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Functional expression of MAP kinase TiHOG1 gene in Tilletia indica inciting Karnal bunt of wheat

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Abstract

Tilletia indica is an important quarantined fungal pathogen inciting Karnal bunt disease of wheat. In fungal pathogens, the Hog1-type MAPK is involved in response to various stresses and virulence. In the present study,we identified, characterized and analyzed functional expression of the TiHog1-type gene. As HOG1 homologous genes are salt-inducible, the TiHOG1 gene (1104 bp) was amplified in 1 M NaCl stressed condition in T. indica; cloned in pJET2.0 cloning vector. The TiHOG1 gene was subcloned in expression vector (pRS426Gpd plasmid) and sequences were analyzed. The TiHOG1 in pRS426GPD (pRS426GPD-TiHOG1) was expressed functionally in heterologous system (Saccaromyces cerevisiae). TiHOG1 protein exhibits high amino acid similarity with the homologous protein sequences in Tilletia caries, Ustilago maydis and Puccinia graminis f. sp. tritici. Functional expression of TiHOG1 in S. cerevisiaehog1 mutant showed that TiHOG1 was restored salinity stress tolerance up to 1 M NaCl, 1 M KCl, 0.25 CsCl2, 0.5 M MgCl2 and 0.5 M CaCl2 and osmostress tolerance up to 1 M sorbitol and 1 M sucrose. The expression of TiHOG1 was elicited up to 19.81-fold in response to a susceptible host, whereas resistant host factors showed 9.65-fold transcripts. This first study revealed involvement of a TiHOG1 gene in stress tolerance and may have a role in pathogenesis of T. indica (Karnal bunt of wheat).

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References

  • Adam AL, Kohut G, Hornok L (2008) Fphog1, a HOG-type MAP kinase gene, is involved in multistress response in Fusarium proliferatum. J Basic Microbiol 48(3):151–159

    Article  CAS  PubMed  Google Scholar 

  • 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(3):333–342

    Article  Google Scholar 

  • Bonde MR, Berner DK, Nester SE, Petersonm GL, Olsen MW, Cunfer BM, Sim T (2004) Survival of Tilletia indica teliospores in different soils. Plant Dis 88(4):316–324

    Article  PubMed  Google Scholar 

  • Brewster JL, Devaloir T, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259(5102):1760–1763

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Du C, Sarfati J, Latge JP, Calderone R (2006) The role of the sakA (Hog1) and tcsB (sln1) genes in the oxidant adaptation of Aspergillus fumigatus. Med Mycol 44(3):211–218

    Article  CAS  PubMed  Google Scholar 

  • Gietz RD, Woods RA (1994) High efficiency transformation with lithium acetate. In Johnston JR (ed) Molecular genetics of yeast: a practical approach. Oxford University Press, Oxford, pp 121–134

    Google Scholar 

  • Goates BJ, Jackson EW (2006) Susceptibility of wheat to Tilletia indica during stages of spike development. Phytopathol 96(9):962–966

    Article  Google Scholar 

  • Gostinc C, Lenassi M, Gunde-Cimerman N, Plemenitas A (2011) Fungal adaptation to extremely high salt concentrations. Adv Appl Microbiol 77:71–96

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gurjar MS, Jogawat A, Kulshresta D, Sharma S, Aggarwal R (2016) Intraspecific variation of Tilletia indica isolates causing Karnal bunt of wheat in India. Indian Phytopathol 69(4):352–356

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hamel LP, Nicole MC, Duplessis S, Ellis BE (2012) Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 24(4):1327–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogawat A, Vadassery J, Verma N, Oelmuller R, Dua M, Nevo E, Johri AK (2016) PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Sci Rep 6:36765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamper J, Kahmann R, Bolker M, Ma LJ et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444(7115):97–101

    Article  PubMed  Google Scholar 

  • Kim J, Oh J, Sung GH (2016) MAP kinase Hog1 regulates metabolic changes induced by hyperosmotic stress. Front Microbiol 7:732

    PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7 molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leng YQ, Zhong SB (2015) The role of mitogen-activated protein (MAP) kinase signaling components in the fungal development, stress response and virulence of the fungal cereal pathogen Bipolaris sorokiniana. PLoS One 10(5):e0128291

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitra M (1931) A new bunt on wheat in India. Ann Appl Biol 18(2):178

    Article  Google Scholar 

  • Moriwaki A, Kubo E, Arase S, Kihara J (2006) Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 257(2):253–261

    Article  CAS  PubMed  Google Scholar 

  • Mumberg D, Mailer R, Funk M (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156(1):119–122

    Article  CAS  PubMed  Google Scholar 

  • Po LI, Gong X, Hui JIA, Fan Y, Zhang Y, Cao Z, Hao Z, Han J, Gu S, Dong J (2016) MAP kinase gene STK1 is required for hyphal, conidial, and appressorial development, toxin biosynthesis, pathogenicity, and hypertonic stress response in the plant pathogenic fungus Setosphaeria turcica. J Integr Agric 15(12):2786–2794

    Article  Google Scholar 

  • Rana M, Arora C, Ram B, Kumar A (2001) Floret specificity of Karnal bunt infection due to presence of fungal growth-promotory activity in wheat spikes. J Plant Biol 28(3):283–290

    Google Scholar 

  • Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11(13):4705–4713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Singh DV, Gogoi R (2011) Karnal bunt of wheat (Triticum sp.): a global scenario. Indian J Agric Sci 81(1):3–14

    Google Scholar 

  • Thirumalaisamy PP, Singh DV (2012) Variability of Indian isolates of Tilletia indica assessed by pathogenicity and molecular markers. J Phytopathol 160(10):525–531

    Article  CAS  Google Scholar 

  • Wang Y, Tian L, Xiong D, Klosterman SJ, Xiao S, Tian C (2016) The mitogen-activated protein kinase gene, VdHog1, regulates osmotic stress response, microsclerotia formation and virulence in Verticillium dahliae. Fungal Genet Biol 88:13–23

    Article  CAS  PubMed  Google Scholar 

  • Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79(1):143–180

    Article  CAS  PubMed  Google Scholar 

  • Yu D, Li R, Yu Z, Cao Z (2016) Molecular characterization of a Hog1-type MAPK, Mlp Hog 1, from Melampsora larici-populina. Phytoparasitica 44(2):251–259

    Article  CAS  Google Scholar 

  • Zhang Y, Lamm R, Pillonel C, Lam S, Xu JR (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen activated protein kinase homologue. Appl Environ Microbiol 68(2):532–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao XH, Mehrabi R, Xu JR (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6(10):1701–1714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng DW, Zhang S, Zhou X, Wang C, Xiang P, Zheng Q, Xu JR (2012) The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum. PLoS One 7(11):e49495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng D, Wang Y, Han Y, Xu JR, Wang C (2016) UvHOG1 is important for hyphal growth and stress responses in the rice false smut fungus Ustilaginoidea virens. Sci Rep 6:srep24824

    Article  Google Scholar 

Download references

Acknowledgements

This work is financially supported by the Indian Council of Agricultural Research (ICAR) -Consortium Research Platform (CRP) on Genomics (ICAR-G/CRP-Genomics/2015-2720/IARI-12-151). We are highly thankful to the Director, Joint Director (Research), ICAR-IARI, New Delhi for providing guidance and facilities for carrying out this study.

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Correspondence to Malkhan Singh Gurjar.

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Gurjar, M.S., Jogawat, A., Sharma, S. et al. Functional expression of MAP kinase TiHOG1 gene in Tilletia indica inciting Karnal bunt of wheat. Indian Phytopathology 71, 325–335 (2018). https://doi.org/10.1007/s42360-018-0058-3

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