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Plant-pathogen interactions during infection process of asparagus with Fusarium spp.

  • Research Article
  • Published:
Central European Journal of Biology

Abstract

Background

Asparagus officinalis L. is often infected by fungi from the Fusarium genus which also contaminate the plant tissues with highly toxic secondary metabolites. To elucidate the plant-pathogen interactions between asparagus and Fusarium oxysporum or F. proliferatum, a fungal mycotoxins profile was assessed together with an impact of the infection on all forms of salicylic acid content.

Methodology

Fungal isolates were identified by their morphological features, species-specific PCR and transcription elongation factor 1a (TEF-1a) sequencing. Mycotoxins were assessed by high-performance liquid chromatography (HPLC). The salicylic acid and its derivatives content was analyzed by the HPLC method combined with fluorometric detection. The levels of free radicals were measured by electron paramagnetic resonance (EPR).

Results

After infection both Fusarium pathogens formed fumonisin B1 and moniliformin. Infection altered salicylic acid biosynthesis and conjugation rates both in the roots and stems when compared with non-inoculated plants. Samples with higher free radical concentrations in stems showed higher concentrations of all forms of salicylic acid.

Conclusions

We postulate that infection by both Fusarium pathogens produces mycotoxins, which may be transported to the upper part of plant. Pathogen attack initiated a plant defense reaction involving increased salicylic acid levels and resulting in increase in free radical levels.

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Abbreviations

APx:

ascorbate peroxidase

CAT:

catalase

EPR:

electron paramagnetic resonance

Foa :

F. oxysporum f. sp. asparagi

FR:

free radicals

FBs:

fumonisins

FB1 :

fumonisin B1

HR:

hypersensitive reaction

IR:

induced resistance

MeSA:

methyl-salicylates

MON:

moniliformin

PDA:

potato dextrose agar

PAL:

phenylalanine ammonia lyase

POD:

peroxidase

PR:

proteins

ROS:

reactive oxygen species

SA:

salicylic acid

SAG:

salicylic acid glucoside esters

SOD:

superoxide dismutase

SAR:

systemic acquired resistance

TSA:

total content of free and glucoside bound salicylic acid

References

  1. Elmer W.H., Johnson D.A., Mink G.I., Epidemiology and management of the diseases causal to asparagus decline, Plant Dis., 1996, 80, 117–125

    Article  Google Scholar 

  2. Karolewski Z., Waśkiewicz A., Irzykowska L., Bocianowski J., Kostecki M., Goliński P., et al., Fungi presence and their mycotoxins distribution in asparagus spears, Polish J. Environ. Stud., 2011, 20, 911–919

    CAS  Google Scholar 

  3. Waśkiewicz A., Irzykowska L., Karolewski Z., Bocianowski J., Kostecki M., Goliński P., et al., Fusarium spp. and mycotoxins present in asparagus spears, Cereal Res. Comm., 2008, 36SB, 405–408

    Google Scholar 

  4. Waśkiewicz A., Goliński P., Karolewski Z., Irzykowska L., Bocianowski J., Kostecki M., et al., Formation of fumonisins and other secondary metabolites by Fusarium oxysporum and F. proliferatum: a comparative study, Food Add. Contam., 2010, 27, 608–615

    Article  Google Scholar 

  5. Weber Z., Kostecki M., von Bargen S., Gossmann M., Waśkiewicz A., Bocianowski J., et al., Fusarium species colonizing spears and forming mycotoxins in field samples of asparagus from Germany and Poland, J. Phytopathol., 2006, 154, 209–216

    Article  CAS  Google Scholar 

  6. Irzykowska L., Baturo A., Genetic polymorphism of Fusarium culmorum isolates originating from roots and stem bases of barley, J. Plant Prot. Res., 2008, 48, 303–311

    Article  CAS  Google Scholar 

  7. Stępień Ł., Koczyk G., Waśkiewicz A., FUM cluster divergence in fumonisins-producing Fusarium species, Fungal Biol., 2011, 15, 112–123

    Google Scholar 

  8. Stępień Ł., Koczyk G., Waśkiewicz A., Genetic and phenotypic variation of Fusarium proliferatum isolates from different host species, J. Appl. Genet., 2011, 52, 487–496

    Article  PubMed  Google Scholar 

  9. Waśkiewicz A., Stępień Ł., Wilman K., Kachlicki P., Diversity of pea-associated F. proliferatum and F. verticillioides populations revealed by FUM1 sequence analysis and fumonisin biosynthesis, Toxins, 2013, 5, 488–503

    Article  PubMed  Google Scholar 

  10. Seefelder W., Gossman M., Humpf H.U., Analysis of fumonisin B1 in Fusarium proliferatum — infected asparagus spears and garlic bulbs from Germany by liquid chromatography-electrospray ionization mass spectrometry, J. Agr. Food Chem., 2002, 50, 2778–2781

    Article  CAS  Google Scholar 

  11. Waśkiewicz A., Beszterda M., Goliński P., Occurrence of fumonisins in food — an interdisciplinary approach to the problem, Food Control, 2012, 26, 491–499

    Article  Google Scholar 

  12. Marasas W.F.O., Discovery and occurrence of the fumonisins: a historical perspective, Environ. Health Perspect., 2001, 109, 239–243

    PubMed  CAS  Google Scholar 

  13. Ueno Y., Iijima K., Wang S.D., Sugiura Y., Sekijima M., Tanaka T., et al., Fumonisins as a possible contributory risk factor for primary liver cancer: a 3-year study of corn harvested in Haiman, China by HPLC and ELISA, Food Chem. Toxicol., 1997, 35, 1143–1150

    Article  PubMed  CAS  Google Scholar 

  14. Missmer S.A., Suarez L., Felkner M., Wang E., Merrill Jr A.H., Rothman K.J., et al., Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border, Environ. Health Perspect., 2006, 114, 237–241

    Article  PubMed  Google Scholar 

  15. Fincham J.E., Marasas W.F.O., Taljaard J.J., Kriek N.P., Badenhorst C.J., Gelderblom W.C., et al., Atherogenic effects in a non-human primate of Fusarium moniliforme cultures added to a carbohydrate diet, Atherosclerosis, 1992, 94, 13–25

    Article  PubMed  CAS  Google Scholar 

  16. International Agency for Research on Cancer (IARC). Fumonisin B1. IARC Monographs on the evaluation of the carcinogenic risks to humans: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene, IARC, Lyon, France, 2002

    Google Scholar 

  17. Pineda-Valdes G., Bullerman L.B., Thermal stability of moniliformin at varying temperature, pH, and time in an aqueous environment, J. Food Prot., 2000, 63, 1598–1601

    PubMed  CAS  Google Scholar 

  18. Commission of European Communities, Commission recommendation of 17 August, 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding, Offi J Eur Union, 23, L229/7, 2006

    Google Scholar 

  19. Delaney T.P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., et al., A central role of salicylic acid in plant disease resistance, Science, 1994, 266, 1247–1250

    Article  PubMed  CAS  Google Scholar 

  20. Molodchenkova O.O., Adamovskaya V.G., Levitskii Y.A., Gontarenko O.V., Sokolov V.M., Maize response to salicylic acid and Fusarium moniliforme, Appl. Biochem. Microbiol., 2002, 38, 381–385

    Article  CAS  Google Scholar 

  21. Vasyukova N.I., Ozeretskovskaya O.L., Induced plant resistance and salicylic acid: a review, Appl. Biochem. Microbiol., 2007, 43, 367–373

    Article  CAS  Google Scholar 

  22. Enyedi A.J., Yalpani N., Silverman P., Raskin I., Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus, Proc. Nat. Acad. Sci. USA, 1992, 89, 2480–2484

    Article  PubMed  CAS  Google Scholar 

  23. O’Donnell P.J., Jones J.B., Antoine F.R., Cialdi J., Klee H.J., Ethylene-dependent salicylic acid regulates an expended cell death response to a plant pathogen, Plant J., 2001, 25, 315–323

    Article  PubMed  Google Scholar 

  24. Yalpani N., Silverman P., Wilson T.M., Kleier D.A., Raskin I., Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco, Plant Cell, 1991, 3, 809–818

    PubMed  CAS  Google Scholar 

  25. Coquoz J.L., Buchala A., Métraux J.P., The biosynthesis of salicylic acid in potato plants, Plant Physiol., 1998, 117, 1095–1101

    Article  PubMed  CAS  Google Scholar 

  26. Meuwly P., Molders W., Buchala A., Metraux J.P., Local and systemic biosynthesis of salicylic acid in infected cucumber plants, Plant Physiol., 1995, 109, 1107–1114

    PubMed  CAS  Google Scholar 

  27. Pancheva T., Popova L., Uzunova A., Effect of salicylic acid in growth and photosynthesis in barley plants, J. Plant Physiol., 1996, 149, 57–63

    Article  CAS  Google Scholar 

  28. Raskin I., Role of salicylic acid in plants, Ann. Rev. Plant Physiol. Plant Mol. Biol., 1992, 43, 439–462

    Article  CAS  Google Scholar 

  29. Raskin I., Ehmann A., Melander W., Meeuse B., Salicylic acid — a natural inducer of heat production in Arum lilies, Science, 1987, 237, 1545–1556

    Article  Google Scholar 

  30. Klessig D.F., Malamy J., The salicylic acid signal in plants, Plant Mol. Biol., 1994, 26, 1439–1458

    Article  PubMed  CAS  Google Scholar 

  31. Eichhorn H., Klinghammer M., Becht P., Tenhaken R., Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid, J. Exp. Bot., 2006, 57, 2193–2201

    Article  PubMed  CAS  Google Scholar 

  32. Durner J., Klessig D.F., Salicylic acid is a modulator of tobacco and mammalian catalases, J. Biol. Chem., 1996, 271, 28492–28501

    Article  PubMed  CAS  Google Scholar 

  33. Rao M., Paliyath G., Ormrod D., Murr D., Watkins C., Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes, Plant Physiol., 1997, 115, 137–149

    Article  PubMed  CAS  Google Scholar 

  34. Rasmussen J.B., Hammerschmidt R., Zook M.N., Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. Syringae, Plant Physiol., 1991, 97, 1342–1347

    Article  PubMed  CAS  Google Scholar 

  35. Troshina N.B., Yarullina L.G., Valeev A.S., Maksimov I.V., Salicylic acid induces resistance to Septoria nodorum Berk. in wheat, Plant Physiol., 2007, 34, 451–456

    CAS  Google Scholar 

  36. Baker C.J., Orlandi E.W., Active oxygen in plant pathogenesis, Ann. Rev. Phytopathol., 1995, 33, 299–321

    Article  CAS  Google Scholar 

  37. Egan M.J., Talbot N.J., Genomes, free radicals and plant cell invasion: recent developments in plant pathogenic fungi, Curr. Opin. Plant Biol., 2008, 11, 367–372

    Article  PubMed  CAS  Google Scholar 

  38. Hipelli S., Rohnert U., Koske D., Elstner E.F., Schneider W., Free radicals in pathogenesis: health-promoting functions of plant- and milkderived antioxidants, Monatsschr Kinderheilk, 1998, Suppl 1, S63–S72

    Article  Google Scholar 

  39. Bhattacharjee S., Reactive oxygen species and oxidative burst: Roles in stress, senescence and signal transduction in plants, Curr. Sci., 2005, 89, 1113–1121

    CAS  Google Scholar 

  40. Kempe S., Metz H., Mäder K., Application of Electron Paramagnetic Resonance (EPR) spectroscopy and imaging in drug delivery research — chances and challenges, Eur. J. Pharm. Biopharm., 2010, 74, 55–56

    Article  PubMed  CAS  Google Scholar 

  41. Morsy M.A., Khaled M.M., Novel EPR characterization of the antioxidant activity of tea leaves, Spectrochimica Acta Part A, 2002, 58, 1271–1277

    Article  CAS  Google Scholar 

  42. Jonas M., Concepts and methods of ESR dating, Radiat Measur, 1997, 27, 943–973

    Article  CAS  Google Scholar 

  43. Booth C., The Genus Fusarium, CABI, Kew, Surrey, 1971

    Google Scholar 

  44. Gerlach W., Nirenberg H., The genus Fusarium. A Pictorial Atlas, Mitt Biol Bundesanst Land Forstwirtschaft, Berlin-Dahlem, 1982

    Google Scholar 

  45. Kwaśna H., Chełkowski J., Zajkowski P., Fungi (Mycota), XXII., Polish Academy of Sciences, Warsaw, Cracow, 1991

    Google Scholar 

  46. Barnett H.L., Hunter B.B., Illustrated genera of imperfect fungi, APS Press, St. Paul, Minnesota, USA, 1998

    Google Scholar 

  47. Mulè G., Susca A., Stea G., Moretti A., Specific detection of the toxigenic species Fusarium proliferatum and F. oxysporum from asparagus plants using primers based on calmodulin gene sequences, FEMS Microbiol. Lett., 2004, 230, 235–240

    Article  PubMed  Google Scholar 

  48. Mulè G., Susca A., Stea G., Moretti A., Corrigendum to “Specific detection of the toxigenic species Fusarium proliferatum and F. oxysporum from asparagus plants using primers based on calmodulin gene sequences”. [FEMS Microbiol. Lett. 230 (2004) 235–240], FEMS Microbiol. Lett., 2004, 232, 229

    Article  Google Scholar 

  49. Irzykowska L., Bocianowski J., Waśkiewicz A., Weber Z., Karolewski Z., Goliński P., et al., Genetic variation of Fusarium oxysporum isolates forming fumonisin B1 and moniliformin, J. Appl. Genet., 2012, 53, 237–247

    Article  PubMed  CAS  Google Scholar 

  50. Sydenham E.W., Thiel P.G., Marasas W.F.O., Shephard G.S., Van Schalkwyk D.J., Natural occurrence of some Fusarium mycotoxins in com from low and high esophageal cancer prevalent areas of the Transkei, southern Africa, J. Agr. Food Chem., 1990, 38, 1900–1903

    Article  CAS  Google Scholar 

  51. Goliński P., Waśkiewicz A., Wiśniewska H., Kiecana I., Mielniczuk E., Gromadzka K., et al., Reaction of winter wheat (Triticum aestivum L.) cultivars to infection with Fusarium spp.: mycotoxin contamination in grain and chaff, Food Add. Contam., 2010, 27, 1015–1024

    Article  Google Scholar 

  52. Sharman M., Gilbert J., Chełkowski J., A survey of the occurrence of the mycotoxin moniliformin in cereal samples from sources worldwide, Food Add. Contam., 1991, 4, 459–466

    Google Scholar 

  53. Payne R., Murrey D., Harding S., Baird D., Soutou D., Lane P., GenStat for Windows (7th edition) — Introduction, VSN International, Oxford, UK, 2003

    Google Scholar 

  54. He C.Y., Wolyn D.J., Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. Sp. Asparagi, Plant Pathol., 2005, 54, 227–232

    Article  CAS  Google Scholar 

  55. Mandal S., Hazra B., Sarkar R., Biswas S., Mandal N., Hemidesmus indicus, an age old plant: study of its in vitro antioxidant and free radical scavenging potentials, Pharmacologyonline, 2009, 1, 604–617

    Google Scholar 

  56. Borowiak K., Rucińska-Sobkowiak R., Rymer K., Gwóźdź E.A., Zbierska J., Biochemical markers of tropospheric ozone: experimentation with testplants, Polish J. Ecol., 2009, 57, 3–14

    CAS  Google Scholar 

  57. Chong J., Baltz R., Schmitt C., Beffa R., Fritig B., Saindrenan P., Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress and weakens virus resistance, Plant Cell, 2002, 14, 1093–1107

    Article  PubMed  CAS  Google Scholar 

  58. Lee H.I., Leon J., Raskin I., Biosynthesis and metabolism of salicylic acid, Proc. Nat. Acad. Sci. USA, 1995, 92, 4076–4079

    Article  PubMed  CAS  Google Scholar 

  59. Malamy J., Carr J.P., Klessig D.F., Raskin I., Salicylic acid: likely endogenous signal in the resistance response of tobacco to viral infection, Science, 1990, 250, 1002–1004

    Article  PubMed  CAS  Google Scholar 

  60. Malamy J., Klessig D.F., Salicylic acid and plant disease resistance, Plant J., 1992, 2, 643–654

    Article  CAS  Google Scholar 

  61. Mölders W., Buchala A., Métraux J.P., Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants, Plant Physiol., 1996, 112, 787–792

    PubMed  Google Scholar 

  62. Enyedi A.J., Raskin I., Induction of UDP-glucose: salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves, Plant Physiol., 1993, 101, 1375–1380

    PubMed  CAS  Google Scholar 

  63. Hennig J., Malamy J., Grynkiewicz G., Indulski J., Klessig D., Interconversion of the salicylic acid and its glucoside in tobacco, Plant J., 1993, 4, 593–600

    Article  PubMed  CAS  Google Scholar 

  64. Shulaev V., Silverman P., Raskin I., Airborne signaling by methyl salicylate in plant pathogen resistance, Nature, 1997, 385, 718–721

    Article  CAS  Google Scholar 

  65. Prell H.H., Day P., Plant-fungal pathogen interaction, A classical and molecular view, 2001, 214

    Google Scholar 

  66. Edgar C.I., McGrath K.C., Dombrecht B., Manners J.M., Maclean D.J., Schenk P.M.P., et al., Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana, Austr. Plant Pathol., 2006, 35, 581–591

    Article  CAS  Google Scholar 

  67. Abbas H.K., Boyette C.D., Hoagland R.E., Phytotoxicity of Fusarium, other fungal isolates, and of the phytotoxins fumonisin, fusaric acid and moniliformin to jimsonweed, Phytoprotect., 1995, 76, 17–25

    Article  CAS  Google Scholar 

  68. Doehlert D.C., Knutson C.A., Vesonder R.F., Phytotoxic effects of fumonisin B1 on maize seedling growth, Mycopathol., 1994, 127, 117–121

    Article  CAS  Google Scholar 

  69. Van Asch M.A.J., Rijkenberg F.H., Coutinho T.A., Phytotoxicity of fumonisins B1, moniliformin, and T-2 toxin to corn callus cultures, Postharv. Pathol. Mycotox., 1992, 82, 1330–1333

    Google Scholar 

  70. Vesonder R.F., Labeda D.P., Peterson R.E., Phytotoxic activity of selected water-soluble metabolites of Fusarium against Lemna minor L. (Duckweed), Mycopathol., 1992, 118, 185–189

    Article  CAS  Google Scholar 

  71. Schmidt-Heydt M., Magan N., Geisen R., Stress induction of mycotoxin biosynthesis genes by abiotic factors, FEMS Microbiol. Lett., 2008, 228, 142–149

    Article  Google Scholar 

  72. Dellinger B., Lomnicki S., Khachatryan L., Maskos Z., Hall R.W., Adounkpe J., et al., Formation and stabilization of persistent free radicals, Proc Combus Inst, 2007, 31, 521–528

    Article  Google Scholar 

  73. Tian L., Koshland C.P., Yano J., Yachandra V.K., Yu I.T.S., Lee S.C., et al., Carbon-centered free radicals in particulate matter emissions from wood and coal combustion, Energy Fuels, 2009, 23, 2523–2526

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Chemistry, Poznan University of Life Sciences, 60-625, Poznań, Poland

    Agnieszka Waśkiewicz, Kinga Drzewiecka & Piotr Goliński

  2. Department of Phytopathology, Poznan University of Life Sciences, 60-594, Poznań, Poland

    Lidia Irzykowska, Zbigniew Weber & Zbigniew Karolewski

  3. Department of Mathematical and Statistical Methods, Poznan University of Life Sciences, 60-637, Poznań, Poland

    Jan Bocianowski

  4. Medical Physics Division, Faculty of Physics, Adam Mickiewicz University, 61-614, Poznań, Poland

    Bernadeta Dobosz & Ryszard Krzyminiewski

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  1. Agnieszka Waśkiewicz
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  2. Lidia Irzykowska
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Correspondence to Agnieszka Waśkiewicz.

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Waśkiewicz, A., Irzykowska, L., Drzewiecka, K. et al. Plant-pathogen interactions during infection process of asparagus with Fusarium spp.. cent.eur.j.biol. 8, 1065–1076 (2013). https://doi.org/10.2478/s11535-013-0217-6

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