Skip to main content
Log in

Antifungal Activity of Serratia rubidaea Mar61-01 Purified Prodigiosin Against Colletotrichum nymphaeae, the Causal Agent of Strawberry Anthracnose

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Strawberry anthracnose, caused by Colletotrichum nymphaeae is an important disease of strawberry. In this study, an endophytic bacterium isolated from the stem of Fragaria × ananassa cv Paros and identified as Serratia rubidaea strain Mar61-01 based on phenotypic, biochemical characteristics and molecular phylogenetic analysis. Antagonistic activities of this endophytic bacterium against C. nymphaeae were investigated under in vitro, in vivo and greenhouse conditions. The strain Mar61-01 reduced mycelial growth and conidial germination of C. nymphaeae in in vitro tests. Furthermore, it reduced disease severity on inoculated strawberry fruits and seedlings compared with uninoculated control. In addition, the strain Mar61-01 produced prodigiosin pigment. The pigment was purified by thin layer chromatography and its chemical structure was characterized by FT-IR and NMR (400 MHz) spectra. The results indicated that prodigiosin is a key feature in biocontrol of C. nymphaeae. The inhibition growth of C. nymphaeae under in vitro, in vivo, and greenhouse conditions showed that S. rubidaea Mar61-01 has the potential for managing of strawberry anthracnose.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aaisha GA, Barate DL (2016) Isolation and identification of pectinolytic bacteria from soil samples of Akola Region, India. Int J Curr Microbiol App Sci 5:514–524

    CAS  Google Scholar 

  • 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. Int J Food Microbiol. https://doi.org/10.1016/j.ijfoodmicro.108276

    Article  PubMed  Google Scholar 

  • Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Micribiol 8:1–8

    Google Scholar 

  • Alstrom S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soils 7:232–238

    Google Scholar 

  • Ben Abdallah RA, Mejdoub-Trabelsi B, Nefzi A, Jabnoun-Khiareddin H, Daami-Remadi M (2016) Isolation of endophytic bacteria from Withania somnifera and assessment of their ability to suppress fusarium wilt disease in tomato and to promote plant growth. J Plant Pathol Microbiol 7:1–11

    Google Scholar 

  • Bergey DH, Holt JG (1994) Bergeys manual of determinative bacteriology, 9th edn. Lippincott Williams and Wilkins, Philadelphia

    Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 4:1327–1350

    Google Scholar 

  • Cerdeño AM, Bibb MJ, Challis GL (2001) Analysis of the prodiginine biosynthesis gene cluster of Streptomyces coelicolor A3 (2): new mechanisms for chain initiation and termination in modular multienzymes. Chem Biol 8:817–829

    PubMed  Google Scholar 

  • Chen Y, Gao X, Chen Y, Qin H, Huang L, Han Q (2014) Inhibitory efficacy of endophytic Bacillus subtilis EDR4 against Sclerotinia sclerotiorum on rapeseed. Biol Control 78:67–76

    Google Scholar 

  • Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Silva NI, Brooks S, Lumyong S, Hyde KD (2019) Use of endophytes as biocontrol agents. Fungal Biol Rev 33:133–148

    Google Scholar 

  • Delp B, Milholland RD (1980) Evaluation strawberry plants for resistance to Colletotrichum fragariae. Plant Dis 64:1071–1073

    Google Scholar 

  • Dennis C, Webbster J (1971) Antagonistic properties of species-groups of Trichoderma. Trans Br Mycol Soc 57:41–48

    CAS  Google Scholar 

  • Devi KA, Pandey P, Sharma GD (2016) Plant growth-promoting endophyte Serratia marcescens AL2-16 enhances the growth of Achyranthes aspera L., a medicinal plant. Hayti J Biosci 23:173–180

    Google Scholar 

  • Dhar Purkayastha G, Mangar P, Saha A, Saha D (2018) Evaluation of the biocontrol efficacy of a Serratia marcescens strain indigenous to tea rhizosphere for the management of root rot disease in tea. PLoS ONE 13(2):e0191761

    PubMed  PubMed Central  Google Scholar 

  • Dias ACF, Costa FEC, Andrete FD, Lacava PT, Teixeira MA, Assumpcao LC, Araujo WL, Azevedo J, Melo I (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195

    CAS  Google Scholar 

  • Duzhak AB, Panfilova ZI, Duzhak TG (2012) Role of prodigiosin and chitinases in antagonistic activity of the bacterium Serratia marcescens against the fungus Didymella applanata. Biochemistry (Mosc) 77:910–916

    CAS  Google Scholar 

  • Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: biosynthesis and regulation. Curr Sci 25:1693–1703

    Google Scholar 

  • Essghaier B, Fardeau MC, Cayol JL, Hajlaoui MR, Boudabous A, Jijakli H, Sadfi-Zouaoui N (2009) Biological control of grey mould in strawberry fruits by halophilic bacteria. J Appl Microbiol 106:833–846

    CAS  PubMed  Google Scholar 

  • Freeman S, Minz D, Kolesnik I, Barbul O, Zveibil A, Maymon M, Nitzani Y, Kirshner B, Rav-David D, Bilu A, Dag A, Shafir S, Elad Y (2004) Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur J Plant Pathol 110(4):361–370

    CAS  Google Scholar 

  • Fürstner A (2003) Chemistry and biology of roseophilin and the prodigiosin alkaloids: a survey of the last 2500 years. Angew Chem Int Ed 42:3582–3603

    Google Scholar 

  • Gerber NN, Lechevalier MP (1976) Prodiginine (prodigiosin-like) pigments from Streptomyces and other aerobic Actinomycetes. Can J Microbiol 22:658–667

    CAS  PubMed  Google Scholar 

  • González-Lamothe R, El Oirdi M, Brisson N, Bouarab K (2012) The conjugated auxin indole-3-acetic acid–aspartic acid promotes plant disease development. Plant Cell 24:762–777

    PubMed  PubMed Central  Google Scholar 

  • Grimont F, Grimont PA (2006) The genus serratia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes proteobacteria: gamma subclass, vol 6. Springer, New York, pp 219–244

    Google Scholar 

  • Gutiérrez-Román MI, Holguín-Meléndez F, Bello-Mendoza R, Guillén-Navarro K, Dunn MF, Huerta-Palacios G (2012) Production of prodigiosin and chitinases by tropical Serratia marcescens strains with potential to control plant pathogens. World J Microbiol Biotechnol 28:145–153

    PubMed  Google Scholar 

  • Gutiérrez-Román MI, Holguín-Meléndez F, Dunn MF, Guillén-Navarro K, Huerta-Palacios G (2015) Antifungal activity of Serratia marcescens CFFSUR-B2 purified chitinolytic enzymes and prodigiosin against Mycosphaerella fijiensis, causal agent of black Sigatoka in banana (Musa spp.). Biocontrol 60:565–572

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Series 41(41):95–98

    CAS  Google Scholar 

  • Holbrook AA, Edge WJW, Bailey F (1961) Spectrophotometric method for determination of Gibberellic acid. Adv Chem 28:159–167

    Google Scholar 

  • Hosseini S, Amini J, Mahmoud KS, Kaivan K, Ilaria P (2020) Perharvest and postharvest application of garlic and rosemary essential oils for controlling anthracnose and quality assessment of strawberry fruit during cold storage. Front Microbiol 11:1855

    PubMed  PubMed Central  Google Scholar 

  • Jangir M, Pathaka R, Sharma S, Sharmab S (2018) Biocontrol mechanisms of Bacillus sp., isolated from tomato rhizosphere, against Fusarium oxysporum f. sp. lycopersici. Biol Control 123:60–70

    CAS  Google Scholar 

  • Kamou NN, Karasali H, Menexes G, Kasiotis KM, Bon MC, Papadakis EN, Tzelepisa GD, Lotosa L, Lagopodi AL (2015) Isolation screening and characterisation of local beneficial rhizobacteria based upon their ability to suppress the growth of Fusarium oxysporum f. sp. radicis-lycopersici and tomato foot and root rot. Biocontrol Sci Technol 25(8):928–949

    Google Scholar 

  • Kamou NN, Dubey M, Tzelepis G, Menexes G, Papadakis EN, Karlsson M, Lagopodi AL, Jensen DF (2016) Investigating the compatibility of the biocontrol agent Clonostachys rosea IK726 with prodigiosin-producing Serratia rubidaea S55 and phenazine-producing Pseudomonas chlororaphis ToZa7. Arch Microbiol 198:369–377

    CAS  PubMed  Google Scholar 

  • Karimi K, Babai Ahari A, Arzanlou M, Amini J, Pertot I, Rota-Stabelli O (2017a) Application of the consolidated species concept to identify the causal agent of strawberry anthracnose in Iran and initial molecular dating of the Colletotrichum acutatum species. Eur J Plant Pathol 147:357–387

    Google Scholar 

  • Karimi K, Babai Ahari A, Arzanlou M, Amini J, Pertot I (2017b) Comparison of indigenous Trichoderma spp. strains to a foreign commercial strain in terms of biocontrol efficacy against Colletotrichum nymphaeae and related biological features. J Plant Dis Prot 124:453–466

    Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320

    CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Huang LL, Buchenauer H, Kang ZS (2010) Isolation and partial characterization of an antifungal protein from the endophytic Bacillus subtilis strain EDR4. Pestic Biochem Physiol 98:305–311

    CAS  Google Scholar 

  • Masiello M, Somma S, Ghionna V, Logrieco A, Moretti A (2019) In vitro and in field response of different fungicides against Aspergillus flavus and Fusarium species causing ear rot disease of maize. Toxins 11:1–18

    Google Scholar 

  • Mates ADPK, de Carvalho PN, de Almeida H-V (2019) Bacillus velezensis GF267 as a multi-site antagonist for the control of tomato bacterial spot. Biol Control 137:104013

    Google Scholar 

  • Moreira RR, Nesi CN, De Mio LLM (2014) Bacillus spp. and pseudomonas putida as inhibitors of the Colletotrichum acutatum group and potential to control Glomerella leaf spot. Biol Control 72:30–37

    Google Scholar 

  • Nalini S, Parthasarathi R (2014) Production and characterization of rhamnolipids produced by Serratia rubidaea SNAU02 under solid-state fermentation and its application as biocontrol agent. Bioresour Technol 173:231–238

    CAS  PubMed  Google Scholar 

  • Okamoto H, Sato Z, Sato M, Koiso Y, Iwasaki S, Isaka M (1998) Identification of antibiotic red pigments of Serratia marcescens F-1-1 a biocontrol agent of damping off of cucumber and antimicrobial activity against other plant pathogens. Jpn J Phytopathol 64:294–298

    CAS  Google Scholar 

  • Patil S, Bheemaraddi MC, Shivannavar CT, Gaddad MS (2014) Biocontrol activity of siderophore producing Bacillus subtilis CTS-G24 against wilt and dry root rot causing fungi in chickpea. IOSR J Agric Vet Sci 7:63–68

    Google Scholar 

  • Rakh RR, Dalvi SM, Musle BB, Raut LS (2017) Production, Extraction and Characterization of Red Pigment Produced by Serratia rubidaea JCM 1240T isolated from Soil. Int J Curr Microbiol App Sci 6:143–154

    CAS  Google Scholar 

  • Rakotoniriana EF, Rafamantanana M, Randriamampionona D, Rabemanantsoa C, Urveg-Ratsimamanga S, El Jaziri M, Munaut F, Corbisier AM, Quetin-Leclercq J, Declerck S (2013) Study in vitro of the impact of endophytic bacteria isolated from Centella asiatica on the disease incidence caused by the hemibiotrophic fungus Colletotrichum higginsianum. Antonie Van Leeuwenhoek 103:121–133

    PubMed  Google Scholar 

  • Saechow S, Thammasittirong A, Kittakoop P, Prachya S, Na-Ranong Thammasittirong SNR (2018) Antagonistic activity against dirty panicle rice fungal pathogens and plant growth-promoting activity of Bacillus amyloliquefaciens BAS23. J Microbiol Biotechnol 28(9):1527–1535

    CAS  PubMed  Google Scholar 

  • Samrot AV, Chandana K, Senthilkumar P, Narendra KG (2011) Optimization of prodigiosin production by Serratia marcescens SU-10 and evaluation of its bioactivity. Int Res J Biotechnol 2:28–133

    Google Scholar 

  • Shahitha S, Poornima K (2012) Enhanced production of prodigiosin production in Serratia marcescens. J Appl Pharm Sci 2:138–140

    Google Scholar 

  • Shanmugaiah V, Mathivanan N, Balasubramanian N, Manoharan PT (2008) Optimization of cultural conditions for production of chitinase by Bacillus laterosporous MML2270 isolated from rice rhizosphere soil. Afr J Biotechnol 7:2562–2568

    CAS  Google Scholar 

  • Someya N, Kataoka N, Komagata T, Hirayae K, Hibi T, Akutsu K (2000) Biological control of cyclamen soilborne diseases by Serratia marcescens strain B2. Plant Dis 84:334–340

    CAS  PubMed  Google Scholar 

  • Sun D, Zhuo T, Hu X, Fan X, Zou H (2017) Identification of a Pseudomonas putida as biocontrol agent for tomato bacterial wilt disease. Biol Control 114:45–50

    Google Scholar 

  • Tiru M, Muleta D, Bercha G, Adugna G (2013) Antagonistic effect of rhizobacteria against coffee wilt disease caused by Gibberella xylarioides. Asian J Plant Pathol 7:109–122

    Google Scholar 

  • Upadhyay RS, Jayaswal RK (1992) Pseudomonas cepacia causes mycelial deformities and inhibition of condition in phytopathogenic fungi. Curr Microbiol 24:181–187

    Google Scholar 

  • Wang K, Yan PS, Cao LX, Ding QL, Shao C, Zhao TF (2013) Potential of chitinolytic Serratia marcescens strain JPP1 for biological control of Aspergillus parasiticus and aflatoxin. Biomed Res Int 2013:1–7

    Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuberer DA, Kenerley CM, Jeger MJ (1988) Populations of bacteria and actinomycetes associated with sclerotia of Phymatotrichum omnivorum buried in Houston black clay. Plant Soil 112(1):69–76

    Google Scholar 

Download references

Acknowledgements

This research was supported by the Plant Protection Department of University of Kurdistan (Grant No: 96/19/30039).

Funding

This research project was funded by University of Kurdistan.

Author information

Authors and Affiliations

Authors

Contributions

ZA: acquisition of data, visualization, writing—original draft, researcher. JA: conceptualization, project administration, funding acquisition. MA: formal analysis, writing—reviewing & editing. BB: advisor, resources.

Corresponding author

Correspondence to Jahanshir Amini.

Ethics declarations

Conflict of interest

We wish to confirm that there are no known conflicts of interest associated with this publication.

Additional information

Handling Editor: Rhonda Peavy.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 7649 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alijani, Z., Amini, J., Ashengroph, M. et al. Antifungal Activity of Serratia rubidaea Mar61-01 Purified Prodigiosin Against Colletotrichum nymphaeae, the Causal Agent of Strawberry Anthracnose. J Plant Growth Regul 41, 585–595 (2022). https://doi.org/10.1007/s00344-021-10323-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10323-4

Keywords

Navigation