Bringing Laboulbeniales into the 21st century: Enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi

IMA Fungus

Volumn 6, Issue 2, 2015, Pages 363-372

  Haelewaters, Danny ^a   Gorczak, Michal ^b   Pfliegler, Walter P ^c,d   Tartally, András ^c   Tischer, Marta ^b   Wrzosek, Marta ^b   Pfister, Donald H ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF WARSAW   (Poland)

^c UNIVERSITY OF DEBRECEN   (Hungary)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Ascomycota; DNA isolation; Insect collections; Laboulbeniales specific primers; Ribosomal DNA; Unculturable fungi

Indexed keywords

EID: 84957056864     PISSN: 22106340     EISSN: 22106359     Source Type: Journal    
DOI: 10.5598/imafungus.2015.06.02.08     Document Type: Article

References (63)

1. A'Hara S, Harling R, McKinlay RG, Topping CJ (1998) RAPD profiling of spider (Araneae) DNA. Journal of Arachnology 26: 397-400.
2. Colgan DJ, Brown S, Major RE, Christie F, Gray MR, Cassis G (2002) Population genetics of wolf spiders of fragmented habitat in the wheat belt of New South Wales. Molecular Ecology 11: 2295-2305.
3. Conger AD, Fairchild LM (1953) A quick-freeze method for making smear slides permanent. Stain Technology 28: 281-283.
4. De Kesel A (1996a) Relative importance of direct and indirect infection in the transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales). Belgian Journal of Botany 128: 124-130.
5. De Kesel A (1996b) Host specificity and habitat preference of Laboulbenia slackensis. Mycologia 88: 565-573.
6. De Kesel A (1998) Identification and host-range of the genus Laboulbenia in Belgium. Sterbeeckia 18: 13-31.
7. De Kesel A (2011) Hesperomyces (Laboulbeniales) and coccinellid hosts. Sterbeeckia 30: 32-37.
8. De Kesel A, Haelewaters D (2012) Belgian records of Laboulbeniales from aquatic insects (2)-Chitonomyces aculeifer. Sterbeeckia 31: 16-18.
9. De Kesel A, Haelewaters D (2014) Laboulbenia slackensis and L. littoralis sp. nov. (Ascomycota, Laboulbeniales), two sibling species as a result of ecological speciation. Mycologia 106: 407-414.
10. Dillon N, Austin AD, Bartowsky E (1996) Comparison of preservation techniques for DNA extraction from hymenopterous insects. Insect Molecular Biology 5: 21-24.
11. Eckhart L, Bach J, Ban J, Tschachler E (2000) Melanin binds reversibly to thermostable DNA polymerase and inhibits its activity. Biochemical and Biophysical Research Communications 271: 726-730.
12. Ferreira AVB, Glass NL (1996) PCR from fungal spores after microwave treatment. Fungal Genetics Newsletter 43: 25-26.
13. Gardes M, Bruns TD (1993) ITS Primers with enhanced specificity for Basidiomycetes-application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
14. Giard A (1892) Sur une Laboulbéniacée (Thaxteria künckeli nov. gen. et sp.), parasite de Mormolyce phyllodes Hagenbach. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 4: 156-158.
15. Goldmann L, Weir A (2012) Position specificity in Chitonomyces (Ascomycota, Laboulbeniomycetes) on Laccophilus (Coleoptera, Dytiscidae): a molecular approach resolves a century-old debate. Mycologia 104: 1143-1158.
16. Goldmann L, Weir A, Rossi W (2013) Molecular analysis reveals two new dimorphic species of Hesperomyces (Ascomycota, Laboulbeniomycetes) parasitic on the ladybird Coleomegilla maculata (Coleoptera, Coccinellidae). Fungal Biology 117: 807-813.
17. Goodwin DC, Lee SB (1993) Microwave miniprep of total genomic DNA from fungi, plants, protists and animals for PCR. BioTechniques 15: 438-441.
18. Haelewaters D (2011) Laboulbeniales: Exploring and testing DNA extraction protocols, carrion beetle hosts and species in 'De Kaaistoep' (Netherlands). Master thesis, Department of Biology, Ghent University, Belgium.
19. Haelewaters D, Comont RF, Zhao SY, Pfister DH (2014) Hesperomyces virescens (Fungi, Ascomycota, Laboulbeniales) attacking Harmonia axyridis (Coleoptera, Coccinellidae) in its native range. Chinese Science Bulletin 59: 528-532.
20. Haelewaters D, De Kock G, van Wielink P (2015a) Nieuwe Laboulbeniales in De Kaaistoep. In: Natuurstudie in De Kaaistoep. Verslag 2014, 20e onderzoeksjaar (Peeters T, van Eck A, Cramer T, eds): 11-18. Tilburg, The Netherlands: TWM Gronden.
21. Haelewaters D, Yaakop S (2014) New and interesting Laboulbeniales from southern and southeastern Asia. Mycotaxon 129: 439-454.
22. Haelewaters D, Zhao SY, De Kesel A, Royer IR, Handlin RE, Farrell BD, Pfister DH (2015b) Laboulbeniales (Ascomycota) of the Boston Harbor Islands I: species parasitizing Coccinellidae and Staphylinidae. Northeastern Naturalist 22: 459-477.
23. Hansen K, Perry BA, Dranginis AW, Pfister DH (2013) A phylogeny of the highly diverse cup-fungus family Pyronemataceae (Pezizomycetes, Ascomycota) clarifies relationships and evolution of selected life history traits. Molecular Phylogenetics and Evolution 67: 311-335.
24. Haugland RA, Heckman JL, Wymer LJ (1999) Evaluation of different methods for the extraction of DNA from fungal conidia by quantitative competitive PCR analysis. Journal of Microbiological Methods 37: 165-176.
25. Henson JM (1992) DNA hybridization and polymerase chain reaction (PCR) tests for identification of Gaeumannomyces, Phialophora and Magnaporthe isolates. Mycological Research 96: 629-636.
26. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycological Research 3: 509-547.
27. Huldén L (1983) Laboulbeniales (Ascomycetes) of Finland and adjacent parts of the U.S.S.R. Karstenia 23: 31-136.
28. Kurtzman CP, Robnett CJ (1997) Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5' end of the large-subunit (26S) ribosomal DNA gene. Journal of Clinical Microbiology 35: 1216-1223.
29. Landvik S, Egger KN, Schumacher T (1997) Towards a subordinal classification of the Pezizales. Nordic Journal of Botany 17: 403-418.
30. Lee SB, Taylor JM (1990) Isolation of total DNA from fungi for amplification by the polymerase chain reaction. In: PCR Protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds): 282-287. San Diego: Academic Press.
31. Majewski T (1994) The Laboulbeniales of Poland. Polish Botanical Studies 7: 1-466.
32. Miadlikowska J, Lutzoni F (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. International Journal of Plant Sciences 161: 925-958.
33. Moncalvo J-M, Rehner SA, Vilgalys R (1993) Systematics of Lyophyllum section Difformia based on evidence from culture studies and ribosomal DNA sequences. Mycologia 85: 788-794.
34. Prieto M, Wedin M (2013) Dating the diversification of the major lineages of Ascomycota (Fungi). PLoS One 8: e65576.
35. Santamaría S (1998) Laboulbeniales, I. Laboulbenia. Flora Mycologica Iberica 4: 1-186.
36. Santamaría S (2003) Laboulbeniales, II. Acompsomyces-Ilyomyces. Flora Mycologica Iberica 5: 1-344.
37. Santamaría S, Espadaler X (2015) Rickia lenoirii, a new ectoparasitic species, with comments on world Laboulbeniales associated with ants. Mycoscience 56: 224-229.
38. Scheloske H-W (1969) Beiträge zur Biologie, ökologie und Systematik der Laboulbeniales (Ascomycetes) unter besondere Berücksichtigung des Parasit-Wirt-Verhältnisses. Parasitologische Schriftenreihe 19: 1-176.
39. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J, et al. (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biology 58: 224-239.
40. Sohrabi M, Myllys L, Stenroos S (2010) Successful DNA sequencing of a 75 year-old herbarium specimen of Aspicilia aschabadensis (J. Steiner) Mereschk. Lichenologist 42: 626-628.
41. Spatafora JW, Sung GH, Johnson D, Hesse C, O'Rourke B, et al. (2006) A five-gene phylogeny of Pezizomycotina. Mycologia 98: 1018-1028.
42. Stoeckle BC, Dworschak K, Gossner MM, Kuehn R (2010) Influence of arthropod sampling solutions on insect genotyping reliability. Entomologia Experimentalis et Applicata 135: 217-223.
43. Sugiyama K, Phanichapol D (1984) Laboulbeniomycetes (Ascomycotina) in Thailand, I. Natural History Bulletin of the Siam Society 31: 47-88.
44. Thaxter R (1896) Contribution towards a monograph of the Laboulbeniaceae. Memoirs of the American Academy of Arts and Sciences 12: 187-429.
45. Thaxter R (1899) Diagnosis of new species of Laboulbeniaceae. I. Proceedings of the American Academy of Arts and Sciences 35: 153-209.
46. Thaxter R (1900) Preliminary diagnosis of new species of Laboulbeniaceae. II. Proceedings of the American Academy of Arts and Sciences 35: 409-450.
47. Thaxter R (1901a) Preliminary diagnosis of new species of Laboulbeniaceae. III. Proceedings of the American Academy of Arts and Sciences 36: 397-414.
48. Thaxter R (1901b) Preliminary diagnosis of new species of Laboulbeniaceae. IV. Proceedings of the American Academy of Arts and Sciences 37: 21-45.
49. Thaxter R (1902) Preliminary diagnosis of new species of Laboulbeniaceae. V. Proceedings of the American Academy of Arts and Sciences 38: 9-57.
50. Thaxter R (1905) Preliminary diagnoses of new species of Laboulbeniaceae. VI. Proceedings of the American Academy of Arts and Sciences 41: 303-318.
51. Thaxter R (1926) Contribution towards a monograph of the Laboulbeniaceae. Part IV. Memoirs of the American Academy of Arts and Sciences 15: 427-580.
52. Thiers B (2015) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http://sweetgum.nybg.org/science/ih/.
53. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One 7: e40863.
54. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238-4246.
55. Wang Y, Tretter ED, Johnson EM, Kandel P, Lichtwardt RW, Novak SJ, Smith JF, White MM (2014) Using a five-gene phylogeny to test morphology-based hypotheses of Smittium and allies, endosymbiotic gut fungi (Harpellales) associated with arthropods. Molecular Phylogenetics and Evolution 79: 23-41.
56. Weir A, Beakes GW (1996) Correlative light-and scanning electron microscope studies on the developmental morphology of Hesperomyces virescens. Mycologia 88: 677-693.
57. Weir A, Blackwell M (2001a) Molecular data support the Laboulbeniales as a separate class of Ascomycota, Laboulbeniomycetes. Mycological Research 105: 1182-1190.
58. Weir A, Blackwell M (2001b) Extraction and PCR amplification of DNA from minute ectoparasitic fungi. Mycologia 93: 802-806.
59. Weir A, Hammond PM (1997) Laboulbeniales on beetles: host utilization patterns and species richness of the parasites. Biodiversity and Conservation 6: 701-719.
60. Weir A, Hughes M (2002) The taxonomic status of Corethromyces bicolor from New Zealand, as inferred from morphological, developmental, and molecular studies. Mycologia 94: 483-493.
61. Whisler HC (1968) Experimental studies with a new species of Stigmatomyces (Laboulbeniales). Mycologia 60: 65-75.
62. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: PCR Protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds): 315-322. San Diego: Academic Press.
63. Wrzosek M (2000) Taksonomia i filogeneza Mucorales (Zygomycetes) w swietle analiz morfometrycznych oraz wybranych markerów molekularnych. [Taxonomy and phylogeny of Mucorales (Zygomycetes) in the light of morphometrical and selected molecular markers analyses]. PhD thesis, University of Warsaw.