Molecular diagnostics on the toxigenic potential of Fusarium spp. plant pathogens

Journal of Applied Microbiology

Volumn 116, Issue 6, 2014, Pages 1607-1620

  Dawidziuk, A ^a   Koczyk, G ^a   Popiel, D ^a   Kaczmarek, J ^a   Busko M ^b  

^a INSTITUTE OF PLANT GENETICS   (Poland)

^b POZNA UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Fungi; Markers; Mycotoxins; Plant pathology

Indexed keywords

ASSAYS; BIOCHEMISTRY; BIOSYNTHESIS; CHEMICAL DETECTION; COST EFFECTIVENESS; GENES;

BIOSYNTHETIC GENE; FUMONISIN; FUSARIUM; MARKER; MOLECULAR DIAGNOSTICS; PLANT PATHOGEN; PLANT PATHOLOGY; TOXIGENIC; TRICHOTHECENES; ZEARALENONE;

MYCOTOXINS;

FUMONISIN; MYCOTOXIN; TRICHOTHECENE DERIVATIVE; ZEARALANONE;

AGRICULTURAL MANAGEMENT; BIOMARKER; FUNGUS; GENE EXPRESSION; PATHOGEN; PLANT COMMUNITY; POLYMERASE CHAIN REACTION; TAXONOMY;

AGRICULTURAL LAND; ARTICLE; BIOSYNTHESIS; COST EFFECTIVENESS ANALYSIS; CROP PROTECTION; ESSENTIAL GENE; FILAMENTOUS FUNGUS; FUNGAL CONTAMINATION; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; FUSARIUM; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC SCREENING; IN VITRO STUDY; MOLECULAR DIAGNOSTICS; NONHUMAN; PLANT DISEASE; PLANT TAXONOMY; SENSITIVITY AND SPECIFICITY; TAXONOMIC IDENTIFICATION;

FUNGI; MARKERS; MYCOTOXINS; PLANT PATHOLOGY;

FUMONISINS; FUSARIUM; GENES, FUNGAL; POLYMERASE CHAIN REACTION; TRICHOTHECENES; ZEARALENONE;

EID: 84900543062     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12488     Document Type: Article

References (54)

1. Baird, R., Abbas, H.K., Windham, G., Williams, P., Baird, S., Ma, P., Kelley, R., Hawkins, L. et al. (2008) Identification of select fumonisin forming Fusarium species using PCR applications of the polyketide synthase gene and its relationship to fumonisin production in vitro. Int J Mol Sci 9, 554-570.
2. Baker, S.E., Perrone, G., Richardson, N.M., Gallo, A. and Kubicek, C.P. (2012) Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma. Microbiology 158, 147-154.
3. Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. and Sayers, E.W. (2013) GenBank. Nucleic Acids Res 41, D36-D42.
4. Berthiller, F., Crews, C., Dall'Asta, C., Saeger, S.D., Haesaert, G., Karlovsky, P., Oswald, I.P., Seefelder, W. et al. (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57, 165-186.
5. Blaszczyk, L., Popiel, D., Chelkowski, J., Koczyk, G., Samuels, G.J., Sobieralski, K. and Siwulski, M. (2011) Species diversity of Trichoderma in Poland. J Appl Genet 52, 233-243.
6. Brown, D., McCormick, S.P., Alexander, N.J., Proctor, R.H. and Desjardins, A.E. (2001) A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet Biol 32, 121-133.
7. Cardoza, R.E., Malmierca, M.G., Hermosa, M.R., Alexander, N.J., McCormick, S.P., Proctor, R.H., Tijerino, A.M., Rumbero, A. et al. (2011) Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl Environ Microbiol 77, 4867-4877.
8. Chaverri, P., Castlebury, L.A., Samuels, G.J. and Gaiser, D.M. (2003) Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol Phylogenet Evol 27, 302-313.
9. Chelkowski, J., Golka, L. and Stepien, L. (2003) Application of STS markers for leaf rust resistance genes in near-isogenic lines of spring wheat cv. Thatcher. J Appl Genet 44, 323-338.
10. Creppy, E.E., Traoré, A., Baudrimont, I., Cascante, M. and Carratú, M.R. (2002) Recent advances in the study of epigenetic effects induced by the phycotoxin okadaic acid. Toxicology 181-182, 433-439.
11. Dall'Erta, A., Cirlini, M., Dall'Asta, M., Del Rio, D., Galaverna, G. and Dall'Asta, C. (2013) Masked mycotoxins are efficiently hydrolyzed by human colonic microbiota releasing their aglycones. Chem Res Toxicol 26, 305-312.
12. Dawidziuk, A., Kaczmarek, J. and Jedryczka, M. (2012) The effect of winter weather conditions on the ability of pseudothecia of Leptosphaeria maculans and L. biglobosa to release ascospores. Eur J Plant Pathol 134, 329-343.
13. Demeke, T. and Jenkins, G.R. (2010) Influence of DNA extraction methods, PCR inhibitors and quantification methods on real-time PCR assay of biotechnology-derived traits. Anal Bioanal Chem 396, 1977-1990.
14. Desjardins, A.E. and Proctor, R.H. (2007) Molecular biology of Fusarium mycotoxins. Int J Food Microbiol 119, 47-50.
15. D'Mello, D., Mehta, D., Pereira, J. and Rao, C.V. (1999) A toxicity study of simultaneous administration of Tamoxifen and Diazepam to female Wistar rats. Exp Toxicol Pathol 51, 549-553.
16. Doohan, F.M., Parry, D.W., Jenkinson, P. and Nicholson, P. (1998) The use of species-specific PCR-based assays to analyze Fusarium ear blight of wheat. Plant Pathol 47, 197-205.
17. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
18. Evans, N., Baier, A., Semenov, M.A., Gladders, P. and Fitt, B.D.L. (2008) Range and severity of a plant disease increased by global warming. J R Soc Interface 5, 525-531.
19. Flicek, P., Amode, M.R., Barrell, D., Beal, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G. et al. (2012) Ensembl. Nucleic Acids Res 40, D84-D90.
20. Geiser, D.M., del Mar Jiménez-Gasco, M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T.J., Zhang, N., Kuldau, G.A. et al. (2004) FUSARIUM-ID v. 1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110, 473-479.
21. González-Jaén, M.T., Mirete, S., Patiño, B., López-Errasquín, E. and Vázquez, C. (2004) Genetic markers for the analysis of variability and for production of specific diagnostic sequences in fumonisin-producing strains of Fusarium verticillioides. Eur J Plant Pathol 110, 525-532.
22. Gromadzka, K., Chelkowski, J., Popiel, D., Kachlicki, P., Kostecki, M. and Golinski, P. (2009) Solid substrate bioassay to evaluate the effect of Trichoderma and Clonostachys on the production of zearalenone by Fusarium species. World Mycotoxin J 2, 45-52.
23. Hibbett, D.S., Binder, M., Bischoff, J.F., Blackwell, M., Cannon, P.F., Eriksson, O.E., Huhndorf, S., James, T. et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111, 509-547.
24. Jiao, F., Kawakami, A. and Nakajima, T. (2008) Effects of different carbon sources on trichothecene production and Tri gene expression by Fusarium graminearum in liquid culture. FEMS Microbiol Lett 285, 212-219.
25. Kaczmarek, J., Jedryczka, M., Fitt, B.D.L., Lucas, J.A. and Latunde-Dada, A.O. (2009) Analyses of air samples for ascospores of Leptosphaeria maculans and L. biglobosa with light microscopic and molecular techniques. J Appl Genet 50, 411-419.
26. Katoh, K. and Toh, H. (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26, 1899-1900.
27. Kim, Y., Hutmacher, R.B. and Davis, R.M. (2005) Characterization of California isolates of Fusarium oxysporum f. sp. vasinfectum. Plant Dis 4, 366-372.
28. Kimura, M., Tokai, T., O'Donnell, K., Ward, T.J., Fujimura, M., Hamamoto, H., Shibata, T. and Yamaguchi, I. (2003) The trichothecene biosynthesis gene cluster of Fusarium graminearum F15 contains a limited number of essential pathway genes and expressed non-essential genes. FEBS Lett 539, 105-110.
29. Kimura, M., Tokai, T., Takahashi-Ando, N., Ohsato, S. and Fujimura, M. (2007) Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 71, 2105-2123.
30. Kristensen, R., Torp, M., Kosiak, B. and Holst-Jensen, A. (2005) Phylogeny and toxigenic potential is correlated in Fusarium species as revealed by partial translation elongation factor 1 alpha gene sequences. Mycol Res 109, 173-186.
31. Kuhn, M. (2008) Building predictive models in R using the caret package. J Stat Softw 28, 1-26.
32. Leslie, J.F. and Summerell, B.A. (2006) The Fusarium Laboratory Manual. Ames, IA: Blackwell Publishing.
33. Li, Y., Shen, Y., Zhu, X. and Du, L. (2009) Introduction of the AAL-toxin polyketide synthase gene ALT1 into FUM1-disrupted Fusarium verticillioides produces metabolites with the fumonisin methylation pattern. J Nat Prod 72, 1328-1330.
34. Lysøe, E., Bone, K.R. and Klemsdal, S.S. (2009) Real-time quantitative expression studies of the zearalenone biosynthetic gene cluster in Fusarium graminearum. Phytopathology 99, 176-184.
35. Ma, Z. and Michailides, T.J. (2007) Approaches for eliminating PCR inhibitors and designing PCR primers for the detection of phytopathogenic fungi. Crop Prot 26, 145-161.
36. Ma, L.J., van der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.J., Di Pietro, A., Dufresne, M., Freitag, M. et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373.
37. Moretti, A., Susca, A., Mulé, G., Logrieco, A.F. and Proctor, R.H. (2013) Molecular biodiversity of mycotoxigenic fungi that threaten food safety. Int J Food Microbiol 167, 57-66.
38. Mulè, G., Susca, A., Stea, G. and Moretti, A. (2004) A species-specific PCR assay based on the calmodulin partial gene for identification of Fusarium verticillioides, F. proliferatum and F. subglutinans. Eur J Plant Pathol 110, 495-502.
39. O'Donnell, K., Rooney, A.P., Proctor, R.H., Brown, D.W., McCormick, S.P., Ward, T.J., Frandsen, R.J.N., Lysøe, E. et al. (2013) Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet Biol 52, 20-31.
40. Owczarzy, R., Moreira, B.G., You, Y., Behlke, M.A. and Walder, J.A. (2008) Predicting stability of DNA duplexes in solutions containing magnesium and monovalent cations. Biochemistry 47, 5336-5353.
41. Proctor, R.H., Busman, M., Seo, J.A., Lee, Y.W. and Plattner, R.D.A. (2008) Fumonisin biosynthetic gene cluster in Fusarium oxysporum strain O-1890 and the genetic basis for B versus C fumonisin production. Fungal Genet Biol 45, 1016-1022.
42. Proctor, R.H., McCormick, S.P., Alexander, N.J. and Desjardins, A.E. (2009) Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 74, 1128-1142.
43. Proctor, R.H., Van Hove, F., Susca, A., Stea, G., Busman, M., van der Lee, T., Waalwijk, C., Moretti, A. et al. (2013) Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium. Mol Microbiol 90, 290-306.
44. Pruitt, K.D., Tatusova, T., Brown, G.R. and Maglott, D.R. (2012) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 40, D130-D135.
45. Rashmi, R., Ramana, M.V., Shylaja, R., Uppalapati, S.R., Murali, H.S. and Batra, H.V. (2013) Evaluation of a multiplex PCR assay for concurrent detection of four major mycotoxigenic fungi from foods. J Appl Microbiol 114, 819-827.
46. Reeves, C.D., Hu, Z., Reid, R. and Kealey, J.T. (2008) Genes for the biosynthesis of the fungal polyketides hypothemycin from Hypomyces subiculosus and radicicol from Pochonia chlamydosporia. Appl Environ Microbiol 74, 5121-5129.
47. SantaLucia, J. Jr (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc Natl Acad Sci USA 95, 1460-1465.
48. Scauflaire, J., Mahieu, O., Louvieaux, J., Foucart, G., Renard, F. and Munaut, F. (2011) Biodiversity of Fusarium species in ears and stalks of maize plants in Belgium. Eur J Plant Pathol 131, 59-66.
49. Stepien, L., Koczyk, G. and Waskiewicz, A. (2011) FUM cluster divergence in fumonisins-producing Fusarium species. Fungal Biol 115, 112-123.
50. Tag, A.G., Garifullina, G.F., Peplow, A.W., Ake, C. Jr, Phillips, T.D., Hohn, T.M. and Beremand, M.N. (2001) A novel regulatory gene, Tri10, controls trichothecene toxin production and gene expression. Appl Environ Microbiol 67, 5294-5302.
51. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
52. Vegi, A. and Wolf-Hall, C.E. (2013) Multiplex real-time PCR method for detection and quantification of mycotoxigenic fungi belonging to three different genera. J Food Sci 78, M70-M76.
53. Wickham, H. (2009) Ggplot2: Elegant Graphics for Data Analysis. New York: Springer Publishing Company, Incorporated.
54. Zhu, X., Vogeler, C. and Du, L. (2008) Functional complementation of fumonisin biosynthesis in FUM1-disrupted Fusarium verticillioides by the AAL-toxin polyketide synthase gene ALT1 from Alternaria alternata f. sp. lycopersici. J Nat Prod 71, 957-960.