Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus

PLOS ONE, Dec 2019

Karnal bunt disease in wheat is caused by hemibiotrophic fungus, Tilletia indica that has been placed as quarantine pest in more than 70 countries. Despite its economic importance, little knowledge about the molecular components of fungal pathogenesis is known. In this study, first time the genome sequence of T. indica has been deciphered for unraveling the effectors’ functions of molecular pathogenesis of Karnal bunt disease. The T. indica genome was sequenced employing hybrid approach of PacBio Single Molecule Real Time (SMRT) and Illumina HiSEQ 2000 sequencing platforms. The genome was assembled into 10,957 contigs (N50 contig length 3 kb) with total size of 26.7 Mb and GC content of 53.99%. The number of predicted putative genes were 11,535, which were annotated with Gene Ontology databases. Functional annotation of Karnal bunt pathogen genome and classification of identified effectors into protein families revealed interesting functions related to pathogenesis. Search for effectors’ genes using pathogen host interaction database identified 135 genes. The T. indica genome sequence and putative genes involved in molecular pathogenesis would further help in devising novel and effective disease management strategies including development of resistant wheat genotypes, novel biomarkers for pathogen detection and new targets for fungicide development.

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Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus

February Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus Anil Kumar 0 1 Vishakha Pandey 0 1 Manoj Singh 0 1 Dinesh Pandey 0 1 M. S. Saharan 1 Soma S. Marla 1 ☯ These authors contributed equally to this work. 1 ak_gupta 1 1 1 0 Department of Molecular biology and Genetic Engineering, G.B. Pant University of Agriculture and Technology , Pantnagar, Uttarakhand , India , 2 Division of Plant Pathology, Indian Agricultural Research Institute , New Delhi , India , 3 Division of Genomic Resources, National Bureau of Plant Genetic Resources , New Delhi , India 1 Editor: Wujun Ma, Murdoch University , AUSTRALIA Karnal bunt disease in wheat is caused by hemibiotrophic fungus, Tilletia indica that has been placed as quarantine pest in more than 70 countries. Despite its economic importance, little knowledge about the molecular components of fungal pathogenesis is known. In this study, first time the genome sequence of T. indica has been deciphered for unraveling the effectors' functions of molecular pathogenesis of Karnal bunt disease. The T. indica genome was sequenced employing hybrid approach of PacBio Single Molecule Real Time (SMRT) and Illumina HiSEQ 2000 sequencing platforms. The genome was assembled into 10,957 contigs (N50 contig length 3 kb) with total size of 26.7 Mb and GC content of 53.99%. The number of predicted putative genes were 11,535, which were annotated with Gene Ontology databases. Functional annotation of Karnal bunt pathogen genome and classification of identified effectors into protein families revealed interesting functions related to pathogenesis. Search for effectors' genes using pathogen host interaction database identified 135 genes. The T. indica genome sequence and putative genes involved in molecular pathogenesis would further help in devising novel and effective disease management strategies including development of resistant wheat genotypes, novel biomarkers for pathogen detection and new targets for fungicide development. - Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work is funded by Department of Biotechnology (Govt. of India), New Delhi (BT/PR/ 14987/AGR/2/914/2015) and G.B. Pant University of Agriculture and Technology, Pantnagar. Competing Interests: The authors have declared that no competing interests exist. Introduction Wheat belongs to genus Triticum of an economically important family Poaceae. In 2015, world production of wheat was 732 million tons, making it the second most produced cereal after maize (972 million tons) (www.igc.int). According to Food and Agriculture Organization (FAO) survey, the wheat was cultivated on approximately 150 million hectares and 732.9 million tons was harvested worldwide in 107 countries in 2015 (www.fao.org). Wheat is used both as cash crop and livestock and poultry feed. Being an excellent source of carbohydrate, vitamins, proteins, dietary fibers and minerals, wheat serve as a staple food of many countries and is a major constituent in many foods. The worldwide increasing demand for wheat and wheat products keeps driving the growth of wheat agriculture. During cultivation, wheat is affected by several diseases such as rusts, smuts, bunts, powdery mildew, leaf blight. Among them, Karnal bunt (KB) incited by smut fungus Tilletia indica (Syn. Neovossia indica) continues to be a limiting factor in increasing wheat yield. The KB disease (also known as partial bunt) that partially convert the kernels into sori filled with fetid teliospores was first reported in 1931 in Karnal, India [ 1 ]. Since then it is widespread in Pakistan, Nepal, Iraq, Iran, Afganistan, South Africa, Mexico and the United States (http://www. nda.agric.za/docs/GenPub/karnalbunt.htm). KB has the potential to reduce the crop yield, seed quality and germination. The wheat lots with 1% or more infected grains make wheat products unpalatable due to unpleasant fishy odor of trimethylamine secreted by teliospores. The wheat containing more than 3% bunted kernels is considered unfit for human consumption [ 2 ], as a result the bread making quality wheat becomes downgraded to feed, leading to large financial losses to the producers. The KB disease not only affects the producers but also the wheat exporting countries face the trade barrier due to restricted export and movement of consignment of wheat grains to countries which are presently free from T. indica. It is now placed as a quarantined pest in more than 70 countries [ 3 ]. Moreover, some countries have even imposed zero tolerance quarantine regulations against the KB pathogen by virtue of which wheat importing countries incur indirect costs due to quarantine measures that must be applied to grain exports [ 4, 5 ]. Hence, KB is regarded as an economically important disease. T. indica is a heterothallic fungi. The teliospores, an infecti (...truncated)


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Anil Kumar, Vishakha Pandey, Manoj Singh, Dinesh Pandey, M. S. Saharan, Soma S. Marla. Draft genome sequence of Karnal bunt pathogen (Tilletia indica) of wheat provides insights into the pathogenic mechanisms of quarantined fungus, PLOS ONE, 2017, Volume 12, Issue 2, DOI: 10.1371/journal.pone.0171323