Skip to main content
Springer Nature Link
Log in

Antifungal activity of Serratia marcescens CFFSUR-B2 purified chitinolytic enzymes and prodigiosin against Mycosphaerella fijiensis, causal agent of black Sigatoka in banana (Musa spp.)

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The ascomycete fungus Mycosphaerella fijiensis causes black Sigatoka disease of banana. Because Serratia marcescens strain CFFSUR-B2 is an effective agent for the biological control of M. fijiensis, it was important to determine the mechanisms by which this bacterium stops or inhibits infection by this phytopathogen. The individual chitinases were effective in reducing germ tube growth to different degrees. We evaluated also the effect of mixtures of purified chitinases (ChiA, ChiB and ChiC) and prodigiosin on the germination and germ tube growth of M. fijiensis ascospores. None of the combinations inhibited ascospore germination. However, a toxic effect similar to that of benzimidazole was observed on ascospore germination by the synergistic action of chitinases and prodigiosin applied in combination. The maximal effect in inhibiting germ tube development observed with a mixture of the chitinases and prodigiosin suggests that these could be used in the effective biocontrol of black Sigatoka disease.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Akutsu K, Hirata H, Yamamoto M, Hirayae K, Okuyama S, Hibi T (1993) Growth inhibition of Botrytis spp by Serratia marcescens B2 isolated from tomato phylloplane. Ann Phytopathol Soc Jpn 59:18–25

    Article  CAS  Google Scholar 

  • Asano S, Ogiwara K, Nakagawa Y, Suzuki K, Hori H, Watanabe T (1999) Prodigiosin produced by Serratia marcescens enhances the insecticidal activity of Bacillus thuringiensis delta-endotoxin (CrylC) against common cutworm, Spodoptera litura. J Pestic Sci 24:381–385

    Article  CAS  Google Scholar 

  • Berger RL, Reynolds DM (1988) Colloidal chitin preparation. Methods Enzymol 161:140–142

  • Brurberg MB, Nes IF, Eijsink VGH (1996) Comparative studies of chitinases A and B from Serratia marcescens. Microbiol 142:1581–1589

    Article  CAS  Google Scholar 

  • Cang S, Sanada M, Johdo O, Ohta S, Nagamatsu Y, Yoshimoto A (2000) High production of prodigiosin by Serratia marcescens grown on ethanol. Biotechnol Lett 22:1761–1765

    Article  CAS  Google Scholar 

  • Chin KM, Kueng FR, Laird D (2000) Aspects of fungicide cross-resistance and implications for strobilurins. Brighton Crop Prot Conf Pests Dis 1:415–420

    Google Scholar 

  • Davidse LC (1981) Mechanism of action of metalaxyl in Phytophthora megasperma f. sp. medicaginis. Neth J Plant Pathol 87:254–255

    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. Biochem (Mosc) 77:910–916

    Article  CAS  Google Scholar 

  • Eckert MR, Rossall S, Selley A, Fitt BDL (2010) Effects of fungicides on in vitro spore germination and mycelial growth of the phytopathogens Leptosphaeria maculans and L. biglobosa (phoma stem canker of oilseed rape). Pest Manag Sci 66:396–405

    CAS  PubMed  Google Scholar 

  • Fouré E (1985) Black leaf streak disease of bananas and plantains (Mycophaerella fijiensis Morelet), study of the symptoms and stages of the disease in Gabon. Irfa, Paris, France

    Google Scholar 

  • Fuchs RL, McPherson SA, Drahos DJ (1986) Cloning of a Serratia marcescens gene encoding chitinase. Appl Environ Microbiol 51:504–509

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gerber NN (1975) Prodigiosin-like pigments. CRC Crit Rev Microbiol 3:469–485

    Article  CAS  PubMed  Google Scholar 

  • Grimont F, Grimont PAD (2006) The genus Serratia. Prokaryotes 6:219–244

    Article  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

    Article  PubMed  Google Scholar 

  • Gutiérrez-Román MI, Dunn MF, Tinoco-Valencia R, Holguín-Meléndez F, Huerta-Palacios G, Guillen-Navarro K (2014) Potentiation of the synergistic activities of chitinases ChiA, ChiB and ChiC from Serratia marcescens CFFSUR-B2 by chitobiase (Chb) and chitin binding protein (CBP). World J Microbiol Biotechnol 30:33–42

    Article  PubMed  Google Scholar 

  • Han SB, Kim HM, Kim YH, Lee CW, Jang ES, Son KH, Kim SU, Kim YK (1998) T-cell specific immunosuppression by prodigiosin isolated from Serratia marcescens. Int J Immunopharmacol 20:1–13

    Article  CAS  PubMed  Google Scholar 

  • Jones DR (2000) Sigatoka leaf spot diseases. In: Jones DR (ed) Diseases of banana, abacá and enset. CABI Publishing, Wallingford, UK, pp 79–92

    Google Scholar 

  • Marín DH, Romero RA, Guzman M, Sutton TB (2003) Black Sigatoka an increasing threat to banana cultivation. Plant Dis 87:208–222

    Article  Google Scholar 

  • McGrath MT (1996) Increased resistance to triadimefon and to benomyl in Sphaerotheca fuliginea populations following fungicide usage over one season. Plant Dis 80:633–639

    Article  CAS  Google Scholar 

  • Meredith DS, Lawrence JS (1969) Black leaf streak disease of bananas (Mycosphaerella fijiensis): symptoms of disease in Hawaii, and notes on the conidial state of the causal fungus. Trans Br Mycol Soc 52:459–476

    Article  Google Scholar 

  • Monreal J, Reese E (1969) The chitinase of Serratia marcescens. Can J Microbiol 15:689–696

    Article  CAS  PubMed  Google Scholar 

  • Mourichon X (1997) Mycosphaerella fijiensis, diversity and possibilities for the early screening of germplasm for resistance. In: Jones, D (ed) The improvement and testing of Musa: a global partnership. First Global conference of the international Musa testing program, La Lima, Honduras, pp 47–53

  • 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. Ann Phytopathol Soc Jpn 64:294–298

    Article  CAS  Google Scholar 

  • Russell PE (2004) Sensitivity baselines in fungicide resistance research and management. FRAC, Cambridge, UK

    Google Scholar 

  • Sastoque-Cala L, Mercado-Reyes M, Santiago-Salgado M (2007) Quevedo-Hidalgo and Pedroza-Rodríguez M. Producción de quitinasas extracelulares con una cepa alcalófila halotolerante de Streptomyces sp aislada de residuos de camarón. Revista Mexicana de Ingeniería Química 6:137–146

  • Schickler H, Haran S, Oppenheim AB, Chet I (1993) Cloned chitinases and their role in biological control of plant pathogenic fungi. In: Muzzarelli RAA (ed) Chitin enzymology. Ancona, Italy, pp 375–382

    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

    Article  Google Scholar 

  • Someya N, Nakajima M, Hirayae K, Hibi T, Akutsu K (2001) Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by the biocontrol bacterium Serratia marcescens strain B2 against the gray mold pathogen, Botrytis cinerea. J Gen Plant Pathol 67:312–317

    Article  CAS  Google Scholar 

  • Someya N, Nakajima M, Watanabe K, Hibi T, Akutsu K (2003) Influence of bacteria isolated from rice plants and rhizospheres on antibiotic production by the antagonistic bacterium Serratia marcescens strain B2. J Gen Plant Pathol 69:342–347

    Article  CAS  Google Scholar 

  • Suzuki K, Sugawara N, Suzuki M, Uchiyama T, Katouno F, Nikaidou N, Watanabe T (2002) Chitinases A, B, and C1 from Serratia marcescens 2170 produced by recombinant Escherichia coli: enzymatic properties and synergism on chitin degradation. Biosci Biotechnol Biochem 66:1075–1083

    Article  CAS  PubMed  Google Scholar 

  • StatSoft Inc. (2006) STATISTICA (data analysis software system) version 7. http://www.statsoft.com

  • Stover RH (1980) Sigatoka leaf spots of bananas and plantains. Plant Dis Rep 64:750–758

    Article  Google Scholar 

  • Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GP (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36:539–556

    Article  CAS  PubMed  Google Scholar 

  • Williams RP, Qadri SMH (1980) The pigment of Serratia. In: von Graevenitz A, Rubin SJ (eds) The genus Serratia. CRC Press Inc., Boca Raton, USA, pp 31–78

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Agricultura, Sociedad y Ambiente, El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km. 2.5, 30700, Tapachula, Chiapas, Mexico

    Martha Ingrid Gutiérrez-Román & Graciela Huerta-Palacios

  2. Laboratorio de Diagnóstico Fitosanitario, El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km. 2.5, 30700, Tapachula, Chiapas, Mexico

    Francisco Holguín-Meléndez

  3. Programa de Genómica Funcional de Procariotes, Centro de Ciencias Genómicas UNAM, Av. Universidad S/N, Col. Chamilpa, 62210, Cuernavaca, Morelos, Mexico

    Michael F. Dunn

  4. Laboratorio de Biotecnología Ambiental y Agroecológica, El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km. 2.5, 30700, Tapachula, Chiapas, Mexico

    Karina Guillén-Navarro

Authors
  1. Martha Ingrid Gutiérrez-Román
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Francisco Holguín-Meléndez
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Michael F. Dunn
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Karina Guillén-Navarro
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Graciela Huerta-Palacios
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Graciela Huerta-Palacios.

Additional information

Handling Editor: Monica Höfte.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gutiérrez-Román, M.I., Holguín-Meléndez, F., Dunn, M.F. et al. 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 (2015). https://doi.org/10.1007/s10526-015-9655-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-015-9655-6

Keywords