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Plant growth promotion and suppression of Phytophthora drechsleri damping-off in cucumber by cellulase-producing Streptomyces

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Abstract

Phytophthora drechsleri damping-off is one of the most important diseases of cucumber (Cucumis sativus). Salinity is a serious problem for crop production and affects diversity and activity of soil microorganisms. Application of salt-tolerant biocontrol agents may be beneficial in order to protect plants against pathogenic fungi in saline soils. In this study, a total of 717 Streptomyces isolates were isolated from the rhizosphere of cucumber, out of which two isolates showed more than 70% inhibitory effect against P. drechsleri and had cellulase activity in the presence and absence of NaCl. In a greenhouse experiment, two Streptomyces isolates with the highest antagonistic activity, strains C 201 and C 801, reduced seedling damping-off of cucumber caused by P. drechsleri by 77 and 80%, respectively, in artificially infested soils. Strain C 201 increased dry weight of seedlings up to 21% in greenhouse experiments. Phylogenetic analyses of 16S rRNA gene sequence reveals that strains C 201 and C 801 are closely related to S. rimosus and S. monomycini respectively. Increased activity of polyphenol oxidase (PPO) and peroxidase (POX) enzymes in Streptomyces-treated plants proved the biocontrol-induced systemic resistance (ISR) in cucumber plants against P. drechsleri.

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References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basilio A, Gonzalez I, Vicente MF, Gorrochategui J, Cabello A, Gonzalez A, Genilloud O (2003) Patterns of antimicrobial activities from soil actinomycetes isolated under different conditions of pH and salinity. J Appl Microbiol 95:814–823

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Marten P, Minkwitz A, Brückner S, Lüth P (2001) Efficient biological control of fungal plant diseases by Streptomyces rimosus DSMZ 12424. Tri-trophic interactions in the rhizosphere. IOBC/WPRS Bull 24:9–14

    Google Scholar 

  • Bhuiyan NH, Selvaraj G, Wei YD, King J (2009) Role of lignification in plant defense. Plant Signal Behav 4:158–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanco FF, Folegatti MV (2002) Salt accumulation and distribution in a greenhouse soil as affected by salinity of irrigation water and leaching management. Rev Bras Eng Agríc Ambient 6:414–419

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Café-Filho AC, Ristaino JB (2008) Fitness of isolates of Phytophthora capsici resistant to mefenoxam from squash and pepper fields in North Carolina. Plant Dis 92:1439–1443

    Article  Google Scholar 

  • Chartzoulakis KS (1992) Effects of NaCl salinity on germination, growth and yield of greenhouse cucumber. J Hortic Sci 67:115–119

    Article  CAS  Google Scholar 

  • Chen C, Bélanger RR, Benhamou N, Paulitz TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23

    Article  CAS  Google Scholar 

  • Chen L, Xin X, Yuan Q, Su D, Liu W (2014) Phytochemical properties and antioxidant capacities of various colored berries. J Sci Food Agric 94:180–188

    Article  CAS  PubMed  Google Scholar 

  • Chun J, Goodfellow M (1995) A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Evol Microbiol 45:240–245

    CAS  Google Scholar 

  • Cominelli E, Conti L, Tonelli C, Galbiati M (2013) Challenges and perspectives to improve crop drought and salinity tolerance. N Biotechnol 30:355–361

    Article  CAS  PubMed  Google Scholar 

  • Conn VM, Walker AR, Franco CM (2008) Endophytic Actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–215

    Article  CAS  PubMed  Google Scholar 

  • Davidson RN, den Boer M, Ritmeijer K (2009) Paromomycin. Trans R Soc Trop Med Hyg 103:653–660

    Article  CAS  PubMed  Google Scholar 

  • Downer AJ, Menge JA, Pond E (2001) Association of cellulytic enzyme activities in Eucalyptus mulches with biological control of Phytophthora cinnamomi. Phytopathology 91:847–855

    Article  CAS  PubMed  Google Scholar 

  • El-Tarabily KA, Nassar AH, Hardy GE, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J Appl Microbiol 106:13–26

    Article  CAS  PubMed  Google Scholar 

  • Esterbauer H, Schwarzl E, Hayn M (1977) A rapid assay for catechol oxidase and laccase using 2-nitro-5-thiobenzoic acid. Anal Biochem 77:486–494

    Article  CAS  PubMed  Google Scholar 

  • Fernando WG, Rajesh Ramarathnam D, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

    Article  CAS  Google Scholar 

  • Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A (2014) Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169:59–65

    Article  CAS  PubMed  Google Scholar 

  • Guyer A, De Vrieze M, Bönisch D, Gloor R, Musa T, Bodenhausen N, Bailly A, Weisskopf L (2015) The anti-Phytophthora effect of selected potato-associated Pseudomonas strains: from the laboratory to the field. Front Microbiol 6:1309

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl Soil Ecol 40:510–517

    Article  Google Scholar 

  • Han J, Shi J, Zeng L, Xu J, Wu L (2015) Effects of nitrogen fertilization on the acidity and salinity of greenhouse soils. Environ Sci Pollut Res Int 22:2976–2986

    Article  CAS  PubMed  Google Scholar 

  • Hatami N, Aminaee MM, Zohdi H, Tanideh T (2013) Damping-off disease in greenhouse cucumber in Iran. Arch Phytopathol Plant Protect 46:796–802

    Article  Google Scholar 

  • Hwang BK, Lim SW, Kim BS, Lee JY, Moon SS (2001) Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Appl Environ Microbiol 67:3739–3745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam S, Akanda AM, Prova A, Islam MT, Hossain MM (2016) Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol 6:1360

    Article  PubMed  PubMed Central  Google Scholar 

  • Jose PA, Santhi VS, Jebakumar SRD (2011) Phylogenetic-affiliation, antimicrobial potential and PKS gene sequence analysis of moderately halophilic Streptomyces sp. inhabiting an Indian saltpan. J Basic Microbiol 51:348–356

    Article  PubMed  Google Scholar 

  • Karimi E, Sadeghi A, Abaszadeh Dahaji P, Dalvand Y, Omidvari M, Kakuei Nezhad M (2012) Biocontrol activity of salt tolerant Streptomyces isolates against phytopathogens causing root rot of sugar beet. Biocontrol Sci Technol 22:333–349

    Article  Google Scholar 

  • Kavitha R, Umesha S (2008) Regulation of defense-related enzymes associated with bacterial spot resistance in tomato. Phytoparasitica 36:144–159

    Article  CAS  Google Scholar 

  • Khare E, Singh S, Maheshwari DK, Arora NK (2011) Suppression of charcoal rot of chickpea by fluorescent Pseudomonas under saline stress condition. Curr Microbiol 62:1548–1553

    Article  CAS  PubMed  Google Scholar 

  • Kroon LPNM, Brouwer H, de Cock AWAM, Govers F (2012) The genus Phytophthora Anno 2012. Phytopathology 102:348–364

    Article  Google Scholar 

  • Kruijt M, Tran H, Raaijmakers JM (2009) Functional, genetic and chemical characterization of biosurfactants produced by plant growth-promoting Pseudomonas putida 267. J Appl Microbiol 107:546–556

    Article  CAS  PubMed  Google Scholar 

  • Li X, Huang P, Wang Q, Xiao L, Liu M, Bolla K, Zhang B, Zheng L, Gan B, Liu X, Zhang L, Zhang X (2014) Staurosporine from the endophytic Streptomyces sp. strain CNS-42 acts as a potential biocontrol agent and growth elicitor in cucumber. Antonie van Leeuwenhoek 106:515–525

    Article  PubMed  Google Scholar 

  • Loliam B, Morinaga T, Chaiyanan S (2012) Biocontrol of Phytophthora infestans, fungal pathogen of seedling damping-off disease in economic plant nursery. Psyche 2012: Article ID 324317

  • Lozovaya VV, Lygin AV, Li S, Hartman GL, Widholm JM (2004) Biochemical response of soybean roots to f. sp. Infection. Crop Sci 44:819–826

    CAS  Google Scholar 

  • Macagnan D, Romeiro RS, Pomella AWV, deSouza JT (2008) Production of lytic enzymes and siderophores, and inhibition of germination of basidiospores of Moniliophthora (ex Crinipellis) perniciosa by phylloplane actinomycetes. Biol Control 47:309–314

    Article  CAS  Google Scholar 

  • Majidi S, Roayaei M, Ghezelbash G (2011) Carboxymethyl cellulase and filter paperase activity of new strains isolated from Persian Gulf. Microbiol J 1:8–16

    Article  Google Scholar 

  • Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331

    Article  CAS  PubMed  Google Scholar 

  • Nazavari K, Jamali F, Bayat F, Modarresi M (2016) Evaluation of resistance to seedling damping-off caused by Phytophthora drechsleri in cucumber cultivars under greenhouse conditions. Biol Forum Int J 8:54–60

    Google Scholar 

  • Nguyen XH, Naing KW, Lee YS, Tindwa H, Lee GH, Jeong BK, Ro HM, Kim SJ, Jung WJ, Kim KY (2012) Biocontrol Potential of Streptomyces griseus H7602 against root rot disease (Phytophthora capsici) in pepper. Plant Pathol J 28:282–289

    Article  Google Scholar 

  • Palaniyandi SA, Yang SH, Suh JW (2013) Extracellular proteases from Streptomyces phaeopurpureus ExPro138 inhibit spore adhesion, germination and appressorium formation in Colletotrichum coccodes. J Appl Microbiol 115:207–217

    Article  CAS  PubMed  Google Scholar 

  • Putter J (1974) Peroxidases. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Verlag Chemie-Academic Press, New York, pp 685–690

    Chapter  Google Scholar 

  • Quecine MC, Araujo WL, Marcon J, Gai CS, Azevedo JL, Pizzirani-Kleiner AA (2008) Chitinolytic activity of endophytic Streptomyces and potential for biocontrol. Lett Appl Microbiol 47:486–491

    Article  CAS  PubMed  Google Scholar 

  • Raj SN, Sarosh BR, Shetty HS (2006) Induction and accumulation of polyphenol oxidase activities as implicated in development of resistance against pearl millet downy mildew disease. Funct Plant Biol 33:563–571

    Article  CAS  Google Scholar 

  • Rangarajan S, Saleena LM, Vasudevan P, Nair S (2003) Biological suppression of rice diseases by Pseudomonas spp. under saline soil conditions. Plant Soil 251:73–82

    Article  Google Scholar 

  • Sabaratnam S, Traquair JA (2002) Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 23:245–253

    Article  CAS  Google Scholar 

  • Sadeghi A, Soltani BM, Salehi Jouzani G, Karimi E, Khayam Nekouei M, Sadeghizadeh M (2014) Taxonomic study of a salt tolerant Streptomyces sp. strain C-2012 and the effect of salt and ectoine on lon expression level. Microbiol Res 169:232–238

    Article  CAS  PubMed  Google Scholar 

  • Salla TD, Astarita LV, Santarém ER (2016) Defense responses in plants of Eucalyptus elicited by Streptomyces and challenged with Botrytis cinerea. Planta 243:1055–1070

    Article  CAS  PubMed  Google Scholar 

  • Sang MK, Chun SC, Kim KD (2008) Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol Control 46:424–433

    Article  Google Scholar 

  • Seo DJ, Nguyen DM, Song YS, Jung WJ (2012) Induction of defense response against Rhizoctonia solani in cucumber plants by endophytic bacterium Bacillus thuringiensis GS1. J Microbiol Biotechnol 22:407–415

    Article  CAS  PubMed  Google Scholar 

  • Shih HD, Liu YC, Hsu FL, Mulabagal V, Dodda R, Huang JW (2003) Fungichromin: a substance from Streptomyces padanus with inhibitory effects on Rhizoctonia solani. J Agric Food Chem 51:95–99

    Article  CAS  PubMed  Google Scholar 

  • Shirzad A, Fallahzadeh-Mamaghani V, Pazhouhandeh M (2012) Antagonistic potential of fluorescent pseudomonads and control of crown and root rot of cucumber caused by Phythophtora drechsleri. Plant Pathol J 28:1–9

    Article  CAS  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Sonneveld C, Voogt SJ (1978) Effects of saline irrigation water on glasshouse cucumbers. Plant Soil 49:595–606

    Article  CAS  Google Scholar 

  • Spadaro D, Gullino ML (2005) Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Prot 24:601–613

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taniguchi T, Imada S, Acharya K, Iwanaga F, Yamanaka N (2015) Effect of soil salinity and nutrient levels on the community structure of the root-associated bacteria of the facultative halophyte, Tamarix ramosissima, in southwestern United States. J Gen Appl Microbiol 61:193–202

    Article  CAS  PubMed  Google Scholar 

  • Thipyapong P, Steffens JC (1997) Tomato polyphenol oxidase. Differential response of the polyphenol oxidase F promoter to injuries and wound signals. Plant Physiol 115:409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157

    Article  CAS  Google Scholar 

  • Tripathi G, Rawal SK (1998) A simple and efficient protocol for isolation of high molecular weight DNA from Streptomyces aureofaciens. Biotechnol Tech 12:629–631

    Article  CAS  Google Scholar 

  • Uppalapati SR, Marek SM, Lee HK, Nakashima J, Tang Y, Sledge MK, Dixon RA, Mysore KS (2009) Global gene expression profiling during Medicago truncatula-Phymatotrichopsis omnivora interaction reveals a role for jasmonic acid, ethylene, and the flavonoid pathway in disease development. Mol Plant Microbe Interact 22:7–17

    Article  CAS  PubMed  Google Scholar 

  • Verma VC, Singh SK, Prakash S (2011) Biocontrol and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. J Basic Microbiol 51:550–556

    Article  CAS  PubMed  Google Scholar 

  • Viaene T, Langendries S, Beirinckx S, Maes M, Goormachtig S (2016) Streptomyces as a plant’s best friend? FEMS Microbiol Ecol 92:fiw119

    Article  PubMed  Google Scholar 

  • Wan MG, Li GQ, Zhang JB, Jiang DH, Huang HC (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control 46:552–559

    Article  Google Scholar 

  • Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y, Cui H (2013) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341:45–51

    Article  CAS  PubMed  Google Scholar 

  • Weselowski B, Nathoo N, Eastman AW, MacDonald J, Yuan ZC (2016) Isolation, identification and characterization of Paenibacillus polymyxa CR1 with potentials for biopesticide, biofertilization, biomass degradation and biofuel production. BMC Microbiol 16:244

    Article  PubMed  PubMed Central  Google Scholar 

  • Widmer TL, Guermache F (2004) Filtrates of rhizosphere bacteria suppressive to Centaurea solstitialis seed germination. J Plant Dis Protect 19:497–502

    Google Scholar 

  • Xiao K, Kinkel LL, Samac DA (2002) Biological control of Phytophthora root rot on alfalfa and soybean with Streptomyces. Biol Control 23:285–295

    Article  CAS  Google Scholar 

  • Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 62:5607–5621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang MM, Xu LP, Xue QY, Yang JH, Xu Q, Liu HX, Guo JH (2012) Screening potential bacterial biocontrol agents towards Phytophthora capsici in pepper. Eur J Plant Pathol 134:811–820

    Article  CAS  Google Scholar 

  • Yekkour A, Sabaou N, Zitouni A, Errakhi R, Mathieu F, Lebrihi A (2012) Characterization and antagonistic properties of Streptomyces strains isolated from Saharan soils and evaluation of their ability to control seedling blight of barley caused by Fusarium culmorum. Lett Appl Microbiol 55:427–435

    Article  CAS  PubMed  Google Scholar 

  • Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and Seed rots. Appl Environ Microbiol 61:3119–3128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zarafeta D, Kissas D, Saye C, Gudbergsdottir SR, Ladoukakis E, Isupov MN, Chatziioannou A, Peng X, Littlechild JA, Skretas G, Kolisis FN (2016) Discovery and characterization of a thermostable and highly halotolerant GH5 cellulase from an icelandic hot spring isolate. PLoS ONE 11(1):e0146454

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao S, Du CM, Tian CY (2012) Suppression of Fusarium oxysporum and induced resistance of plants involved in the biocontrol of cucumber Fusarium wilt by Streptomyces bikiniensis HD-087. World J Microbiol Biotechnol 28:2919–2927

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to the Agricultural Biotechnology Research Institute of Iran (ABRII), for financial support of this Project (Project No:01-05-05-9454).

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  1. Agricultural Biotechnology Research Institute of Iran, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

    Akram Sadeghi, Parisa Koobaz, Ebrahim Karimi & Ali Reza Akbari

  2. Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

    Hossein Azimi

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  1. Akram Sadeghi
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  2. Parisa Koobaz
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  3. Hossein Azimi
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Correspondence to Akram Sadeghi.

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Sadeghi, A., Koobaz, P., Azimi, H. et al. Plant growth promotion and suppression of Phytophthora drechsleri damping-off in cucumber by cellulase-producing Streptomyces . BioControl 62, 805–819 (2017). https://doi.org/10.1007/s10526-017-9838-4

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