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.
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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
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
Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Micribiol 8:1–8
Alstrom S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soils 7:232–238
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
Bergey DH, Holt JG (1994) Bergeys manual of determinative bacteriology, 9th edn. Lippincott Williams and Wilkins, Philadelphia
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 4:1327–1350
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
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
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
De Silva NI, Brooks S, Lumyong S, Hyde KD (2019) Use of endophytes as biocontrol agents. Fungal Biol Rev 33:133–148
Delp B, Milholland RD (1980) Evaluation strawberry plants for resistance to Colletotrichum fragariae. Plant Dis 64:1071–1073
Dennis C, Webbster J (1971) Antagonistic properties of species-groups of Trichoderma. Trans Br Mycol Soc 57:41–48
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
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
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
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
Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: biosynthesis and regulation. Curr Sci 25:1693–1703
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
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
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
Gerber NN, Lechevalier MP (1976) Prodiginine (prodigiosin-like) pigments from Streptomyces and other aerobic Actinomycetes. Can J Microbiol 22:658–667
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
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
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
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
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
Holbrook AA, Edge WJW, Bailey F (1961) Spectrophotometric method for determination of Gibberellic acid. Adv Chem 28:159–167
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
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
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
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
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
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
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
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
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
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
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
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
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
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
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
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
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
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
Shahitha S, Poornima K (2012) Enhanced production of prodigiosin production in Serratia marcescens. J Appl Pharm Sci 2:138–140
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
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
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
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
Upadhyay RS, Jayaswal RK (1992) Pseudomonas cepacia causes mycelial deformities and inhibition of condition in phytopathogenic fungi. Curr Microbiol 24:181–187
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
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703
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
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This research was supported by the Plant Protection Department of University of Kurdistan (Grant No: 96/19/30039).
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This research project was funded by University of Kurdistan.
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ZA: acquisition of data, visualization, writing—original draft, researcher. JA: conceptualization, project administration, funding acquisition. MA: formal analysis, writing—reviewing & editing. BB: advisor, resources.
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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
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DOI: https://doi.org/10.1007/s00344-021-10323-4