The effect of Pseudomonas protegens CHA0 and an endophyte fungus Serendipita indica on resistance induction with defense genes expression of wheat against Septoria leaf blotch disease

Document Type : Research Article

Authors

1 Ph.D. Student, of plant protection, department of plant production,, Gorgan University of Agricultural Sciences and Natural Resources, Golestan, Iran;

2 Associate professors of plant protection department faculty of plant production, Gorgan University of Agricultural Sciences and Natural Resources, Golestan, Iran

3 Department of plant protection, Sari Agricultural sciences and Natural Resources university, Mazandaran, Iran

4 Associate professors of department of biotechnology faculty of plant production, Gorgan University of Agricultural Sciences and Natural Resources, Golestan, Iran

5 Professor, Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland

Abstract

Septoria leaf blotch (STB) caused by Zymoseptoria tritici, is one of the important wheat disease. The endophytic fungus Serendipita indica and the plant-protecting bacteria Pseudomonas protegens induce systemic resistance to plant pathogens. In this study, the expression rate of several defense genes in Tajan susceptible wheat cultivar treated by S. indica and P. protegens and in control plants at different times point after inoculation with Z. tritici were investigated by Real-time qPCR technique. The results showed that, the expression of PAL and LOX genes in plants treated with P. protegens was higher than other treatments. The expression of NPR1 and PR5 genes were higher in co-inoculated plants that treated by S. indica and P. protegens. The results of phenotypic evaluation of two mentioned treatments also show, the expression of these genes is effective in inducing resistance.The results indicate the active role of these two biocontrol agents in protection of susceptible Tajan cultivar against STB due to increased expression of these genes compared to control.

Keywords


AHANGAR, L., BABAEZAD, V.A., and RANJBAR, G.A. 2014. Analysis of NPR1 gene expression in wheat infected with powdery mildew after treatment with salicylic acid and Piriformospora indica. Published Only in NCBI Database, KM017012.1.
AHANGAR, L., RANJBAR, G.A., BABAEZAD, V.A., ZARRINI, H.N., and BIABANI, A. 2014. Assay of NPR1 gene expression in wheat under powdery mildew Stress. J. Crop Prot, 6 (1): 157-166.
AHANGAR, L., BABAEZAD, V.A., RANJBAR, G.A. ZARRINI, H.N., and BIABANI, A.2016. Study of PR Gene ExpressionPattern related to in Induced Resistance to Powdery Mildew in Susceptible Wheat Genotype after Treating with Salicylic Acid. Journal of Crop Breeding. 8(17):208-218.
AKHA,A. 2009. Barley powdery mildew (Blumeria graminis f. sp. hordei): Interaction, Resistance and Tolerance. Egypt. J. Exp. Biol. (Bot), 5:1-20.
ASHRAFI,J., RAHNAMA , K., BABAEIZAD, V., RAMEZANPOUR , S.S., and KEEL , C. 2019. Investigating the mode distribution of Septoria leaf blotch and evaluating the resistance of wheat cultivars in Golestan province. Iran J Entomol and Phytopathol, 86(2):37-47.
BAI,W., CHERN, M., RUAN, D., CANLAS, P.E., SZE-TO, W.H., and RONALD, P.C. 2011. Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog. Plant biotechnology journal. 9:205-215.
BARBER, M.S. and HALL, S.A. 2000. Mapping of a novel wheat phenylalanine ammonia-lyase to chromosome six using nullitetrasomic and ditelosomic stocks. Published Only in NCBI Database, AY005474.
BECCARI, G., COVARELLI, L., and NICHOLSON, P. 2011. Infection processes and soft wheat response to root rot and crown rot caused by Fusarium culmorum. Plant Pathol, 60:671-684.
BUETEHORN, B., RHODY, D., and FRANKEN, P. 2000. Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1-alpha of the root endophyte Piriformospora indica. Plant Biol. 2:687-692.
CAO,H., GLAZBROOK, J., CLARKE, J., VOLKO, S., and DONG, X. 1997. The Arabidopsis npr1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 88:57-63.
CHARTRAIN, L., BRADING, P., MAKEPEACE, J., and BROWN, J. 2004. Sources of resistance to Septoria tritici blotch and implications for wheat breeding. Plant Pathol, J. 53(4):454-60.
CHEN,X., BARNABY, J.Y., SREEDHARAN, A., HUANG, X., ORBOVIC, V., and GROSSER, J.W. 2013. Over expression of citrus gene, CtNH1 confers resistance to bacterial canker disease. PHYSIOL MOL PLANT P. 84:115-122.
CROFT,K.P.C., JUTTNER, F., and SLUSARENKO, A.J. 1993. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. Phaseolical. Plant Physiol, 101:13-24.
DEHGHANPOUR-FARASHAH, S., TAHERI, P., and FALAHATI-RASREGAR, M. 2019. Effect of polyamines and nitric oxide in Piriformospora indica induced resistance and basal immunity of wheat against Fusarium pseudograminearum. Biol Control, 104006:1-49.
DING, L.N., YANG, G.X., YANG, R.Y., CAO, J., and ZHOU, Y. 2016.Investigating interactions of salicylic acid and jasmonic acid signaling pathways in monocots wheat. Physiol. Mol. Plant Pathol, 93:67–74.
DORNELES, K.R., DALLAGNOL, L.J., PAZDIORA, P.C., RODRIGUES, F.A., and DEUNER, S. 2017. Silicon potentiates biochemical defense responses of wheat against tan spot. PHYSIOL MOL PLANT P, 97: 69-78.
DUBA, A., GORIEWA-DUBA, K., WACHOWSKA, U., GLOWACKA, K., and WIWART, M. 2019. The Associations between Leaf Morphology, Phenylalanine Ammonia Lyase Activity, Reactive Oxygen Species, and Fusarium Resistance in Selected Species of Wheat with Di_erent Ploidy Levels. Plants, 8:1-19.
ESSE, H.P.V., REUBER, T.L., and der DOES., D.V. 2020. Genetic modification to improve disease resistance in crops. New Phytologist, 225: 70–86.
EYAL, Z., SCHAREN, A.L., PRESCOTT, J.M., and vAN GINKEL, M. 1987. The Septoria diseases of wheat: concepts and methods of disease management. Mexico, D.F.; CIMMYT, p.46.
FARHANGI, M.B., SAFARI SINEGANI, A.A., MOSADDEGHI, M.R., UNC, A., and KHODAKARAMIAN, G. 2014. Survival of Pseudomonas fluorescens CHA0 in soil; impact of calcium carbonate and temperature. ARID LAND RES MANAG, 28(1):36-48.
GARRIDO-SANZ, D., ARREBOLA, E.,  MARTINEZ-GRANERO, F., GARCIA-MENDEZ, S., MURIEL, C., BLANCO-ROMERO, E., MARTIN, M., RIVILLA, R., REDONDO-NIETO, M. 2017. Classification of Isolates from the Pseudomonas fluorescens Complex into Phylogenomic Groups Based in Group-Specific Markers. FRONT MICROBIOL. 8(413): 1-10.
GHOLAMNEZHAD, J., SANJARIAN, P., GOLTAPEH, E.M., SAFAIE, N., and RAZAVI, K. 2016. Effect of Salicylic Acid on Enzyme Activity in Wheat in Immediate Early Time after Infection with Mycosphaerella graminicola. Plant Sciences, Scientia agriculturae Bohemica, 47(1): 1–8.
GORLACH, J., VOLRATH, S., KNAUF-BEITER, G., HENGY, G., BECKHOVE, U., KOGEL, K.H., OOSTENDORP, M., STAUB, T., WARD, E., KESSMAN, H., and RYALS, J.1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell, 8:629-643.
HAAS,D.and KEEL C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol, 41(1):117-53.
HIBBETT, D.S. 2006. A phylogenetic overview of the Agaricomycotina. Mycologia. 98:917-925. 
HIMI, E. and NODA, K. 2004. Isolation of wheat actin gene. Published Only in NCBI Database, 2: AB181991.1
HON,W.C., GRIFFITH, M., MLYNARZ, A., KWOK, Y.C., and YANG, D.S.C. 1995. Antifreeze proteins in winter rye are similar to pathogenesis related proteins. Plant physiology. 109:879-889.
KARISTO, P., HUND, A., Yu, K., ANDEREGG, J., WALTER, A., MASCHER, F., MC DONALD, B.A., and MIKABERIDZE, A. 2018. Ranking quantitative resistance to Septoria tritici blotch in elite wheat cultivars using automated image analysis. Phytopathology, 108(5):568-581.
KIA, S. and TORABI, M. 2008. Effects of infection with Septoria leaf blotch (Septoria tritici Rob. Ex. Desm.) at different growth stages on yield and yield components ofwheat cultivars in Gorgan. Seed and Plant, 24:237-250 (in Persian).
KIA, Sh., RAHNAMA, K., SOLTANLOO, H., BABAEIZAD, V., and AGHAJANI, M.A. 2017. Effectiveness of Resistance Genes to Septoria tritici Blotch (Stb) in Differential Cultivares of Wheat against Zymoseptoria tritici Isolates. J. Appl. Plant Prot, 6:109-123.
KIA, Sh., RAHNAMA, K., SOLTANLOO, H., BABAEIZAD, V., and AGHAJANI, M.A. 2017. Identification of Resistance Sources to Septoria tritici Blotch with Causal Agent Zymoseptoria tritici in Bread Wheat Genotypes. Journal of Agricultural Biotechnology, 10:51-67.
KIA, S., RAHNAMA, K., SOLTANLOO, H., BABAEIZAD, V., and AGHAJANI, M. A. 2018. Effectiveness of Resistance Genes to Septoria tritici Blotch (Stb) in Differential Cultivares of Wheat against Zymoseptoria tritici Isolates.J. Appl. Plant Prot. 6: 109-123.
KOGEL, K.H., FRANKEN, P., and HU¨CKELHOVEN, R. 2006. Endophyte or parasite-what decides? Curr Opin Plant Biol. 9:358–363.
KONONOWICZ, A.K., NELSON, D.E., SINGH, N.K., HASEGAWA, P.M., and BRESSAN, R.A. 1992. Regulation of the osmotin gene promotor. The Plant Cell. 4:513-524.
LEMIRE,G., SIAH, A., NOELLE BRISSET, M., GAUCHER, M., DELEU, M., and JIJAKLI, H. 2018. Surfactin Protects Wheat against Zymoseptoria tritici and Activates Both Salicylic Acid- and Jasmonic Acid-Dependent Defense Responses. Agriculture, 8(11): 1-14.
LIN,V.C., LU, C.F., WU, J.W., CHENG, M.L., and CHENG, C.P. 2004. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Biomedical and Life Sciences. 13:567-581.
LINTHORST, H.J.M. 1991. Pathogenesis-related proteins of plants. Crit. Rev. Plant Sci.10: 123–150.
MACHOLDT, and J. HONERMEIER, B. 2017. Yield Stability in Winter Wheat Production: A Surveyon German Farmers’ and Advisors’ Views. Agronomy, 45(7):2-18.
MAUMENE, C., SIAH, A., ORS, M.E., COULEAUD, G., RANDOUX, B., RIGOLLE, P., SELIM, S., HALAMA, P., and REIGNAULT, P. 2010. Interaction entre stimulateurs de défense des plantes et génotypes de blé tendre dans la lutte contre la septoriose. FSOV: 1-10.
MOLDOVAN, V., MOLDOVAN, M., and KADAR, R. 2005.Assesment of winter wheat cultivars for resistance to fusarium heat blight. AWN, 51: 97-98.
MOLITOR, A. and KOGEL, K.H. 2009. Induced resistance triggered by Piriformospora indica. Plant Signaling Behavior, 4: 215-216.
MOUSAVI,S.H., BABAEI ZAD, V., SHARIFNABI, B., TAJIC GHANBARI, M.A., MASSAHA, A. and ALAVI, S.M., 2014. Induction of blast disease resistance in rice plants endophyte fungus Piriformospora indica. Iranian J Plant Pathol, 50:127-9. (in Persian with English Summary)
MURRAY,M. and THOMPSON, W.F. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res, 8(19):4321-6.
NGADZE, E., ICISHAHAYO, D., COUTINHO, T.A., and VAN DER WAALS, J.E. 2012. Role of polyphenol oxidase, peroxidase, phenylalanine ammonia lyase, chlorogenic acid, and total soluble phenols in resistance of potatoes to soft rot. Plant Dis, 96:186–192.
ORS, M., RANDOUX, B., SIAH, A., COULEAUD, G., MAUMENE, C., SAHMER, K., REIGNAULT, PH., HALAMA, P., and SELIM, S. 2017. A plant nutrient and microbial protein-based resistance inducer elicits wheat cultivar dependent resistance against Zymoseptoria tritici. Phytopathology. 43:1-45.
PANDELOVA, I., FIGUEROA, M., WILHELM, L.J., MANNING, V.A., MANKANEY, A.N., MOCKLER, T.C., and CIUFFETI, L.M. 2012. Host-selective toxins of Pyrenophora tritici-repentis induce common responses associated with host susceptibility. PLoS One, 7:402-440.
PALMER, C.L. and SKINNER, W. 2002. Mycosphaerella graminicola: latent infection, crop devastation and genomics. Mol Plant Pathol, 3(2):63-70.
PESKAN-BERGHOFER, T., SHAHOLLARI, B., GIONG, P.H., HEHI, S., MARKERT, C., BLANKE, V., KOST, G., VARMA, A., and OELMULLER, R. 2004. Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant–microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane, Physiologia Plantarum. 122:465-477.
PIAFAL,M.W., HORGAN, G.W., and DEMPFLE, L. 2002. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic acids research, 30(9) pp.36-36.
RAIRDAN, J.G., DONOFRIO, N.M., and DELANEY, T.P. 2001. Salicylic acid and N1M1/NPR1 independent gene induction by incompatible Peronospora parasitica in Arabidopsis. Molecular Plant Microb Interaction. 14:1235-1246.
RAZA, A., RAZZAQ, A., MEHMOOD, S.S., ZOU, X., ZHANG, X., and LV, Y. 2019. Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants, 8(2):1-29.
SAMAIN, E., AUSSENAC, T., and SELIM, S. 2019. The Effect of Plant Genotype, Growth Stage, and Mycosphaerella graminicola Strains on the Efficiency and Durability of Wheat-Induced Resistance by Paenibacillus sp. Strain B2. Frontiers in Plant Science, 10(587):1-16.
SAARI, E. E., and PRESCOTT, J. M. 1975.A scale for appraising the foliar intensity of
wheat disease. Plant Dis. 59: 377-380.
SCHAFFRATH,U., ZABBAI, F., and DUDLER, R. 2000. Characterization of RCI-1, a chloroplastic rice lipoxygenase whose synthesis is induced by chemical plant resistance activators. Eur. J. Biochem, 267:5935-5942.
Seed and Plant Improvement Institute Annual Report. 2015. Introduction of cultivars, food safety and health. SPII. p.44. www.SPII.ir
SHARIFI-TEHRANI, A., FARZANEH, M., AFSHARI, F., BEHBODI, K., KELENBERJER, E., and PECHY-TAR, M. 2011. Evaluation of Pseudomonas fluorescens CHA0mcherry in colonization of different wheat varieties and induction resistance to Puccinia triticina. J Iranian Plant Prot Sci, 42(1):85-94.
SHATTER, R.G., BOYKIN, L.M., and LAPOINTE, S.L. 2006. Phylogenetic and structural relationships of the PR5 gene family reveal an ancient multigene family conserved in plants and select animal taxa. J. Mol. Evol. 63:12-29.
SOMAI-JEMMALI, L., MAGNIN-ROBERT, M., RANDOUX, B., SIAH, A., TIS-SERANT, B., HALAMA, P., REIGNAULT, P., and HAMADA, W. 2015. Ascorbic acid control Mycosphaerellaa graminicola in wheat through direct effect on the pathogen and indirect actin on the plant. Comm. Appl. Biol. Sci, Ghent University, 40:1-20.
SOMAI-JEMMALI, L., SIAH, A., HARBAOUI, K., FERGAOUI, S., RANDOUX, B., MAGNIN-ROBERT, M., HALAMA, P., REIGNAULT, P., and HAMADA, W. 2017. Correlation of fungal penetration, CWDE activities and defense-related genes with resistance of durum wheat cultivars to Zymoseptoria tritici. PHYSIOL MOL PLANT P, 100:117-125.
STOTZ, H.U., THOMSON, J.G., and WANG, Y. 2009. Plant defensins defense, development and application. Plant Signaling and Behavior. 11: 1010-1012.
TAYEH, C.,RANDOUX, B., TISSERANT, B., KHONG, G., JACQUES, P., and REIGNAULT, P. 2015. Are ineffective defense reactions potential target for induced resistance during the compatible wheat-powdery mildew interaction?. PLANT PHYSIOL BIOCH, 96:9-19.
VALLAD, G.E. and GOODMAN, R.M. 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science, 44:1920-1934.
WALLER, F., ACHATZ, B., BALTRUSCHAT, H., FODER, J., BECKER, K., FISCHER, M., HEIER, T., CKELHOVEN, R.H., NEUMANN, C., WETTSTEIN, D., FRANKEN, P., and KOGEL, K.H. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS, 102:13386–13391.
WALLER, F., ACHATZ, B., and KOGEL, K.H. 2007. Analysis of the plant protective potential of the root endopytic fungus Piriformospora indica in cereals. Berlin Heidelbeg: Spriger-Verlag, 45:343–354.
VAN HULTEN, M., PELSER, M., VANLOON, L.C., PIETERSE, C.M.J., and TON, J. 2006. Costs and benefits of priming for defense in Arabidopsis. PNAS USA. 103:5602–5607.
VAN LOON, L.C., REP, M., and PIETERSE, C.M. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol, 44:135-162.
VARMA, S., VARMA, A., REXER, K.H., HASSEL, A., KOST, G., SARBHOY, A., BISEN, P., BUTEHORN, B., and FRANKEN, P. 1998. Piriformospora indica, gen. et sp. nov., a new root colonizing fungus. Mycologia, 90:896-903.
VARMA, A., VERMA, S., SUDHA, N., BUTEHORN, B., and FRANKEN, P. 1999. Piriformospora indica, a cultivable plant growth-promoting root endophyte. APPL ENVIRON MICROB. 65:2741-2744.
VELAZHAHAN, R., CHEN-COLE, K., ANURATHA, C.S., and MUTHUKRISHNAN, S. 1998. Induction of thaumatin-like proteins (TLPs) in Rhizoctonia solani infected rice and characterization of two new cDNA clones. Physiol. Plant. 102:21-28.
VIERHEILING, H., COUGHLAN, A.P., WYSS, U. and PICHE, Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol,64:5004–5007.
VICK, B.A.andZIMMERMAN, D.C. 1983. The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem. Biophys. Res. Commun. 111:470-477.
VON FELTEN, A., DEFAGO, G., MAURHOFER, M. 2010. Quantification of Pseudomonas fluorescens strains F113, CHA0 and Pf153 in the rhizosphere of maize by strain-specific real-time PCR unaffected by the variability of DNA extraction efficiency. J. Microbiol. Methods. 81:108–115.
 
WELLER, D.M. 2007. Pseudomonas biocontrol agents of soil borne pathogens: Looking back over 30 years. Phytopathology, 97:250-256.
YU, L., NIU, J.S., MA, Z.Q., CHEN, P.D., and LIU, D.J. 2001. Cloning, location and expression of thaumatin-like protein gene (Ta-TLP) from wheat. NCBI, AF384146.1.
ZHANG, X., HALEY, S., and JIN, Y. 2001. Inheritance of Septoria tritici blotch resistance in winter wheat. CROP SCI, 41(2):323-326.
ZHANG, X., FRANCIS, M.I., DAWSON, W.O., GRAHAM, J.H., ORBOVIC, V., TRIPLETT, E.W., and MAU, Z.H. 2010. Over expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker. Eur. J. Plant Pathol.. 128:91-100.