Effect of the endophytic plant growth promoting Enterobacter ludwigii EB4B on tomato growth

M.E.A. Bendaha 1 , 2  and H.A. Belaouni 3
  • 1 Department of biology, Faculty of Nature and Life Sciences, University Mustapha Stambouli of Mascara, Mascara, Algeria
  • 2 Laboratoire de Biologie Moléculaire, Génomique et Bioinformatique (LBMGB), University Hassiba Ben Bouali of Chlef, Algeria
  • 3 Laboratoire de Biologie des Systèmes Microbiens (LBSM), , Algiers, Algeria

Summary

This study aims to develop a biocontrol agent against Fusarium oxysporum f.sp. radicis-lycopersici (FORL) in tomato. For this, a set of 23 bacterial endophytic isolates has been screened for their ability to inhibit in vitro the growth of FORL using the dual plate assay. Three isolates with the most sound antagonistic activity to FORL have been qualitatively screened for siderophore production, phosphates solubilization and indolic acetic acid (IAA) synthesis as growth promotion traits. Antagonistic values of the three candidates against FORL were respectively: 51.51 % (EB4B), 51.18 % (EB22K) and 41.40 % (EB2A). Based on 16S rRNA gene sequence analysis, the isolates EB4B and EB22K were closely related to Enterobacter ludwigii EN-119, while the strain EB2A has been assigned to Leclercia adecarboxylata NBRC 102595. The promotion of tomato growth has been assessed in vitro using the strains EB2A, EB4B and EB22K in presence of the phytopathogen FORL. The treatments with the selected isolates increased significantly the root length and dry weight. Best results were observed in isolate EB4B in terms of growth promotion in the absence of FORL, improving 326.60 % of the root length and 142.70 % of plant dry weight if compared with untreated controls. In the presence of FORL, the strain EB4B improved both root length (180.81 %) and plant dry weight (202.15 %). These results encourage further characterization of the observed beneficial effect of Enterobacter sp. EB4B for a possible use as biofertilizer and biocontrol agent against FORL.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Adesemoye, A.O., Torbert, H.A. and Kloepper, J.W. 2009. Plant growth promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microbial Ecology, 58: 921–929.

  • Ahemad, F., Ahmad, I. and Khan, M.S. 2008. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiological Research, 163: 173–181.

  • Bashan, Y., Holguin, G. and Lifshitz, R. 1993. Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick B.R. and Thompson, J.E. (eds). Methods in plant molecular biology and biotechnology. Boca Raton: CRC, p. 331–345.

  • Bloemberg, G.V. and Lugtenberg, B.J.J. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Current Opinion in Plant Biology, 4: 343-350.

  • Bric, J.M., Bosrock, R.M. and Silversone, S.E. 1991. Rapid in situ assay for indole acetic acid production by bacteria immobilization on a nitrocellu-lose membrane. Applied and Enviromental Microbiology, 57: 535–538.

  • Chauhan, H., Bagyaraj, D.J., Selvakumar, G. and Sundaram, S.P. 2015. Novel plant growth promoting rhizobacteria - Prospects and potential. Applied Soil Ecology, 95: 38–53.

  • Dekkers, L.C., Phoelich, C.C., Fits, L.V. and Lugtenberg, B.J. 1997. A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. Microbiology, 7051–7056.

  • Dey, R., Pal, K.K., Bhatt, D.M. and Chauhan, S.M. 2004. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiological Research, 159: 371–394.

  • Dias, M.P., Bastos, M.S., Xavier, V.B., Cassel, E., Astarita, L.V. and Santarém, E.R. 2017. Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiology and Biochemistry, 118: 479–493.

  • Dutta, J. and Thakur, D. 2017. Evaluation of multi-farious plant growth promoting traits, antagonistic potential and phylogenetic affiliation of rhizobacteria associated with commercial tea plants grown in Darjeeling, India. PLOS ONE, 12(8): e0182302.

  • Costacurta, A., Mazzafera, P. and Rosato, Y.B. 2006. Indole-3-acetic acid biosynthesis by Xanthomonas axonopodis pv. citri is increased in the presence of plant leaf extracts. Microbiology Letters, 159: 215–220.

  • El Aoufir, A. 2001. Étude du Flétrissement Vasculaire du Pois Chiche (Cicer arietinum) Causé par le Fusarium oxysporum f. sp. ciceri. Evaluation de la Fiabilité de L’analyse Isoenzymatique et de la Compatibilité Végétative pour la Caractérisation des Races Physiologiques, Canada: University of Laval, PhD Theses.

  • Evans, H. C., Holmes, K. A. and Thomas, S.E. 2003. Endophytes and mycoparasites associated with an indigenous forest tree, the obromagileri, in Ecuador and preliminary assessment of their potentiel as biocontrol agents of cocoa diseases. Mycological Progress, 2: 149–160.

  • Fallahzadeh-Mamaghani, V., Ahmadzadeh, M. and Sharifi, R. 2009. Screening systemic resistance inducing fluorescent pseudomonads for control of bacterial blight of cotton caused by Xanthomonas campestris pv. malvacearum. Journal of Plant Pathology, 663–670.

  • Forchetti, G., Masciarelli, O., Izaguirre, M.J., Alemano, S., Alvarez, D. and Abdala, G. 2010. endophytic bacteria improve seedling growth of sunflower under water stress, produce salicylic acid, and inhibit growth of pathogenic fungi. Current Microbiology, 61(6): 485–493.

  • Gopalakrishnan, S., Upadhyaya, H.D., Vadlamudi, S., Humayun, P., Vidya, M.S., Alekhya, G., Singh, A., Vijayabharathi, R., Bhimineni, R.K., Seema, M., Rathore, A. and Rupela, O. 2012. Plant growth-promoting traits of biocontrol potential bacteria isolated from rice rhizosphere. Springer Plus, 1: 71.

  • Grobelak, A., Napora, A. and Kacprzak, M. 2015. Using plant growth-promoting rhizobacteria (PGPR) to improve plant growth. Ecological Engineering, 84: 22–28.

  • Gupta, M., Kiran, S., Gulatic, A., Singh, B. and Tewari, R. 2012. Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiological Research, 167: 358–363.

  • Haas, D. and Défago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3: 307–319.

  • Heidari, M. and Golpayegani, A. 2012. Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). Journal of the Saudi Society of Agricultural Sciences, 11: 57–61.

  • Husen, E. 2003. Screening of soil bacteria for plant growth promotion activities in vitro. Indian Journal of Agricultural Sciences, 4: 27–31.

  • Ji, S.H., Gururani, M.A. and Chun, S.C. 2014. Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiological Research, 169(1): 83–98.

  • Johansson, P.M., Johnsson, L. and Gerhardson B. 2003. Suppression of wheat-seedling diseases caused by Fusarium culmorum and Microdochium nivale using bacterial seed treatment. Plant Pathology, 52: 219–227.

  • Kadir, J., Rahman, M., Mahmud, T., Rahman, R.A., and Begum, M. 2008. Extraction of antifungal substances from Burkholderia cepacia with antibiotic activity against Colletotrichum gloeosporioides on papaya (Carica papaya L.). International Journal of Agriculture and Biology, 15–20.

  • Kapoor, R., Gupta, M.K., Naveen, K. and Kanwar, S.S. 2017. Analysis of nhaA gene from salt tolerant and plant growth promoting Enterobacter ludwigii. Rhizosphere, 4: 62–69.

  • Karlidag, H., Yildirim, E., Turan, M., Pehluvan, M. and Donmez, F. 2013. Plant growth promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria × ananassa). Horticultural Science, 48(5): 563–567.

  • Khan, A.L., Waqas, M., Kang, S-M., Al-Harrasi, A., Hussain, J., Al-Rawahi, A., Al-Khiziri, S., Ullah, I., Ali, L., Jung, H-Y. and Lee, I.J. 2014. Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. Journal of Microbiology, 52(8): 689–695.

  • Kisiel, A. and Kepczynska, E. 2016. Medicago truncatula Gaertn. as a model for understanding the mechanism of growth promotion by bacteria from rhizosphere and nodules of alfalfa. Planta, 243: 1169–1189.

  • Kokalis-Burelle, N., Vavrina, C.S., Rossskopf, E.N. and Shelby, R.A. 2002. Field evaluation of plant growth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant and Soil, 238: 257–266.

  • Landa, B., Navas-Cortés, J., Hervás, A. and Jiménez-Díaz, R. 2001. Influence of Temperature and Inoculum Density of Fusarium oxysporum f.sp. ciceris on Suppression of Fusarium Wilt of Chick-pea by Rhizosphere Bacteria. The American Phytopathological Society, 91(8): 807–16.

  • Lemanceau, P., Expert, D., Gaymard, F., Bakker, P.A.H.M. and Briat, J.F. 2009. Role of iron in plant–microbe interactions. Advances in Botanical Research, 51: 491–549.

  • Lemanceau, P. and Alabouvette, C. 1991. Biological control of fusarium diseases by fluorescent Pseudomonas and non pathogenic Fusarum. Crop Protection, 10: 279–286.

  • Lee, S., Ahn, I., Sim, S., Lee, S., Seo, M. and Kim, S. 2010. Pseudomonas sp. LSW25R, antagonistic to plant pathogens, promoted plant growth, and reduced blossom-end rot of tomato fruits in a hydroponic system. European Journal of Plant Pathology, 1–11.

  • Liu, C., Wang, Y., Jin, Y., Pan, K., Zhou, X. and Li, N. 2017. Photoprotection regulated by phosphorus application can improve photosynthetic performance and alleviate oxidative damage in dwarf bamboo subjected to water stress. Plant Physiology and Biochemistry, 118: 88–97.

  • Loaces, I., Ferrando, L. and Scavino, A.F. 2011. Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microbial Ecology, 61: 606–618.

  • Ma, Y., Prasad, M.N.V., Rajkumar, M. and Freitas, H. 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances, 29: 48–58.

  • Madhaiyan, M., Poonguzhali, S., Lee, J.S., Senthil-kumar, M., Lee, K.C. and Sundaram, S. 2010. Mucilaginibacter gossypii sp. nov. and Mucilaginibacter gossypiicola sp. nov., plant-growth-promoting bacteria isolated from cotton rhizo-sphere soils. International Journal of Systematic and Evolutionary Microbiology, 60: 2451–2457.

  • Martinez-Viveros, O., Jourquera, M.A., Crowley, D.E., Gajardo, G. and Mora, M.L. 2010. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. Journal of Soil Science and Plant Nutrition, 10: 293–319.

  • Melo, J., Carolino, M., Carvalho, L., Correia, P., Tenreiro, R., Chaves, S., Meleiro, A I., de Souza, S B., Dias, T., Cruz, C. and Ramos, A.C. 2016. Crop management as a driving force of plant growth promoting rhizobacteria physiology. Springer Plus, 5: 1574.

  • Mendes, R., Garbeva, P. and Raaijmakers, J.M. 2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37(5): 634–663.

  • Nadeem, S.M., Ahmad, M, Zahir, Z.A., Javaid, A. and Ashraf, M. 2013. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Advances, 32(2): 429–48.

  • Naveed, M., Iftikhar, A., Nauman, K. and Mumtaz, A.S. 2014. Bioinformatics based structural characterization of glucose dehydrogenase (gdh) gene and growth promoting activity of Leclercia sp. QAU-66. Brazilian Journal of Microbiology, 45(2): 603–611.

  • Kloepper, J.W., Lifshitz, R. and Zablotwicz, R.M. 1989. Free-living bacterial inocula for enhancing crop productivity. Trends In Biotechnoly, 7: 39–43.

  • Piccoli, P. and Bottini, R. 2013. Abiotic Stress Tolerance Induced by Endophytic PGPR. In: Aroca R. (eds) Symbiotic Endop. Soil Biology, vol 37hytes. Springer, Berlin, Heidelberg.

  • Pikovskaya, R. 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya, 17, 362-370.

  • Piromyou, P., Buranabanyat, B., Tantasawat, P., Tittabutr, P., Boonkerd, N. and Neung, T. 2011. Effect of plant growth promoting rhizobacteria (PGPR) inoculation on microbial community structure in rhizosphere of forage corn cultivated in Thailand. European Journal of Soil Biology, 47: 44–54.

  • Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V. and Samiyappan, R. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protection, 20: 1–11.

  • Ryan, R.P., Germaine, K., Franks, A., Ryan, D.J. and Dowling, D.N. 2008. Bacterial endophytes: recent developments and applications. FEMS Microbiology Letters, 278(1): 1–9.

  • Reddy, P.P. 2013. Recent advances in crop protection. New Delhi: Springer, p. 131–158.

  • Rubini, M.R., Silva-Ribeiro, R.T., Pomella, A.W.V., Maki, C.S., Araujo, W.L., Santos, D.R. and Azevedo, J.L. 2005. Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of witches broom disease. International Journal of Biological Sciences,1: 24–33.

  • Santos-Villalobos, S., Barrera-Galicia, G.C., Miranda-Salcedo, M.A. and Peña-Cabriales, J.J. 2012. Burkholderia cepacia XXVI siderophore with biocontrol capacity against Colletotrichum gloeosporioides. World Journal of Microbiology and Biotechnology, 28: 2615–2623.

  • Sasirekha, B. and Shivakumar, S. 2016. Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agriculture and Natural Resources, 50(4): 250–256.

  • Schmidt, C.S., Agostini, F., Leifert, C., Killham, K. and Mullins, C.E. 2004. Influence of soil tempereature and matric potential on sugar beet seed-limg colonization and suupression of Pythium damping-of by the antagonistic bacteria Pseudomonas fluorescens and Bacillius subtilis. Phytopathology, 94: 351–363.

  • Schwyn, B. and Neilands, J.B. 1987. Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160: 47–56.

  • Shoebitz, M., Ribaudo, C.M., Pardo, M.A., Cantore, M.L. and Curá, J.A. 2009. Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perennerhizosphere. Soil Biology and Biochemistry, 415(9): 1768–1774.

  • Szepesi, A., Csiszar, J., Genus, K., Horvath, E., Horvath, F., Simon, M.I. and Tari, I. 2009. Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and absiscic acid accumulation and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology, 166: 914–925.

  • Tyler, H.L. and Triplett, E.W. 2008. Plants as a habitat for beneficial and/or human pathogenic bacteria. The Annual Review of Phytopathology, 46: 53–73.

  • Van Loon, L.C. 2007. Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology, 119: 243–254.

  • Van Veen, J.A., Van Overbeek, L.S. and Van Elsas, J.D. 1997. Fate and activity of microorganisms introduced into soil. Microbiology and Molecular Biology Reviews, 61: 121–135.

  • Venkat, K.S., Menon, S., Agarwal, H. and Gopalakrishnan, D. 2017. Characterization and optimization of bacterium isolated from soil samples for the production of siderophores. Resource-Efficient Technologies, 1–6.

  • Vessey, K.J. 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil, 255: 571–586.

  • Vos, C.M., Yang, Y., De Coninck, B. and Cammue B.P.A. 2014. Fungal (-like) biocontrol organisms in tomato disease control. Biological control, 74: 65–81.

  • Weller, D.M., Landa, B.B., Mavrodi, O.V., Schroeder, K.L., de la Fuente, L., Blouin-Bankhead, S.B., Allende-Molar, R., Bonsall, R.F., Mavrodi, D.V. and Thomashow, L.S. 2007. Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biology, 9: 4–20.

  • Weller, D.M., Raaijmakers, J.M., McSpadden Gardener, B.B. and Thomashaw, L.S. 2002. Microbial populations responsible for specific soil suppressiveness plant pathogens. Annual Review of Phytopathology, 40: 309–348.

  • Whipps, J.M. 2001. Microbial interactions and bio-control in the rhizosphere. Journal of Experimental Botany, 52: 487–511.

OPEN ACCESS

Journal + Issues

Search