In vitro and in vivo antifungal activity of different bacterial isolates against Botrytis gray mold of tomato

Authors

  • Latifa ASKARNE Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA) https://orcid.org/0000-0002-3139-2276
  • M’barka ELQDHY Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)
  • Boujemaa AJDI Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)
  • Mohamed AIT HAMZA Ibn Zohr University, Faculty of Sciences, Laboratory of Biotechnology and Valorization of Natural Resources (LBVRN), B.P 8106, 80000 Agadir; Ibn Zohr University, Faculty of Applied Sciences- Ait Melloul, National Road N10. BP 6146 Azrou (MA)
  • Nadiya AMKRAZ Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir; Ibn Zohr University, Faculty of Sciences, Laboratory of Biotechnology and Valorization of Natural Resources (LBVRN), B.P 8106, 80000 Agadir (MA)
  • Hicham LAKHTAR Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)
  • El Hassane BOUDYACH Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)
  • Abdellah AIT BEN AOUMAR Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)
  • Hassan BOUBAKER Ibn Zohr University, Faculty of Sciences, Laboratory of Microbial Biotechnology and Plant Protection (LBMPV), BP 8106, 80000 Agadir (MA)

DOI:

https://doi.org/10.55779/nsb16312048

Keywords:

biological control, fungal disease, gray mold rot, postharvest, tomato

Abstract

Gray mold rot, caused by Botrytis cinerea, is considered as one of the most harmful fungal diseases affecting postharvest tomato fruits. In the current work, we explore the biocontrol potential of 174 bacterial strains isolated from tomato rhizosphere, argan rhizosphere and a vermicompost to control this fungal pathogen. The in vitro dual culture study of isolated bacterial strains and the fungus-causing pathogen revealed that 31 isolates exhibited a substantial antifungal activity against B. cinerea mycelial growth. The inhibition rates ranged from 55.36 to 85.07%. Twelve bacterial strains which showed the highest antifungal properties (more than 79.6%) were subsequently investigated for their ability to produce compounds with antifungal activity, including diffusible substances, volatile compounds and hydrocyanic acid. These strains were then evaluated in vivo for their ability to reduce fruit decay caused by the fungus. Indeed, isolates VC-B1 (from vermicompost), RS-TB3, and RS-T6 (from the rhizosphere of tomato root), and RH-TB11 (from the tomato rhizoplane) released the most active diffusible substances, which totally inhibited the mycelial growth of B. cinerea. In addition, bacterial strains RS-TB1 and RS-T6 isolated both from the tomato rhizospheric soil were among the isolates that produced the most effective volatile compounds. They reduced the mycelial growth of the fungal pathogen by 75.36% ± 7.24% and 72.94 ± 4.129% respectively. Moreover, RS-TB3, RS-TB4, RH-TB1, and VC-B1 exhibited the highest production of hydrocyanic acid, followed by RS-TB1, VC-3, and VC-13. In vivo bioassays showed disease reduction ranging from 37.92% to 93.14%, with VC-1, VC-5, and RS-T4 showing the highest efficacy. This study identifies several bacterial strains with high potential for biocontrol of B. cinerea in postharvest tomatoes, presenting a promising alternative to chemical fungicides for managing gray mold rot.

Metrics

Metrics Loading ...

References

Ait Hou M, Grazia C, Malorgio G (2015). Food safety standards and international supply chain organization: A case study of the Moroccan fruit and vegetable exports. Food Control 55:190-199. https://doi.org/10.1016/j.foodcont.2015.02.023

Alijani Z, Amini J, Ashengroph M, Bahramnejad B (2019). Antifungal activity of volatile compounds produced by Staphylococcus sciuri strain MarR44 and its potential for the biocontrol of Colletotrichum nymphaeae, causal agent strawberry anthracnose. International Journal of Food Microbiology 307:108276. https://doi.org/10.1016/j.ijfoodmicro.2019.108276

Amkraz N, Boudyach E, Boubaker H, Bouizgarne B, Ait Ben Aoumar A (2010). Screening for fluorescent pseudomonades, isolated from the rhizosphere of tomato, for antagonistic activity toward Clavibacter michiganensis subsp. michiganensis. World Journal of Microbiology and Biotechnology 26(6):1059-1065. https://doi.org/10.1007/s11274-009-0270-5

Arrarte E, Garmendia G, Rossini C, Wisniewski M, Vero S (2017). Volatile organic compounds produced by Antarctic strains of Candida sake play a role in the control of postharvest pathogens of apples. Biological Control 109:14-20. https://doi.org/10.1016/j.biocontrol.2017.03.002

Berrada I, Benkhemmar O, Swings J, Bendaou N, Amar M (2012). Selection of halophilic bacteria for biological control of tomato gray mould caused by Botrytis cinerea. Phytopathologia Mediterranea 51(3):625-630. https://doi.org/10.14601/Phytopathol_Mediterr-10627

Borges ÁV, Saraiva RM, Maffia LA (2014). Key factors to inoculate Botrytis cinerea in tomato plants. Summa Phytopathologica 40(3):221-225. https://doi.org/10.1590/0100-5405/1929

Bu S, Munir S, He P, Li Y, Wu Y, Li X, Kong B, He P, He Y (2021) Bacillus subtilis L1-21 as a biocontrol agent for postharvest gray mold of tomato caused by Botrytis cinerea. Biological Control 157:104568. https://doi.org/10.1016/j.biocontrol.2021.104568

Calvo H, Mendiara I, Arias E, Gracia AP, Blanco D, Venturini ME (2020). Antifungal activity of the volatile organic compounds produced by Bacillus velezensis strains against postharvest fungal pathogens. Postharvest Biology and Technology 166:111208. https://doi.org/10.1016/j.postharvbio.2020.111208

Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J (2019). Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Frontiers in Microbiology (Review) 10(FEB). https://doi.org/10.3389/fmicb.2019.00302

Cloutier A, Tran S, Avis TJ (2020). Suppressive effect of compost bacteria against grey mould and Rhizopus rot on strawberry fruit. Biocontrol Science and Technology 30(2):143-159. https://doi.org/10.1080/09583157.2019.1695745

Dean R, Van Kan JA, Pretorius ZA, Hammond‐Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J (2012). The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13(4):414-430. https://doi.org/10.1111/j.1364-3703.2011.00783.x

Devi AR, Sharma GD, Majumdar PB, Pandey P (2018). A multispecies consortium of bacteria having plant growth promotion and antifungal activities, for the management of Fusarium wilt complex disease in potato (Solanum tuberosum L.). Biocatalysis and Agricultural Biotechnology 16:614-624. https://doi.org/10.1016/j.bcab.2018.10.003

Elad Y, Yunis H, Katan T (1992). Multiple fungicide resistance to benzimidazoles, dicarboximides and diethofencarb in field isolates of Botrytis cinerea in Israel. Plant Pathology 41(1):41-46. https://doi.org/10.1111/j.1365-3059.1992.tb02314.x

Etesami H, Alikhani HA, Mirseyed Hosseini H (2019). Root bacterial endophytes as potential biological control agents against fungal rice pathogens. Archives of Phytopathology and Plant Protection 52(7-8):560-581. https://doi.org/10.1080/03235408.2018.1557884

Ezrari S, Mhidra O, Radouane N, Tahiri A, Polizzi G, Lazraq A, Lahlali R (2021). Potential role of rhizobacteria isolated from citrus rhizosphere for biological control of citrus dry root rot. Plants 10(5):872. https://doi.org/10.3390/plants10050872

Fagundes C, Pérez-Gago MB, Monteiro AR, Palou L (2013). Antifungal activity of food additives in vitro and as ingredients of hydroxypropyl methylcellulose-lipid edible coatings against Botrytis cinerea and Alternaria alternata on cherry tomato fruit. International Journal of Food Microbiology 166(3):391-398. https://doi.org/10.1016/j.ijfoodmicro.2013.08.001

FAOSTAT (2023). Food and Agriculture Organization of the United Nations (accessed 16/05/2023), https://www.fao.org/faostat/en/#compare

Fravel DR (1988). Role of antibiosis in the biocontrol of plant diseases. Annual Review of Phytopathology 26(1):75-91. https://doi.org/10.1146/annurev.py.26.090188.000451

Gao P, Qin J, Li D, Zhou S (2018). Inhibitory effect and possible mechanism of a Pseudomonas strain QBA5 against gray mold on tomato leaves and fruits caused by Botrytis cinerea. PloS One 13(1):1-15. https://doi.org/10.1371/journal.pone.0190932

Gong A-D, Li H-P, Yuan Q-S, Song X-S, Yao W, He W-J, Zhang J-B, Liao Y-C (2015). Antagonistic mechanism of iturin A and plipastatin A from Bacillus amyloliquefaciens S76-3 from wheat spikes against Fusarium graminearum. PloS One 10(2):1-18. https://doi.org/10.1371/journal.pone.0116871

Haidar R, Fermaud M, Calvo-Garrido C, Roudet J, Deschamps A (2016). Modes of action for biological control of Botrytis cinerea by antagonistic bacteria. Phytopathologia Mediterranea 301-322.

Halime S, Chtaina N, Mokhtari W, Elaissami A (2019). First report of Botrytis resistance in red berries fruit towards fenhaxamid and fludioxonil+ cyprodinil mixture, and its sensitivity feature towards other single site fungicides in Morocco. Pakistan Journal of Phytopathology 31(2):229-236. https://doi.org/10.33866/phytopathol.031.02.0515

Hernández-León R, Rojas-Solís D, Contreras-Pérez M, del Carmen Orozco-Mosqueda M, Macías-Rodríguez LI, Reyes-de la Cruz H, Valencia-Cantero E, Santoyo G (2015). Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biological Control 81:83-92. https://doi.org/10.1016/j.biocontrol.2014.11.011

Hmouni A, Massoui M, Douira A (1999). Etude de l’activité antagoniste de Trichoderma spp. et de Gliocladium spp. à l’égard de Botrytis cinerea, agent causal de la pourriture grise de la tomate. Al Awamia 99:75-92. https://www.inra.org.ma/sites/default/files/09906.pdf

Hmouni A, Oihabi L, Badoc A, Douira A (2003). Étude de la résistance de Botrytis cinerea aux benzimidazoles, dicarboximides et dithiocarbamates dans les cultures abritées de tomate de la région du Gharb (Maroc). Bulletin de la Société de Pharmacie de Bordeaux 142(1-4):79-100.

Jiang C-H, Wu F, Yu Z-Y, Xie P, Ke H-J, Li H-W, Yu Y-Y, Guo J-H (2015). Study on screening and antagonistic mechanisms of Bacillus amyloliquefaciens 54 against bacterial fruit blotch (BFB) caused by Acidovorax avenae subsp. citrulli. Microbiological research 170:95-104. https://doi.org/10.1016/j.micres.2014.08.009

Kamali M, Ahmadi J, Naeimi S, Guo D (2019). Characterization of Bacillus isolates from the rhizosphere of tomato suppressing Fusarium wilt disease. Acta Phytopathologica et Entomologica Hungarica 54(1):53-68. https://doi.org/10.1556/038.54.2019.006

Kefi A, Slimene IB, Karkouch I, Rihouey C, Azaeiz S, Bejaoui M, Belaid R, Cosette P, Jouenne T, Limam F (2015). Characterization of endophytic Bacillus strains from tomato plants (Lycopersicon esculentum) displaying antifungal activity against Botrytis cinerea Pers. World Journal of Microbiology and Biotechnology 31:1967-1976. https://doi.org/10.1007/s11274-015-1943-x

Köhl J, Kolnaar R, Ravensberg WJ (2019). Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science 845. https://doi.org/10.3389/fpls.2019.00845

Köhl J, Medeiros FH, Lombaers-van der Plas C, Groenenboom-de Haas L, van den Bosch T (2020). Efficacies of bacterial and fungal isolates in biocontrol of Botrytis cinerea and Pseudomonas syringae pv. tomato and growth promotion in tomato do not correlate. Biological Control 150:104375. https://doi.org/10.1016/j.biocontrol.2020.104375

Lahlali R, Mchachti O, Radouane N, Ezrari S, Belabess Z, Khayi S, Mentag R, Tahiri A, Ait Barka E (2020). The potential of novel bacterial isolates from natural soil for the control of brown rot disease (Monilinia fructigena) on apple fruits. Agronomy 10(11):1814. https://doi.org/10.3390/agronomy10111814

Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2012). Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biological Control 61(2):113-120. https://doi.org/10.1016/j.biocontrol.2011.10.014

Li Y, Guo Q, Li Y, Sun Y, Xue Q, Lai H (2019). Streptomyces pactum Act12 controls tomato yellow leaf curl virus disease and alters rhizosphere microbial communities. Biology and Fertility of Soils 55(2):149-169. https://doi.org/10.1007/s00374-019-01339-w

Li Z, Guo B, Wan K, Cong M, Huang H, Ge Y (2015). Effects of bacteria-free filtrate from Bacillus megaterium strain L2 on the mycelium growth and spore germination of Alternaria alternata. Biotechnology & Biotechnological Equipment 29(6):1062-1068. https://doi.org/10.1080/13102818.2015.1068135

Lian Q, Zhang J, Gan L, Ma Q, Zong Z, Wang Y (2017). The biocontrol efficacy of Streptomyces pratensis LMM15 on Botrytis cinerea in tomato. BioMed Research International 2017. https://doi.org/10.1155/2017/9486794

Martins SJ, Faria AF, Pedroso MP, Cunha MG, Rocha MR, Medeiros FHV (2019). Microbial volatiles organic compounds control anthracnose (Colletotrichum lindemuthianum) in common bean (Phaseolus vulgaris L.). Biological Control 131:36-42. https://doi.org/10.1016/j.biocontrol.2019.01.003

Mew T, Rosales A (1986). Bacterization of rice plants for control of sheath blight caused by Rhizoctonia solani. Phytopathology 76(11):1260-1264. https://doi.org/10.1094/Phyto-76-1260

Ni L, Punja ZK (2019). Management of fungal diseases on cucumber (Cucumis sativus L.) and tomato (Solanum lycopersicum L.) crops in greenhouses using Bacillus subtilis. Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol 2:1-28. https://doi.org/10.1007/978-3-030-15175-1_1

Nigro F, Schena L, Ligorio A, Pentimone I, Ippolito A, Salerno MG (2006). Control of table grape storage rots by pre-harvest applications of salts. Postharvest Biology and Technology 42(2):142-149. https://doi.org/10.1016/j.postharvbio.2006.06.005

Parafati L, Vitale A, Restuccia C, Cirvilleri G (2015). Biocontrol ability and action mechanism of food-isolated yeast strains against Botrytis cinerea causing post-harvest bunch rot of table grape. Food Microbiology 47:85-92. https://doi.org/10.1016/j.fm.2014.11.013

Peng G, Sutton J, Li D (1996). Sites of infection in tomato stems by Botrytis cinerea. Canadian Journal of Plant Pathology 18:97.

Qessaoui R, Lahmyed H, Ajerrar A, Furze J, Timothy P, Alouani M, Chebli B, Mayad E, Bouharroud R (2021). Solutions rhizosphériques: Isolats de Pseudomonas contre Botrytis cinerea de la tomate. African and Mediterranean Agricultural Journal-Al Awamia (131):50-72. https://doi.org/10.34874/IMIST.PRSM/afrimed-i131.31366

Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M, del Carmen Rocha-Granados M, Macías-Rodríguez L, Santoyo G (2018). Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. Biocatalysis and Agricultural Biotechnology 13:46-52. https://doi.org/10.1016/j.bcab.2017.11.007

Sadfi-Zouaoui N, Essghaier B, Hajlaoui MR, Fardeau ML, Cayaol JL, Ollivier B, Boudabous A (2008). Ability of moderately halophilic bacteria to control grey mould disease on tomato fruits. Journal of Phytopathology 156(1):42-52. https://doi.org/10.1111/j.1439-0434.2007.01329.x

Sharifi R, Ryu C-M (2016). Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Frontiers in Microbiology (Original Research) 7. https://doi.org/10.3389/fmicb.2016.00196

Spadaro D, Droby S (2016). Development of biocontrol products for postharvest diseases of fruit: The importance of elucidating the mechanisms of action of yeast antagonists. Trends in Food Science & Technology 47:39-49. https://doi.org/10.1016/j.tifs.2015.11.003

Tahiri Alaoui F, Askarne L, Boubaker H, Boudyach EH, Ait Ben Aoumar A (2017). Control of gray mold disease of tomato by postharvest application of organic acids and salts. Plant Pathology Journal 16(2):62-72. https://doi.org/10.3923/ppj.2017.62.72

Taqarort N, Echairi A, Chaussod R, Nouaim R, Boubaker H, Benaoumar AA, Boudyach E (2008). Screening and identification of epiphytic yeasts with potential for biological control of green mold of citrus fruits. World Journal of Microbiology and Biotechnology 24(12):3031-3038. https://doi.org/10.1007/s11274-008-9849-5

Veloso J, Díaz J (2012). Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathology 61(2):281-288. https://doi.org/10.1111/j.1365-3059.2011.02516.x

Wang C, Wang Y, Wang L, Fan W, Zhang X, Chen X, Wang M, Wang J (2021). Biocontrol potential of volatile organic compounds from Pseudomonas chlororaphis ZL3 against postharvest gray mold caused by Botrytis cinerea on Chinese cherry. Biological Control 159:104613. https://doi.org/10.1016/j.biocontrol.2021.104613

Wang H, Shi Y, Wang D, Yao Z, Wang Y, Liu J, Zhang S, Wang A (2018). A biocontrol strain of Bacillus subtilis WXCDD105 used to control tomato Botrytis cinerea and Cladosporium fulvum Cooke and promote the growth of seedlings. International Journal of Molecular Sciences 19(5):1371. https://doi.org/10.3390/ijms19051371

Wu Z, Huang Y, Li Y, Dong J, Liu X, Li C (2019). Biocontrol of Rhizoctonia solani via induction of the defense mechanism and antimicrobial compounds produced by Bacillus subtilis SL-44 on pepper (Capsicum annuum L.). Frontiers in Microbiology 10:2676. https://doi.org/10.3389/fmicb.2019.02676

Zhang X, Gao Z, Zhang X, Bai W, Zhang L, Pei H, Zhang Y (2020). Control effects of Bacillus siamensis G-3 volatile compounds on raspberry postharvest diseases caused by Botrytis cinerea and Rhizopus stolonifer. Biological Control 141:104135. https://doi.org/10.1016/j.biocontrol.2019.104135

Downloads

Published

2024-09-24

How to Cite

ASKARNE, L., ELQDHY, M., AJDI, B., AIT HAMZA, M., AMKRAZ, N., LAKHTAR, H., BOUDYACH, E. H., AIT BEN AOUMAR, A., & BOUBAKER , H. (2024). In vitro and in vivo antifungal activity of different bacterial isolates against Botrytis gray mold of tomato. Notulae Scientia Biologicae, 16(3), 12048. https://doi.org/10.55779/nsb16312048

Issue

Section

Research articles
CITATION
DOI: 10.55779/nsb16312048

Most read articles by the same author(s)