Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2016, Vol. 51, № 3, p. 275-284.

doi: 10.15389/agrobiology.2016.3.275eng

UDC 632.4.01/.08:582.282.192.3:57.065:577.21

Acknowledgements:
Supported by Russian Foundation for Basic Research, project № 15-29-05902.

 

MOLECULAR GENETIC APPROACHES FOR INVESTIGATION OF TAXONOMY AND SPECIFIC IDENTIFICATION OF TOXIN-PRODUCING Fusarium SPECIES: ACHIEVEMENTS AND PROBLEMS (review)

A.A. Stakheev1, L.V. Samokhvalova1, D.Yu. Ryazantsev1, S.K. Zavriev1,2

1M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Federal Agency of Scientific Organizations, 16/10, ul. Miklukho-Maklaya, Moscow, 117997 Russia, e-mail samokhlar@mail.ru, d.yu.ryazantsev@gmail.com, stakheev.aa@gmail.com;
2All-Russian Research Institute of Phytopathology, Federal Agency of Scientific Organizations, 5, Institute, pos. Bol’shie Vyazemy, OdintsovskiiRegion,Moscow Province, 143050 Russia, e-mail szavriev@ibch.ru

Received January 13, 2015

 

Ascomycetous fungi of the genus Fusarium, which was separated as a single taxonomic group in 1809 by Heinrich Friedrich Link, are distributed worldwide and have different ecological niches. They have been found in soil and plants as endophytes, saprotrophs and parasites. Infections of agricultural plants, caused by Fusarium fungi, lead to annual damage, estimated in hundred million dollars. In addition to decrease harvest quality and quantity, Fusarium fungi are able to produce toxic metabolites (fusariotoxins). The consumption of fusariotoxin-contaminated winter grain led to deaths of tens of thousands of people in Volga and Ural regions in 1930s-1940s. These factors make necessary investigation of morphology, biochemistry and genetics of those organisms. Nowadays there is no universal taxonomic system of the genus Fusarium, so it is not possible to identify an isolate to species level in many cases. The high variability of morphological structures, and, on the other side, their similarity for closely related species, are major problems for researchers which use classical methods for identification and systematization of this group of fungi. Today, the molecular methods, based on the use of specific DNA sequence, are playing an increasingly important role in Fusarium systematics. The application of this approach has led to establishment of a number of new species in the genus. T. Yli-Mattila et al. (2009, 2011) used multilocus phylogenetic analysis to describe the novel species F. sibiricum and F. ussurianum which were found in Siberia and Far East and proved to be morphologically similar to F. graminearum and F. langsethiae, respectively. The authors of this paper identified the species F. torulosum (morphologically similar to F. avenaceum) in Russia for the first time based on the use of DNA markers. It is no less important that the analysis of inter- and intraspecific polymorphism makes possible the development of highly-specific assays for molecular detection of Fusarium fungi, including ones which infect plants and produce mycotoxins. The use of these assays (for example, ones described by M. Nicolaisen et al., 2009 and A.A. Stakheev et al., 2011) allows not only to detect the contamination of plants by mycotoxin producers, but also to estimate the quantity of their content in a probe. At the same time, a lot of questions are still unanswered: particularly, simultaneous application of different species concepts (morphological, biological and phylogenetic) makes it difficult to develop universal taxonomic system of the genus; also the most informative and reliable marker, which would reflect the evolutionary history of the genus, has not been found. The main achievements and problems of Fusarium phylogenetics, and perspectives of the application of molecular approach for studies of this group of organisms are discussed in this review.

Keywords: genus Fusarium, taxonomy, DNA marker, mycotoxins, phylogenetic analysis.

 

Full article (Rus)

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REFERENCES

  1. Nelson P.E. History of Fusarium systematics. Phytopathology, 1991, 81(9): 1045-1048.
  2. Nelson P.E., Dignani M.C., Anaissie E.J. Taxonomy, biology, and clinical aspects of Fusarium species. Clin. Microbiol. Rev., 1994, 7(4): 479-504 CrossRef
  3. Leslie J.F., Summerell B.A. The Fusarium laboratory manual. Blackwell Publishing, 2006.
  4. Snyder W.C., Hansen H.N. Variation and speciation in the genus Fusarium. Annals of the New York Academy of Sciences, 1954, 60: 16-23.
  5. Gerlach W. The present concept of Fusarium classification. Pennsylvania State University Press, 1981.
  6. Gagkaeva T.Yu., Gavrilova O.P., Levitin M.M., Novozhilov K.V. Zashchita i karantin rastenii, 2011, 5: 69-120 (in Russ.).
  7. Dobzhnsky T. Mendelian populations and their evolution. American Naturalist, 1950, 84(9): 401-418.
  8. Mayr E. Animal species and evolution. Harvard University Press, 1963.
  9. Britz H., Coutinho T.A., Wingfield M.J., Marasas W.F.O., Gordon T.R., Leslie J.F. Fusarium subglutinans f. sp. pini represents a distinct mating population in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol., 1999, 65(3): 1198-1201.
  10. Proctor R.H., Brown D.W. Fusarium: genomics, molecular and cellular biology. Caister Academic Press, 2013.
  11. Leslie J.F. Mating populations in Gibberella fujikuroi. Phytopathology, 1991, 81: 1058-1060.
  12. Leslie J.F. Gibberella fujikuroi: available populations and variable traits. Can. J. Bot., 1995, 73(Suppl. 1): S282-S291 CrossRef
  13. Leslie J.F. Genetic status of the Gibberella fujikuroi species complex. Plant Pathol. J., 1999, 15: 259-269.
  14. Harrington T.C., Rizzo D.M. Defining species in the fungi. In: Structure and dynamics of fungal populations. J.J. Worrall (ed.). Kluwer Academic Publishers, 1999.
  15. Stakheev A.A., Ryazantsev D.Yu., Zavriev S.K. Bioorganicheskaya khimiya, 2011, 37(5): 662-671 (in Russ.) CrossRef
  16. Turner A.S., Lees A.K., Rezanoor H.N., Nicholson P. Refinement of PCR-detection of Fusarium avenaceum and evidence from DNA marker studies for phonetic relatedness to Fusarium tricinctum. Plant Pathol., 1998, 47: 278-288 CrossRef
  17. Nirmaladevi D., Venkataramana M., Srivastava R.K., Uppalapati S.R., Gupta V.K., Yli-Mattila T., Tsui K.M.C., Srinivas C., Niranjana S.R., Chandra N.S. Molecular phylogeny, pathogenicity and toxigenicity of Fusarium oxysporum f. sp. lycopersici. Sci. Rep., 2016,6: 21367 CrossRef
  18. Jurgenson J.E., Bowden R.L., Zeller K.A., Leslie J.F., Alexander N.J., Plattner R.D. A genetic map of Gibberella zeae (Fusarium graminearum). Genetics, 2002, 160: 1452-1460.
  19. Zeller K.A., Bowden R.L., Leslie J.F. Diversity of epidemic populations of Gibberella zeae from small quadrats in Kansas and North Dakota. Phytopathology, 2003, 93: 874-880 CrossRef
  20. Paran I., Michelmore R.W. Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor. Appl. Genet., 1993, 85: 985-993 CrossRef
  21. Crespo A., Lumbsch H.T. Cryptic species in lichen-forming fungi. IMA Fungus, 2010, 1(2): 167-170.
  22. Taylor J.W., Turner E., Pringle A. Fungal species: thoughts on their recognition, maintenance and selection. In: Fungi in the environment. G.M. Gadd, S.C. Watkinson, P.S. Dyer (eds.). Cambridge University Press, 2007.
  23. Taylor J.W., Jacobson D.J., Kroken S., Kasuga T., Geiser D.M., Hibbert D.S., Fisher M.C. Phylogenetic species recognition and species concepts in fungi. Fung. Genet. Biol., 2000, 31: 21-32 CrossRef
  24. Shneer V.S. Zhurnal obshchei biologii, 2009, 70(4): 296-315 (in Russ.).
  25. Schoch C.L., Seifert K.A., Huhndorf S., Robert V., Spouge J.L., Leves-
    que C.A., Chen W., Fungal Barcoding Consortium. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS, 2012, 109: 6241-6246 CrossRef
  26. Harrow S.A., Farrokhi-Nejad R., Pitman A.R., Scott I.A.W., Bentley A., Hide C., Cromey M.G. Characterization of New Zealand Fusarium populations using a polyphasic approach differentiates the F. avenaceum/F.acuminatum/F.tricinctum species complex in cereal and grassland systems. Fungal Biology, 2010, 114: 293-311 CrossRef
  27. Geiser D.M., Klich M.A., Frisvad J.C., Peterson S.W., Varga J., Samson R.A. The current status of the species recognition and identification in Aspergillus. Stud. Mycol., 2007, 59: 1-10 CrossRef
  28. Seifert K.A., Samson R.A., deWaard J.R. Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. PNAS USA, 2007, 104: 3901-3906 CrossRef
  29. Aveskamp M.M., de Gruyter J., Woudenberg J.H.C. Highlights of the Didymellaceae: a polyphasic approach to characterize Phoma and related pleosporalean genera. Stud. Mycol., 2010, 65: 1-60 CrossRef
  30. Kristensen R., Torp M., Kosiak B., Holst-Jensen A. Phylogeny and toxigenic potential is correlated in Fusarium species as revealed by partial translation elongation factor 1 alpha gene sequences. Mycol. Res., 2005, 109: 173-186 CrossRef
  31. Yli-Mattila T., Paavanen-Huhtala S., Bulat S.A., Alekhina I.A., Nirenberg H.I. Molecular, morphological and phylogenetic analysis of the Fusarium avenaceum/F. arthrosporioides/F. tricinctum species complex — a polyphasic approach. Mycol. Res., 2002, 106(6): 655-669 CrossRef
  32. Stakheev A.A., Khairulina D.R., Zavriev S.K. Four-locus phylogeny of Fusarium avenaceum and related species and their species-specific identification based on partial phosphate permease gene sequences. Int. J. Food Microbiol., 2016, 225: 25-37 CrossRef
  33. Yli-Mattila T., Ward T.J., O’Donnell K., Proctor R.H., Burkin A.A., Kononenko G.P., Gavrilova O.P., Aoki T., McCormick S.P., Gagkaeva T.Y. Fusarium sibiricum sp. nov, a novel type A trichothecene-producing Fusarium from northern Asia closely related to F. sporotrichioides and F. langsethiae. Int. J. Food Microbiol., 2011, 147: 58-68 CrossRef
  34. Fernández-Ortuño D., Loza-Reyes E., Atkins S.L., Fraaije B.A. The CYP51C gene, a reliable marker to resolve interspecific phylogenetic relationships within the Fusarium species complex and a novel target for species-specific PCR. Int. J. Food Microbiol., 2010, 144: 301-309 CrossRef
  35. Watanabe M., Yonezava T., Lee K-I., Kumagai S., Sugita-Konishi Y., Goto K., Hara-Kudo Y. Evaluation of genetic markers for identifying isolates of the species of the genus Fusarium. J. Sci. Food Agr., 2011, 91: 2500-2504 CrossRef
  36. Watanabe M., Yonezava T., Lee K-I., Kumagai S., Sugita-Konishi Y., Goto K., Hara-Kudo Y. Molecular phylogeny of the higher and lower taxonomy of the Fusarium genus and differences in the evolutionary histories of multiple genes. BMC Evol. Biol., 2011, 11: 322 CrossRef
  37. Llorens A., Hinojo M.J., Mateo R., Gonsales-Jaen M.T., Valle-Algarra F.M., Logriecco A., Jimenez M. Characterization of Fusarium spp. isolates by PCR-RFLP analysis of the rRNA gene (rDNA). Int. J. Food Microbiol., 2006, 106: 297-306 CrossRef
  38. Yli-Mattila T., Paavanen-Huhtala S., Parikka P., Konstantinova P., Gagkaeva T.Y. Molecular and morphological diversity of Fusarium species in Finland and north-western Russia. Eur. J. Plant Pathol., 2004, 110: 573-585 CrossRef
  39. Geiser D.M., Jimenes-Gasco M., Kang S., Makalowska I., Veeraraghavan N., Ward T.J., Zhang N., Kuldau G.A., O’Donnell K. FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur. J. Plant Pathol., 2004, 110: 473-479 CrossRef
  40. Scott J.B., Chakraborty S. Multilocus sequence analysis of Fusarium pseudograminearum reveals a single phylogenetic species. Mycol. Res., 2006, 110: 1413-1425 CrossRef
  41. Obanor F., Erginbas-Orakci G., Tunali B., Nicol J.M., Chakraborty S. Fusarium culmorum is a single phylogenetic species based on multilocus sequence analysis. Fungal Biol., 2010, 114: 753-765 CrossRef
  42. Kulik T., Pszczolkowska A., Lojko M. Multilocus phylogenetics show high intraspecific variability within Fusarium avenaceum. Int. J. Mol. Sci., 2011, 12: 5626-5640 CrossRef
  43. O’Donnell K., Sutton D.A., Rinaldi M.G., Gueidan C., Crous P.W., Geiser D.M. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. J. Clin. Microbiol., 2009, 47: 3851-3861 CrossRef
  44. Yli-Mattila T., Gagkaeva T., Ward T.J., Aoki T., Kistler H.C., O’Donnell K. A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from Russian Far East. Mycologia, 2009, 101(6): 841-852 CrossRef
  45. O’Donnell K., Ward T.J., Geiser D.M., Kistler H.C., Aoki T. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol., 2004, 41: 600-623 CrossRef
  46. Marín P., Moretti A., Ritieni A., Jurado M., Vázquez C., Gonzalez Jaén M.T. Phylogenetic analyses and toxigenic profiles of Fusarium equiseti and Fusarium acuminatum from cereals from Southern Europe. Food Microbiol., 2012, 31: 229-237 CrossRef
  47. Gagkaeva T.Yu., Gavrilova O.P., Stakheev A.A., Ryazantsev D.Yu., Zavriev S.K. Mikologiya i fitopatologiya, 2012, 46: 86-91 (in Russ.).
  48. Booth C. The genus Fusarium. Commonwealth Mycological Institute, 1971.
  49. Gerlach W., Nirenberg H.I. The genus Fusarium — a pictorial atlas. Mitt. Biol. Bundesanst Land-u Forstwirsch Berlin-Dahlem, 1982.
  50. Nelson P.E., Toussoun T.A., Marasas W.F.O. Fusarium species: an illustrated manual for identification. Pennsylvania State University Press, 1983.
  51. Jestoi M. Emerging Fusarium mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin — a review. Critical Reviews in Food Science and Nutrition, 2008, 48: 21-49 CrossRef
  52. Fernández-Ortuño D., Waalwijk C., Van der Lee T., Fan J., Atkins S., West J.S., Fraaije B.A. Simultaneous real-time PCR detection of Fusarium asiaticum, F. ussurianum and F. vorosii, representing the Asian clade of the F. graminearum species complex. Int. J. Food Microbiol., 2013, 166: 148-154 CrossRef
  53. Fredlund E., Gidlund A., Sulyok M., Börjesson T., Krska R., Olsen M., Lindblad M. Deoxynivalenol and other selected Fusarium toxins in Swedish oats — occurrence and correlation to specific Fusarium species. Int. J. Food Microbiol., 2013, 167: 276-283 (dx.doi.org/10.1016/j.ijfoodmicro.2013.06.026) CrossRef
  54. Jurado M., Vazquez C., Marin S., Sanchis V., Tereza Ganzalez-Jaen M. PCR-based strategy to detect contamination with mycotoxigenic Fusarium species in maize. Syst. Appl. Microbiol., 2006, 29: 681-689 CrossRef
  55. Kulik T. Detection of Fusarium tricinctum from cereal grain using PCR assay. J. Appl. Genet., 2008, 49: 305-311 CrossRef
  56. Kulik T., Jestoi M. Quantification of Fusarium poae DNA and associated mycotoxins in asymptomatically contaminated wheat. Int. J. Food Microbiol., 2009, 130: 233-237 CrossRef
  57. Nicolaisen M., Suproniene S., Nielsen L.K., Lazzaro I., Spliid N.H., Justesen A.F. Real-time PCR for quantification of eleven individual Fusarium species in cereals. J. Microbiol. Meth., 2009, 76: 234-240 CrossRef
  58. Niessen M.L., Vogel R.F. Group-specific PCR detection of potential trichothecene-producing Fusarium species in pure cultures and cereal samples. Syst. Appl. Microbiol., 1998, 21: 618-631 CrossRef
  59. Stakheev A.A., Ryazantsev D.Yu., Gagkaeva T.Yu., Zavriev S.K. PCR detection of Fusarium fungi with similar profiles of the produced mycotoxins. Food Control, 2011, 22: 462-468 CrossRef
  60. Yli-Mattila T., Paavanen-Huhtala S., Parikka P., Jestoi M., Klemsdal S.S., Rizzo A. Genetic variation, real-time PCR, metabolites and mycotoxins of Fusarium avenaceum and related species. Mycotoxin Res., 2006, 2: 79-86 CrossRef
  61. Ryazantsev D.Yu., Abramova S.L., Evstratova S.V., Gagkaeva T.Yu., Zavriev S.K.. Bioorganicheskaya khimiya, 2008, 34(6): 799-807 (in Russ.) CrossRef
  62. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem., 2009, 55: 611-622 CrossRef
  63. Niessen L., Grafenhan T., Vogel R.F. ATP citrate lyase 1 (acl1) gene-based loop-mediated amplification assay for the detection of the Fusarium tricinctum species complex in pure cultures and in cereal samples. Int. J. Food Microbiol., 2012, 158: 171-185 CrossRef
  64. Notomi T., Okayama H., Masubuchi H., Yonekawa T., Watanabe K., Amino N., Hase T. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res., 2000, 28: e63.

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