30980247
Chaudhari P, Ahmed B, et al. Effector biology during biotrophic invasion of plant cells. Virulence. 2014;5(7):703–9.
pubmed: 25513771
pmcid: 4189876