Rapid identification and detection of pine pathogenic fungi associated with mountain pine beetles by padlock probes

Journal of Microbiological Methods

Volumn 83, Issue 1, 2010, Pages 26-33

  Tsui, Clement K M ^a   Wang, Bin ^b   Khadempour, Lily ^a   Alamouti, Sepideh Massoumi ^a   Bohlmann, Jörg ^a   Murray, Brent W ^c   Hamelin, Richard C ^a,d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF NORTHERN BRITISH COLUMBIA   (Canada)

^d LAURENTIAN FORESTRY CENTRE   (Canada)

Author keywords

Bst polymerase; Circular probe; Diagnostics; Forestry; Isothermal amplification; Ligation; Lodgepole pine; Ophiostoma; Real time PCR; Sapstain

Indexed keywords

LARGE SUBUNIT RIBOSOMAL RNA; SPACER DNA;

AMPLICON; ANIMAL TISSUE; ARTICLE; BEETLE; CONTROLLED STUDY; FUNGAL DETECTION; FUNGAL STRAIN; FUNGUS IDENTIFICATION; GROSMANNIA CLAVIGERA; LEPTOGRAPHIUM LONGICLAVATUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPHIOSTOMATALES; PINE; PRIORITY JOURNAL; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION;

ANIMALS; BEETLES; DNA PRIMERS; DNA, FUNGAL; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; OPHIOSTOMATALES; PINUS; PLANT DISEASES; POLYMERASE CHAIN REACTION;

CLAVIGERA; COLEOPTERA; DENDROCTONUS PONDEROSAE; FUNGI; LEPTOGRAPHIUM LONGICLAVATUM; OPHIOSTOMA; OPHIOSTOMATALES; PINUS CONTORTA; PINUS MUGO;

EID: 77956418136     PISSN: 01677012     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mimet.2010.07.016     Document Type: Article

References (54)

1. Adams A.S., Six D.L. Temporal variation in mycophagy and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae (Coleoptera: Curculionidae). Environ. Entomol. 2007, 36:64-72.
2. Adams A.S., Six D.L., Adams S.M., Holben W.E. In vitro interactions between yeasts and bacteria and fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microb. Ecol. 2008, 56:460-466.
3. Bleiker K.P., Potter S.E., Lauzon C.R., Six D.L. Transport of fungal symbionts by mountain pine beetles. Canad. Entomol. 2009, 141:503-514.
4. Carroll A.L., Taylor S.W., Regniere J., Safranyik L. Effects of climate change on range expansion by the mountain pine beetle in British Columbia. Mountain Pine Beetle Symposium: Challenges and Solutions. 30 and 31 October 2003 2003, 223-232. Can. For. Serv. Pac. For. Cent. Inf. Rep. BC-X-399, Victoria, BC, Canada. T.L. Shore, J.E. Brooks, J.E. Stone (Eds.).
5. DiGuistini S., Liao N.Y., Platt D., Robertson G., Seidel M., Chan S.K., Docking T.R., Birol I., Holt R.A., Hirst M., Mardis E., Marra M.A., Hamelin R.C., Bohlmann J., Breuil C., Jones S.J.M. De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biol. 2009, 10:R94.
6. Eriksson R., Jobs M., Ekstrand C., Ullberg M., Herrmann B., Landegren U., Nilsson M., Blomberg J. Multiplex and quantifiable detection of nucleic acid from pathogenic fungi using padlock probes, generic real time PCR and specific suspension array readout. J. Microbiol. Methods 2009, 78:195-202.
7. Faruqi A.F., Hosono S., Driscoll M.D., Dean F.B., Alsmadi O., Bandaru R., Kumar G., Grimwade B., Zong Q., Sun Z., Du Y., Kingsmore S., Knott T., Lasken R.S. High-throughput genotyping of single nucleotide polymorphisms with rolling circle amplification. BMC Genomics 2001, 2:4.
8. Harrington T.C. Biology and taxonomy of fungi associated with bark beetles. Beetle-Pathogen Interactions in Conifer Forests 1993, 37-51. Academic Press, San Diego, USA. T.D. Schowalter, G.M. Filip (Eds.).
9. Hausner G., Iranpour M., Kim J.-J., Breuil C., Davis C.N., Gibb E.A., Reid J., Loewen P.C., Hopkin A.A. Fungi vectored by the introduced bark beetle Tomicus piniperda in Ontario, Canada, and comments on the taxonomy of Leptographium lundbergii, Leptographium terebrantis, Leptographium truncatum, and Leptographium wingfieldii. Can. J. Bot. 2005, 83:1222-1237.
10. Jacobs K., Wingfield M.J. Leptographium Species: Tree Pathogens, Insect Associates, and Agents of Blue Stain 2001, APS Press, St. Paul, MN, USA.
11. Jacobs K., Wingfield M.J., Wingfield B.D. Phylogenetic relationships in Leptographium based on morphological and molecular characters. Can. J. Bot. 2001, 79:719-732.
12. Kaocharoen S., Wang B., Tsui K.M., Trilles L., Kong F., Meyer W. Hyperbranched rolling circle amplification as a rapid and sensitive method for species identification within the Cryptococcus species complex. Electrophoresis 2008, 29:3183-3191.
13. Kurz W.A., Dymond C.C., Stinson G., Rampley G.J., Neilson E.T., Carroll A.L., Ebata T., Safranyik L. Mountain pine beetle and forest carbon feedback to climate change. Nature 2008, 452:987-990.
14. Lee S., Kim J.J., Fung S., Breuil C. A PCR-RFLP marker distinguishing Ophiostoma clavigerum from morphologically similar Leptographium species associated with bark beetles. Can. J. Bot. 2003, 81:1104-1112.
15. Lee S., Kim J.-J., Breuil C. Leptographium longiclavatum sp. nov., a new species associated with the mountain pine beetle, Dendroctonus ponderosae. Mycol. Res. 2005, 109:1162-1170.
16. Lee S., Kim J.-J., Breuil C. Pathogenicity of Leptographium longiclavatum associated with Dendroctonus ponderosae to Pinus contorta. Can. J. For. Res. 2006, 36:2864-2872.
17. Lee S., Kim J.-J., Breuil C. Diversity of fungi associated with the mountain pine beetle, Dendroctonus ponderosae and infested lodgepole pines in British Columbia. Fungal Divers. 2006, 22:91-105.
18. Lee S., Hamelin R.C., Six D.L., Breuil C. Genetic diversity and the presence of two distinct groups in Ophiostoma clavigerum associated with Dendroctonus ponderosae in British Columbia and the northern Rocky Mountains. Phytopathology 2007, 97:1177-1185.
19. Lim Y.W., Massoumi Alamouti S., Kim J.-J., Lee S., Breuil C. Multigene phylogenies of Ophiostoma clavigerum and closely related species from bark beetle-attacked Pinus in North America. FEMS Microbiol. Lett. 2004, 237:89-96.
20. Lim Y.W., Kim J.-J., Lu M., Breuil C. Determining fungal diversity on Dendroctonus ponderosae and Ips pini affecting lodgepole pine using cultural and molecular methods. Fungal Divers. 2005, 19:79-94.
21. Lizardi P.M., Huang X.H., Zhu Z.G., Bray-Ward P., Thomas D.C., Ward D.C. Mutation detection and single-molecule counting using isothermal rolling-circle amplification. Nat. Genet. 1998, 19:225-232.
22. Martin K.J., Rygiewicz P.T. Fungal specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 2005, 5:28.
23. Mullineux T., Hausner G. Evolution of rDNA ITS1 and ITS2 sequences and RNA secondary structures within members of the fungal genera Grosmannia and Leptographium. Fungal Genet. Biol. 2009, 46:855-867.
24. Nilsson M. Lock and roll: single-molecule genotyping in situ using padlock probes and rolling-circle amplification. Histochem. Cell Biol. 2006, 126:159-164.
25. Nilsson M., Malmgren H., Samiotaki M., Kwiatkowski M., Chowdhary B.P., Landegren U. Padlock probes: circularizing oligonucleotides for localized DNA detection. Science 1994, 265:2085-2088.
26. Nilsson R.H., Kristiansson E., Ryberg M., Hallenberg N., Larsson K.-H. Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequences databases and its implications for molecular species identification. Evol. Bioinform. 2008, 4:193-201.
27. Persson Y., Vasaitis R., Långström B., Öhrn P., Ihrmark K., Stenlid J. Fungi vectored by the bark beetle Ips typographus following hibernation under the bark of standing trees and in the forest litter. Microb. Ecol. 2009, 58:651-659.
28. Plattner A., Kim J.-J., DiGuistini S., Breuil C. Variation in pathogenicity of a mountain pine beetle-associated blue-stain fungus, Grosmannia clavigera, on young lodgepole pine in British Columbia. Can. J. Plant Pathol. 2008, 30:457-466.
29. Raffa K.F., Berryman A.A. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). Can. Entomol. 1983, 115:723-734.
30. Rambaut, A., 1999. Se-Al: Sequence Alignment Editor. Available at Department of Zoology, University of Oxford, UK. http://evolve.zoo.ox.ac.uk/.
31. Rice A.V., Langor D.W. Mountain pine beetle-associated blue-stain fungi in lodgepole×jack pine hybrids near Grande Prairie, Alberta (Canada). For. Path. 2009, 39:323-334.
32. Rice A.V., Thormann M.N., Langor D.W. Virulence of, and interactions among, mountain pine beetle associated blue-stain fungi on two pine species and their hybrids in Alberta. Can. J. Bot. 2007, 85:316-323.
33. Sambrook J., Russell D.W. Molecular Cloning: a Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd Ed.
34. Schweigkofler W., Otrosina W.J., Smith S.L., Cluck D.R., Maeda K., Peay K.G., Garbelotto M. Detection and quantification of Leptographium wageneri, the cause of black-stain root disease, from bark beetles (Coleoptera: Scolytidae) in Northern California using regular and real-time PCR. Can. J. For. Res. 2005, 35:1798-1808.
35. Six D.L. A comparison of mycangial and phoretic fungi of individual mountain pine beetles. Can. J. For. Res. 2003, 33:1331-1334.
36. Six D.L., Klepzig K.D. Dendroctonus bark beetles as model systems for studies on symbiosis. Symbiosis 2004, 37:207-232.
37. Six D.L., Paine T.D. Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environ. Entomol. 1998, 27:1393-1401.
38. Six D.L., Harrington T.C., Steimel J., McNew D., Paine T.D. Genetic relationships among Leptographium terebrantis and the mycangial fungi of three western Dendroctonus bark beetles. Mycologia 2003, 95:781-792.
39. Solheim H., Krokene P. Growth and virulence of mountain pine beetle associated blue-stain fungi, Ophiostoma clavigerum and Ophiostoma montium. Can. J. Bot. 1998, 76:561-566.
40. Steain M.C., Dwyer D.E., Hurt A.C., Kol C., Saksena N., Cunningham A.L., Wang B. Detection of influenza A H1N1 and H2N2 mutation conferring resistance to oseltamivir using rolling circle amplification. Antiviral Res. 2009, 84:242-248.
41. Szemes M., Bonants P., de Weerdt M., Baner J., Landegren U., Schoen C.D. Diagnostic application of padlock probes - multiplex detection of plant pathogens using universal microarrays. Nucleic Acids Res. 2005, 33:e70.
42. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
43. Tong Z., Kong F., Wang B., Zeng X., Gilbert G.L. A practical method for subtyping of Streptococcus agalactiae serotype III, of human origin, using rolling circle amplification. J. Microbiol. Methods 2007, 70:39-44.
44. Tsuneda A., Hiratsuka Y. Sympodial and annellidic conidiation in Ceratocystis clavigera. Can. J. Bot. 1984, 62:2618-2624.
45. van Doorn R., Szemes M., Bonants P., Kowalchuk G.A., Salles J.F., Ortenberg E., Schoen C.D. Quantitative multiplex detection of plant pathogens using a novel ligation probe-based system coupled with universal, high-throughput real-time PCR on OpenArrays™. BMC Genomics 2007, 8:276.
46. van Doorn R., Slawiak M., Szemes M., Dullemans A.M., Bonants P., Kowalchuk G.A., Schoen C.D. Robust detection and identification of multiple oomycetes and fungi in environmental samples by using a novel cleavable padlock probe-based ligation detection assay. Appl. Environ. Microbiol. 2009, 75:4185-4193.
47. Vasanthakumar A., Handelsman J., Schloss P.D., Bauer L.S., Raffa K.F. Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environ. Entomol. 2008, 37:1344-1353.
48. Wang B., Potter S.J., Lin Y., Cunningham A.L., Dwyer D.E., Su Y., Ma X., Hou Y., Saksena N.K. Rapid and sensitive detection of severe acute respiratory syndrome coronavirus by rolling circle amplification. J. Clin. Microbiol. 2005, 43:2339-2444.
49. Wright S.H.A., Berch S.M., Berbee M.L. The effect of fertilization on the below ground diversity and community composition of ectomycorrhizal fungi associated with western hemlock (Tsuga heterophylla). Mycorrhiza 2009, 19:267-276.
50. Yamaoka Y., Hiratsuka Y., Maruyama P.J. The ability of Ophiostoma clavigerum to kill mature lodgepole-pine trees. Eur. J. For. Pathol. 1995, 25:401-404.
51. Zambino P.J., Harrington T.C. Correspondence of isozyme characterization with morphology in the asexual genus Leptographium and taxonomic implications. Mycologia 1992, 84:12-25.
52. Zhang N., Suh S.O., Blackwell M. Microorganisms in the gut of beetles: evidence from molecular cloning. J. Invertebr. Pathol. 2005, 84:226-233.
53. Zhou X., Kong F., Sorrell T.C., Wang H., Duan Y., Chen S.C.A. Practical method for detection and identification of Candida, Aspergillus, and Scedesporium spp. by use of rolling circle amplification. J. Clin. Microbiol. 2008, 46:2423-2427.
54. Zipfel R.D., de Beer Z.W., Jacobs K., Wingfield B.D., Wingfield M.J. Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud. Mycol. 2006, 55:75-97.