Application of electron tomography to fungal ultrastructure studies

New Phytologist

Volumn 172, Issue 2, 2006, Pages 208-220

  Hohmann Marriott, Martin F ^a   Uchida, Maho ^a   Van De Meene, Allison M L ^a   Garret, Matthew ^a   Hjelm, Brooke E ^a   Kokoori, Shylaja ^b   Roberson, Robert W ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Aspergillus nidulans; Cryofixation; Cytoskeleton; Electron tomography; Spitzenk rper

Indexed keywords

BIOLOGICAL METHOD; CRYOPRESERVATION; FUNGUS; INSTRUMENTATION; TOMOGRAPHY; TWO-DIMENSIONAL MODELING; ULTRASTRUCTURE;

ASPERGILLUS NIDULANS; COMPUTER ASSISTED TOMOGRAPHY; CRYOELECTRON MICROSCOPY; CYTOPLASM; FUNGUS; FUNGUS HYPHAE; HISTOLOGY; METHODOLOGY; REVIEW; THREE DIMENSIONAL IMAGING; TISSUE PRESERVATION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ASPERGILLUS NIDULANS; CRYOELECTRON MICROSCOPY; CYTOPLASM; FUNGI; HYPHAE; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, TRANSMISSION; TISSUE EMBEDDING; TISSUE PRESERVATION; TOMOGRAPHY, X-RAY COMPUTED;

EMERICELLA NIDULANS;

EID: 33748792023     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2006.01868.x     Document Type: Review

References (90)

1. Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Salamin LM, Norlen LPO, Richter K, Blanc NS, Studer D, Dubochet J. 2004a. Cryo-electron microscopy of vitreous sections. European Molecular Biology Organization Journal 23: 3583-3588.
2. Al-Amoudi A, Norlen LPO, Dubochet J. 2004b. Cryo-electron microscopy of vitreous sections of native biological cells and tissues. Journal of Structural Biology 148: 131-135.
3. Al-Amoudi A, Studer D, Dubochet J. 2005. Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy. Journal of Structural Biology 150: 109-121.
4. Bajaj C, Yu Z, Auer M. 2003. Volumetric feature extraction and visualization of tomographic molecular imaging. Journal of Structural Biology 144: 132-143.
5. Bartnicki-García S. 2002. Hyphal tip growth: outstanding questions. In: Osiewacz HD, ed. Molecular biology of fungal development. New York: Marcel Dekker, 29-58.
6. Bartnicki-García S, Lippman E. 1969. Fungal morphogenesis: cell wall construction in Mucor rouxii. Science 165: 302-304.
7. Bartnicki-García S, Bracker CE, Reyes E, Ruiz-Herrera J. 1978. Isolation of chitosomes from taxonomically diverse fungi and synthesis of chitin microfibrils in vitro. Experimental Mycology 2: 173-192.
8. Bartnicki-García S, Bartnicki DD, Gierz G, López-Franco R, Bracker CE. 1995. Evidence that Spitzenkörper behavior determines the shape of a fungal hypha: a test of the hyphoid model. Experimental Mycology 19: 53-159.
9. Baumeister W. 2002. Electron tomography: towards visualizing the molecular organization of the cytoplasm. Current Opinion in Structural Biology 12: 679-684.
10. Brandt S, Heikkonen J, Engelhardt P. 2001. Automatic alignment of transmission electron microscope tilt series without fiducial markers. Journal of Structural Biology 136: 201-213.
11. Conway JF, Trus BL, Booy FP, Newcomb WW, Brown JC, Steven AC. 1993. The effects of radiation damage on the structure of frozen hydrated HSV-1 capsids. Journal of Structural Biology 111: 222-233.
12. Cormack AM. 1963. Representation of a function by its line integrals, with some radiological applications. Journal of Applied Physics 34: 2722-2727.
13. Dahl R, Staehelin LA. 1989. High-pressure freezing for the preservation of biological structure. Theory and practice. Journal of Electron Microscopy Technique 13: 165-174.
14. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, McDowall AW, Schultz P. 1988. Cryo-electron microscopy of vitrified specimens. Quarterly Review of Biophysics 21: 129-228.
15. Fisher KE, Lowry DS, Roberson RW. 2000. Cytoplasmic cleavage in zoosporangia of Allomyces macrogynus. Journal of Microscopy 198: 260-270.
16. Frangakis AS, Hegerl R. 2001. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. Journal of Structural Biology 135: 239-250.
17. Frank J. 1992. Introduction: principles of electron tomography. In: Frank J, ed. Electron tomography, three dimensional imaging with the transmission electron microscope. New York, USA: Plenum Press, 1-16.
18. Frank J, McEwen BF. 1992. Alignment by cross-correlation. In: Frank J, ed. Electron tomography, three dimensional imaging with the transmission electron microscope. New York: Plenum Press, 205-213.
19. Frey TG, Perkins GA, Ellisman MH. 2006. Electron tomography of membrane-bound cellular organelles. Annual Review of Biophysics and Biomolecular Structure 35: 199-224.
20. Giddings TH. 2003. Freeze-substitution protocols for improved visualization of membranes in high-pressure frozen samples. Journal of Microscopy 212: 53-61.
21. Gilbert PFC. 1972. The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. II. Direct methods. Proceedings of the Royal Society of London, Series B - Biological Sciences 182: 89-102.
22. Gilkey LC, Staehelin. A. 1986. Advances in ultrarapid freezing for preservation of cellular ultrastructure. Journal of Electron Microscopy Techniques 3: 177-210.
23. Girbardt M. 1957. Der Spitzenkörper von Polystictus versicolor. Planta 50: 47-59.
24. Girbardt M. 1969. Die ultrastruktur der apikalregion von pilzhyphen. Protoplasma 67: 413-411.
25. Grove SN, Bracker CE. 1970. Protoplasmic organization of hyphal tips among fungi. Vesicles and Spitzenkörper. Journal of Bacteriology 104: 989-1009.
26. Harding MW, Stutz JC, Roberson RW. 1999. Host-parasite relationships in bean cultivars of varying susceptibility to bean rust. Canadian Journal of Botany 77: 1551-1559.
27. Harris SD, Momany M. 2004. Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genetics and Biology 41: 391-400.
28. Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M. 2005. Spitzenkörper meets polarisome: microscopy, genetics, and genomics converge. Eukaryotic Cell 4: 225-229.
29. Hart RG. 1968. Electron microscopy of unstained biological material: the polytropic montage. Science 159: 1464-1467.
30. Hoch HC. 1986. Freeze-substitution of fungi. In: Aldrich HC, Todd WJ, eds. Ultrastructure techniques of microorganisms. New York: Plenum Press, 183-211.
31. Hoch HC, Howard RJ. 1981. Ultrastructure of freeze substituted hyphae of the basidiomycete Laetisaria arvalis. Protoplasma 103: 281-297.
32. Hoch HC, Staples RC. 1983. Ultrastructural organization of non-differentiated uredospore germlings of Uromyces phaseoli variety typical. Mycologia 75: 795-824.
33. Hounsfield GN. 1973. Computerized transverse axial scanning tomography: part I description of the system. British Journal of Radiology (London) 46: 1016-1022.
34. Howard RJ. 1981. Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze-substitution. Journal of Cell Science 48: 89-103.
35. Howard RJ, Aist JR. 1979. Hyphal tip cell ultrastructure of the fungus Fusarium: improved preservation by freeze substitution. Journal of Ultrastructural Research 66: 224-234.
36. Howard RJ, O'Donnell KL. 1987. Freeze substitution of fungi for cytological analysis. Experimental Mycology 11: 250-269.
37. Hsieh CE, Marko M, Frank J, Mannella CA. 2002. Electron tomographic analysis of frozen-hydrated tissue sections. Journal of Structural Biology 138: 63-73.
38. Hyde GJ, Lancelle S, Hepler PK, Hardham AR. 1991. Freeze substitution reveals a new model for sporangial cleavage in Phytophthora, a result with implications for cytokinesis in other eukaryotes. Journal of Cell Science 100: 735-746.
39. Iancu CV, Wright ER, Benjamin J, Tivol WF, Dias DP, Murphy GE, Morrison RC, Heymann JB, Jensen GJ. 2005. A 'flip-flop' rotation stage for routine dual-axis electron cryotomography. Journal of Structural Biology 151: 288-297.
40. Jing Z, Sachs F. 1991. Alignment of tomographic projections using an incomplete set of fiducial markers. Ultramicroscopy 35: 37-43.
41. Kiss JZ, Giddings TH, Staehelin LA, Sack FD. 1990. Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips of Nicotiana and Arabidopsis. Protoplasma 157: 64-74.
42. Knauf GM, Welter KM, Müller M, Mendgen K. 1989. The haustorial host-parasite interface in rust-infected bean leaves after high-pressure freezing. Physiological and Molecular Plant Pathology 34: 519-530.
43. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. Journal of Structural Biology 116: 71-76.
44. Larabell C, Le Gros MA. 2004. X-ray tomography generates 3-D reconstructions of the yeast, Saccharomyces cerevisiae, at 60-nm resolution. Molecular Biology of the Cell 15: 957-962.
45. Lucic LV, Forster F, Baumeister W. 2005. Structural studies by electron tomography: from cells to molecules. Annual Review of Biochemistry 74: 833-865.
46. Luther PK. 1992. Sample shrinkage and radiation damage. In: Frank J, ed. Electron tomography, three-dimensional imaging with the transmission electron microscope. New York: Plenum Press, 39-60.
47. Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR. 2001. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proceedings of the National Academy of Sciences, USA 98: 2399-2406.
48. Martone ME, Deerinck TJ, Yamada N, Bushong E, Ellisman MH. 2000. Correlated 3-D light and electron microscopy: use of high voltage electron microscopy and electron tomography for imaging large biological structures. Journal of Histochemical Technique 23: 261-270.
49. Mastronarde DN. 1997. Dual axis tomography: an approach with alignment methods that preserves resolution. Journal of Structural Biology 120: 343-352.
50. McDaniel DP, Roberson RW. 1998. γ-Tubulin is a component of the Spitzenkörper and centrosomes in hyphal tip cells of Allomyces macrogynus. Protoplasma 203: 118-123.
51. McDaniel DP, Roberson RW. 2000. Intracellular motility and mechanisms of control during hyphal tip growth in Allomyces. Fungal Genetics and Biology 31: 223-234.
52. McDonald K, Morphew MK. 1993. Improved ultrastructure in difficult-to-fix organisms by high pressure freezing and freeze substitution. I. Drosophila melanogaster and Strongylocentrotus purpuratus embryos. Microscopic Research and Techniques 24: 465-473.
53. McEwen BF, Downing KH, Glaeser RM. 1995. The relevance of dose fractionation in tomography of radiation-sensitive specimens. Ultramicroscopy 60: 357-373.
54. McIntosh JR. 2001. Electron microscopy of cells: a new beginning for a new century. Journal of Cell Biology 153: F25-F32.
55. McIntosh R, Nicastro D, Mastronarde D. 2005. New views of cells in 3D: an introduction to electron tomography. Trends in Cell Biology 15: 43-51.
56. Medalia O, Weber I, Frangakis AS, Nicastro D, Gerisch G, Baumeister W. 2002. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 5596: 1209-1213.
57. van de Meene A, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW. 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Archives of Microbiology 184: 259-270.
58. Michel M, Hillmann T, Muller M. 1991. Cryosectioning of plant material frozen at high pressure. Journal of Microscopy 163: 3-18.
59. Mims CW, Celio GJ, Richardson EA. 2003. The use of high pressure freezing and freeze substitution to study host-pathogen interactions in fungal diseases of plants. Microscopy and Microanalysis 9: 522-531.
60. Mims CW, Richardson EA. 2005. Ultrastructure of urediniospore development in Coleosporium ipomoeae as revealed by high-pressure freezing followed by freeze substitution. International Journal of Plant Sciences 166: 219-225.
61. Mims CW, Roberson RW, Richardson EA. 1988. Ultrastructure of freeze-substituted and chemically fixed basidiospores of Gynmosporangium juniperi-virginianae. Mycologia 80: 356-364.
62. Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE. 2004. Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5: 338-345.
63. Momany M. 2005. Growth control and polarization. Medical Mycology 43: S23-S25.
64. Moor H. 1987. Theory and practice of high pressure freezing. In: Steinbrecht RA, Zierold K, eds. Cryotechniques in biological electron microscopy. Berlin: Springer-Verlag, 175-191.
65. Müller WH, Koster AJ, Humbel BM, Ziese U, Verkleij AJ, Aelst AC, van der Krift TP, Montijn RC, Boekhout T. 2000. Automated electron tomography of the septal pore cap in Rhizoctonia solani. Journal of Structural Biology 131: 10-18.
66. Nicastro D, Frangakis AS, Typke D, Baumeister W. 2000. Cryo-electron tomography of Neurospora mitochondria. Journal of Structural Biology 129: 48-56.
67. Nickel S, Förster F, Linaroudis A, Del Net W, Beck F, Hegerl R, Baumeister W, Plitzko JM. 2005. TOM software toolbox: acquisition and analysis for electron tomography. Journal of Structural Biology 149: 227-234.
68. O'Toole ET, Giddings TH, McIntosh RJ, Dutcher SK. 2003. Three-dimensional organization of basal bodies from wild-type and ã-tubulin deletion strains of Chlamydomonas reinhardtii. Molecular Biology of the Cell 14: 2999-3012.
69. O'Toole ET, Winey M, McIntosh JR. 1999. High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Molecular Biology of the Cell 10: 2017-2031.
70. O'Toole ET, Winey M, McIntosh JR, Mastronarde DN. 2002. Electron tomography of yeast cells. Methods in Enzymology 351: 81-95.
71. Radermacher M. 1992. Weighted back-projection methods. In: Frank J, ed. Electron tomography, three-dimensional imaging with the transmission electron microscope. New York: Plenum Press, 91-115.
72. Radon J. 1917. Über die Bestimmung von Funktionen durch ihre Integralwerte längs gewisser Manningfaltigkeiten. Berichte über die Verhandlungen der Königlich-Sächsische Gesellschaft der Wissenschaften zu Leipzig, Mathematische-Physikalische Klasse 69: 262-277.
73. Riquelme M, Bartnicki-García S. 2004. Key differences between lateral and apical branching in hyphae of Neurospora crassa. Fungal Genetics and Biology 41: 842-851.
74. Riquelme M, Reynaga-Peña CG, Gierz G, Bartnicki-García S. 1998. What determines growth direction in fungal hyphae? Fungal Genetics and Biology 24: 101-109.
75. Riquelme M, Roberson RW, McDaniel DP, Bartnicki-García S. 2002. The effect of ropy-1 mutation on cytoplasmic organization in mature hyphae of Neurospora crassa. Fungal Genetics and Biology 37: 171-179.
76. Robards AW, Sleytr JB. 1985. Low temperature methods in biological electron microscopy. Practical Methods in Electron Microscopy, 10.
77. Roberson RW. 1992. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84: 41-51.
78. Roberson RW. 1993. Cryofixation and freeze substitution of teliospores of Gymnosporangium clavipes: an ultrastructural investigation. Mycological Research 97: 195-204.
79. Roberson RW, Chandler DE. 1998. Rapid freezing and deep etching of cells and molecules. In: Spector D, Goldman R, Leinwand L, eds. Cell biology: a laboratory handbook. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press, 129.1-130.7.
80. Roberson RW, Fuller MS. 1988. Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma 146: 143-149.
81. Sartori N, Richeter K, Dubochet J. 1993. Vitrification depth can be increased more than 10-fold by high-pressure freezing. Journal of Microscopy 172: 55-61.
82. Skepper JN. 2000. Immunocytochemical strategies for electron microscopy: choice or compromise. Journal of Microscopy 199: 1-36.
83. Steven AC, Aebi U. 2003. The next ice age: cryo-electron tomography of intact cells. Trends in Cell Biology 13: 107-110.
84. Subramaniam S. 2005. Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Current Opinion in Microbiology 8: 316-322.
85. Vanhecke D, Graber W, Herrmann G, Al-Amoudi A, Eggli P, Studer D. 2003. A rapid microbiopsy system to improve the preservation of biological samples prior to high-pressure freezing. Journal of Microscopy 212: 3-12.
86. Vargas M, Aronson JM, Roberson RW. 1993. Cytological organization of hyphal tip cells of Allomyces macrogynus. Protoplasma 176: 43-52.
87. Volkmann N. 2002. A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. Journal of Sturctural Biology 138: 123-129.
88. Welter K, Müller M, Mendgen K. 1988. The hyphae of Uromyces appendiculatus within the leaf tissue after high pressure freezing and freeze substitution. Protoplasma 147: 91-99.
89. Winey M, Morgan GP, Straigh PD, Giddings TH Jr, Mastronarde ND. 2005. Three-dimensional ultrastructure of Saccharomyces cerevisiae meiotic spindles. Molecular Biology of the Cell 16: 1178-1188.
90. Zheng QS, Braundeld MB, Sedat JW, Agard DA. 2004. An improved strategy for automated electron microscopic tomography. Journal of Sturctural Biology 147: 91-101.