Skip to main content
SpringerLink
Log in

Salicylate Degradation by the Fungal Plant Pathogen Sclerotinia sclerotiorum

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The fungal plant pathogen Sclerotinia sclerotiorum was studied to determine its ability to degrade salicylate, an important defense-signaling molecule in plants. S. sclerotiorum D-E7 was grown at 25 °C in an undefined medium (50 ml) containing minerals, 0.1 % soytone, 50 mM MES buffer (pH 6.5), 25 mM glucose, and 1 mM salicylate. Glucose, oxalate, and salicylate concentrations were monitored by HPLC. S. sclerotiorum D-E7 was found to be active in salicylate degradation. However, salicylate alone was not growth supportive and, at higher levels (10 mM), inhibited glucose-dependent growth. Biomass formation (130 mg [dry wt] of mycelium per 50 ml of undefined medium), oxalate concentrations (~10 mM), and culture acidification (final culture pH approximated 5) were essentially the same in cultures grown with or without salicylate (1 mM). Time-course analyses revealed that salicylate degradation and glucose consumption were complete after 7 days of incubation and was concomitant with growth. Trace amounts of catechol, a known intermediate of salicylate metabolism, were detected during salicylate degradation. Overall, these results indicated that S. sclerotiorum has the ability to degrade salicylate and that the presence of low levels of salicylate did not affect growth or oxalate production by S. sclerotiorum.

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

Similar content being viewed by others

References

  1. Agrios GN (1997) Plant pathology, 4th edn. Academic Press, San Diego

    Google Scholar 

  2. Amborabé B-E, Fleurat-Lessard P, Chollet J-F, Roblin G (2002) Antifungal effects of salicylic acid and other benzoic acid derivatives towards Eutypa lata: structure–activity relationship. Plant Physiol Biochem 40:1051–1060

    Article  Google Scholar 

  3. Amin AR, Vyas P, Modi VV (1984) Catabolism of benzoate and salicylate by Aspergillus japonicus. Indian J Exp Biol 22:220–221

    PubMed  CAS  Google Scholar 

  4. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier J-M, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, Da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun M-H, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230. doi:10.1371/journal.pgen.1002230

    Article  PubMed  CAS  Google Scholar 

  5. Anderson JJ, Dagley S (1980) Catabolism of aromatic acids in Trichosporon cutaneum. J Bacteriol 141:534–543

    PubMed  CAS  Google Scholar 

  6. Bachman DM, Dragoon B, John S (1960) Reduction of salicylate to saligenin by Neurospora. Arch Biochem Biophys 91:326

    Article  PubMed  CAS  Google Scholar 

  7. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  8. Beckers GJM, Spoel SH (2005) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol 8:1–10

    Article  Google Scholar 

  9. Bergauer P, Fonteyne P-A, Nolard N, Schinner F, Margesin R (2005) Biodegradation of phenol and phenol-related compounds by psychrophilic and cold-tolerant alpine yeasts. Chemosphere 59:909–918

    Article  PubMed  CAS  Google Scholar 

  10. Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16:93–108

    Article  Google Scholar 

  11. Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16

    Article  PubMed  CAS  Google Scholar 

  12. Buswell JA, Paterson A, Salkinoja-Salonen MS (1980) Hydroxylation of salicylic acid to gentisate by a bacterial enzyme. FEMS Microbiol Lett 8:135–137

    Article  CAS  Google Scholar 

  13. Cain RB, Bilton RF, Darrah JA (1968) The metabolism of aromatic acids by micro-organisms. Biochem J 108:797–828

    PubMed  CAS  Google Scholar 

  14. Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582

    PubMed  CAS  Google Scholar 

  15. Culbertson BJ, Furumo NC, Daniel SL (2007) Impact of nutritional supplements and monosaccharides on growth, oxalate accumulation, and culture pH by Sclerotinia sclerotiorum. FEMS Microbiol Lett 270:132–138

    Article  PubMed  CAS  Google Scholar 

  16. Culbertson BJ, Krone J, Gatebe E, Furumo NC, Daniel SL (2007) Impact of carbon sources on growth and oxalate synthesis by the phytopathogenic fungus Sclerotinia sclerotiorum. World J Microbiol Biotechnol 23:1357–1362

    Article  CAS  Google Scholar 

  17. Dagley S (1971) Catabolism of aromatic compounds by microorganisms. Adv Microb Physiol 6:1–46

    Article  PubMed  CAS  Google Scholar 

  18. de Bary A (1886) Ueber einige Sclerotinen und Sclerotienkrankheiten. Bot Z 44:377–387, 393–404, 409–426

    Google Scholar 

  19. Deveryshetty J, Suvekbala V, Varadamshetty G, Phale P (2007) Metabolism of 2-, 3- and 4-hydroxybenzoates by soil isolates Alcaligenes sp. strain PPH and Pseudomonas sp. strain PPD. FEMS Microbiol Lett 268:59–66

    Article  PubMed  CAS  Google Scholar 

  20. Dodge AG, Wackett LP (2005) Metabolism of bismuth subsalicylate and intracellular accumulation of bismuth by Fusarium sp. strain BI. Appl Environ Microbiol 71:876–882

    Article  PubMed  CAS  Google Scholar 

  21. Engelhardt G, Rast HG, Wallnöfer PR (1979) Degradation of aromatic carboxylic acids by Nocardia spec. DSM 43251. FEMS Microbiol Lett 5:245–251

    Article  CAS  Google Scholar 

  22. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  23. Godoy G, Steadman JR, Dickman MB, Dam R (1990) Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerorinia sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 37:179–191

    Article  CAS  Google Scholar 

  24. Grau CR, Hartman GL (1999) Sclerotinia stem rot. In: Hartman GL, Sinclair JB, Rupe JC (eds) Compendium of soybean diseases. APS Press, St. Paul, pp 46–48

    Google Scholar 

  25. Grund E, Knorr C, Eichenlaub R (1990) Catabolism of benzoate and monohydroxylated benzoates by Amycolatopsis and Streptomyces spp. Appl Environ Microbiol 56:1459–1464

    PubMed  CAS  Google Scholar 

  26. Guo X, Stotz HU (2007) Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol Plant-Microbe Interact 20:1384–1395

    Article  PubMed  CAS  Google Scholar 

  27. Halim VA, Vess A, Scheel D, Rosahl S (2006) The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol 8:307–313

    Article  PubMed  CAS  Google Scholar 

  28. Haribabu B, Kamath AV, Vaidyanathan CS (1984) Degradation of substituted benzoic acids by a Micrococcus species. FEMS Microbiol Lett 21:197–200

    Article  CAS  Google Scholar 

  29. Hinter JP, Lechner C, Riegert U, Kuhm AE, Storm T, Reemtsma T, Stolz A (2001) Direct ring fission of salicylate by a salicylate 1,2-dioxygenase activity from Pseudaminobacter salicylatoxidans. J Bacteriol 183:6936–6942

    Article  Google Scholar 

  30. Ishiyama D, Vujaklija D, Davies J (2004) Novel pathway of salicylate degradation by Streptomyces sp. strain WA46. Appl Environ Microbiol 70:1297–1306

    Article  PubMed  CAS  Google Scholar 

  31. Iwasaki Y, Gunji H, Kino K, Hattori T, Ishii Y, Kirimura K (2010) Novel metabolic pathway for salicylate biodegradation via phenol in yeast Trichosporon moniliiforme. Biodegradation 21:557–564

    Article  PubMed  CAS  Google Scholar 

  32. Jouanneau Y, Micoud J, Meyer C (2007) Purification and characterization of a three-component salicylate 1-hydroxylase from Sphingomonas sp. strain CHY-1. Appl Environ Microbiol 73:7515–7521

    Article  PubMed  CAS  Google Scholar 

  33. Karegoudar TB, Kim C-K (2000) Microbial degradation of monohydroxybenzoic acids. J Microbiol 38:53–61

    CAS  Google Scholar 

  34. Kocaçalışkana I, Talanb I, Terzic I (2006) Antimicrobial activity of catechol and pyrogallol as allelochemicals. Z Naturforsch 61c:639–642

    Google Scholar 

  35. Krupka LR, Racle FA (1967) Degradation of salicylate by Aspergillus niger. Nature 216:486–487

    Article  PubMed  CAS  Google Scholar 

  36. Krupka LR, Racle FA, Marderosian AD (1969) Salicylate degradation by Aspergillus niger: influence of glucose. J Pharm Sci 58:270–272

    Article  PubMed  CAS  Google Scholar 

  37. Kuswandi K, Roberts CF (1992) Genetic control of protocatechuic acid pathway in Aspergillus nidulans. J Gen Microbiol 138:817–823

    Article  CAS  Google Scholar 

  38. Lanfranconi MP, Christie-Oleza JA, Martin-Cardona C, Suárez-Suárez LY, Lalucat J, Nogales B, Bosch R (2009) Physiological role of NahW, the additional salicylate hydroxylase found in Pseudomonas stutzeri AN10. FEMS Microbiol Lett 300:265–272

    Article  PubMed  CAS  Google Scholar 

  39. Magro P, Marciano P, Di Lenna P (1984) Oxalic acid production and its role in pathogenesis of Sclerotinia sclerotiorum (sunflower). FEMS Microbiol Lett 24:9–12

    Article  CAS  Google Scholar 

  40. Marciano P, Lenna PD, Magro P (1983) Oxalic acid, cell wall-degrading enzymes and pH in pathogenesis and their significance in the virulence of two Sclerotinia sclerotiorum isolates on sunflower. Physiol Plant Pathol 22:339–345

    CAS  Google Scholar 

  41. Marciano P, Magro P, Favaron F (1989) Sclerotinia sclerotiorum growth and oxalic acid production on selected culture media. FEMS Microbiol Lett 61:57–69

    Article  CAS  Google Scholar 

  42. Matera I, Ferraroni M, Burger S, Scozzafova A, Stolz A, Briganti F (2008) Salicylate 1,2-dioxygenase from Pseudaminobacter salicylatoxidans: crystal structure of a peculiar ring-cleaving dioxygenase. J Mol Biol 380:856–868

    Article  PubMed  CAS  Google Scholar 

  43. Maxwell DP, Lumsden RD (1970) Oxalic acid production by Sclerotinia sclerotiorum in infected bean and in culture. Phytopathology 60:1395–1398

    Article  CAS  Google Scholar 

  44. Middelhoven WJ (1993) Catabolism of benzene compounds by ascomycetous and basidiomycetous yeasts and yeastlike fungi. Antonie Van Leeuwenhoek 63:125–144

    Article  PubMed  CAS  Google Scholar 

  45. Mills SC, Child JJ, Spencer JFT (1971) The utilization of aromatic compounds by yeasts. Antonie Van Leeuwenhoek 37:281–287

    Article  PubMed  CAS  Google Scholar 

  46. Mouttaki H, Nanny MA, McInerney MJ (2009) Metabolism of hydroxylated and fluorinated benzoates by Syntrophus aciditrophicus and detection of a fluorodiene metabolite. Appl Environ Microbiol 75:998–1004

    Article  PubMed  CAS  Google Scholar 

  47. Noyes RD, Hancock JG (1981) Role of oxalic acid in the Sclerotinia wilt of sunflower. Physiol Plant Pathol 18:123–132

    CAS  Google Scholar 

  48. Park S-W, Kaimoyo E, Kumar D, Mosher S, Klessig D (2007) Methyl salicylate is a crucial mobile signal for plant systemic acquired resistance. Science 318:113–116

    Article  PubMed  CAS  Google Scholar 

  49. Peng R-H, Xiong A-S, Xue Y, Fu X-Y, Gao F, Zhao W, Tian Y-S, Yao Q-H (2008) Microbial degradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955

    Article  PubMed  CAS  Google Scholar 

  50. Purdy LH (1979) Sclerotinia sclerotiorum: history, diseases and symptomatology, host range, geographic distribution, and impact. Phytopathology 69:875–880

    Article  Google Scholar 

  51. Qi P-F, Johnston A, Balcerzak M, Rocheleau H, Harris L, Long X-Y, Wei Y-M, Zheng Y-L, Ouellet T (2012) Effect of salicylic acid on Fusarium graminearum, the major causal agent of fusarium head blight in wheat. Fungal Biol 116:413–426

    Article  PubMed  CAS  Google Scholar 

  52. Rollins JA, Dickman MB (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl Environ Microbiol 67:75–81

    Article  PubMed  CAS  Google Scholar 

  53. Sazonova OI, Izmalkova TY, Kosheleva IA, Boronin AM (2008) Salicylate degradation by Pseudomonas putida strains not involving the “classical” nah2 operon. Microbiology 77:710–716

    Article  CAS  Google Scholar 

  54. Sclerotinia sclerotiorum Sequencing Project (2012) Broad Institute of Harvard and MIT. www.broadinstitute.org/annotation/genome/sclerotinia_sclerotiorum/MultiHome.html

  55. Shailubhai K, Somayaji R, Rao NN, Modi VV (1983) Metabolism of resorcinol and salicylate in Aspergillus niger. Experientia 39:70–72

    Article  PubMed  CAS  Google Scholar 

  56. Smith JL, Moraes CMD, Mescher MC (2009) Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manage Sci 65:497–503

    Article  CAS  Google Scholar 

  57. Steadman JR (1983) White mold-a serious yield limiting disease of bean. Plant Dis 67:346–350

    Article  Google Scholar 

  58. Suemori A, Nakajima K, Kurane R, Nakamura Y (1995) o-, m-, and p-Hydroxybenzoate degradative pathways in Rhodococcus erythropolis. FEMS Microbiol Lett 125:31–36

    Article  PubMed  CAS  Google Scholar 

  59. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  PubMed  CAS  Google Scholar 

  60. Tu JC (1985) Tolerance of white bean (Phaseolus vulgaris) to white mold (Sclerotinia sclerotiorum) associated with tolerance to oxalic acid. Physiol Plant Pathol 26:111–117

    Article  CAS  Google Scholar 

  61. Vega RR, Corsini D, Le Tourneau D (1970) Nonvolatile organic acids produced by Sclerotinia sclerotiorum in synthetic liquid media. Mycologia 62:332–338

    Article  PubMed  CAS  Google Scholar 

  62. Wang Z, Tan X, Zhang Z, Gu S, Li G, Shi H (2012) Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Sci 184:75–82

    Article  PubMed  CAS  Google Scholar 

  63. Willetts HJ, Wong JA-L (1980) The biology of Sclerotinia sclerotiorum, S. trifoliorum, and S. minor with emphasis on specific nomenclature. Bot Rev 46:100–165

    Article  Google Scholar 

  64. Zhao S, Qi X (2008) Signaling in plant disease resistance and symbiosis. J Integr Plant Biol 50:799–807

    Article  PubMed  CAS  Google Scholar 

  65. Ziman L, Jedryczka M, Srobarova A (1998) Relationship between morphological and biochemical characteristics of Sclerotinia sclerotiorum isolates and their aggressivity. Z Pflanzenkr Pflanzenschutz 105:283–288

    Google Scholar 

Download references

Acknowledgments

We express appreciation to the National Soybean Pathogen Collection Center at the University of Illinois at Urbana-Champaign for providing us with cultures of S. sclerotiorum. Funding for this project was provided by two Biological Sciences undergraduate research grants (CDP), a College of Sciences seed grant (SLD), and a Proposal Initiative Fund grant (SLD), all from Eastern Illinois University.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Eastern Illinois University, 600 Lincoln Avenue, Charleston, IL, 61920, USA

    Cory D. Penn & Steven L. Daniel

Authors
  1. Cory D. Penn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven L. Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven L. Daniel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Penn, C.D., Daniel, S.L. Salicylate Degradation by the Fungal Plant Pathogen Sclerotinia sclerotiorum . Curr Microbiol 67, 218–225 (2013). https://doi.org/10.1007/s00284-013-0349-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-013-0349-y

Keywords

Search

Navigation