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European Journal of Plant Pathology

, Volume 136, Issue 2, pp 337–353 | Cite as

Cyanobacteria mediated plant growth promotion and bioprotection against Fusarium wilt in tomato

  • Radha Prasanna
  • Vidhi Chaudhary
  • Vishal Gupta
  • Santosh Babu
  • Arun Kumar
  • Rajendra Singh
  • Yashbir Singh Shivay
  • Lata Nain
Original Research

Abstract

Cyanobacteria - phytopathogenic fungi - tomato plant interactions were evaluated for developing suitable biological options for combating biotic stress (Fusarium wilt) and enhancing plant vigour. Preliminary evaluation was undertaken on the fungicidal and hydrolytic enzyme activity of the cyanobacterial strains (Anabaena variabilis RPAN59, A. laxa RPAN8) under optimized environmental/nutritional conditions, followed by amendment in compost-vermiculite. Such formulations were tested against Fusarium wilt challenged tomato plants, and the Anabaena spp. (RPAN59/8) amended composts significantly reduced mortality in fungi challenged treatments, besides fungal load in soil. Cyanobacteria amended composts also led to an enhancement in soil organic C, nitrogen fixation, besides significant improvement in growth, yield, fruit quality parameters, N, P and Zn content. The tripartite interactions also enhanced the activity of defence and pathogenesis related enzymes in tomato plants. A positive correlation (r = 0.729 to 0.828) between P content and pathogenesis/defense enzyme activity revealed their role in enhancing the resistance of the plant through improved nutrient uptake. Light and scanning electron microscopy (SEM) revealed cyanobacterial colonization, which positively correlated with reduced fungal populations. The reduced disease severity coupled with improved plant growth/ yields, elicited by cyanobacterial treatments, illustrated the utility of such novel formulations in integrated pest and nutrient management strategies for Fusarium wilt challenged tomato crop.

Keywords

Defense enzymes Disease severity Fungicidal Hydrolytic enzymes Scanning electron microscopy Compost-vermiculite formulations 

Notes

Acknowledgments

This study was supported by the Indian Council of Agricultural Research (ICAR)-AMAAS Network Project on Microorganisms, New Delhi, India. We are grateful to the authorities of the Division of Microbiology, IARI, New Delhi, for providing facilities for this study. We also thank Dr. V.V. Ramamurthy and the project staff of the Network Project on Insect Biosystematics in the Division of Entomology, IARI, for assistance in the scanning electron microscopy analyses.

Supplementary material

10658_2013_167_Fig6_ESM.jpg (84 kb)
Supplementary Fig. 1

(a) Experimental set up for evaluating the formulations in tomato crop (b) Effect of cyanobacteria untreated/treated seedlings on leaf morphology of tomato seedlings (JPEG 83 kb)

10658_2013_167_MOESM1_ESM.tif (999 kb)
High resolution image (TIFF 998 kb)
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Supplementary Fig. 2

Effect of different treatments on growth of tomato plants (left-right) fungi challenged control treatment and RPAN50amended compost treated plants (JPEG 1967 kb)

10658_2013_167_MOESM2_ESM.tif (18.2 mb)
High resolution image (TIFF 18610 kb)
10658_2013_167_Fig8_ESM.jpg (101 kb)
Supplementary Fig. 3

Effect of different treatments on number of fruits per plant. The treatments include RPAN8C-T1; RPAN8O-T2; RPAN59C-T3; RPAN59O-T4; RPAN16C-T5; Bacillus subtilis-T6; Chemical (Thiram + Carbendazim)-T7; Trichoderma sp.-T8; Control-T9 (JPEG 100 kb)

10658_2013_167_MOESM3_ESM.eps (115 kb)
High resolution image (EPS 115 kb)
10658_2013_167_MOESM4_ESM.doc (104 kb)
ESM 4 (DOC 104 kb)

References

  1. Adesemoye, A., Torbert, H., & Kloepper, J. (2009). Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microbial Ecology, 58, 921–929.PubMedCrossRefGoogle Scholar
  2. Ahmed, M., Stal, L. J., & Hasnain, S. (2011). DTAF: an efficient probe to study cyanobacterial-plant interaction using confocal laser scanning microscopy (CLSM). Journal of Industrial Microbiology and Biotechnology, 38, 249–255.PubMedCrossRefGoogle Scholar
  3. Benhamou, N., Belanger, R. R., & Paulitz, T. C. (1996). Induction of differential host responses by Pseudomonas fluorescens in Ri T-DNA-transformed pea roots after challenged with Fusarium oxysporum f. sp. pisi and Pythium ultimum. Phytopathology, 86, 114–118.Google Scholar
  4. Bozzola, J. J. & Russell, L. D. (1998). Electron microscopy: Principles and techniques for biologists. Jones and Bartlett Publishers.Google Scholar
  5. Bramhall, R. A., & Higgins, V. J. (1988). The effect of glyphosate on resistance of tomato to Fusarium crown and root rot disease and on the formation of host structural defensive barriers. Canadian Journal of Botany, 66, 1547–1555.CrossRefGoogle Scholar
  6. Chaudhary, V., Prasanna, R., & Bhatnagar, A. K. (2012a). Modulation of fungicidal potential of Anabaena strains by light and temperature. Folia Microbiologica, 57, 199–208.PubMedCrossRefGoogle Scholar
  7. Chaudhary, V., Prasanna, R., & Bhatnagar, A. K. (2012b). Influence of phosphorus and pH on the fungicidal potential of Anabaena strains. Journal of Basic Microbiology. doi: 10.1002/jobm.201100520. Published online: 26 June 2012.
  8. Chen, C., Belanger, R. R., Benhamaou, N., & Paulitz, T. (2000). Defense enzymes induced in cucumber roots by treatment with plant growth promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiological and Molecular Plant Pathology, 56, 13–23.CrossRefGoogle Scholar
  9. Christopher, D. J., Raj, T. S., Rani, S. U., & Udhayakumar, R. (2010). Role of defense enzymes activity in tomato as induced by Trichoderma virence against Fusarium wilt caused by Fusarium oxysporum f sp. lycopersici. Journal of Biopesticides, 3, 158–162.Google Scholar
  10. Commonwealth Agricultural Bureaux. (1968). Plant pathologist’s pocketbook (p. 239). Kew: Commonwealth Mycological Institute.Google Scholar
  11. Compant, S., Duffy, B., Nowak, J., Clement, C., & Barka, E. A. (2005). Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology, 71, 4951–4959.PubMedCrossRefGoogle Scholar
  12. Dukare, A. S. (2010). Evaluation of disease suppressiveness of microbe amended compost(s) against soil borne pathogens of tomato. M. Sc. thesis, Division of Microbiology, Indian Agricultural Research Institute, New Delhi, India.Google Scholar
  13. Dukare, A. S., Prasanna, R., Dubey, S. C., Nain, L., Chaudhary, V., Singh, R., & Saxena, A. K. (2011). Evaluating novel microbe amended composts as biocontrol agents in tomato. Crop Protection, 30, 436–442.CrossRefGoogle Scholar
  14. Fish, W. W., Perkins-Veazie, P., & Collins, J. K. (2002). A quantitative assay for lycopene that utilizes reduced volumes of organic solvents. Journal of Food and Computational Analysis, 15, 309–317.CrossRefGoogle Scholar
  15. Fridlender, M., Inbar, J., & Chet, I. (1993). Biological control of soil borne plant pathogens by a β-1, 3 glucanase producing Pseudomonas cepacia. Soil Biology and Biochemistry, 25, 1211–1221.CrossRefGoogle Scholar
  16. Ghosh, T. K., Bailey, H. J., Bisaria, V. S., & Enari, T. M. (1983). Measurement of cellulase activities. Final recommendations, Commission of Biotechnology. International Union of Pure and Applied Chemistry, 59, 1–13.Google Scholar
  17. Gohel, V., Singh, A., Vimal, M., Ashwini, P., & Chhatpar, H. S. (2006). Bioprospecting and antifungal potential of chitinolytic microorganism. African Journal of Biotechnology, 5, 54–72.Google Scholar
  18. Gotz, M., Gomes, N. C. M., Dratwinski, A., Costa, R., Berg, G., Peixoto, M. H. L., & Smalla, K. (2006). Survival of gfp-tagged antagonistic bacteria in the rhizosphere of tomato plants and their effects on the indigenous bacterial community. FEMS Microbiology Ecology, 56, 207–218.PubMedCrossRefGoogle Scholar
  19. Gupta, V., Prasanna, R., Natarajan, C., Srivastava, A. K., & Sharma, J. (2010). Identification, characterization and regulation of a novel antifungal chitosanase gene (cho) in Anabaena sp. Applied and Environmental Microbiology, 76, 2769–2777.PubMedCrossRefGoogle Scholar
  20. Gupta, V., Natarajan, C., Kumar, K., & Prasanna, R. (2011). Identification and characterization of endoglucanases for fungicidal activity in Anabaena laxa. Journal of Applied Phycology, 23, 73–81.CrossRefGoogle Scholar
  21. Hariprasad, P., Divakara, S. T., & Niranjana, S. R. (2011). Isolation and characterization of chitinolytic rhizobacteria for the management of Fusarium wilt in tomato. Crop Protection, 30, 1606–1612.CrossRefGoogle Scholar
  22. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species- opportunistic, avirulent plant symbionts. Nature Reviews, 2, 43–56.PubMedCrossRefGoogle Scholar
  23. Heil, M., & Bostock, R. M. (2002). Induced Systemic Resistance (ISR) against pathogens in the context of induced plant defences. Annals of Botany, 89, 503–512.PubMedCrossRefGoogle Scholar
  24. Hesse, P. R. (1971). A textbook of soil chemical analysis. London, England: John Murray.Google Scholar
  25. Hofte, M., & Altier, N. (2010). Fluorescent pseudomonads as biocontrol agents for sustainable agricultural systems. Research in Microbiology, 161, 464–471.PubMedCrossRefGoogle Scholar
  26. Hoitink, H. A. J., & Fahy, P. C. (1986). Basis for the control of soilborne plant pathogens with composts. Annual Review of Phytopathology, 24, 93–114.CrossRefGoogle Scholar
  27. Jaiswal, P., Prasanna, R., Nayak, S., Sood, A., & Suseela, M. R. (2008). Characterization of rhizo-cyanobacteria and their associations with wheat seedlings. Egyptian Journal of Biology, 10, 20–27.Google Scholar
  28. Jetiyanon, K., & Kloepper, J. W. (2002). Mixtures of plant growth promoting bacteria for induction of systemic resistance against multiple plant diseases. Biological Control, 24, 285–291.CrossRefGoogle Scholar
  29. Karthikeyan, N., Prasanna, R., Lata, & Kaushik, B. D. (2007). Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. European Journal of Soil Biology, 43, 23–30.CrossRefGoogle Scholar
  30. Karthikeyan, N., Prasanna, R., Sood, A., Jaiswal, P., Nayak, S., & Kaushik, B. D. (2009). Physiological characterization and electron microscopic investigations of cyanobacteria associated with wheat rhizosphere. Folia Microbiologica, 54, 43–51.PubMedCrossRefGoogle Scholar
  31. Kaushik, B. D. (1987). Laboratory methods for Blue-Green algae (p. 171). New Delhi: Assoc. Publ. Co.Google Scholar
  32. Kavitha, R., & Umesha, S. (2008). Regulation of defense-related enzymes associated with bacterial spot resistance in tomato. Phytoparasitica, 36, 144–159.CrossRefGoogle Scholar
  33. Kerkeni, A., Daami-Remadi, M., Tarchoun, N., & Khedher, M. B. (2007). In vitro and in vivo suppression of Fusarium oxysporum f. sp. radicis-lycopersici the causal agent of Fusarium crown and root rot of tomato by some compost fungi. International Journal of Agricultural Research, 2, 1022–1029.CrossRefGoogle Scholar
  34. Kessmann, H., Staub, T., Hofmann, C., Maetzke, T., Herzog, J., Ward, E., Uknes, S., & Ryals, J. (1994). lnduction of systemic acquired resistance in plants by chemicals. Annual Reviews of Phytopathology, 32, 439–459.CrossRefGoogle Scholar
  35. Kloepper, J. W., Schippers, B., & Bakker, P. A. H. M. (1992). Proposed elimination of the term endorhizosphere. Phytopathology, 82, 726–727.Google Scholar
  36. Kucey, R. M. N., Janzen, H. H., & Leggett, M. E. (1989). Microbially mediated increases in plant-available phosphorus. Advances in Agronomy, 42, 199–228.CrossRefGoogle Scholar
  37. Kulik, M. M. (1995). The potential for using cyanobacteria (blue green algae) and algae in the biological control of plant pathogenic bacteria and fungi. European Journal of Plant Pathology, 101, 585–599.CrossRefGoogle Scholar
  38. Ling, N., Huang, Q., Guo, S., & Shen, Q. (2011). Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f. sp. niveum. Plant and Soil, 341, 485–493.CrossRefGoogle Scholar
  39. MacKinney, G. (1941). Absorption of light by chlorophyll solutions. Journal of Biology and Chemistry, 140, 315–322.Google Scholar
  40. Mader, P., Kaiser, F., Adholeya, A., Singh, R., Uppal, H. S., Sharma, A. K., Srivastava, R., Sahai, V., Aragno, M., Wiemken, A., Johri, B. N., & Fried, P. M. (2011). Inoculation of root microorganisms for sustainable wheat rice and wheat black gram rotations in India. Soil Biology and Biochemistry, 43, 609–619.CrossRefGoogle Scholar
  41. Mandal, B., Vlek, P. L. G. & Mandal, L. N. (1999). Beneficial effects of blue-green algae and Azolla, excluding supplying nitrogen, on wetland rice fields: a review. Biology and Fertility of Soils, 28, 329–342Google Scholar
  42. Manjunath, M., Prasanna, R., Nain, L., Dureja, P., Singh, R., Kumar, A., Jaggi, S., & Kaushik, B. D. (2010). Biocontrol potential of cyanobacterial metabolites against damping off disease caused by Pythium aphanidermatum in solanaceous vegetables. Archives of Phytopathology and Plant Protection, 43, 666–677.CrossRefGoogle Scholar
  43. Nain, L., Rana, A., Joshi, M., Jadhav, S. D., Kumar, D., Shivay, Y. S., Paul, S., & Prasanna, R. (2010). Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat. Plant and Soil, 331, 217–230.CrossRefGoogle Scholar
  44. Nannipieri, P., Ascher, J., Ceccherini, M. T., Landi, L., Pietramellara, G., & Renella, G. (2003). Microbial diversity and soil functions. European Journal of Soil Science, 54, 655–670.CrossRefGoogle Scholar
  45. Natarajan, C., Prasanna, R., Gupta, V., Dureja, P., & Lata. (2012). Dissecting the fungicidal activity of Calothrix elenkinii using chemical analyses and microscopy. Applied Biochemistry and Microbiology, 48, 53–57.CrossRefGoogle Scholar
  46. Nayak, S., Prasanna, R., Pabby, A., Dominic, T. K., & Singh, P. K. (2004). Effect of urea and BGA- Azolla biofertilizers on nitrogen and chlorophyll accumulation in soil cores from rice fields. Biology and Fertility of Soils, 40, 67–72.CrossRefGoogle Scholar
  47. Ohtakara, A. (1988). Chitosanase and β-N-acetyl hexosamine from Pycnosporus cinnabarinus. Methods in Enzymology, 168, 464–468.Google Scholar
  48. Osman, M. E. H., El-Sheekh, M. M., El-Naggar, A. H., & Gheda, S. F. (2010). Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant. Biology and Fertility of Soils, 46, 861–875.CrossRefGoogle Scholar
  49. Pandey, V. N., & Dubey, N. K. (1994). Antifungal potential of leaves and essential oils from higher plants against soil phytopathogens. Soil Biology and Biochemistry, 26, 1417–1421.CrossRefGoogle Scholar
  50. Paulitz, T. C., & Schroeder, K. L. (2005). A new method for the quantification of Rhizoctonia solani and Rhizoctonia oryzae from soil. Plant Disease, 89, 767–772.CrossRefGoogle Scholar
  51. Pozo, M. J., Azcon-Aguilar, C., Dumas-Gaudot, E., & Barea, J. M. (1999). β-1, 3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Science, 141, 149–157.CrossRefGoogle Scholar
  52. Prasad, R., Shivay, Y. S., Kumar, D., & Sharma, S. N. (2006). Learning by doing exercises in soil fertility (a practical manual for soil fertility) (p. 68). New Delhi: Division of Agronomy, Indian Agricultural Research Institute.Google Scholar
  53. Prasanna, R., Tripathi, U., Dominic, T. K., Singh, A. K., Yadav, A. K., & Singh, P. K. (2003). An improvised technique for measurement of nitrogen fixation by blue-green algae and Azolla using intact soil cores. Experimental Agriculture, 39, 145–150.CrossRefGoogle Scholar
  54. Prasanna, R., Jaiswal, P., Singh, Y. V., & Singh, P. K. (2008a). Influence of biofertilizers and organic amendments on nitrogenase activity and phototrophic biomass of soil under wheat. Acta Agronomica Hungarica, 56, 149–159.CrossRefGoogle Scholar
  55. Prasanna, R., Lata, Tripathi, R., Gupta, V., Middha, S., Joshi, M., Ancha, R., & Kaushik, B. D. (2008b). Evaluation of fungicidal activity of extracellular filtrates of cyanobacteria - possible role of hydrolytic enzymes. Journal of Basic Microbiology, 48, 186–194.PubMedCrossRefGoogle Scholar
  56. Prasanna, R., Jaiswal, P., Nayak, S., Sood, A., & Kaushik, B. D. (2009a). Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Industrial Journal of Microbiology, 49, 89–97.CrossRefGoogle Scholar
  57. Prasanna, R., Nain, L., Ancha, R., Shrikrishna, J., Joshi, M., & Kaushik, B. D. (2009b). Rhizosphere dynamics of inoculated cyanobacteria and their growth-promoting role in rice crop. Egyptian Journal of Biology, 11, 26–36.Google Scholar
  58. Prasanna, R., Gupta, V., Natarajan, C., & Chaudhary, V. (2010a). Allele mining for chitosanases and microcystin-like compounds in Anabaena strains. World Journal of Microbiology and Biotechnology, 26, 717–724.CrossRefGoogle Scholar
  59. Prasanna, R., Sood, A., Jaiswal, P., Nayak, S., Gupta, V., Chaudhary, V., Joshi, M., & Natarajan, C. (2010b). Rediscovering cyanobacteria as valuable sources of bioactive compounds. Applied Biochemistry and Microbiology, 46, 133–147.CrossRefGoogle Scholar
  60. Prasanna, R., Singh, R. N., Joshi, M., Madhan, K., Pal, R. K., & Lata. (2011). Monitoring the biofertilizing potential and establishment of inoculated cyanobacteria in soil using physiological and molecular markers. Journal of Applied Phycology, 23, 301–308.CrossRefGoogle Scholar
  61. Prasanna, R., Joshi, M., Rana, A., Shivay, Y. S., & Nain, L. (2012). Influence of co-inoculation of bacteria- cyanobacteria on crop yield and C- N sequestration in soil under rice crop. World Journal of Microbiology and Biotechnology (Online First™, 31 October 2011).Google Scholar
  62. Radhakrishnan, B., Prasanna, R., Jaiswal, P., Nayak, S., & Dureja, P. (2009). Modulation of biocidal activity of Calothrix sp. and Anabaena sp. by environmental factors. Biologia, 64, 881–889.CrossRefGoogle Scholar
  63. Rai, A. N., & Bergman, B. (2002). Creation of new nitrogen-fixing cyanobacteria associations. Proceedings of the Royal Irish Academy, 102B, 65–68. Suppl. Issue - Biology and Environment.CrossRefGoogle Scholar
  64. Ramamoorthy, V., Raguchander, T., & Samiyappan, R. (2002). Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant and Soil, 239, 55–68.CrossRefGoogle Scholar
  65. Rana, A., Joshi, M., Prasanna, R., Shivay, Y. S., & Nain, L. (2012). Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. European Journal of Soil Biology, 50, 118–126.CrossRefGoogle Scholar
  66. Rastogi, R. P., & Sinha, R. P. (2009). Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnological Advances, 27, 521–539.CrossRefGoogle Scholar
  67. Roger, P. A., Zimmerman, W. J., & Lumpkin, T. (1993). Microbiolgical management of wetland rice fields. In B. Metting (Ed.), Soil microbial ecology (pp. 417–455). New York: M. Dekker.Google Scholar
  68. Ross, W. W., & Sederoff, R. R. (1992). Phenylalanine ammonia lyase from loblolly Pine: purification of the enzyme and isolation of complementary DNA clone. Plant Physiology, 98, 380–386.CrossRefGoogle Scholar
  69. Sergeeva, E., Liaimer, A., & Bergman, B. (2002). Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta, 215, 229–238.PubMedCrossRefGoogle Scholar
  70. Stanier, R. Y., Kunisawa, R., Mandal, M., & Cohen-Bazire, G. (1971). Purification and properties of unicellular blue green algae (order: Chroococcales). Bacteriological Reviews, 35, 171–305.PubMedGoogle Scholar
  71. Tassara, C., Zaccaro, C. M., Storni, M. M., Palma, M., & Zulpa, G. (2008). Biological control of lettuce white mold with cyanobacteria. International Journal of Agriculture and Biology, 10, 487–492.Google Scholar
  72. Venkataraman, G. S. (1981). Blue green algae: a possible remedy to nitrogen scarcity. Current Science, 50, 253–256.Google Scholar
  73. Vessey, J. K. (2003). Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil, 255, 571–586.CrossRefGoogle Scholar
  74. Yu, X., Ai, C., Xin, L., & Zhou, G. (2011). The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. European Journal of Soil Biology, 47, 138–145.CrossRefGoogle Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  • Radha Prasanna
    • 1
  • Vidhi Chaudhary
    • 1
  • Vishal Gupta
    • 1
  • Santosh Babu
    • 1
  • Arun Kumar
    • 1
  • Rajendra Singh
    • 2
  • Yashbir Singh Shivay
    • 3
  • Lata Nain
    • 1
  1. 1.Division of MicrobiologyIndian Agricultural Research Institute (IARI)New DelhiIndia
  2. 2.National Phytotron FacilityIndian Agricultural Research Institute (IARI)New DelhiIndia
  3. 3.Division of AgronomyIndian Agricultural Research Institute (IARI)New DelhiIndia

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