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Disease resistance and virulence screen in Solanum tuberosum–Alternaria tenuissima interaction: the role of pathogenicity factors

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Abstract

Early blight, caused by different species of Alternaria, is a major and destructive disease of potato worldwide. In recent years, Alternaria tenuissima is recognized as the most prevalent species of this phytopathogenic fungus in potato fields of Asian countries, which causes high yield losses every year. Any potato cultivar with complete resistance to early blight is not recognized, so far. Therefore, screening resistance levels of potatoes, identification of the pathogen’s pathogenicity factors and plant defense mechanisms against the disease might be important for designing novel and effective disease management strategies. In this research, nine potato cultivars and five A. tenuissima isolates were used to investigate potential of these fungal isolates to infect various cultivars and determine resistance levels of the host plant. Cultivar Ramus had the highest level of resistance and Bamba was the most susceptible among all tested cultivars. Different levels of virulence and aggressiveness were observed for various isolates of A. tenuissima. Analyzing the activity of cell wall degrading enzymes (CWDEs), including cellulase, pectinase, lipase and xylanase produced by the fungal isolates revealed higher activity of these enzymes for the isolates with higher levels of pathogenicity on potato. Therefore, these findings suggested that activity levels of CWDEs, as pathogenicity factors, are correlated with virulence and aggressiveness of A. tenuissima on potato cultivars. This is the first report on screening host plant resistance, together with investigating association between pathogenicity factors and pathogenesis of A. tenuissima isolates, causing blight disease on potato.

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References

  • Abdel-Razik AA (1970) The parasitism of white Sclerotium cepivorum Berk, the incitant of white rot of onion. Ph.D. thesis, Fac Agric, Assiut University, Assiut, Egypt

  • Anand T, Bhaskaran R, Raguchander T, Karthikeyan G, Rajesh M, Senthilraja G (2008) Production of cell wall degrading enzymes and toxins by Colletotrichum capsici and Alternaria alternata causing fruit rot of chillies. J Plant Prot Res 48:437–451

    Article  CAS  Google Scholar 

  • Bailey MJ, Biely P, Poutanen K (1992) Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 23:257–270

    Article  CAS  Google Scholar 

  • Bessadat N, Benichou S, Kihal M, Henni DE (2014) Aggressiveness and morphological variability of small spore Alternaria species isolated from Algeria. J Exp Biol Agric Sci 2:265–278

    Google Scholar 

  • Boedo C, Le Clerc V, Briard M, Simoneau P, Chevalier M, Georgeault S, Poupard P (2007) Impact of carrot resistance on development of the Alternaria leaf blight pathogen (Alternaria dauci). Eur J Plant Pathol 121:55–66

    Article  Google Scholar 

  • Cho Y (2015) How the necrotrophic fungus Alternaria brassicicola kills plant cells remains an enigma. Eukaryot Cell 14:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho Y, Cramer RA Jr, Kim KH, Davis J, Mitchell TK, Figuli P, Pryor BM, Lemasters E, Lawrence CB (2007) The Fus3/Kss1 MAP kinase homolog Amk1 regulates the expression of genes encoding hydrolytic enzymes in Alternaria brassicicola. Fungal Genet Biol 44:543–553

    Article  CAS  PubMed  Google Scholar 

  • Cho Y, Kim KH, Rota ML, Scott D, Santopietro G, Callihan M, Mitchell TK, Lawrenc CB (2009) Identification of novel virulence factors associated with signal transduction pathways in Alternaria brassicicola. Mol Microbiol 72:1316–1333

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Kim KT, Jeon J, Lee YH (2013) Fungal plant cell wall-degrading enzyme database: a platform for comparative and evolutionary genomics in fungi and Oomycetes. BMC Genom 14:S7

    Article  Google Scholar 

  • Christ B, Maczuga S (1989) The effect of fungicide schedules and inoculum levels on early blight severity and yield of potato. Plant Dis 73:695–698

    Article  Google Scholar 

  • Colowich SP (1995) Methods in enzymology. Academic Prees Inc., London

    Google Scholar 

  • Deep S, Sharma P, Behera N (2014) Optimization of extracellular cellulase enzyme production from Alternaria brassicicola. Int J Curr Microbiol App Sci 3:127–139

    CAS  Google Scholar 

  • Gaillardin C (2010) Lipases as pathogenicity factors of fungi. In: Timmis KN, McGenity T, van der Meer R, de Lorenzo V (eds) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin

    Google Scholar 

  • Gibson DM, King BC, Hayes ML, Bergstrom GC (2011) Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Cur Opin Microbiol 14:264–270

    Article  CAS  Google Scholar 

  • Harteveld DOC, Akinsanmi OA, Drenth A (2014) Pathogenic variation of Alternaria species associated with leaf blotch and fruit spot of apple in Australia. Eur J Plant Pathol 139:789–799

    Article  Google Scholar 

  • Hou Y, Ma X, Wan W, Long N, Zhang J, Tan Y, Duan S, Zeng Y, Dong Y (2016) Comparative genomics of pathogens causing brown spot disease of tobacco: Alternaria longipes and Alternaria alternata. PLoS ONE 11:e0155258. https://doi.org/10.1371/journal.pone.0155258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubballi M, Sornakili A, Nakkeeran S, Anand T, Raguchander T (2011) Virulence of Alternaria alternate infecting noni associated with production of cell wall degrading enzymes. J Plant Prot Res 51:87–92

    Article  Google Scholar 

  • Kakueinezhad M, Taheri P, Mahmoudi B, Tarighi S (2017) Sources of resistance to Phytophthora root rot within the genus Beta. Euphytica 213:193

    Article  Google Scholar 

  • Khaledi N, Taheri P, Falahati Rastegar M (2017) Identification, virulence factors characterization, pathogenicity and aggressiveness analysis of Fusarium spp., causing wheat head blight in Iran. Eur J Plant Pathol 147:897–918

    Article  CAS  Google Scholar 

  • Khanna S, Gauri A (1993) Regulation, purification, and properties of xylanase from cellulomonas fimi. Enzym Microb Technol 15:990–995

    Article  CAS  Google Scholar 

  • MacMillan JD, Voughin RH (1964) Purification and properties of a polyglacturonic acid-transeliminase produced by Clastridium multiformentans. Biochemistry 3:564–572

    Article  CAS  PubMed  Google Scholar 

  • McRoberts N, Lennard HJ (1996) Pathogen behaviour and plant cell reaction in interactions between Alternaria species and leaves of host and non-host plants. Plant Pathol 45:742–752

    Article  Google Scholar 

  • Meena M, Gupta SK, Swapnil P, Zehra A, Dubey MK, Upadhyay RS (2017) Alternaria toxins: potential virulence factors and genes related to pathogenesis. Front Microbiol 8:1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Meng JW, ZhuW He MH, Wu EJ, Yang LN, Shang LP, Zhan J (2015) High genotype diversity and lack of isolation by distance in the Alternaria solani populations from China. Plant Pathol 64:434–441

    Article  CAS  Google Scholar 

  • Meng JW, He DC, Zhu W, Yang LN, Wu EJ, Xie JH, Shang L-P, Zhan J (2018) Human-mediated gene flow contributes to metapopulation genetic structure of the pathogenic fungus Alternaria alternata from potato. Front Plant Sci 9:198

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analyt Chem 31:426–428

    Article  CAS  Google Scholar 

  • Noda J, Brito N, Gonzalez C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Odilbekov F, Carlson-Nilsson U, Liljeroth E (2014) Phenotyping early blight resistance in potato cultivars and breeding clones. Euphytica 197:87–97

    Article  Google Scholar 

  • Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB (2002) Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36:176–186

    Article  CAS  PubMed  Google Scholar 

  • Ortega LM, Kikot GE, Astoreca AL, Alconada TM (2013) Screening of Fusarium graminearum isolates for enzymes extracellular and deoxynivalenol production. J Mycol 358140:1–7

    Google Scholar 

  • Pannecoucque J, Höfte M (2009) Interactions between cauliflower and Rhizoctonia anastomosis groups with different levels of aggressiveness. BMC Plant Biol 9:95

    Article  PubMed  PubMed Central  Google Scholar 

  • Pariaud B, Ravigné V, Halkett F, Goyeau H, Carlier J, Lannou C (2009) Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol 58:409–424

    Article  Google Scholar 

  • Pelletier J, Fry W (1989) Characterization of resistance to earlyblight in three potato cultivars: incubation period, lesion expansion rate, and spore production. Phytopathology 79:511–517

    Article  Google Scholar 

  • Robl D, Delabona PDS, Mergel CM, Rojas JD, Costa PDS, Pimentel IC, Vicente VA, Pradella JGC, Padilla G (2013) The capability of endophytic fungi for production of hemicellulases and related enzymes. BMC Biotechnol 13:94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shahbazi H, Aminian H, Sahebani N, Halterman DA (2010) Biochemical evaluation of resistance responses of potato to different isolates of Alternaria solani. Phytopathology 100:454–459

    Article  CAS  PubMed  Google Scholar 

  • Shtienberg D, Bergeron S, Nicholson A, Fry W, Ewing E (1990) Development and evaluation of a general model for yield loss assessment in potatoes. Phytopathology 80:466–472

    Article  Google Scholar 

  • Silva BMA, Prados-Rosales R, Espadas-Moreno J, Wolf JM, Luque-Garcia JL, Gonçalves T, Casadevall A (2014) Characterization of Alternaria infectoria extracellular vesicles. Med Mycol 52:202–210

    Article  CAS  PubMed  Google Scholar 

  • Taheri P (2018) Cereal diseases caused by Fusarium graminearum: from biology of the pathogen to oxidative burst-related host defense responses. Eur J Plant Pathol 152:1–20

    Article  CAS  Google Scholar 

  • Taheri P, Kakooee T (2017) Reactive oxygen species accumulation and homeostasis are involved in plant immunity to an opportunistic fungal pathogen. J Plant Physiol 216:152–163

    Article  CAS  PubMed  Google Scholar 

  • Taheri P, Tarighi S (2010) Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J Plant Physiol 167:201–208

    Article  CAS  PubMed  Google Scholar 

  • Taheri-Ardestani S, Sharif-Nabi B, Zare R, Abbassi-Moghadam A (2010) New Alternaria species associated with potato leaf spot in various potato growing regions of Iran. Iran J Plant Pathol 45:83–86

    Google Scholar 

  • Tymon LS, Cummings TF, Johnson DA (2016) Pathogenicity and aggressiveness of three Alternaria spp. on potato foliage in the U.S. North-west. Plant Dis 100:797–800

    Article  PubMed  Google Scholar 

  • Wood TM, Bhat M (1988) Methods for measuring cellulase activities. Methods Enzymol 160:87–112

    Article  CAS  Google Scholar 

  • Zheng HH, Zhao J, Wang TY, Wu XH (2014) Characterization of Alternaria species associated with potato foliar diseases in China. Plant Pathol 64:425–433

    Article  Google Scholar 

Download references

Acknowledgements

The author would like to thank Ferdowsi University of Mashhad, Iran, for financial support of this research with Project Number 39608.

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  1. Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, P.O.Box: 91775-1163, Mashhad, Iran

    Parissa Taheri

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Taheri, P. Disease resistance and virulence screen in Solanum tuberosum–Alternaria tenuissima interaction: the role of pathogenicity factors. Euphytica 215, 15 (2019). https://doi.org/10.1007/s10681-019-2337-1

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