Prospecting bacterial volatile organic compounds antifungal activities against postharvest diseases

Manel Chaouachi; Takwa Marzouk; Jihed  Aouini; Amani Ben Alaya; Bilel Khiari; Naceur Djébali

doi:10.56027/JOASD.182022

Authors

Manel Chaouachi
Takwa Marzouk
Jihed Aouini
Amani Ben Alaya
Bilel Khiari
Naceur Djébali

DOI:

https://doi.org/10.56027/JOASD.182022

Keywords:

Anthracnose of citrus, Biofungicides, Gray mould, N-Ethylaniline, Lemon fruit, Tomato fruit

Abstract

Chemical pesticides have a plenty of negative impacts on human health and on the environment. Thus, modern agriculture cropping systems are moving towards more eco-friendly alternatives. This study aims to investigate the bioprotective effect of three volatile organic compounds (VOCs: N-Ethylaniline, 2-Heptanone and 3-Methylbutan-1-ol) produced by endophytic bacteria against 21 phytopathogenic fungal strains and their bioprotective effect on horticulture products i.e. tomato and lemon fruits and Potato tubers. The results showed that N-Ethylaniline and 3-methylbutan-1-ol had better antagonistic activity against the fungal strains by inhibiting the mycelia growth of the studied fungal strains at different concentrations. The N-Ethylaniline showed the lowest effective concentration (EC50) against B. cinerea strain S5 (0,258 mL/L headspace), Fusarium solani strain SB4.15.1 (0,496 mL/L headspace) and Colletotrichum gloeosporioides strain ManS3Fr02 (0,206 mL/L headspace). At EC50 this compound significantly reduced B. cinerea and C. gloeosporioides infections on tomato and lemon fruits, respectively. However, N-Ethylaniline didn’t showed significant effect on F. solani infection on Potato tubers. This study showed the broad spectrum of in vitro antifungal activity of N-Ethylaniline and its effect to reduce postharvest infections of some fungal diseases suggesting its potential use as a biofumigant.

References

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 postharvestpathogens of apples. Biol. Control 109, 14–20.

Ayed, A., Kalai-Grami, L., Ben Slimene, I., Chaouachi, M., Mankai, H., Karkouch, I., ... & Limam, F. (2021). Antifungal activity of volatile organic compounds from Streptomyces sp. strain S97 against Botrytis cinerea. Biocontrol Science and Technology, 31(12), 1330-1348,

Ben Alaya, A., Khiari, B., Ben Slimene, I., Djebali, N. (2021). Establishment and morphological characterization of a core collection of pathogenic fungal strains isolated from wilting Medicago sativa plants. Zenodo. https://doi.org/10.5281/zenodo.5914582.

Ben Slimene, I., Tabbene, O., Djebali, N., Cosette, P., Schmitter, J.M., Jouenne, T., Urdaci, M.C., Limam, F. (2012). Putative use of a Bacillus subtilis L194 strain for biocontrol of Phoma medicaginis in Medicago truncatula seedlings. Res. Microbiol. 163, 388–397.

Benmeddour T, Fenni M. (2018). Phytotoxicité des extraits de trois espèces végétales sur le blé dur et sur kochiascoparia: adventice envahissante des périmètres agricoles dans la wilaya de biskra. Courrier du Savoir, 25 : 173-178

Bitas, V., Kim, H.S., Bennett, J.W., Kang, S. (2013). Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol. Plant-Microbe Interact. 26, 835 – 843.

Boukaew, S., Cheirsilp, B., Prasertsan, P., Yossan, S. (2021). Antifungal effect of volatile organic compounds produced by Streptomyces salmonis PSRDC-09 against anthracnose pathogen Colletotrichum gloeosporioides PSU-03 in postharvest chili fruit. J. Appl. Microbiol. 131, 1452–1463.

Briard B, Heddergott C, Latgé J. (2016). Volatile compounds emitted by Pseudomonas aeruginosa stimulate growth of the fungal pathogen Aspergillus fumigatus. mBio 7(2):e00219-16.

Calvo, H., Mendiara, I., Arias, E., Gracia, A.P., Blanco, D., Venturini, M.E. (2020). Antifungal activity of the volatile organic compounds produced by Bacillus velezensis strains against postharvest fungal pathogens. Postharvest Biol. Technol. 166, 111208.

Chaouachi, M., Marzouk, T., Jallouli, S., Elkahoui, S., Gentzbittel, L., Ben, C., Djébali, N. (2021). Activity assessment of tomato endophytic bacteria bioactive compounds for the postharvest biocontrol of Botrytis cinerea. Postharvest Biol. Technol. 172.

Chebbi, H. E., Pellissier, J. P., Khechimi, W., Rolland, J. P. (2019). Rapport de synthèse sur l’agriculture en Tunisie (Doctoral dissertation, CIHEAM-IAMM).

Chung, J.H., Song, G.C. , Ryu, C.M. (2016). Sweet scents from good bacteria: Case studies on bacterial volatile compounds for plant growth and immunity. Plant Mol Biol 90, 677–687.

Compant, S., Duffy, B., Nowak, J., Clément, C., Ait Barka, E. (2005). Biocontrol of plant diseases using plant growth-promoting bacteria (PGPB): Principles, mechanisms of action and future prospects. Appl. Environ. Microbiol. 71, 4951–4959.

Coulibaly, N.D., Ossey, C.L., Gadji, A.G., De Paul N’Gbesso, M.F., Fondio, L., Soro, O.T. (2021). Etude De L’arrière Effet Des Légumineuses Alimentaires Sur La Productivité Des Légumes : Cas De La Tomate (Solanum Lycopersicum), Cultivée Dans La Localité De Bouaké Au Centre De La Côte d’Ivoire. Eur. Sci. Journal, ESJ 17, 125.

Di Francesco, A., Di Foggia, M., Baraldi, E. (2020). Aureobasidium pullulans volatile organic compounds as alternative postharvest method to control brown rot of stone fruits. Food Microbiol. 87, 103395.

Djebali, N. (2013). Aggressiveness and host range of Phoma medicaginis isolated from Medicago species growing in Tunisia. Phytopathologia Mediterranea, 52(1), 3-15.

Djébali, N., Elkahoui, S., Taamalli, W., Hessini, K., Tarhouni, B., Mrabet, M. (2014). Tunisian Rhizoctonia solani AG3 strains affect potato shoot macronutrients content, infect faba bean plants and show in vitro resistance to azoxystrobin. Australasian Plant Pathology, 43(3), 347-358.

Dougoud, J., Clottey, V., Bateman, M., Wood, A. (2018). Étude sur la protection des cultures dans les pays où le programme “Centres d’Innovations Vertes pour le Secteur Agro-Alimentaire” est actif Rapport national pour le ProCIVA au Bénin.

Elkahoui, S., Djébali, N., Yaich, N., Azaiez, S., Hammami, M., Essid, R., Limam, F. (2015). Antifungal activity of volatile compounds-producing Pseudomonas P2 strain against Rhizoctonia solani. World J. Microbiol. Biotechnol. 31, 175–185.

Guevara-Avendaño ,E., Bejarano-Bolívar, A.A ., Kiel-Martínez, A.L., Ramírez-Vázquez ,M ., Méndez-Bravo, A., Aguirre von Wobeser ,E., Sánchez-Rangel, D., Guerrero-Analco , J.A., Eskalen,A., Reverchon, F. (2019). Avocado rhizobacteria emit volatile organic compounds with antifungal activity against Fusarium solani, Fusarium sp. associated with Kuroshio shot hole borer, and Colletotrichum gloeosporioides, Microbiological Research, 219, 74-83.

Hernandez-Leon, R., Rojas-Solís, D., Contreras-Perez, M., Del Carmen Orozco- Mosqueda, M., Macías-Rodríguez, L.I., Reyes-de la Cruz, H., et al. (2015). Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol. Control 81, 83 – 92.

Kammoun, L. G., Gargouri, S., Hajlaoui, M. R., & Marrakchi, M. (2009). Occurrence and distribution of Microdochium and Fusarium species isolated from durum wheat in northern Tunisia and detection of mycotoxins in naturally infested grain. Journal of phytopathology, 157(9), 546-551.

Kanchiswamy, C.N., Malnoy, M., Maffei, M.E. (2015). Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci. 20, 206 – 211. https://doi.org/ 10.1016/j.tplants.2015.01.004.

Lee S.O., Kim H.Y., Choi G.J., Lee H.B., Jang K.S., Choi Y.H. & Kim J.-C. (2009). Mycofumigation with Oxyporus latemarginatus EF069 for control of postharvestappledecay and Rhizoctoniaroot rot on mothorchid. J. Appl. Microbiol. 106(4), 1213– 1219.

Marzouk, T., Chaouachi, M., Sharma, A., Jallouli, S., Mhamdi, R., Kaushik, N., Djébali, N. (2021). Biocontrol of Rhizoctonia solani using volatile organic compounds of solanaceae seed-borne endophytic bacteria. Postharvest Biol. Technol. 181.

Rajaofera, M.J.N., Wang, Y., Dahar, G.Y., Jin, P., Fan, L., Xu, L., et al. (2019). Volatile organic compounds of Bacillus atrophaeus HAB-5 inhibit the growth of Colletotrichum gloeosporioides. Pestic. Biochem. Phys. 156, 170 – 176.

Ruiu, L. (2019). Microbial Biopesticides in Agroecosystems. Agronomy , 8, 235.

Ryan, Robert P., Kieran Germaine, Ashley Franks, David J. Ryan, and David N. Dowling. (2008). Bacterial Endophytes: Recent Developments and Applications. FEMS Microbiology Letters 278 (1): 1–9.

Schalchli, H., Tortella, G.R., Rubilar, O., Parra, L., Hormazabal, E., Quiroz, A. (2016). Fungal volatiles: an environmentally friendly tool to control pathogenic microorganisms in plants. Crit. Rev. Biotechnol. 36, 144 – 152.

Sharifi, R., Ryu, C.M. (2018). Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann. Bot. 122, 349 – 358.

Slimene, I.B., Tabbene, O., Gharbi, D., Mnasri, B., Schmitter, J.M., Urdaci, M.C., Limam, F. (2015). Isolation of a chitinolytic Bacillus licheniformis S213 strain exerting a biological control against Phoma medicaginis infection. Appl. Biochem. Biotechnol,175, 3494–3506.

Syrokou, M.K.; Paramithiotis, S.; Kanakis, C.D.; Papadopoulos, G.K.; Tarantilis, P.A.; Skandamis, P.N.; Bosnea, L.; Mataragas, M.; Drosinos, E.H. (2022) Effect of Dough-Related Parameters on the Antimold Activity of Wickerhamomyces anomalus Strains and Mold-Free Shelf Life of Bread. Appl. Sci., 12, 4506.

Tyagi, S., Mulla, S.I., Lee, K.J., Chae, J.C., Shukla, P. (2018). VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Crit. Rev. Biotechnol. 38, 1277 – 1296.

Yang, M., Lu, L., Pang, J., Hu, Y., Guo, Q., Li, Z., et al. (2019). Biocontrol activity of volatile organic compounds from Streptomyces alboflavus TD-1 against Aspergillus flavus growth and aflatoxin production. J. Microbiol. 57, 396 – 404.

Zhang, Y., Li, T., Liu, Y., Li, X., Zhang, C., Feng, Z., et al. (2019). Volatile organic compounds produced by Pseudomonas chlororaphis subsp. aureofaciens SPS-41 as biological fumigants to control Ceratocystis fimbriata in postharvest sweet potatoes. J. Agric. Food Chem. 67, 3702 – 3710.