Skip to main content

Advertisement

SpringerLink
Log in

Comparison of the biocontrol efficacy of culture filtrate from Streptomyces philanthi RL-1-178 and acetic acid against Penicillium digitatum, in vitro and in vivo

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

The antifungal compounds in a culture filtrate of Streptomyces philanthi RL-1-178 (culture filtrate RL-1-178) have been found to include acetic acid as their major component. The aim of this study was to compare the biocontrol efficacy of culture filtrate RL-1-178 with its major component at various concentrations, in inhibiting the growth of green mold disease from Penicillium digitatum, in vitro and in orange fruits. S. philanthi RL-1-178 was able to produce both antifungal metabolites and volatile compounds which inhibited the mycelial growth of P. digitatum. The effective dose of culture filtrate RL-1-178 was 2.5 mL/10 mL on PDA. Both culture filtrate RL-1-178 and commercial acetic acid at 1.5 mM completely suppressed the mycelial growth of P. digitatum and inhibited spore germination but did not kill the spores. Orange fruits treated with culture filtrate RL-1-178 showed less disease symptoms, disease incidence (12%) and a smaller lesion diameter (1.8 mm) than those treated with 1.5 mM acetic acid (25% and 5.6 mm, respectively). Moreover, a combination of both the culture filtrate and acetic acid (1.5 mM) was able to completely suppress the disease. The results revealed that culture filtrate RL-1-178 alone or acetic acid alone, as well as their combination were successful in controlling green mold disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahima, J., Zhang, X., Yang, Q., Zhao, L., Tibiru, A. M., & Zhang, H. (2019). Biocontrol activity of Rhodotorula mucilaginosa combined with salicylic acid against Penicillium digitatum infection in oranges. Biological Control, 135, 23–32.

    CAS  Google Scholar 

  • Boukaew, S., Chuenchit, S., & Petcharat, V. (2011). Evaluation of Streptomyces spp. for biological control of Sclerotium root and stem rot and Ralstonia wilt of chili. BioControl, 56, 365–347.

    Google Scholar 

  • Boukaew, S., Plubrukarn, A., & Prasertsan, P. (2013). Effect of volatile substances from Streptomyces philanthi RM-1-138 on growth of Rhizoctonia solanion rice leaf. BioControl, 58, 471–482.

    CAS  Google Scholar 

  • Boukaew, S., & Prasertsan, P. (2014). Suppression of rice sheath blight disease using heat stable culture filtrate of Streptomyces philanthi RM-1-138. Crop Protection, 6, 1–10.

    Google Scholar 

  • Boukaew, S., Prasertsan, P., Troulet, C., & Bardin, M. (2017). Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp. BioControl, 62, 793–803.

    CAS  Google Scholar 

  • Boukaew, S., Petlamul, W., Bunkrongcheap, R., Chookaew, T., Kabbua, T., Thippated, A., & Prasertsan, P. (2018). Fumigant activity of volatile compounds of Streptomyces philanthi RM-1-138 and pure chemicals (acetophenone and phenylethyl alcohol) against anthracnose pathogen in postharvest chili fruit. Crop Protection, 103, 1–8.

    CAS  Google Scholar 

  • Boukaew, S., Petlamul, W., Phitthayaphinant, P., & Prasertsan, P. (2019). Potential use of Streptomyces mycarofaciens SS-2-243 as a biofumigant to protect maize seeds against two aflatoxin producing fungi. European Journal of Plant Pathology, 155, 489–503.

    CAS  Google Scholar 

  • Boukaew, S., Petlamul, W., & Prasertsan, P. (2020). Efficacy of Streptomyces philanthi RL-1-178 culture filtrate against growth and aflatoxin B1 production by two aflatoxigenic fungi on maize seeds. European Journal of Plant Pathology, 156, 1041–1051.

    CAS  Google Scholar 

  • Choudhary, B., Nagpure, A., & Gupta, R. K. (2014). Fungal cell-wall lytic enzymes, antifungal metabolite(s) production, and characterization from Streptomyces exfoliatus MT9 for controlling fruit-rotting fungi. Journal of Basic Microbiology, 54, 1295–1309.

    CAS  PubMed  Google Scholar 

  • Choudhary, B., Nagpure, A., & Gupta, R. K. (2015). Biological control of toxigenic citrus and papaya-rotting fungi by Streptomyces violascens MT7 and its extracellular metabolites. Journal of Basic Microbiology, 55, 1343–1356.

    CAS  PubMed  Google Scholar 

  • Cordovez, V., Carrion, V. J., Etalo, D. W., Mumm, R., Zhu, H., van Wezel, G. P., & Raaijmakers, J. M. (2015). Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Frontiers in Microbiology, 6, 1081.

    PubMed  PubMed Central  Google Scholar 

  • Droby, S., Wisniewski, M., Ghaouth, A. E., & Wilson, C. (2003). Influence of food additives on the control of postharvest rots of apple and peach and efficacy of the yeast-based biocontrol product aspire. Postharvest Biology and Technology, 27, 127–135.

    CAS  Google Scholar 

  • Gao, L., Sun, J., Secundo, F., Gao, X., Xue, C., & Mao, X. (2018). Cloning, characterization and substrate degradation mode of a novel chitinase from Streptomyces albolongus ATCC 27414. Food Chemistry, 261, 329–336.

    CAS  PubMed  Google Scholar 

  • Grahovac, J., Grahovac, M., Dodić, J., Bajić, B., & Balaž, J. (2014). Optimization of cultivation medium for enhanced production of antifungal metabolites by Streptomyces hygroscopicus. Crop Protection, 65, 143–152.

    CAS  Google Scholar 

  • El-Goorani, M. A., El-Kascheir, H. M., Kabeel, M. T., & Shoeib, A. A. (1984). Resistance to benzimidazole of Penicillium italicum and Penicillium digitatum isolated from packinghouses and orchards in Egypt. Plant Disease, 68, 100–102.

    CAS  Google Scholar 

  • Fallanaj, F., Ippolito, A., Ligorio, A., Garganese, F., Zavanella, C., & Sanzani, S. M. (2016). Electrolyzed sodium bicarbonate inhibits Penicillium digitatum and induces defence responses against green mould in citrus fruit. Postharvest Biology and Technology, 115, 18–29.

    CAS  Google Scholar 

  • Habiba, N. R., Ali, S. A., Hasan, K. A., Sultana, V., Ara, J., & Ehteshamul-Haque, S. (2019). Evaluation of biocontrol potential of epiphytic yeast against postharvest Penicillium digitatum rot of stored Kinnow fruit (Citrus reticulata) and their effect on its physiochemical properties. Postharvest Biology and Technology, 148, 38–48.

    Google Scholar 

  • Hu, X., Cheng, B., Du, D., Huang, Z., Pu, Z., Chen, G., Peng, A., & Lu, L. (2019). Isolation and identification of a marine actinomycete strain and its control efficacy against citrus green and blue moulds. Biotechnol Biotec Eq, 1, 719–729.

    Google Scholar 

  • Lafuente, M. T., Ballester, A. R., & González-Candelas, L. (2019). Involvement of abscisic acid in the resistance of citrus fruit to Penicillium digitatum infection. Postharvest Biology and Technology, 154, 31–40.

    CAS  Google Scholar 

  • Li, Q., Ning, P., Zheng, L., Huang, J., Li, G., & Hsiang, T. (2010). Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biology and Technology, 58, 157–165.

    CAS  Google Scholar 

  • Li, Q., Jiang, Y., Ning, P., Zheng, L., Huang, J., Li, G., Jiang, D., & Hsiang, T. (2011). Suppression of Magnaporthe oryzae by culture filtrates of Streptomyces globisporus JK-1. Biological Control, 58, 139–148.

    CAS  Google Scholar 

  • 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, 113–120.

    CAS  Google Scholar 

  • Li, J., Li, H., Ji, S., Chen, T., Tian, S., & Qin, G. (2019). Enhancement of biocontrol efficacy of Cryptococcus laurentii by cinnamic acid against Penicillium italicum in citrus fruit. Postharvest Biology and Technology, 149, 42–49.

    CAS  Google Scholar 

  • Liu, Y., Wang, W., Zhou, Y., Yao, S., Deng, L., & Zeng, K. (2017). Isolation, identification and in vitro screening of Chongqing orangery yeasts for the biocontrol of Penicillium digitatum on citrus fruit. Biological Control, 110, 18–24.

    Google Scholar 

  • Ma, J., Hong, Y., Deng, L., Yi, L., & Zeng, K. (2019). Screening and characterization of lactic acid bacteria with antifungal activity against Penicillium digitatum on citrus. Biological Control, 138, 104044.

    CAS  Google Scholar 

  • Maldonado, M. C., Orosco, C. E., Gordillo, M. A., & Navarro, A. R. (2010). In vivo and in vitro antagonism of Streptomyces sp. RO3 against Penicillium digitatum and Geotrichum candidum. African Journal of Microbiology Research, 4, 2451–2456.

    Google Scholar 

  • Najmeh, S., Hosein, S. B. G., Sareh, S., & Bonjar, L. S. (2014). Biological control of citrus green mould, Penicillium digitatum, by antifungal activities of Streptomyces isolates from agricultural soils. African Journal of Microbiology Research, 8, 1501–1509.

    Google Scholar 

  • Palaniyandi, S. A., Yang, S. H., Cheng, J. H., Meng, L., & Suh, J. W. (2011). Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp.MJM5763. Applied Microbiology, 111, 443–455.

    CAS  Google Scholar 

  • Parafati, L., Vitale, A., Restuccia, C., & Cirvilleri, G. (2016). The effect of locust bean gum (LBG)-based edible coatings carrying biocontrol yeasts against Penicillium digitatum and Penicillium italicum causal agents of postharvest decay of mandarin fruit. Food Microbiology, 58, 87–94.

    CAS  PubMed  Google Scholar 

  • Perez, M. F., Ibarreche, J. P., Isas, A. S., Sepulveda, M., Ramallo, J., & Dib, J. R. (2017). Antagonistic yeasts for the biological control of Penicillium digitatum on lemons stored under export conditions. Biological Control, 115, 135–140.

    Google Scholar 

  • Perez, M. F., Díaza, M. A., Pereyra, M. M., Córdoba, J. M., Isas, A. S., Sepúlveda, M., Ramallo, J., & Dib, J. R. (2019). Biocontrol features of Clavispora lusitaniae against Penicillium digitatum on lemons. Postharvest Biology and Technology, 155, 57–64.

    Google Scholar 

  • Pornpukdeewattana, S., Kerdpiboon, S., Jindaprasert, A., Pandee, P., Teerarak, M., & Krusong, W. (2017). Upland rice vinegar vapor inhibits spore germination, hyphal growth and aflatoxin formation in Aspergillus flavus on maize grains. Food Control, 71, 88–93.

    CAS  Google Scholar 

  • Qin, G. Z., Tian, S. P., Xu, Y., & Wan, Y. K. (2003). Enhancement of biocontrol efficacy of antagonistic yeasts by salicylic acid in sweet cherry fruit. Molecular Plant Pathology, 6, 147–154.

    Google Scholar 

  • Qin, X., Xiao, H., Xue, C., Yu, Z., Yang, R., Cai, Z., & Si, L. (2015). Biocontrol of gray mold in grapes with the yeast Hanseniaspora uvarum alone and in combination with salicylic acid or sodium bicarbonate. Postharvest Biology and Technology, 100, 160–167.

    CAS  Google Scholar 

  • Rodríguez-Chávez, J. L., Juárez-Campusano, Y. S., Delgado, G., & Aguilar, J. R. P. (2019). Identification of lipopeptides from Bacillus strain Q11 with ability to inhibit the germination of Penicillium expansum, the etiological agent of postharvest blue mold disease. Postharvest Biology and Technology, 155, 72–79.

    Google Scholar 

  • Sakdapetsiri, C., Fukuta, Y., Aramsirirujiwet, Y., Shirasaka, N., & Kitpreechavanich, V. (2016). Antagonistic activity of endo-b-1,3-glucanase from a novel isolate, Streptomyces sp. 9X166, against black rot in orchids. Journal of Basic Microbiology, 56, 469–479.

    CAS  PubMed  Google Scholar 

  • Shi, Z., Wang, F., Lu, Y., & Deng, J. (2018). Combination of chitosan and salicylic acid to control postharvest green mold caused by Penicillium digitatum in grapefruit fruit. Scientia Horticulturae, 233, 54–60.

    CAS  Google Scholar 

  • Tian, Z., Chen, C., Chen, K., Liu, P., Fan, Q., Zhao, J., & Long, C. (2020). Biocontrol and the mechanisms of Bacillus sp. w176 against postharvest green mold in citrus. Postharvest Biol Technol, 159, 111022.

  • Tunsagool, P., Jutidamrongphan, W., Phaonakrop, N., Jaresitthikunchai, J., Roytrakul, S., & Leelasuphakul, W. (2019). Insights into stress responses in mandarins triggered by Bacillus subtilis cyclic lipopeptides and exogenous plant hormones upon Penicillium digitatum infection. Plant Cell Reports, 38, 559–575.

    CAS  PubMed  Google Scholar 

  • Venditti, T., Ladu, G., Cubaiu, L., Myronycheva, O., & D’hallewin, G. (2017). Repeated treatments with acetic acid vapors during storage preserve table grapes fruit quality. Postharvest Biol Technol, 125, 91–98.

  • Wan, M., Li, G., Zhang, J., Jiang, D., & Huang, H. C. (2008). Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biological Control, 46, 552–559.

    Google Scholar 

  • Watve, M. G., Tichoo, R., Jog, M. M., & Bhole, B. D. (2001). How many antibiotics are proced by the genus Streptomyces. Archives of Microbiology, 176, 386–390.

    CAS  PubMed  Google Scholar 

  • Wu, Y., Yuan, J. E. Y., Raza, W., Shen, Q., & Huang, Q. (2015). Effects of volatile organic compounds from Streptomyces albulus NJZJSA2 on growth of two fungal pathogens. Journal of Basic Microbiology, 55, 1104–1117.

    PubMed  Google Scholar 

  • Xin, Z., Yang, Q., Wan, C., Che, J., Li, L., Chen, J., & Tao, N. (2019). Isolation of antofine from Cynanchum atratum BUNGE (Asclepiadaceae) and its antifungal activity against Penicillium digitatum. Postharvest Biology and Technology, 157, 110961.

    CAS  Google Scholar 

  • Yu, T., & Zheng, X. D. (2007). Indole-3-acetic acid enhances the biocontrol of Penicillium expansum and Botrytis cinerea on pear fruit by Cryptococcus laurentii. FEMS Yeast Research, 7, 459–464.

    CAS  PubMed  Google Scholar 

  • Zadoks, J.C., & Schein, R.D. (1979). Epidemiology and plant disease management, Oxford University Press, New York, p. 427 p..

  • Zhang, Q., Yong, D., Zhang, Y., Shi, X., Li, B., Li, G., Liang, W., & Wang, C. (2016). Streptomyces rochei A-1induces resistance and defense-related responses against Botryosphaeria dothidea in apple fruit during storage. Postharvest Biology and Technology, 115, 30–37.

    CAS  Google Scholar 

  • Zhu, Y., Yu, J., Brecht, J. K., Jiang, T., & Zheng, X. (2016). Pre-harvest application of oxalic acid increases quality and resistance to Penicillium expansum in kiwifruit during postharvest storage. Food Chemistry, 190, 537–543.

    CAS  PubMed  Google Scholar 

  • Zhu, C., Lei, M., Andargie, M., Zeng, J., & Li, J. (2019). Antifungal activity and mechanism of action of tannic acid against Penicillium digitatum. Physiol Mol Plant Path, 107, 46–50.

    CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the financial support of Thailand Research Fund under Grant No. RTA6080010. Our great appreciation is extended to Mr. Michael Currie for editing the manuscript.

Author information

Authors and Affiliations

  1. College of Innovation and Management, Songkhla Rajabhat University, Songkhla, 90000, Thailand

    Sawai Boukaew & Wanida Petlamul

  2. Research and Development Office, Prince of Songkla University, Hatyai, Songkhla, 90112, Thailand

    Poonsuk Prasertsan

Authors
  1. Sawai Boukaew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wanida Petlamul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Poonsuk Prasertsan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sawai Boukaew.

Ethics declarations

Competing interests

The authors declare that no competing interest exists.

Human and animals rights

No human and/or animal participants were involved in this research.

Electronic supplementary material

ESM 1

(DOCX 21391 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boukaew, S., Petlamul, W. & Prasertsan, P. Comparison of the biocontrol efficacy of culture filtrate from Streptomyces philanthi RL-1-178 and acetic acid against Penicillium digitatum, in vitro and in vivo. Eur J Plant Pathol 158, 939–949 (2020). https://doi.org/10.1007/s10658-020-02128-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02128-0

Keywords

Search

Navigation