Development of a hydrolysis probe-based real-time assay for the detection of tropical strains of Fusarium oxysporum f. Sp. Cubense race 4

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Aguayo, Jaime ^a   Mostert, Diane ^b   Fourrier Jeandel, Céline ^a   Cerf Wendling, Isabelle ^a   Hostachy, Bruno ^a   Viljoen, Altus ^b   Ioos, Renaud ^a  

^a FRENCH AGENCY FOR FOOD   (France)

^b STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; DNA PROBE; SPACER DNA;

ACCURACY; ARTICLE; BANANA; CONTROLLED STUDY; FUNGAL GENE; FUSARIUM OXYSPORUM; HYDROLYSIS; MEASUREMENT REPEATABILITY; MUSA AAA GROUP; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SPECIES INTRODUCTION; STRAIN IDENTIFICATION; VALIDATION STUDY; VIRULENCE GENE; ANALYSIS OF VARIANCE; CLASSIFICATION; DNA PROBE; FUSARIUM; GENETICS; MICROBIOLOGY; MUSA; PLANT DISEASE; PROCEDURES; REPRODUCIBILITY;

ANALYSIS OF VARIANCE; DNA PROBES; DNA, FUNGAL; DNA, INTERGENIC; FUSARIUM; MUSA; PLANT DISEASES; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 85012217318     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171767     Document Type: Article

References (68)

1. Fraser-Smith S, Czislowski E, Meldrum RA, Zander M, O'Neill W, Balali GR, et al. Sequence variation in the putative effector gene SIX8 facilitates molecular differentiation of Fusarium oxysporum f. Sp. Cubense. Plant Pathology. 2014; 63(5):1044-52.
2. Fourie G, Steenkamp ET, Ploetz RC, Gordon TR, Viljoen A. Current status of the taxonomic position of Fusarium oxysporum formae specialis cubense within the Fusarium oxysporum complex. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2011; 11(3):533-42. Epub 2011/01/25. doi: 10.1016/j.meegid.2011.01.012 PMID: 21256980
3. Ploetz RC. Fusarium Wilt of Banana Is Caused by Several Pathogens Referred to as Fusarium oxysporum f. Sp. Cubense. Phytopathology. 2006; 96(6):653-6. doi: 10.1094/PHYTO-96-0653 PMID: 18943184
4. Ploetz RC. Management of Fusarium wilt of banana: A review with special reference to tropical race 4. Crop Protection. 2015;(0).
5. Chen Q, Li B, Liu P, Lan C, Zhan Z, Weng Q. Development and evaluation of specific PCR and LAMP assays for the rapid detection of Phytophthora melonis. European Journal of Plant Pathology. 2013; 137(3):597-607.
6. Pocasangre LE, Ploetz RC, Molina AB, Vicente LP. Raising awareness of the threat of Fusarium wilt tropical race 4 in Latin America and the Caribbean. 2011;(897):331-7.
7. Butler D. Fungus threatens top banana. Nature. 2013; 504(7479):195-6. doi: 10.1038/504195a PMID: 24336262
8. Li M, Shi J, Xie X, Leng Y, Wang H, Xi P, et al. Identification and application of a unique genetic locus in diagnosis of Fusarium oxysporum f. Sp. Cubense tropical race 4. Canadian Journal of Plant Pathology. 2013; 35(4):482-93.
9. Fourie G, Steenkamp ET, Gordon TR, Viljoen A. Evolutionary relationships among the Fusarium oxysporum f. Sp. Cubense vegetative compatibility groups. Applied and environmental microbiology. 2009; 75(14):4770-81. Epub 2009/06/02. PubMed Central PMCID: PMC2708428. doi: 10.1128/AEM.00370-09 PMID: 19482953
10. Dita MA, Waalwijk C, Buddenhagen IW, Souza MT Jr, Kema GHJ. A molecular diagnostic for tropical race 4 of the banana fusarium wilt pathogen. Plant Pathology. 2010; 59(2):348-57.
11. Ploetz R, Correll J. Vegetative compatibility among races of Fusarium oxysporum f. Sp. Cubense. Plant Disease. 1988; 72(4):325-8.
12. Ghag SB, Shekhawat UKS, Ganapathi TR. Fusarium wilt of banana: biology, epidemiology and management. International Journal of Pest Management. 2015; 61(3):250-63.
13. Li C, Mostert G, Zuo C, Beukes I, Yang Q, Sheng O, et al. Diversity and distribution of the banana wilt pathogen Fusarium oxysporum f. Sp. Cubense in China. Fungal Genomics & Biology. 2013.
14. Groenewald S, Van Den Berg N, Marasas WFO, Viljoen A. The application of high-throughput AFLP's in assessing genetic diversity in Fusarium oxysporum f. Sp. Cubense. Mycological research. 2006; 110 (3):297-305.
15. Ordonez N, Seidl MF, Waalwijk C, Drenth A, Kilian A, Thomma BPHJ, et al. Worse Comes to Worst: Bananas and Panama Disease-When Plant and Pathogen Clones Meet. PLoS pathogens. 2015; 11 (11):e1005197. doi: 10.1371/journal.ppat.1005197 PMID: 26584184
16. Koenig RL, Ploetz RC, Kistler HC. Fusarium oxysporum f. Sp. Cubense consists of a small number of divergent and globally distributed clonal lineages. Phytopathology. 1997; 87(9):915-23. Epub 2008/10/ 24. doi: 10.1094/PHYTO.1997.87.9.915 PMID: 18945062
17. García-Bastidas F, Ordóñez N, Konkol J, Al-Qasim M, Naser Z, Abdelwali M, et al. First Report of Fusarium oxysporum f. Sp. Cubense Tropical Race 4 Associated with Panama Disease of Banana outside Southeast Asia. Plant Disease. 2013; 98(5):694-.
18. Ordonez N, Garcia FA, Laghari H, Akkary M, Harfouche EN, Al Awar BN, et al. First report of Fusarium oxysporum f. Sp. Cubense tropical race 4 causing Panama disease in Cavendish bananas in Pakistan and Lebanon. Plant Disease. 2015.
19. Daniells J, O'Neill W, Hermanto C, Ploetz R. Banana Varieties and Fusarium oxysporum f. Sp. Cubense in Indonesia-Observations from Fusarium Wilt Disease Databases. Acta horticulturae. 2011; (897):475.
20. Ploetz RC. Panama disease, an old nemesis rears its ugly head: part 2, the cavendish era and beyond. Plant Health Progress. 2006.
21. Molina A, Williams R, Hermanto C, Suwanda M, Komolong B, Kokoa P. Mitigating the threat of banana Fusarium wilt: understanding the agroecological distribution of pathogenic forms and developing disease management strategies. Australia: ACIAR, GPO Box. 2010; 1571:2010-12.
22. Kema GHJ, Weise S. Pathogens: Appeal for funds to fight banana blight. Nature. 2013; 504(7479):218.
23. Pérez-Vicente L, Dita MA, Martínez-de la Parte E. Technical Manual. Prevention and diagnostic of Fusarium Wilt (Panama disease) of banana caused by Fusarium oxysporum f. Sp. Cubense Tropical Race 4 (TR4). Rome, Italy: FAO, 2014.
24. Ploetz RC, Kema GHJ, Ma L-J. Impact of Diseases on Export and Smallholder Production of Banana. Annual Review of Phytopathology. 2015; 53(1):null.
25. EPPO. PM 7/76 (2): Use of EPPO diagnostic protocols. EPPO Bulletin. 2010; 40(3):350-2.
26. Lin Y-H, Su C-C, Chao C-P, Chen C-Y, Chang C-J, Huang J-W, et al. A molecular diagnosis method using real-time PCR for quantification and detection of Fusarium oxysporum f. Sp. Cubense race 4. European Journal of Plant Pathology. 2013; 135(2):395-405.
27. Lin Y-H, Chang J-Y, Liu E-T, Chao C-P, Huang J-W, Chang P-F. Development of a molecular marker for specific detection of Fusarium oxysporum f. Sp. Cubense race 4. European Journal of Plant Pathology. 2009; 123(3):353-65.
28. Li B, Du J, Lan C, Liu P, Weng Q, Chen Q. Development of a loop-mediated isothermal amplification assay for rapid and sensitive detection of Fusarium oxysporum f. Sp. Cubense race 4. European Journal of Plant Pathology. 2013; 135(4):903-11.
29. Yang L-L, Sun L-X, Ruan X-L, Qiu D-Y, Chen D-H, Cai X-Q, et al. Development of a single-tube duplex real-time fluorescence method for the rapid quantitative detection of Fusarium oxysporum f. Sp. Cubense race 1 (FOC1) and race 4 (FOC4) using TaqMan probes. Crop Protection. 2015; 68(0):27-35.
30. Peng J, Zhang H, Chen F, Zhang X, Xie Y, Hou X, et al. Rapid and quantitative detection of Fusarium oxysporum f. Sp. Cubense race 4 in soil by real-time fluorescence loop-mediated isothermal amplification. Journal of Applied Microbiology. 2014; 117(6):1740-9. doi: 10.1111/jam.12645 PMID: 25200557
31. Zhang X, Zhang H, Pu J, Qi Y, Yu Q, Xie Y, et al. Development of a Real-Time Fluorescence Loop-Mediated Isothermal Amplification Assay for Rapid and Quantitative Detection of Fusarium oxysporum f. Sp. Cubense Tropical Race 4 In Soil. PloS one. 2013; 8(12):e82841. Epub 2014/01/01. PubMed Central PMCID: PMC3869718. doi: 10.1371/journal.pone.0082841 PMID: 24376590
32. Dita MA, Waalwijk C, Mutua P, Daly A, Chang PFL, Corcolon BM, et al. Detecting Fusarium oxysporum f. Sp. Cubense tropical race 4 in soil and symptomless banana tissues. 2013;(986):127-30.
33. Boonham N, Glover R, Tomlinson J, Mumford R. Exploiting generic platform technologies for the detection and identification of plant pathogens. In: Collinge D, Munk L, Cooke BM, editors. Sustainable disease management in a European context: Springer Netherlands; 2008. p. 355-63.
34. Gachon C, Mingam A, Charrier B. Real-time PCR: what relevance to plant studies? Journal of experimental botany. 2004; 55(402):1445-54. doi: 10.1093/jxb/erh181 PMID: 15208338
35. Lievens B, Brouwer M, Vanachter ACRC, Cammue BPA, Thomma BPHJ. Real-time PCR for detection and quantification of fungal and oomycete tomato pathogens in plant and soil samples. Plant Science. 2006; 171:155-65.
36. Schaad NW, Frederick RD. Real-time PCR and its application for rapid plant disease diagnostics. Canadian Journal of Plant Pathology. 2002; 24(3):250-8.
37. Harper SJ, Ward LI, Clover GRG. Development of LAMP and Real-Time PCR Methods for the Rapid Detection of Xylella fastidiosa for Quarantine and Field Applications. Phytopathology. 2010; 100 (12):1282-8. doi: 10.1094/PHYTO-06-10-0168 PMID: 20731533
38. Lievens B, Rep M, Thomma BPHJ. Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. Pest management science. 2008; 64(8):781-8. doi: 10.1002/ps.1564 PMID: 18335459
39. McTaggart AR, van der Nest MA, Steenkamp ET, Roux J, Slippers B, Shuey LS, et al. Fungal Genomics Challenges the Dogma of Name-Based Biosecurity. PLoS pathogens. 2016; 12(5):e1005475. doi: 10.1371/journal.ppat.1005475 PMID: 27149511
40. van Dam P, Fokkens L, Schmidt SM, Linmans JHJ, Kistler HC, Ma L-J, et al. Effector profiles distinguish formae speciales of Fusarium oxysporum. Environmental Microbiology. 2016:n/a-n/a.
41. Does HCvd, Lievens B, Claes L, Houterman PM, Cornelissen BJC, Rep M. The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environmental Microbiology. 2008; 10(6):1475-85. doi: 10.1111/j.1462-2920.2007.01561.x PMID: 18312397
42. Lievens B, Houterman PM, Rep M. Effector gene screening allows unambiguous identification of Fusarium oxysporum f. sp. lycopersici races and discrimination from other formae speciales. FEMS microbiology letters. 2009; 300(2):201-15. doi: 10.1111/j.1574-6968.2009.01783.x PMID: 19799634
43. de Sousa MV, Machado JdC, Simmons HE, Munkvold GP. Real-time quantitative PCR assays for the rapid detection and quantification of Fusarium oxysporum f. sp. phaseoli in Phaseolus vulgaris (common bean) seeds. Plant Pathology. 2014:n/a-n/a.
44. Sutherland R, Viljoen A, Myburg AA, Berg Nvd. Pathogenicity associated genes in Fusarium oxysporum f. Sp. Cubense race 4. South African Journal of Science. 2013; 109(5/6):61-70.
45. Besseris GJ. A Fast-and-Robust Profiler for Improving Polymerase Chain Reaction Diagnostics. PloS one. 2014; 9(9):e108973. doi: 10.1371/journal.pone.0108973 PMID: 25269015
46. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. 1990; 18(1):315-22.
47. Ioos R, Fourrier C, Iancu G, Gordon TR. Sensitive Detection of Fusarium circinatum in Pine Seed by Combining an Enrichment Procedure with a Real-Time Polymerase Chain Reaction Using Dual-Labeled Probe Chemistry. Phytopathology. 2009; 99(5):582-90. doi: 10.1094/PHYTO-99-5-0582 PMID: 19351254
48. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004; 32(5):1792-7. doi: 10.1093/nar/gkh340 PMID: 15034147
49. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3-new capabilities and interfaces. Nucleic Acids Research. 2012; 40(15):e115. doi: 10.1093/nar/gks596 PMID: 22730293
50. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC bioinformatics. 2012; 13(1):1-11.
51. Ballantyne KN, van Oorschot RA, Mitchell RJ. Reduce optimisation time and effort: Taguchi experimental design methods. Forensic Science International: Genetics Supplement Series. 2008; 1(1):7-8.
52. Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, et al. Package 'car'. 2015.
53. EPPO. PM 7/98 (1): Specific requirements for laboratories preparing accreditation for a plant pest diagnostic activity. EPPO Bulletin. 2010; 40(1):5-22.
54. Arzanlou M, Abeln ECA, Kema GHJ, Waalwijk C, Carlier J, Vries Id, et al. Molecular Diagnostics for the Sigatoka Disease Complex of Banana. Phytopathology. 2007; 97(9):1112-8. doi: 10.1094/PHYTO-97-9-1112 PMID: 18944176
55. Bentley S, Pegg KG, Moore NY, Davis RD, Buddenhagen IW. Genetic Variation Among Vegetative Compatibility Groups of Fusarium oxysporum f. Sp. Cubense Analyzed by DNA Fingerprinting. Phytopathology. 1998; 88(12):1283-93. Epub 2008/10/24. doi: 10.1094/PHYTO.1998.88.12.1283 PMID: 18944830
56. Riska J, Hermanto C. Confirm the status of VCG Fusarium oxysporum f. Sp. Cubense in West Sumatera Indonesia. ARPN J of Agric and Bio Sci. 2012; 7(4):244-49.
57. Boehm E, Ploetz R, Kistler HC. Statistical analysis of electrophoretic karyotype variation among vegetative compatibility groups of Fusarium oxysporum f. Sp. Cubense. MPMI-Molecular Plant Microbe Interactions. 1994; 7(2):196-207.
58. Cai L, Giraud T, Zhang N, Begerow D, Cai G, Shivas R. The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Diversity. 2011; 50(1):121-33.
59. Peng Y, Jin J, Wu C, Yang J, Li X. Orthogonal array design in optimizing ERIC-PCR system for fingerprinting rat's intestinal microflora. Journal of Applied Microbiology. 2007; 103(6):2095-101. doi: 10. 1111/j.1365-2672.2007.03440.x PMID: 18045393
60. Rao RS, Kumar CG, Prakasham RS, Hobbs PJ. The Taguchi methodology as a statistical tool for biotechnological applications: A critical appraisal. Biotechnology Journal. 2008; 3(4):510-23. doi: 10.1002/ biot.200700201 PMID: 18320563
61. Chen D, Yang Z, Xia H, Huang J- F, Zhang Y, Jiang T- N, et al. Enhanced Specificity of TPMT∗2 Genotyping Using Unidirectional Wild-Type and Mutant Allele-Specific Scorpion Primers in a Single Tube. PloS one. 2014; 9(4):e91824. doi: 10.1371/journal.pone.0091824 PMID: 24705376
62. Thanakiatkrai P, Welch L. Using the Taguchi method for rapid quantitative PCR optimization with SYBR Green I. Int J Legal Med. 2012; 126(1):161-5. doi: 10.1007/s00414-011-0558-5 PMID: 21336638
63. Dabrowski W, Czekajo-Koodziej U, Mdrala D, Giedrys-Kalemba S. Optimisation of AP-PCR fingerprinting discriminatory power for clinical isolates of Pseudomonas aeruginosa. FEMS microbiology letters. 2003; 218(1):51-7. PMID: 12583897
64. Cobb BD, C'Iarkson JM. A simple procedure for optimising the polymerase chain reaction (PCR) using modified Taguchi methods. Nucleic Acids Research. 1994; 22(18):3801-5. PMID: 7937094
65. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical chemistry. 2009; 55 (4):611-22. doi: 10.1373/clinchem.2008.112797 PMID: 19246619
66. Bustin SA. The reproducibility of biomedical research: Sleepers awake! Biomolecular Detection and Quantification. 2014; 2:35-42.
67. Nel B, Steinberg C, Labuschagne N, Viljoen A. Isolation and characterization of nonpathogenic Fusarium oxysporum isolates from the rhizosphere of healthy banana plants. Plant Pathology. 2006; 55 (2):207-16.
68. Grosdidier M, Aguayo J, Marçais B, Ioos R. Detection of plant pathogens using real-time PCR: How reliable are late Ct values? Plant Pathology. 2016:n/a-n/a.