Simultaneous specific in planta visualization of root-colonizing fungi using fluorescence in situ hybridization (FISH)

Mycorrhiza

Volumn 24, Issue 4, 2014, Pages 259-266

  Vági, Pál ^a,b   Knapp, Dániel G ^a   Kósa, Annamária ^a   Seress, Diána ^a   Horváth, Áron N ^a   Kovács, Gábor M ^a,b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Cadophora; CLSM; Dark septate; Endophyte; FISH; Glomus; Microscopy; Rhizophagus; Root; rRNA

Indexed keywords

ARBUSCULAR MYCORRHIZA; DETECTION METHOD; DYE; ECTOMYCORRHIZA; ENDOPHYTE; FLUORESCENCE; FUNGUS; HYBRIDIZATION; MUTUALISM; PATHOGEN; ROOT COLONIZATION; VISUALIZATION;

ARBUSCULAR; CADOPHORA; FUNGI; GLOMUS; RHIZOPHAGUS;

RIBOSOME RNA;

CONFOCAL MICROSCOPY; ENDOPHYTE; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE MICROSCOPY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MYCORRHIZA; PLANT ROOT; PROCEDURES;

ENDOPHYTES; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MYCORRHIZAE; PLANT ROOTS; RNA, RIBOSOMAL;

EID: 84899482373     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-013-0533-8     Document Type: Article

References (42)

1. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541-549. doi: 10. 1890/05-1459.
2. Baker BJ, Hugenholtz P, Dawson SC, Banfield JF (2003) Extremely acidophilic protists host Rickettsiales-lineage endosymbionts with an intervening sequence in their 16S rRNA genes. Appl Environ Microbiol 69: 5512-5518. doi: 10. 1128/AEM. 69. 9. 5512-5518. 2003.
3. Baschien C, Manz W, Neu TR, Marvanová L, Szewcyk U (2008) In situ detection of freshwater fungi in an alpine stream by new taxon-specific fluorescence in situ hybridization probes. Appl Environ Microbiol 74: 6427-6436. doi: 10. 1128/AEM. 00815-08.
4. Bergero R, Harrier LA, Franken P (2003) Reporter genes: applications to the study of arbuscular mycorrhizal (AM) fungi and their symbiotic interactions with plant roots. Plant and Soil 255: 143-155. doi: 10. 1104/pp. 011882.
5. Błaszkowski J, Kovács GM, Gáspár BK, Balázs KT, Buscot F, Ryszka P (2012) The arbuscular mycorrhizal Paraglomus majewskii sp. nov. represents a distinct basal lineage in Glomeromycota. Mycologia 104: 148-156. doi: 10. 3852/10-430.
6. Czymmek KJ, Bourett TM, Howard RJ (2005) Fluorescent protein probes in fungi. In: Savidge T, Pothoulakis C (eds) Methods in microbiology, vol 34. Microbial Imaging Elsevier, Amsterdam, pp 27-62.
7. da Silva GA, Lumini E, Maia LC, Bonfante P, Bianciotto V (2006) Phylogenetic analysis of Glomeromycota by partial LSU rDNA sequences. Mycorrhiza 16: 183-189. doi: 10. 1007/s00572-005-0030-9.
8. Daims H, Stoecker K, Wagner M (2005) Fluorescence in situ hybridization for the detection of prokaryotes. In: Osborn AM, Smith C (eds) Molecular microbial ecology. New York, USA, Taylor and Francis, pp 213-239.
9. Dickson S, Kolesik P (1999) Visualisation of mycorrhizal fungal structures and quantification of their surface area and volume using laser scanning confocal microscopy. Mycorrhiza 9: 205-213. doi: 10. 1007/s005720050268.
10. Diagne N, Escoute J, Lartaud M, Verdeil JL, Franche C, Kane A, Bogusz D, Diouf D, Duponnois R, Svistoonoff S (2011) Uvitex2B: a rapid and efficient stain for detection of arbuscular mycorrhizal fungi within plant roots. Mycorrhiza 21: 315-321. doi: 10. 1007/s00572-010-0357-8.
11. Dreyer B, Morte A, Pérez-Gilabert M, Honrubia M (2006) Autofluorescence detection of arbuscular mycorrhizal fungal structures in palm roots: an underestimated experimental method. Mycol Res 110: 887-897. doi: 10. 1016/j. mycres. 2006. 05. 011.
12. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186-194. doi: 10. 1038/nature10947.
13. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
14. Girlanda M, Perotto S, Luppi AM (2006) Molecular diversity and ecological roles of mycorrhiza-associated sterile fungal endophytes in Mediterranean ecosystems. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin-Heidelberg, pp 207-226. doi: 10. 1007/3-540-33526-9_12.
15. Grünig CR, Queloz V, Sieber TN, Holdenrieder O (2008) Dark septate endophytes (DSE) of the Phialocephala fortinii s. l. - Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany 86: 1355-1369. doi: 10. 1139/B08-108.
16. Hansen K, Lobuglio KF, Pfister DH (2005) Evolutionary relationships of the cup-fungus genus Peziza and Pezizaceae inferred multiple nuclear genes: RPB2, β-tubulin, and LSU rDNA. Mol Phylogenet Evol 36: 1-23. doi: 10. 1016/j. ympev. 2005. 03. 010.
17. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide Web? Nature 394: 431. doi: 10. 1038/28764.
18. Hibbett DS, Ohman A, Kirk PM (2009) Fungal ecology catches fire. New Phytol 184: 279-282. doi: 10. 1111/j. 1469-8137. 2009. 03042. x.
19. Hoch HC, Galvani CD, Szarowski DH, Turner JN (2005) Two new fluorescent dyes applicable for visualization of fungal cell walls. Mycologia 97: 580-588. doi: 10. 3852/mycologia. 97. 3. 580.
20. Hood ME, Shew HD (1996) Applications of KOH-aniline blue fluorescence in the study of plant-fungal interactions. Phytopathology 86: 704-708. doi: 10. 1094/Phyto-86-704.
21. Jones MD, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, Richards TA (2011) Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474: 200-203. doi: 10. 1038/nature09984.
22. Kohout P, Sýkorová Z, Čtvrtlíková M, Rydlová J, Suda J, Vohník M, Sudová R (2012) Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiol Ecol 80: 216-235. doi: 10. 1111/j. 1574-6941. 2011. 01291. x.
23. Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious-dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS ONE 7: e32570. doi: 10. 1371/journal. pone. 0032570.
24. Kovács GM, Szigetvári C (2002) Mycorrhizae and other root-associated fungal structures of the plants of a sandy grassland on the Great Hungarian Plain. Phyton Ann Rei Bot 42: 211-223.
25. Lorang JM, Tuori RP, Martinez JP, Sawyer TL, Redman RS, Rollins JA, Wolpert TJ, Johnson KB, Rodriguez RJ, Dickman MB, Ciuffetti LM (2001) Green fluorescent protein is lighting up fungal biology. Appl Environ Microbiol 67: 1987-1994. doi: 10. 1128/AEM. 67. 5. 1987-1994. 2001.
26. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90. doi: 10. 1038/nature11237.
27. Mandyam K, Jumpponen A (2008) Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza 18: 145-155. doi: 10. 1007/s00572-008-0165-6.
28. Prieto P, Moore G, Shaw P (2007) Fluorescence in situ hybridization on vibratome sections of plant tissues. Nat Protoc 2: 1831-1838. doi: 10. 1038/nprot. 2007. 265.
29. Qian XM, Kottke I, Oberwinkler F (1998) Activity of different ectomycorrhizal types studied by vital fluorescence. Plant and Soil 199: 91-98. doi: 10. 1023/A: 1004226220283.
30. Regvar M, Likar M, Piltaver A, Kugonič N, Smith JE (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant and Soil 330: 345-356. doi: 10. 1007/s11104-009-0207-7.
31. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109: 6241-6246. doi: 10. 1073/pnas. 1117018109.
32. Schulz BJE, Boyle CJC, Sieber TN (eds) (2006) Microbial root endophytes. Soil biology, vol 9. Springer, Berlin-Heidelberg.
33. Séjalon-Delmas N, Magnier A, Douds DD, Bécard G (1998) Cytoplasmic autofluorescence of an arbuscular mycorrhizal fungus Gigaspora gigantea and nondestructive fungal observations in planta. Mycologia 90: 921-926.
34. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Cambridge.
35. Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187: 461-474. doi: 10. 1111/j. 1469-8137. 2010. 03262. x.
36. Stoyke G, Egger KN, Currah RS (1992) Characterization of sterile endophytic fungi from the mycorrhizae of sub-alpine plants. Can J Bot 70: 2009-2016. doi: 10. 1139/b92-250.
37. Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11: 3166-3178. doi: 10. 1111/j. 1462-2920. 2009. 02020. x.
38. Trouvelot S, van Tuinen D, Hijri M, Gianinazzi-Perason V (1999) Visualization of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hybridization. Mycorrhiza 8: 203-206. doi: 10. 1007/s005720050235.
39. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol Plant 125: 393-404. doi: 10. 1111/j. 1399-3054. 2005. 00564. x.
40. Wagner M, Haider S (2012) New trends in fluorescence in situ hybridization for identification and functional analyses of microbes. Curr Opin Biotech 23: 96-102. doi: 10. 1016/j. copbio. 2011. 10. 010 pp. 96-102.
41. Wagg C, Pautler M, Massicote HB, Peterson RL (2008) The co-occurrence of ectomycorrhizal, arbuscular mycorrhizal, and dark septate fungi in seedlings of four members of the Pinaceae. Mycorrhiza 18: 103-110. doi: 10. 1007/s00572-007-0157-y.
42. Yilmaz LS, Parnerkar S, Noguera DR (2011) mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization. Appl Environ Microbiol 77: 1118-1122. doi: 10. 1128/AEM. 01733-10.