Biocontrol of Pythium Damping-Off on Pepper (Capsicum Annuum) with Selected Fungal and Rhizobacterial Agents

Sabrine Mannai, Hayfa Jabnoun-Khiareddine, Bouzid Nasraoui, Mejda Daami-Remadi

Abstract


Pythium ultimum is common soilborne pathogen causing serious losses of pepper seedlings in nurseries and few weeks post-planting. Two pepper associated-P. ultimum isolates (P1 and P2) were shown pathogenic to pepper cv. Altar causing post-emergence damping-off with P2 isolate being the most aggressive. Fungal and bacterial antagonists have been evaluated in vitro and in vivo for their ability to suppress P. ultimum. In dual culture assay, Trichoderma harzianum, T. viride and Gliocladium virens inhibited pathogen radial growth by 18.54, 17.52 and 15.24%, respectively, relative to control, while none of the tested bacteria was shown able to significantly inhibit pathogen growth. However, drastic changes in pathogen hyphae expressed as strong lysis, formation of mycelial cords and mycoparasitism have been observed. Pepper seeds treated with fungal antagonists’ conidial suspensions showed 60, 50 and 60% less pre-emergence damping-off infections, respectively, compared to positive control. When tested as root dipping, only G. virens resulted in 40% reduced post-emergence damping-off. An improved seedlings fresh weight, by 79.31 and 76%, was respectively induced by G. virens-, and T. viride-based treatments while an increment of 27.58, 25.33 and 22.22 % was recorded following treatments with G. virens, T. viride and T. harzianum, relative to positive control. The majority of tested bacterial isolates, applied as seed treatment, had significantly improved the emergence percentage of inoculated seedlings as compared to control with Burkholderia glathei isolate 35 being the most efficient. When applied as root dipping, reduction of post-emergence damping-off ranged between 40 and 100% with Pseudomonas aureofaciens isolate 314 being the most effective agent. Seedlings treated with P. aureofaciens (314) and Bacillus pumilus (420) showed 35.38 and 28.51% higher heights, respectively. Plant weight was enhanced by 73.06, 61.18, 77.39, 61.8 and 67.93% over control following treatments with P. aureofaciens isolates 314 and 31, Bacillus pumilus 420, P. fluorescens and P. putida 227.


Keywords


Aggressiveness; biological control; disease severity; pepper; Pythium ultimum

References


Abdelzaher, H. M. A. 2003. Biological control of root rot of cauliflower (caused by Pythium ultimum var. ultimum) using selected antagonistic rhizospheric strains of Bacillus subtilis. New Zealand Journal of Crop and Horticultural Science, 31: 209-20. https://doi.org/10.1080/01140671.2003.9514255

Anonymous. 2019. GIL: Interprofessional grouping of vegetablesMinistry of Agriculture and Hydraulic Resources and Fisheries. Tunis, Tunisia.

Ayed, F., M. Daami-Remadi, H. Jabnoun-Khiareddine and M. E. Mahjoub. 2006. Potato vascular Fusarium wilt in Tunisia: Incidence and biocontrol by Trichoderma spp. Plant Pathology Journal, 5: 92-98. https://doi.org/10.3923/ppj.2006.92.98

Benhamou, N., R. R. Belanger and T. C. Paulitz. 1996. Pre-inoculation of Ri T-DNA-transformed pea roots with Pseudomonas fluorescens inhibits colonization by Pythium ultimum Trow: An ultrastructural and cytochemical study. Planta, 199: 105-17. https://doi.org/10.1007/BF00196887

Buysens, S., K. Heungens, J. Poppe and M. Hofte. 1996. Involvement of pyochelin and pyoverdin in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Applied and environmental microbiology, 62: 865-71. https://doi.org/10.1128/AEM.62.3.865-871.1996

Carisse, O., J. Bernier and N. Benhamou. 2003. Selection of biological agents from composts for control of damping-off of cucumber caused by Pythium ultimum. Canadian Journal of Plant Pathology, 25: 258-67. https://doi.org/10.1080/07060660309507078

Chen, J., G. E. Harman, A. Comis and G.-W. Cheng. 2005. Proteins related to the biocontrol of Pythium damping-off in maize with Trichoderma harzianum Rifai. Journal of Integrative Plant Biology, 47: 988-97. https://doi.org/10.1111/j.1744-7909.2005.00053.x

Daami-Remadi, M. 2001. Antagonistic activity of Trichoderma harzianum against Pythium aphanidermatum and Pythium ultimum pathogens causing potato leak. Annales de l'INRAT, 74: 167-86.

El-Katatny, M. H., H. M. A. Abdelzaher and M. A. Shoulkamy. 2006. Antagonistic actions of Pythium oligandrum and Trichoderma harzianum against phytopathogenic fungi (Fusarium oxysporum and Pythium ultimum var. ultimum). Archives Of Phytopathology And Plant Protection, 39: 289-301. https://doi.org/10.1080/03235400500222396

El-Mohamedy, R. S. R. 2012. Biological control of Pythium root rot of broccoli plants under greenhouse conditions. Journal of Agricultural Technology, 8: 1017-28.

Elad, Y., D. R. David, T. Levi, A. Kapat, B. Kirshner, E. Guvrin and A. Levine. 1999. Trichoderma harzianum T-39 mechanisms of biocontrol of foliar pathogens. In: H. Lyr, P. E. Russell, H. W. Dehne and H. D. Sisler (eds.), Modern Fungicides and Antifungal Compounds II Intercept, Andover, Hants: UK.

Ellis, R. J., T. M. Timms-Wilson, J. E. Beringer, D. Rhodes, A. Renwick, L. Stevenson and M. J. Bailey. 1999. Ecological basis for biocontrol of damping-off disease by Pseudomonas fluorescens 54/96. Journal of Applied Microbiology, 87: 454-63. https://doi.org/10.1046/j.1365-2672.1999.00851.x

Elshahawy, I. E. and R. S. El-Mohamedy. 2019. Biological control of Pythium damping-off and root-rot diseases of tomato using Trichoderma isolates employed alone or in combination. Journal of Plant Pathology, 101: 597-608. https://doi.org/10.1007/s42161-019-00248-z

Georgakopoulos, D. G., P. Fiddaman, C. Leifert and N. E. Malathrakis. 2002. Biological control of cucumber and sugar beet damping-off caused by Pythium ultimum with bacterial and fungal antagonists. Journal of Applied Microbiology, 92: 1078-86. https://doi.org/10.1046/j.1365-2672.2002.01658.x

Gravel, V., C. Martinez, H. Antoun and R. J. Tweddell. 2005. Antagonist microorganisms with the ability to control Pythium damping-off of tomato seeds in rockwool. Biocontrol, 50: 771-86. https://doi.org/10.1007/s10526-005-1312-z

Green, H., N. Heiberg, K. Lejbølle and D. F. Jensen. 2001. The use of a GUS transformant of Trichoderma harzianum, strain T3a, to study metabolic activity in the spermosphere and rhizosphere related to biocontrol of Pythium damping-off and root rot. European journal of plant pathology, 107: 349-59. https://doi.org/10.1023/A:1011274432090

Haran, S., H. Schickler and I. Chet. 1996. Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum. Microbiology, 142: 2321-31. https://doi.org/10.1099/00221287-142-9-2321

Harman, G. E. 2000. Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzinum T-22. Plant Disease, 84: 377-93. https://doi.org/10.1094/PDIS.2000.84.4.377

Howell, C. R. 1980. Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology, 70: 712-15. https://doi.org/10.1094/Phyto-70-712

Howell, C. R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Disease, 87: 4-10. https://doi.org/10.1094/PDIS.2003.87.1.4

Hultberg, M., B. Alsanius and P. Sundin. 2000. In-vivo and in-vitro interactions between Pseudomonas fluorescens and Pythium ultimum in the suppression of damping-off in tomato seedlings. Biological Control, 19: 1-8. https://doi.org/10.1006/bcon.2000.0840

Idris, H. A., N. Labuschagne and L. Korsten. 2008. Suppression of Pythium ultimum root rot of sorghum by rhizobacterial isolates from Ethiopia and South Africa. Biological Control, 45: 72-84. https://doi.org/10.1016/j.biocontrol.2007.11.004

Jabnoun-Khiareddine, H., M. Daami-Remadi, F. Ayed and M. El Mahjoub. 2009. Biocontrol of tomato Verticillium wilt by using indigenous Gliocladium spp. and Penicillium sp. isolates. Dynamic Soil, Dynamic Plant, 3: 70-79.

Jayaraj, J., N. V. Radhakrishnan and R. Velazhahan. 2006. Development of formulations of Trichoderma harzianum strain M1 for control of damping-off of tomato caused by Pythium aphanidermatum. Archives Of Phytopathology And Plant Protection, 39: 1-8. https://doi.org/10.1080/03235400500094720

Kerkeni, A., M. Daami-Remadi, N. Tarchoun and M. B. Khedher. 2007. In-vitro and in-vivo suppression of Pythium ultimum the causal agent of the cucumber damping-off by some compost fungi. Asian Journal of Agricultural Research, 1: 50-58. https://doi.org/10.3923/ajar.2007.50.58

Khabbaz, S. E. and P. A. Abbasi. 2014. Isolation, characterization, and formulation of antagonistic bacteria for the management of seedlings damping-off and root rot disease of cucumber. Canadian Journal of Microbiology, 60: 25-33. https://doi.org/10.1139/cjm-2013-0675

Khare, A. and R. S. Upadhyay. 2009. Induction of mutant strains of Trichoderma viride 1433 for biocontrol of Pythium aphanidermatum. Environmental Biology and Conservation, 14: 21-27.

Kim, D.-S., R. J. Cook and D. M. Weller. 1997. Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. Phytopathology, 87: 551-58. https://doi.org/10.1094/PHYTO.1997.87.5.551

Lamichhane, J. R., C. Dürr, A. A. Schwanck, M.-H. Robin, J.-P. Sarthou, V. Cellier, A. Messéan and J.-N. Aubertot. 2017. Integrated management of damping-off diseases. A review. Agronomy for Sustainable Development, 37: 25. https://doi.org/10.1007/s13593-017-0417-y

Lewis, J. A. and G. C. Papavizas. 1987. Reduction of inoculum of Rhizoctonia solani in soil by germlings of Trichoderma hamatum. Soil Biology and Biochemistry, 19: 195-201. https://doi.org/10.1016/0038-0717(87)90081-2

Li, Z., S. R. M. Pinson, M. A. Marchetti, J. W. Stansel and W. D. Park. 1995. Characterization of quantitative trait loci (QTLs) in cultivated rice contributing to field resistance to sheath blight (Rhizoctonia solani). Theoretical and Applied Genetics, 91: 382-88. https://doi.org/10.1007/BF00220903

Lumsden, R. D. 1989. Biological control of damping-off caused by Pythium ultimum and Rhizoctonia solani with Gliocladium virens in soilless mix. Phytopathology, 79: 361-66. https://doi.org/10.1094/Phyto-79-361

Mannai, S., J. Khiareddine H, N. B and D. Remadi M. 2018. Rhizoctonia root rot of pepper (Capsicum annuum): Comparative pathogenicity of causal agent and biocontrol attempt using fungal and bacterial agents. Journal of Plant Pathology & Microbiology, 09: 431-36. https://doi.org/10.4172/2157-7471.1000431

Manoranjitham, S. K., V. Prakasam, K. Rajappan and G. Amutha. 2000. Control of chilli damping-off using bioagents. Journal of Mycology and Plant Pathology, 30: 225-28.

Muthukumar, A., A. Eswaran and K. Sanjeevkumas. 2011. Exploitation of Trichoderma species on the growth of Pythium aphanidermatum in Chilli. Brazilian Journal of Microbiology, 42: 1598-607. https://doi.org/10.1590/S1517-83822011000400047

Naseby, D. C., J. A. Pascual and J. M. Lynch. 2001. Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. Journal of Applied Microbiology, 88: 161-69. https://doi.org/10.1046/j.1365-2672.2000.00939.x

Naseby, D. C., J. A. Way, N. J. Bainton and J. M. Lynch. 2001. Biocontrol of Pythium in the pea rhizosphere by antifungal metabolite producing and non-producing Pseudomonas strains. Journal of Applied Microbiology, 90: 421-29. https://doi.org/10.1046/j.1365-2672.2001.01260.x

Nasraoui, B., M. R. Hajlaoui, S. Gargouri and R. J. Kremer. 2007. Biological control of wheat take-all disease. II. rapid screening for selection of bacteria suppressive Gaeumannomyces graminis var. tritici in laboratory with greenhouse and field confirmation trials. Tunisian Journal of Plant Protection, 2: 35-46.

Osburn, R. M. 1989. Dynamics of sugar beet seed colonization by Pythium ultimum and Pseudomonas species: Effects on seed rot and damping-off. Phytopathology, 79: 709-16. https://doi.org/10.1094/Phyto-79-709

Papavizas, G. C. 1985. Trichoderma and Gliocladium: Biology, ecology, and potential for biocontrol. Annual Review of Phytopathology, 23: 23-54. https://doi.org/10.1146/annurev.py.23.090185.000323

Parke, J. L. 1990. Population dynamics of Pseudomonas cepacia in the pea spermosphere in relation to biocontrol of Pythium. Phytopathology, 80: 1307-11. https://doi.org/10.1094/Phyto-80-1307

Paulitz, T. C., J. S. Ahmad and R. Baker. 1990. Integration of Pythium nunn and Trichoderma harzianum isolate T-95 for the biological control of Pythium damping-off of cucumber. Plant and Soil, 121: 243-50. https://doi.org/10.1007/BF00012318

Rafin, C. and Y. Tirilly. 1995. Characteristics and pathogenicity of Pythium spp. associated with root rot of tomatoes in soilless culture in Brittany, France. Plant Pathology, 44: 779-85. https://doi.org/10.1111/j.1365-3059.1995.tb02735.x

Ramamoorthy, V., T. Raguchander and R. Samiyappan. 2002. Enhancing resistance of tomato and hot pepper to Pythium diseases by seed treatment with fluorescent pseudomonads. European journal of plant pathology, 108: 429-41. https://doi.org/10.1023/A:1016062702102

Rossman, D. R., A. Rojas, J. L. Jacobs, C. Mukankusi, J. D. Kelly and M. I. Chilvers. 2017. Pathogenicity and virulence of soilborne oomycetes on Phaseolus vulgaris. Plant Disease, 101: 1851-59. https://doi.org/10.1094/PDIS-02-17-0178-RE

Sivasithamparam, K. and F. L. Ghisalberti. 1998. Secondary metabolism in Trichoderma and Gliocladium. In: C.P. Kubicek and G E Harman (eds.), Trichoderma and Gliocladium Taylor and Francis Ltd: London, UK.

Soumaya, A. B. S., R. Haouala, H. Jabnoun-Khiareddine and M. Daami-Remadi. 2013. Evaluation de l'activité antifongique de Trichoderma spp., Gliocladium spp. et Aspergillus spp. contre Rhizoctonia solani par double culture et test de leurs filtrats de culture. Microbiologie et Hygiène Alimentaire, 25: 3-8.

STAT, F. 2013. Food and Agriculture Organization Statistics. Tunisia.

Tojo, M., T. Shigematsu, H. Morita, Y. Li, T. Matsumoto and S. T. Ohki. 2005. Pythium rot of Chinese cabbage (Brassica rapa L. subsp. pekinensis) caused by Pythium aphanidermatum. Journal of General Plant Pathology, 71: 384-86. https://doi.org/10.1007/s10327-005-0218-z

van West, P., A. A. Appiah and N. A. R. Gow. 2003. Advances in research on oomycete root pathogens. Physiological and Molecular Plant Pathology, 62: 99-113. https://doi.org/10.1016/S0885-5765(03)00044-4

Whipps, J. M. and R. D. Lumsden. 1991. Biological control of Pythium species. Biocontrol Science and Technology, 1: 75-90. https://doi.org/10.1080/09583159109355188

Zhani, K., B. F. Mariem, M. Fardaous and H. Cherif. 2012. Impact of salt stress (NaCl) on growth, chlorophyll content and fluorescence of Tunisian cultivars of chili pepper (Capsicum frutescens L.). Journal of Stress Physiology & Biochemistry, 8: 236-52.


Full Text: PDF

DOI: 10.33687/phytopath.009.01.3083

Refbacks

  • There are currently no refbacks.




Copyright (c) 2020 Hayfa Jabnoun-Khiareddine

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.