Skip to main content
SpringerLink
Log in

Identification and Toxicological Characterization of Alternaria japonica Strains

  • Published:
Doklady Biological Sciences Aims and scope Submit manuscript

Abstract

Fungi of the genus Alternaria are producers of biologically active compounds. Alternaria japonica is pathogenic to small radish and certain other crucifers, but has not been studied in sufficient detail. Discrepant data on its toxic metabolites are available in the literature, possibly because a limited set of nutritive substrates was used in culturing or species identification of the strains was incorrect. The objectives of this study were to accurately identify the Russian A. japonica strains and to assess the A. japonica toxigenic potential. Four Russian A. japonica strains were identified using a multifaceted approach, which included analyses of morphological characters (the diameter and morphology of colonies grown on the diagnostic media potato carrot agar (PCA) and yeast extract–glucose (YES) agar for one week), the conidial size, and the presence of chlamydospores), the nucleotide sequences of DNA markers (ITS and EF1α regions), and chemotaxonomic data (mycotoxin production). Biomass and extractive substance yields of A. japonica cultures were found to significantly depend on the composition of the liquid medium. Minor differences between the A. japonica strains were detected via metabolite profiling by HPLC/MS-UV. Extracts of A. japonica cultures exerted phytotoxic activity toward small radish leaves and cytotoxicity toward Paramecium caudatum to a level comparable with that of A. tenuissima extracts. Brassicicolin A, dihydrobrassicicolin A, and phomenins A and B, which are known for several species of the genus Alternaria, were identified in A. japonica extracts. Mycotoxins (alternariol, its methyl ether, tentoxin, tenuazonic acid, and altenuene), which are characteristic of the cosmopolitan species A. tenuissima, were not detected in cultures of the A. japonica strains. Extract toxicity and the yield of extractive substances were studied in the A. japonica strains, and strain MFP244011 proved promising as a producer of known and, presumably, new toxins upon culture on the M1D synthetic medium or semisynthetic liquid media (e.g., the Sabouraud medium).

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.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

REFERENCES

  1. Al-lami, H.F.D., You, M.P., and Barbetti, M.J., Incidence, pathogenicity, and diversity of Alternaria spp. associated with Alternaria leaf spot of canola (Brassica napus) in Australia, Plant Pathol., 2018, vol. 68, no. 3, pp. 492‒503.

    Article  Google Scholar 

  2. Al-lami, H.F.D., You, M.P., and Barbetti, M.J., Role of foliage component and host age on severity of Alternaria leaf spot (caused by Alternaria japonica and A. brassicae) in canola (Brassica napus) and mustard (B. juncea) and yield loss in canola, Crop Pasture Sci., 2019a, vol. 70, no. 11, pp. 969‒980.

    Article  Google Scholar 

  3. Al-lami, H.F.D., You, M.P., and Mohammed, A.E., et al., Virulence variability across the Alternaria spp. population determines incidence and severity of Alternaria leaf spot on rapeseed, Plant Pathol., 2019b, vol. 69, no. 3, pp. 506‒517.

    Article  Google Scholar 

  4. Altomare, C., Pernfuss, B., and Strasser, H., Assessing potential cytotoxicity of biocontrol microorganisms using invertebrate assays beneficial microorganisms in agriculture, food and the environment, in Beneficial Microorganisms in Agriculture, Food, and the Environment: Safety Assessment and Regulation, Sundh, I., Wilcks, A., and Goettel, M.S., Eds., Wallingford: CAB Int., 2012, pp. 240‒255.

    Google Scholar 

  5. Andersen, B., Dongo, A., and Pryor, B.M., Secondary metabolite profiling of Alternaria dauci, A. porri, A. solani, and A. tomatophila, Mycol. Res., 2008, vol. 112, no. 2, pp. 241–250.

    Article  CAS  PubMed  Google Scholar 

  6. Andreev, V.A., Andreeva, E.Yu., Erdniyev, L.P., et al., Using the Paramecium caudatum test object to determine acute toxicity of physiologically active substances, Vestn. Voen.-Med. Akad., 2019, vol. 66, no. 2, pp. 110–113.

    Google Scholar 

  7. Berestetskiy, A.O., Dalinova, A.A., Dubovik, V.R., et al., Analysis and isolation of secondary metabolites of Bipolaris sorokiniana by different chromatography techniques and the spectrum of their biological activity, Prikl. Biokhim. Mikrobiol., 2020, vol. 56, no. 5, pp. 483‒496.

    Google Scholar 

  8. Berestetskiy, A.O., Gannibal, Ph.B., Minkovich, E.V., et al., Spectrum of biological activity of the Alternaria fungi isolated from the phyllosphere of herbaceous plants, Microbiology, 2018, vol. 87, no. 6, pp. 806‒816.

    Article  CAS  Google Scholar 

  9. Berestetskiy, A.O., Inyusheva, V.V., Petrova, M.O., et al., Insecticidal, acaricidal, and cytotoxic activity of extracts from some phyllosphere fungi and soil hypocrealean micromycetes, Mikol. Fitopatol., 2019, vol. 53, no. 1, pp. 17‒25.

    Google Scholar 

  10. Blagojević, J.D., Vukojević, J.B., and Ivanović, Ž.S., Occurrence and characterization of Alternaria species associated with leaf spot disease in rapeseed in Serbia, Plant Pathol., 2020, vol. 69, no. 5, pp. 883‒900.

    Article  Google Scholar 

  11. Corlett, M. and Corlett, M.E., Alternaria japonica, Can. J. Plant Pathol., 1999, vol. 21, no. 3, pp. 298–300.

    Article  Google Scholar 

  12. Da Cruz Cabral, L., Rodriguero, M., Stenglein, S., et al., Characterization of small-spored Alternaria from Argentinean crops through a polyphasic approach, Int. J. Food Microbiol., 2017, vol. 257, pp. 206–215.

    Article  PubMed  Google Scholar 

  13. Dalinova, A.A., Salimova, D.R., and Bereste-tskiy, A.O., Alternaria fungi as producers of biologically active compounds and bioherbicides, Prikl. Biohim. Mikrobiol., 2020, vol. 56, no. 3, pp. 223‒241.

    Google Scholar 

  14. Domsch, K.H., Gams, W., and Anderson, T.-H., Compendium of Soil Fungi, Eching: IHW-Verlag, 2007.

  15. Dutta, W., Ray, D., and Ray, P., Molecular characterization and host range studies of indigenous fungus as prospective mycoherbicidal agent of water hyacinth, Indian J. Weed Sci., 2015, vol. 47, no. 1, pp. 59‒65.

    Google Scholar 

  16. Gannibal, Ph.B., Monitoring al’ternariozov sel’sko-khozyaistvennykh kul’tur i identifikatsiya gribov roda Alternaria (Monitoring of Alternarioses of Crops and Identification of Fungi of the Genus Alternaria), VIZR, St. Petersburg: Vseross. Nauchno-Issled. Inst. Zashch. Rast., 2011.

  17. Gannibal, Ph.B., Species of the genus Alternaria revealed in Russia and some neighboring territories, Mikol. Fitopatol., 2015, vol. 49, no. 6, pp. 374‒385.

    Google Scholar 

  18. Gilardi, G., Demarchi, S., Ortu, G., et al., Occurrence of Alternaria japonica on seeds of wild and cultivated rocket, J. Phytopathol., 2014, vol. 163, no. 5, pp. 419–422.

    Article  Google Scholar 

  19. Gilardi, G., Gullino, M.L., and Garibaldi, A., Emerging foliar and soil-borne pathogens of leafy vegetable crops: a possible threat to Europe, EPPO Bull., 2018, vol. 48, no. 1, pp. 116‒127.

    Article  Google Scholar 

  20. Gloer, J.B., Poch, G.K., Short, D.M., et al., Structure of brassicicolin A: A novel isocyanide antibiotic from the phylloplane fungus Alternaria brassicicola, J. Org. Chem., 1988, vol. 53, no. 16, pp. 3758–3761.

    Article  CAS  Google Scholar 

  21. Hu, Z., Sun, W., Li, F., et al., Fusicoccane-derived diterpenoids from Alternaria brassicicola: investigation of the structure-stability relationship and discovery of an IKKB inhibitor, Org. Lett., 2018, vol. 20, no. 17, pp. 5198‒5202.

    Article  CAS  PubMed  Google Scholar 

  22. Iturrieta-González, I., Pujol, I., Iftime, S., et al., Polyphasic identification of three new species in Alternaria section Infectoriae causing human cutaneous infection, Mycoses, 2020, vol. 63, pp. 212–224.

    Article  PubMed  Google Scholar 

  23. Ivanova, L., Petersen, D., and Uhlig, S., Phomenins and fatty acids from Alternaria infectoria, Toxicon, 2010, vol. 55, no. 6, pp. 1107‒1114.

    Article  CAS  PubMed  Google Scholar 

  24. Javaid, A., Khan, I.H., Jabeen, K., et al., Evaluation of mycochemical profile of Alternaria japonica through GC-MS analysis, Pak. J. Phytopathol., 2019, vol. 31, no. 2, pp. 171‒175.

    Google Scholar 

  25. Javaid, A., Mubeen, T., Bashir, U., et al., Management of Parthenium weed using metabolites of Alternaria japonica, Planta Daninha, 2017, vol. 35, p. e017161195.

    Article  Google Scholar 

  26. Kono, Y., Gardner, J.M., and Takeuchi, S., Structure of the host-selective toxins produced by a pathotype of Alternaria citri causing brown spot disease of mandarins, Agr. Biol. Chem., 1986, vol. 50, no. 3, pp. 801‒804.

  27. Liebermann, B., Ellinger, R., Günther, W., et al., Tricycloalternarenes produced by Alternaria alternata related to ACTG-toxins, Phytochemistry, 1997, vol. 46, no. 2, pp. 297‒303.

    Article  CAS  Google Scholar 

  28. Lou, J., Fu, L., Peng, Y., et al., Metabolites from Alternaria fungi and their bioactivities, Molecules, 2013, vol. 18, no. 5, pp. 5891‒5935.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nishikawa, J. and Nakashima, C., Japanese species of Alternaria and their species boundaries based on host range, Plant Fungal Syst., 2020, vol. 5, pp. 197–281.

    CAS  Google Scholar 

  30. Ostry, V., Alternaria mycotoxins: an overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs, World Mycotoxin J., 2008, vol. 1, no. 2, pp. 175‒188.

    Article  CAS  Google Scholar 

  31. Pankova, A.V., Valiullin, L.R., Afordoanyi, D.V., et al., Identification of phytotoxic and phytopathogenic fungi on grains and wheat seedlings, in International Scientific and Practical Conference “AgroSMART—Smart Solutions for Agriculture,” Tyumen, 2018, pp. 759‒765.

  32. Pedras, M.S., Erosa-López, C.C., Quail, J.W., et al., Phomalairdenone: A new host-selective phytotoxin from a virulent type of the blackleg fungus Phoma lingam, Bioorg. Med. Chem. Lett., 1999, vol. 9, no. 23, pp. 3291‒3294.

    Article  CAS  PubMed  Google Scholar 

  33. Pedras, M.S.C. and Yu, Y., Phytotoxins, elicitors and other secondary metabolites from phytopathogenic “blackleg” fungi: Structure, phytotoxicity and biosynthesis, Nat. Prod. Commun., 2009, vol. 4, no. 9, pp. 1291–1304.

    CAS  PubMed  Google Scholar 

  34. Pedras, M.S.C. and Park, M.R., Metabolite diversity in the plant pathogen Alternaria brassicicola: Factors affecting production of brassicicolin A, depudecin, phomapyrone A, and other metabolites, Mycologia, 2015, vol. 107, no. 6, pp. 1138–1150.

    Article  PubMed  Google Scholar 

  35. Pluskal, T., Castillo, S., Villar-Briones, A., et al., MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data, BMC Bioinf., 2010, vol. 11, no. 1, pp. 1‒11.

    Article  Google Scholar 

  36. Rahimloo, T. and Ghosta, Y., The occurrence of Alternaria species on cabbage in Iran, Phytotoaxa, 2015, vol. 102, no. 3, pp. 343‒350.

    Google Scholar 

  37. Schüffler, A., Sterne, O., and Anke, H., Cytotoxic α-pyrones from Xylaria hypoxylon. Z. Naturforsch, C. J. Biosci., 2007, vol. 62, nos. 3‒4, pp. 169‒172.

    Google Scholar 

  38. Scott, J.K., Raphanus raphanistrum L.—wild radish, in Biological Control of Weeds in Australia 1960 to 2010, Julien, M., McFadyen, R., and Cullen, J. Eds., Collingwood: CSIRO Publ., 2012, pp. 486‒492.

    Google Scholar 

  39. Siciliano, I., Ortu, G., Gilardi, G., et al., Mycotoxin production in liquid culture and on plants infected with Alternaria spp. isolated from rocket and cabbage, Toxins, 2015, vol. 7, no. 3, pp. 743‒754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Siciliano, I., Gilardi, G., Ortu, G., et al., Identification and characterization of Alternaria species causing leaf spot on cabbage, cauliflower, wild and cultivated rocket by using molecular and morphological features and mycotoxin production, Eur. J. Plant Pathol., 2017, vol. 149, no. 2, pp. 401–413.

    Article  CAS  Google Scholar 

  41. Sokornova, S.V., Gasich, E.L., Bemova, V.D., et al., Characterization and identification of naturally transgenic species Linaria vulgaris pathogenic micromycetes, Ekol. Genet., 2018, vol. 16, no. 1, pp. 27‒34.

    Article  Google Scholar 

  42. Suemitsu, R., Horiuchi, K., Horiuchi, M., et al., Detection of Tentoxin by Alternaria solani, A. cucumerina, A. bataticola, and A. japonica, Biosci. Biotech. Biochem., 1992, vol. 56, no. 1, pp. 139‒139.

    Article  CAS  Google Scholar 

  43. Tringali, C., Parisi, A., Piattelli, M., et al., Phomenins A and B, bioactive polypropionate pyrones from culture fluids of Phoma tracheiphila, Nat. Prod. Lett., 1993, vol. 3, no. 2, pp. 101‒106.

    Article  CAS  Google Scholar 

  44. Wang, J.T., Ma, Z.H., Wang, G.K., et al., Four meroterpenoids from Alternaria alternata isolated from Paeonia lactiflora, Phytochem. Lett., 2019, vol. 31, pp. 1‒4.

    Article  Google Scholar 

  45. Woudenberg, J.H.C., Groenewald, J.Z., Binder, M., et al., Alternaria redefined, Stud. Mycol., 2013, vol. 75, pp. 171–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are grateful to A.S. Zolotukhina, a student of the St. Petersburg Technological University, for valuable help.

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 19-34-90181).

Author information

Authors and Affiliations

  1. All-Russian Institute of Plant Protection, St. Petersburg, Russia

    D. R. Salimova, S. V. Sokornova, A. S. Orina, F. B. Gannibal & A. O. Berestetskiy

  2. Institute of Hygiene, Occupational Pathology, and Human Ecology, St. Petersburg, Russia

    D. S. Kochura

Authors
  1. D. R. Salimova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. S. Kochura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Sokornova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. S. Orina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. B. Gannibal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. O. Berestetskiy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to D. R. Salimova or D. S. Kochura.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

This article does not contain any studies involving animals or human subjects performed by any of the authors.

Additional information

Translated by T. Tkacheva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Salimova, D.R., Kochura, D.S., Sokornova, S.V. et al. Identification and Toxicological Characterization of Alternaria japonica Strains. Dokl Biol Sci 507, 402–415 (2022). https://doi.org/10.1134/S0012496622060175

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0012496622060175

Keywords:

Search

Navigation