Identification and Differentiation of Verticillium Species and V. longisporum Lineages by Simplex and Multiplex PCR Assays

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Inderbitzin, Patrik ^a   Davis, R Michael ^a   Bostock, Richard M ^a   Subbarao, Krishna V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ELONGATION FACTOR 1ALPHA; FUNGAL DNA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTERNAL TRANSCRIBED SPACER; TRYPTOPHAN SYNTHASE;

AMPLICON; ARTICLE; ASCOMYCETES; DIPLOIDY; DNA EXTRACTION; DNA SEQUENCE; FUNGUS CULTURE; GENETIC CODE; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SIMPLEX POLYMERASE CHAIN REACTION; SPECIES DIFFERENTIATION; SPECIES IDENTIFICATION; VERTICILLIUM; VERTICILLIUM ALBO ATRUM; VERTICILLIUM ALFALFAE; VERTICILLIUM DAHLIAE; VERTICILLIUM ISAACII; VERTICILLIUM KLEBAHNII; VERTICILLIUM LONGISPORUM; VERTICILLIUM NONALFALFAE; VERTICILLIUM NUBILUM; VERTICILLIUM TRICORPUS; VERTICILLIUM ZAREGAMSIANUM; CLASSIFICATION; GENETICS; PHYLOGENY; PROCEDURES; SEQUENCE HOMOLOGY; VALIDATION STUDY;

ASCOMYCOTA; FUNGI; SORDARIOMYCETES; VERTICILLIUM (HYPOCREALES); VERTICILLIUM (PHYLLACHORALES); VERTICILLIUM ALBO-ATRUM; VERTICILLIUM DAHLIAE; VERTICILLIUM NUBILUM; VERTICILLIUM TRICORPUS;

DNA, FUNGAL; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, NUCLEIC ACID; VERTICILLIUM;

EID: 84879166309     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065990     Document Type: Article

References (66)

1. Pegg GF, Brady BL (2002) Verticillium wilts. Wallingford, Oxon, UK: CABI Publishing. 552 p.
2. Subbarao KV, Hubbard JC, Greathead AS, Spencer GA (1997) Verticillium wilt. In: Davis RM, Subbarao KV, Raid RN, Kurtz EA, editors. Compendium of Lettuce Diseases. St. Paul, MN: The American Phytopathological Society. pp. 26-27.
3. Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV, (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47: 39-62.
4. Inderbitzin P, Bostock RM, Davis RM, Usami T, Platt HW, et al. (2011) Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLoS ONE 6: e28341.
5. Zare R, Gams W, Starink-Willemse M, Summerbell RC, (2007) Gibellulopsis, a suitable genus for Verticillium nigrescens, and Musicillium, a new genus for V. theobromae. Nova Hedwigia 85: 463-489.
6. Gams W, Zare R, Summerbell RC, (2005) Proposal to conserve the generic name Verticillium (anamorphic Ascomycetes) with a conserved type. Taxon 54: 179.
7. Hawksworth DL, Talboys PW (1970) Verticillium dahliae. CMI Descriptions of Pathogenic Fungi and Bacteria 256.
8. Platt HW, MacLean V, Mahuku G, Maxwell P (2000) Verticillium wilt of potatoes caused by three Verticillium species. In: Tjamos EC, Rowe RC, Heale JB, Fravel DR, editors. Advances in Verticillium: Research and disease management. St. Paul, MN: APS Press. pp. 59-62.
9. Heale JB, Isaac I, (1963) Wilt of lucerne caused by species of Verticillium. IV. Pathogenicity of V. albo-atrum and V. dahliae to lucerne and other crops; spread and survival of V. albo-atrum in soil and weeds; effect upon lucerne production. Ann Appl Biol 52: 439-451.
10. Hawksworth DL, Talboys PW (1970) Verticillium albo-atrum. CMI Descriptions of Pathogenic Fungi and Bacteria 255.
11. Dunker S, Keunecke H, Steinbach P, von Tiedemann A, (2008) Impact of Verticillium longisporum on yield and morphology of winter oilseed rape (Brassica napus) in relation to systemic spread in the plant. J Phytopathol 156: 698-707.
12. Babadoost M, Chen W, Bratsch AD, Eastman CE, (2004) Verticillium longisporum and Fusarium solani: two new species in the complex of internal discoloration of horseradish roots. Plant Pathol 53: 669-676.
13. Down G, Barbara D, Radišek S, (2007) Verticillium albo-atrum and V. dahliae on hop. Bull OEPP 37: 528-535.
14. Radišek S, Jakše J, Javornik B, (2006) Genetic variability and virulence among Verticillium albo-atrum isolates from hop. Eur J Plant Pathol 116: 301-314.
15. Isaac I, (1953) A further comparative study of pathogenic isolates of Verticillium: V. nubilum Pethybr. and V. tricorpus sp. nov. Trans Br mycol Soc 36: 180-195.
16. Usami T, Kanto T, Inderbitzin P, Itoh M, Kisaki G, et al. (2010) Verticillium tricorpus causing lettuce wilt in Japan differs genetically from California lettuce isolates. J Gen Plant Pathol 77: 17-23.
17. Qin QM, Vallad GE, Subbarao KV, (2008) Characterization of Verticillium dahliae and V. tricorpus isolates from lettuce and artichoke. Plant Disease 92: 69-77.
18. Wilhelm S, (1955) Longevity of the Verticillium wilt fungus in the laboratory and field. Phytopathology 45: 180-181.
19. Harris DC, Yang JR, (1996) The relationship between the amount of Verticillium dahliae in soil and the incidence of strawberry wilt as a basis for disease risk prediction. Plant Pathol 45: 106-114.
20. Isaac I, (1949) A comparative study of pathogenic isolates of Verticillium. Trans Br mycol Soc 32: 137-157.
21. Zeise K, von Tiedemann A, (2002) Host specialization among vegetative compatibility groups of Verticillium dahliae in relation to Verticillium longisporum. J Phytopathol 150: 112-119.
22. Eynck C, Koopmann B, Grunewaldt-Stoecker G, Karlovsky P, von Tiedemann A, (2007) Differential interactions of Verticillium longisporum and V. dahliae with Brassica napus detected with molecular and histological techniques. Eur J Plant Pathol 118: 259-274.
23. Larsen RC, Vandemark GJ, Hughes TJ, Grau CR, (2007) Development of a real-time polymerase chain reaction assay for quantifying Verticillium albo-atrum DNA in resistant and susceptible alfalfa. Phytopathology 97: 1519-1525.
24. Nazar RN, Hu X, Schmidt J, Culham D, Robb J, (1991) Potential use of PCR-amplified ribosomal intergenic sequences in detection and differentiation of Verticillium wilt pathogens. Physiol Mol Plant Pathol 39: 1-11.
25. Carder JH, Morton A, Tabrett AM, Barbara DJ (1994) Detection and differentiation by PCR of subspecific groups within two Verticillium species causing vascular wilts in herbaceous hosts. In: Schots A, Dewey FM, Oliver RP, editors. Modern assays for plant pathogenic fungi: Identification, detection and quantification. Wallingford, Oxford: CAB International. pp. 91-97.
26. Koike M, Itaya Y, Hoshino K, Nagao H, Ohshima S, (1997) PCR detection of Japanese isolates of Verticillium dahliae and V. albo-atrum using European subgroup-specific primers. Microbes Environ 12: 15-18.
27. Lievens B, Brouwer M, Vanachter ACRC, Cammue BPA, Thomma BPHJ, (2006) Real-time PCR for detection and quantification of fungal and oomycete tomato pathogens in plant and soil samples. Plant Science 171: 155-165.
28. Dan H, Ali-Khan ST, Robb J, (2001) Use of quantitative PCR diagnostics to identify tolerance and resistance to Verticillium dahliae in potato. Plant Dis 85: 700-705.
29. Platt HW, Mahuku GS, Maxwell P, MacLean V (2000) Detection techniques for research on Verticillium species in potato soils. In: Tjamos EC, Rowe RC, Heale JB, Fravel DR, editors. Advances in Verticillium: Research and disease management. St. Paul, MN: APS Press. 140-143.
30. Banno S, Saito H, Sakai H, Urushibara T, Ikeda K, et al. (2011) Quantitative nested real-time PCR detection of Verticillium longisporum and V. dahliae in the soil of cabbage fields. J Gen Plant Pathol 77: 282-291.
31. Gayoso C, Martínez de Ilárduya O, Pomar F, Merino de Cáceres F, (2007) Assessment of real-time PCR as a method for determining the presence of Verticillium dahliae in different Solanaceae cultivars. Eur J Plant Pathol 118: 199-209.
32. Kuchta P, Jecz T, Korbin M, (2008) The suitability of PCR-based techniques for detecting Verticillium dahliae in strawberry plants and soil. Journal of Fruit and Ornamental Plant Research 16: 295-304.
33. Li KN, Rouse DI, Eyestone EJ, German TL, (1999) The generation of specific DNA primers using random amplified polymorphic DNA and its application to Verticillium dahliae. Mycol Res 103: 1361-1368.
34. Atallah ZK, Bae J, Jansky SH, Rouse DI, Stevenson WR, (2007) Multiplex real-time quantitative PCR to detect and quantify Verticillium dahliae colonization in potato lines that differ in response to Verticillium wilt. Phytopathology 97: 865-872.
35. Volossiouk T, Robb EJ, Nazar RN, (1995) Direct DNA extraction for PCR-mediated assays of soil organisms. Appl Environ Microbiol 61: 3972-3976.
36. Mahuku GS, Platt HW, (2002) Quantifying Verticillium dahliae in soils collected from potato fields using a competitive PCR assay. Am J Potato Res 79: 107-117.
37. Kageyama K, Komatsu T, Suga H, (2003) Refined PCR protocol for detection of plant pathogens in soil. J Gen Plant Pathol 69: 153-160.
38. Debode J, Van Poucke K, França SC, Maes M, Höfte M, et al. (2011) Detection of multiple Verticillium species in soil using density flotation and real-time polymerase chain reaction. Plant Dis 95: 1571-1580.
39. Schena L, Nigro F, Ippolito A, (2004) Real-time PCR detection and quantification of soilborne fungal pathogens: the case of Rosellinia necatrix, Phytophthora nicotianae, P. citrophthora, and Verticillium dahliae. Phytopathol Mediterr 43: 273-280.
40. Bilodeau GJ, Koike ST, Uribe P, Martin FN, (2012) Development of an assay for rapid detection and quantification of Verticillium dahliae in soil. Phytopathology 102: 331-343.
41. Karajeh MR, Masoud SA, (2006) Molecular detection of Verticillium dahliae Kleb. in asymptomatic olive trees. J Phytopathol 154: 496-499.
42. Duressa D, Rauscher G, Koike ST, Mou B, Hayes RJ, et al. (2012) A real-time PCR assay for detection and quantification of Verticillium dahliae in spinach seed. Phytopathology 102: 443-451.
43. Karapapa VK, Typas MA, (2001) Molecular characterization of the host-adapted pathogen Verticillium longisporum on the basis of a group-I intron found in the nuclear SSU-rRNA gene. Curr Microbiol 42: 217-224.
44. Steventon LA, Fahleson J, Hu Q, Dixelius C, (2002) Identification of the causal agent of Verticillium wilt of winter oilseed rape in Sweden, V. longisporum. Mycol Res 106: 570-578.
45. Moukhamedov R, Hu X, Nazar RN, Robb J, (1994) Use of polymerase chain reaction-amplified ribosomal intergenic sequences for the diagnosis of Verticillium tricorpus. Phytopathology 84: 256-259.
46. Robb J, Hu X, Platt H, Nazar R (1994) PCR-based assays for the detection and quantification of Verticillium species in potato. In: Schots A, Dewey FM, Oliver R, editors. Modern assays for plant pathogenic fungi: Identification, detection and quantification. Wallingford, Oxford: CAB International. 83-90.
47. Inderbitzin P, Davis RM, Bostock RM, Subbarao KV, (2011) The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS ONE 6: e18260.
48. Nilsson HR, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, et al. (2006) Taxonomic reliability of DNA sequences in public sequence databases: A fungal perspective. PLoS ONE 1: e59.
49. Du XH, Zhao Q, Yang ZL, Hansen K, Taskin H, et al. (2012) How well do ITS rDNA sequences differentiate species of true morels (Morchella)? Mycologia 104: 1351-1368.
50. Gräfenhan T, Schroers HJ, Nirenberg HI, Seifert KA, (2011) An overview of the taxonomy, phylogeny, and typificiation of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutella. Stud Mycol 68: 79-113.
51. Gams W, Zare R, (2001) A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia 72: 329-337.
52. Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, et al. (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57: 5-59.
53. Piel WH, Donoghue MJ, Sanderson MJ, (2002) TreeBASE: a database of phylogenetic knowledge. In: Shimura J, Wilson KL, Gordon D, editors. To the interoperable "Catalog of Life" -with partners Species 2000 Asia Oceanea. Tsukuba, Japan: Research Report from the National Institute for Environmental Studies No. 171: 41-47.
54. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, et al. (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7: e1002137.
55. Pramateftaki PV, Antoniou PP, Typas MA, (2000) The complete DNA sequence of the nuclear ribosomal RNA gene complex of Verticillium dahliae: Intraspecific heterogeneity within the intergenic spacer region. Fungal Genet Biol 29: 19-27.
56. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity of basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
57. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols. San Diego: Academic Press, Inc. 315-322.
58. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
59. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
61. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2010) Geneious v4.8.5. Available: http://www.geneious.com.
62. Kwok S, Chang SY, Sninsky JJ, Wang A, (1994) A guide to the design and use of mismatched and degenerate primers. Genome Res 3: S39-S47.
63. Kibbe WA, (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35: W43-W46.
64. Sambrook J, Russell DW (2001) Molecular Cloning. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
65. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.
66. Inderbitzin P, Landvik S, Abdel-Wahab MA, Berbee ML, (2001) Aliquandostipitaceae, a new family for two new tropical ascomycetes with unusually wide hyphae and dimorphic ascomata. Am J Bot 88: 52-61.