Real-time PCR detection and discrimination of the Ceratocystis coerulescens complex and of the fungal species from the Ceratocystis polonica complex validated on pure cultures and bark beetle vectors

Canadian Journal of Forest Research

Volumn 44, Issue 9, 2014, Pages 1103-1111

  Lamarche, Josyanne ^a   Stewart, Don ^a   Pelletier, Gervais ^a   Hamelin, Richard C ^a,b   Tanguay, Philippe ^a  

^a LAURENTIAN FORESTRY CENTRE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Ceratocystis; DNA based detection; Exotic forest pathogens; Ips; qPCR

Indexed keywords

DNA; FORESTRY;

CANADIAN BOREAL FOREST; CERATOCYSTIS; ENVIRONMENTAL SAMPLE; FOREST PATHOGENS; IPS; MOLECULAR DETECTION; QPCR; RELIABLE DETECTION;

POLYMERASE CHAIN REACTION;

EID: 84906718066     PISSN: 00455067     EISSN: 12086037     Source Type: Journal    
DOI: 10.1139/cjfr-2014-0082     Document Type: Article

References (61)

1. Aguileta, G., Marthey, S., Chiapello, H., Lebrun, M.-H., Rodolphe, F., Fournier, E., Gendrault-Jacquemard, A., and Giraud, T. 2008. Assessing the performance of single-copy genes for recovering robust phylogenies. Syst. Biol.57(4): 613-627. doi:10.1080/10635150802306527.
2. Allen, E.A., and Humble, L.M. 2002. Nonindigenous species introductions: a threat to Canada's forests and forest economy. Can. J. Plant Pathol.24: 103-110. doi:10.1080/07060660309506983.
3. Ayliffe, M.A., Dodds, P.N., and Lawrence, G.J. 2001. Characterisation of a-tubulin gene from Melampsora liniand comparison of fungal-tubulin genes. Mycol. Res.105(7): 818-826. doi:10.1017/S0953756201004245.
4. Ayyadevara, S., Thaden, J.J., and Reis, R.J.S. 2000. Discrimination of primer 3=-nucleotide mismatch by Taq DNA polymerase during polymerase chain reaction. Anal. Biochem.284: 11-18. doi:10.1006/abio.2000.4635.
5. Calderon-Cortés, N., Quesada, M., Cano-Camacho, H., and Zavala-Paramo, G. 2010. A simple and rapid method for DNA isolation from xylophagous insects. Int. J. Mol. Sci.11(12): 5056-5064. doi:10.3390/ijms11125056.
6. Christiansen, E. 1985. Ceratocystis polonicainoculated in Norway spruce: bluestaining in relation to inoculum density, resinosis and tree growth. Eur. J. For. Pathol.15: 160-167. doi:10.1111/j.1439-0329.1985.tb00880.x.
7. Christiansen, E., and Solheim, H. 1990. The bark beetle-associated blue-stain fungusOphiostoma polonicumcan kill various spruces and Douglas fir. Eur. J. Plant Pathol.20: 436-446. doi:10.1111/j.1439-0329.1990.tb01159.x.
8. Desprez-Loustau, M.-L. 2009. Alien fungi of Europe. In Handbook of alien species in Europe. Springer, Dordrecht, Netherlands. pp. 15-28.
9. Gardes, M., and Bruns, T.D. 1993. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol.2(2): 113-118.
10. Gerson, H., Illson-Skinner, B., Guthrie, R., and Turgeon, J.J. 2012. Live insects found in wood packaging materials after implementation of ISPM 15. In2012 Forest Pest Management Forum, 4-6 December 2012, Ottawa, Ontario, Canada. Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, Sault Ste. Marie, Ontario.
11. Giordano, L., Garbelotto, M., Nicolotti, G., and Gonthier, P. 2013. Characterization of fungal communities associated with the bark beetleIps typographus varies depending on detection method, location, and beetle population levels. Mycol. Prog.12(1): 127-140. doi:10.1007/s11557-012-0822-1.
12. Haack, R.A. 2001. Intercepted Scolytidae (Coleoptera) at U.S. port of entry: 1985-2000. Integr. Pest Manag. Rev.6: 253-282. doi:10.1023/A:1025715200538.
13. Halik, S., and Bergdahl, D.R. 2002. Potential beetle vector ofSirococcus clavigignentijuglandacearum on butternut. Plant Dis.86: 521-527. doi:10.1094/PDIS.2002. 86.5.521.
14. Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser.41: 95-98.
15. Harding, S. 1989. The influence of mutualistic blue stain fungi on bark beetle population dynamics. Department of Zoology, Royal Veterinary and Agricultural University, Copenhagen, Denmark.
16. Harrington, T.C., and Wingfield, M.J. 1998. TheCeratocystisspecies on conifers. Can. J. Bot.76(8): 1446-1457. doi:10.1139/b98-145.
17. Harrington, T.C., Steimel, J., Wingfield, M.J., and Kile, G.A. 1996. Isozyme variation and species delimitation in theCeratocystis coerulescens complex. Mycologia,88: 104-113. doi:10.2307/3760789.
18. Horntvedt, R., Christiansen, E., Solheim, H., and Wang, S. 1983. Artificial inoculation with Ips typographus-associated blue-stain fungi can kill healthy Norway spruce trees. Medd. Nor. Inst. Skogforsk.38: 1-20.
19. Humble, L.M., and Allen, E.B. 2006. Forest biosecurity: alien invasive species and vectored organisms. Can. J. Plant Pathol.28: S256-S269. doi:10.1080/ 07060660609507383.
20. Jacobs, K., Bergdahl, D.R., Wingfield, M.J., Halik, S., Seifert, K.A., Bright, D.E., and Wingfield, B.D. 2004. Leptographium wingfieldiiintroduced into North America and found associated with exoticTomicus piniperdaand native bark beetles. Mycol. Res.108(4): 411-418. Cambridge University Press. doi:10.1017/ S0953756204009748.
21. Jankowiak, R. 2005. Fungi associated withIps typographusonPicea abiesin southern Poland and their succession into the phloem and sapwood of beetleinfested trees and logs. For. Pathol. 35: 37-55. doi:10.1111/j.1439-0329.2004. 00395.x.
22. Jankowiak, R., Rossa, R., and Mista, K. 2007. Survey of fungal species vectored by Ips cembrae to European larch trees in Raciborskie forests (Poland). Czech Mycol.59(2): 227-239.
23. Jankowiak, R., Kacprzyk, M., and Mlynarczyk, M. 2009. Diversity of ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) colonizing branches of Norway spruce (Picea abies) in southern Poland. Biologia, 64(6): 1170-1177. doi:10.2478/s11756-009-0188-2.
24. Juen, A., and Traugott, M. 2006. Amplification facilitators and multiplex PCR: tools to overcome PCR-inhibition in DNA-gut-content analysis of soil-living invertebrates. Soil Biol. Biochem.38(7): 1872-1879. doi:10.1016/j.soilbio.2005. 11.034.
25. Kirisits, T. 2004. Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In Bark and wood boring insects in living trees in Europe: a synthesis. Edited byF. Lieutuer, K.R. Day, J.C. Grégoire, and H. Evans. Kluwer Academic Publishers, Dordrecht, Netherlands. pp. 181-235.
26. Kirisits, T. 2010. Fungi isolated fromPicea abiesinfested by the bark beetle Ips typographus in the Białowież a forest in north-eastern Poland. For. Pathol. 40(2): 100-110. doi:10.1111/j.1439-0329.2009.00613.x.
27. Kirisits, T., and Offenthaler, I. 2002. Xylem sapflow of Norway spruce after inoculation with the blue-stain fungus Ceratocytis polonica. Plant Pathol. 51: 359-364. doi:10.1046/j.1365-3059.2002.00722.x.
28. Krokene, P., and Solheim, H. 1996. Fungal associates of five bark beetles species colonizing Norway spruce. Can. J. For. Res.26(12): 2115-2122. doi:10.1139/x26-240.
29. Lefever, S., Pattyn, F., Hellemans, J., and Vandesompele, J. 2013. Single-nucleotide polymorphisms and other mismatches reduce performance of quantitative PCR assays. Clin. Chem.59(10): 1470-1480. doi:10.1373/clinchem.2013.203653.
30. Loppnau, P.A., and Breuil, C. 2003. Species level identification of conifer associatedCeratocystissapstain fungi by PCR-RFLP on a-tubulin gene fragment. FEMS Microbiol. Lett.222: 143-147. doi:10.1016/S0378-1097(03)00256-8.
31. Luduena, R.F. 1993. Are tubulin isotypes functionally significant. Mol. Biol. Cell, 4(5): 445-457. doi:10.1091/mbc.4.5.445.
32. Margam, V., Gachomo, E., Shukle, J., Ariyo, O., Seufferheld, M., and Kotchoni, S. 2010. A simplified arthropod genomic-DNA extraction protocol for polymerase chain reaction (PCR)-based specimen identification through barcoding. Mol. Biol. Rep.37(7): 3631-3635. doi:10.1007/s11033-010-0014-5.
33. Marin, M., Preisig, O., Wingfield, B.D., Kirisits, T., Yamaoka, Y., and Wingfield, M.J. 2005. Phenotypic and DNA sequence data comparisons reveal three discrete species in theCeratocystis polonicaspecies complex. Mycol. Res. 109(10): 1137-1148. doi:10.1017/S095375620500362X.
34. Marin, M., Preisig, O., Wingfield, B.D., Kirisits, T., and Wingfield, M.J. 2009. Single sequence repeat markers reflect diversity and geographic barriers in Eurasian populations of the conifer pathogenCeratocystis polonica. For. Pathol. 39: 249-265. doi:10.1111/j.1439-0329.2009.00585.x.
35. Novotny, D. 2010. First record ofCeratocystis laricicola(Ascomycota, Ceratocystidaceae) in the Czech Republic. Czech Mycol.62(1): 59-65.
36. Persson, Y., Vasaitis, R., Langstrom, B., Ohrn, P., Ihrmark, K., and Stenlid, J. 2009. Fungi vectored by the bark beetleIps typographusfollowing hibernation under the bark of standing trees and in the forest litter. Microb. Ecol.58: 651-659. doi:10.1007/s00248-009-9520-1.
37. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
38. Redfern, D.B., Stoackley, J.T., Steele, H., and Minter, D.W. 1987. Dieback and death of larch caused byCeratocystis laricicolasp. nov. following attack byIps cembrae. Plant Pathol. 36: 467-480. doi:10.1111/j.1365-3059.1987.tb02264.x.
39. Rutledge, R.G. 2004. Sigmoidal curve-fitting redefines quantitative real-time PCR with the prospective of developing automated high-throughput applications. Nucleic Acids Res.32(22): e178. doi:10.1093/nar/gnh177.
40. Santini, A., Ghelardini, L., De Pace, C., Desprez-Loustau, M.L., Capretti, P., Chandelier, A., Cech, T., Chira, D., Diamandis, S., Gaitniekis, T., Hantula, J., Holdenrieder, O., Jankovsky, L., Jung, T., Jurc, D., Kirisits, T., Kunca, A., Lygis, V., Malecka, M., Marcais, B., Schmitz, S., Schumacher, J., Solheim, H., Solla, A., Szabò, I., Tsopelas, P., Vannini, A., Vettraino, A.M., Webber, J., Woodward, S., and Stenlid, J. 2013. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol.197(1): 238-250. doi:10.1111/j.1469-8137.2012.04364.x.
41. Schmitt, I., Crespo, A., Divakar, P.K., Fankhauser, J.D., Herman-Sackett, E., Kalb, K., Nelsen, M.P., Nelson, N.A., Rivas-Plata, E., Shimp, A.D., Widhelm, T., and Lumbsch, H.T. 2009. New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia-Int. Mycol. J.23(1): 35-40. doi:10.3767/003158509X470602.
42. Schweigkofler, W., Otrosina, W.J., Smith, S.L., Cluck, D.R., Maeda, K., Peay, K.G., and Garbelotto, M. 2005. 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.35(8): 1798-1808. doi:10.1139/x05-077.
43. Seifert, K.A. 1993. Sapstain of commercial lumber by species ofOphiostomaand Ceratocystis. In Ceratocystis andOphiostoma. Taxonomy, ecology and pathogenicity. Edited byM.J. Wingfield, K.A. Seifert, and J.F. Webber. American Phytopathological Society, St. Paul, Minnesota. pp. 141-152.
44. Six, D.L., and Wingfield, M.J. 2011. The role of phytopathogenicity in bark beetlefungus symbiosis: a challenge to the classic paradigm. Annu. Rev. Entomol. 56: 255-272. doi:10.1146/annurev-ento-120709-144839.
45. Solheim, H. 1986. Species of Ophiostomataceae isolated fromPicea abiesinfested by the bark beetleIps typographus. Nord. J. Bot.6(2): 199-207. doi:10.1111/j.1756-1051.1986.tb00874.x.
46. Solheim, H. 1992a. The early stages of fungal invasion in Norway spruce infested by the bark beetleIps typographus. Can. J. Bot. 70(1): 1-5. doi:10.1139/b92-001.
47. Solheim, H. 1992b. Fungal succession in sapwood of Norway spruce infested by the bark beetleIps typographus. Eur. J. For. Pathol. 22(3): 136-148. doi:10.1111/ j.1439-0329.1992.tb01440.x.
48. Solheim, H. 1993. Fungi associated with the spruce bark beetleIps typographusin an endemic area in Norway. Scand. J. For. Res.8(1-4): 118-122. doi:10.1080/ 02827589309382760.
49. Solheim, H., and Safranyik, L. 1997. Pathogenicity to Sitka spruce ofCeratocystis rufipenniandLeptographium abietinum, blue stain fungi associated with the spruce bark beetle. Can. J. For. Res.27(9): 1336-1341. doi:10.1139/x97-096.
50. Stauffer, C., Kirisits, T., Nussbaumer, C., Pavlin, R., and Wingfield, M.J. 2001. Phylogenetic relationships between the European and Asian eight spined larch bark beetle populations (Coleoptera, Scolytidae) inferred from DNA sequences and fungal associates. Eur. J. Entomol.98: 99-105. doi:10.14411/eje. 2001.014.
51. Uzunovic, A., Yang, D.-Q., Gagné, P., Breuil, C., Bernier, L., Byrne, A., Gignac, M., and Kim, S.H. 1999. Fungi that cause sapstain in Canadian softwoods. Can. J. Microbiol.45(11): 914-922. doi:10.1139/w99-090.
52. Viiri, H. 1997. Fungal associates of the spruce bark beetleIps typographusL. (Col. Scolytidae) in relation to different trapping methods. J. Appl. Entomol. 121(1-5): 529-533. doi:10.1111/j.1439-0418.1997.tb01444.x.
53. Viiri, H., and Lieutier, F. 2004. Ophiostomatoid fungi associated with the spruce bark beetle, Ips typographus, in three areas in France. Ann. For. Sci. 61: 215-219. doi:10.1051/forest:2004013.
54. White, T.J., Bruns, T., Lee, S., and Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR protocols: a guide to methods and applications. Academic Press. Chapter 38. pp. 315-322.
55. Witthuhn, R.C., Wingfield, B.D., Wingfield, M.J., and Harrington, T.C. 1999. PCRbased identification and phyologeny of species ofCeratocystissensu stricto. Mycol. Res.103(6): 743-749. doi:10.1017/S0953756298007679.
56. Witthuhn, R.C., Harrington, T.C., Steimel, J.P., Wingfield, B.D., and Wingfield, M.J. 2000. Comparison of isozymes, rDNA spacer regions and MAT-2 DNA sequences as phylogenetic characters in the analysis of the Ceratocystis coerulescens complex. Mycologia, 92(3): 447-452. doi:10.2307/ 3761503.
57. Wu, J.-H., Hong, P.-Y., and Liu, W.-T. 2009. Quantitative effects of position and type of single mismatch on single base primer extension. J. Microbiol. Methods,77(3): 267-275. doi:10.1016/j.mimet.2009.03.001.
58. Yamaoka, Y., Wingfield, M.J., Takahashi, I., and Solheim, H. 1997. Ophiostomatoid fungi associated with the spruce bark beetleIps typographusf. japonicusin Japan. Mycol. Res.101(10): 1215-1227. doi:10.1017/S0953756297003924.
59. Yamaoka, Y., Wingfield, M.J., Ohsawa, M., and Kuroda, Y. 1998. Ophiostomatoid fungi associated withIps cembraein Japan and their pathogenicity to Japanese larch. Mycoscience,39: 367-378. doi:10.1007/BF02460897.
60. Yamaoka, Y., Takahashi, I., and Igushi, K. 2000. Virulence of ophiostomatoid fungi associated with the spruce bark beetleIps typographusf. japonicusin Yezo spruce. J. For. Res.5: 87-94. doi:10.1007/BF02762525.
61. Zolan, M.E., and Pukkila, P.J. 1986. Inheritance of DNA methylation inCoprinus cinereus. Mol. Cell. Biol. 6(1): 195-200.