Advertisement

9 Subcellular Structure and Biochemical Characters in Fungal Phylogeny

  • David J. McLaughlin
  • T. K. Arun Kumar
  • Meredith Blackwell
  • Peter M. Letcher
  • Robert W. Roberson
Part of the The Mycota book series (MYCOTA, volume 7B)

Abstract

To clarify the past and potential roles of ultrastructural and biochemical characters in understanding fungal phylogeny and to make these data available for a wider range of fungal studies, we review the history of their study, especially since the mid-twentieth century. Recent molecular phylogenetic studies have revealed major gaps in the structural and biochemical data for Fungi as well as the incompleteness of studies within well-known taxonomic groups. We also consider the efforts to make the limited data on subcellular and biochemical characters available in the Structural and Biochemical Database. This database is a compilation of subcellular and biochemical information from the literature in a standardized format to permit precise data comparisons, identify phylogenetically informative characters, and provide character state coding and illustrations of character states; data are linked to voucher information for each taxon. The data are exportable in NEXUS format, which permits phylogenetic tree and ancestral character state reconstructions. Methods for incorporating structural and biochemical data into phylogenetic and other analyses are discussed, as is the role of the Fungal Subcellular Ontology in promoting data retrieval for use in related cellular, genetic, and ecological studies. Methods for obtaining subcellular data for Fungi are described to provide guidance for the evaluation of existing data and to assist in future data acquisition.

Keywords

Structural Character Glycine Betaine Xylose Reductase Apical Organization Spindle Pole Body 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This work was supported by the National Science Foundation Assembling the Fungal Tree of Life award (DEB-0732550) to D.J.M., (DEB-0732599) to P.M.L., (DEB-0732671) and the Boyd Professor Research Fund to M.B., (DEB-0732503) to R.W.R., College of Biological Sciences and Imaging Center, University of Minnesota, and the Minnesota Supercomputing Institute for support of the Structural and Biochemical Database development. The authors wish to thank Mahajabeen Padamsee and Maritza Abril for their contributions to the AFTOL2 project and Rosanne Healy for assistance with figures and helpful discussion. M.B. acknowledges a Radcliffe Institute Fellowship that provided the time and environment for writing.

References

  1. Alexopoulos CJ (1952) Introductory mycology. Wiley, New York, NYGoogle Scholar
  2. Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory mycology. Wiley, New York, NYGoogle Scholar
  3. Amicucci A, Balestrini R, Kohel A, Barbieri E, Saltarelli R, Faccio A, Roberson RW, Bonfante P, Stocchi V (2010) Hyphal and cytoskeleton polarization in Tuber melanosporum: a genomic and cellular analysis. Fungal Genet Biol 48:561–572PubMedGoogle Scholar
  4. Ammirati JF, Traquair JA, Horgen PA (1985) Poisonous mushrooms of the northern United States and Canada. University of Minnesota Press, Minneapolis, MNGoogle Scholar
  5. Baldauf SL, Battacharya D, Cockrill J, Hugenholtz P, Pawlowski J, Simpson AGB (2004) The tree of life: an overview. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, Oxford, pp 43–75Google Scholar
  6. Baral H-O (1987) Lugol’s solution/IKI versus Melzer’s reagent: hemiamyloidity, a universal feature of the ascus wall. Mycotaxon 29:399–450Google Scholar
  7. Barr DJS (1981) The phylogenetic and taxonomic implications of flagellar rootlet morphology among zoosporic fungi. Biosystems 14:359–370PubMedGoogle Scholar
  8. Barr DJS (1992) Evolution and kingdoms of organisms from the perspective of a mycologist. Mycologia 84:1–11Google Scholar
  9. Barr DJS, Hartmann VE (1977) Zoospore ultrastructure of Olpidium brassicae and Rhizophlyctis rosea. Can J Bot 55:1221–1235Google Scholar
  10. Barrell D, Dimmer E, Huntley RP, Binns D, O’Donovan C, Apweiler R (2009) The GOA database in 2009—an integrated Gene Ontology Annotation resource. Nucleic Acids Res 37:D396–D403PubMedCentralPubMedGoogle Scholar
  11. Bartnicki-Garcia S (1970) Cell wall composition and other biochemical markers in fungal phylogeny. In: Harborne JB (ed) Phytochemical phylogeny. Academic Press, London, pp 81–103Google Scholar
  12. Bartnicki-Garcia S (1987) The cell wall: a crucial structure in fungal evolution. In: Rayner ADM, Brazier CM, Moore D (eds) Evolutionary biology of the fungi. Cambridge University Press, London, pp 389–403Google Scholar
  13. Bartnicki-Garcia S (2006) Chitosomes: past, present and future. FEMS Yeast Res 6:957–965PubMedGoogle Scholar
  14. Bauer R, Oberwinkler F (1991) The symplechosome: a unique cell organelle of some basidiomycetes. Bot Acta 104:93–97Google Scholar
  15. Bauer R, Bergerow D, Oberwinkler F, Piepenbring M, Berbee ML (2001) Ustilaginomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7B, Systematics and evolution. Springer, Berlin, pp 57–83Google Scholar
  16. Beckett A, Heath IB, McLaughlin DJ (1974) An atlas of fungal ultrastructure. Longman Group, LondonGoogle Scholar
  17. Bellemere A (1994) Asci and ascospores in ascomycete systematics. In: Hawksworth DL (ed) Ascomycete systematics: problems and perspectives in the nineties. Plenum, New York, NY, pp 111–125Google Scholar
  18. Benjamin RK (1959) The merosporangiferous Mucorales. El Aliso 4:321–433Google Scholar
  19. Benny GL (1972) Histochemistry of the cell wall and septum of vegetative cells of selected species of Dimargaritaceae and Kickxellaceae. Mycologia 64:854–862Google Scholar
  20. Bentivenga SP, Kumar TKA, Kumar L, Robeson RW, McLaughlin DJ (2013) Cellular organization in germ tubes of Gigaspora. Mycologia 105:1087–1099. doi: 10.3852/12-291 PubMedGoogle Scholar
  21. Bergerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analysis and morphological data. Mycologia 98:900–916Google Scholar
  22. Bonfante P, Balestrini R, Mendgen K (1994) Storage and secretion processes in the spore of Gigaspora margarita Becker & Hall as revealed by high-pressure freezing and freeze substitution. New Phytol 128:93–101Google Scholar
  23. Bourett TM, Howard RJ (1991) Ultrastructural immunolocalization of actin in a fungus. Protoplasma 163:199–202Google Scholar
  24. Bourett TM, Howard RJ (1994) Enhanced labelling of concanavalin A binding sites in fungal endomembranes using a double-sided, indirect method. Mycol Res 98:769–775Google Scholar
  25. Bourett TM, McLaughlin DJ (1986) Mitosis and septum formation in the basidiomycete Helicobasidium mompa. Can J Bot 64:130–145Google Scholar
  26. Bourett TM, Picollelli MA, Howard RJ (1993) Postembedment labeling of intracellular concanavalin A-binding sites in freeze-substituted fungal cells. Exp Mycol 17:223–235Google Scholar
  27. Bracker CE (1967) Ultrastructure of fungi. Annu Rev Phytopathol 5:343–372Google Scholar
  28. Bracker CE, Butler EE (1963) The ultrastructure and development of septa in hyphae of Rhizoctonia solani. Mycologia 55:35–58Google Scholar
  29. Bracker CE, Grove SN (1971) Continuity between cytoplasmic endomembranes and outer mitochondrial membranes in fungi. Protoplasma 73:15–34PubMedGoogle Scholar
  30. Bracker CE, Morré DJ, Grove SN (1996) Structure, differentiation, and multiplication of Golgi apparatus in fungal hyphae. Protoplasma 194:250–274Google Scholar
  31. Braselton JP (2001) Plasmodiophoromycota. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7A, Systematics and evolution. Springer, Berlin, pp 81–91Google Scholar
  32. Buller AHR (1933) The translocation of protoplasm through septate mycelium of certain pyrenomycetes, discomycetes, and hymenomycetes. In: Researches on fungi, vol 5. Longmans, Green, London, pp 75–167Google Scholar
  33. Buser C, McDonald K (2010) Correlative GFP-immunoelectron microscopy in yeast. Method Enzymol 470:603–618Google Scholar
  34. Camon E, Magrane M, Barrell D, Lee V, Dimmer E, Maslen J, Binns D, Harte N, Lopez R, Apweiler R (2004) The Gene Ontology Annotation (GOA) database: sharing knowledge in UniProt with gene ontology. Nucleic Acids Res 32:D262–D266PubMedCentralPubMedGoogle Scholar
  35. Cavalier-Smith T (2001) What are fungi? In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7A, Systematics and evolution. Springer, Berlin, pp 3–37Google Scholar
  36. Celio GJ, Richardson EA, Mims CW (2000) Ultrastructure of the infection of poinsettia by Oidium sp. using high pressure freezing and freeze substitution. Microsc Microanal Proc 6:684–685Google Scholar
  37. Celio GJ, Padamsee M, Dentinger BTM, Bauer R, McLaughlin DJ (2006) Assembling the fungal tree of life: constructing the structural and biochemical database. Mycologia 98:850–859PubMedGoogle Scholar
  38. Celio GJ, Padamsee M, Dentinger BTM, Josephsen KA, Jenkinson TS, McLaughlin EG, McLaughlin DJ (2007) Septal pore apparatus and nuclear division of Auriscalpium vulgare. Mycologia 99:644–654PubMedGoogle Scholar
  39. Chandler DE, Roberson RW (2009) Current concepts in light and electron microscopy. Jones and Bartlett, Boston, MAGoogle Scholar
  40. Chong J, Barr DJS (1974) Ultrastructure of the zoospores of Entophlyctis confervae-glomeratae, Rhizophydium patellarium and Catenaria anguillulae. Can J Bot 52:1197–1204Google Scholar
  41. Cole GT (1979) Contributions of electron microscopy to fungal classification. Am Zool 19:589–608Google Scholar
  42. Dewel RA, Dewel WC (1990) The fine structure of the zoospore of Sorochytrium milnesiophthora. Can J Bot 68:1968–1977Google Scholar
  43. Dhavale T, Jedd G (2007) The fungal woronin body. In: Howard RJ, Gow NAR (eds) The mycota, vol 8, Biology of the fungal cell, 2nd ed. Springer, Berlin, pp 87–96Google Scholar
  44. Dick MW (2001) The peronosporomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7A, Systematics and evolution. Springer, Berlin, pp 39–72Google Scholar
  45. Dodd JL, McCracken DA (1972) Starch in fungi. Mycologia 64:1341–1343PubMedGoogle Scholar
  46. Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND (2000) Confocal microscopy of FM4-64 as a tool for analyzing endocytosis and vesicle trafficking in living fungal hyphae. J Microsc 198:246–259PubMedGoogle Scholar
  47. Fisher KE, Lowry DS, Roberson RW (2000) Cytoplasmic cleavage in zoosporangia of Allomyces macrogynus. J Microsc 198:260–270PubMedGoogle Scholar
  48. Frieders EM, McLaughlin DJ (1996) Mitosis in the yeast phase of Agaricostilbum pulcherrimum and its evolutionary significance. Can J Bot 74:1392–1406Google Scholar
  49. Fuller MS (1977) The zoospore, hallmark of the aquatic fungi. Mycologia 69:1–20Google Scholar
  50. Fuller MS (2001) Hyphochytriomycota. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7A, Systematics and evolution. Springer, Berlin, pp 73–80Google Scholar
  51. Fuller MS, Jaworski A (1987) Zoosporic fungi in teaching and research. Southeastern Publishing, Athens, GAGoogle Scholar
  52. Gene Ontology Consortium, Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29Google Scholar
  53. Gene Ontology Consortium (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261Google Scholar
  54. Gene Ontology Consortium (2006) The Gene Ontology (GO) project in 2006. Nucleic Acids Res 34:D322–D326PubMedCentralGoogle Scholar
  55. Gene Ontology Consortium (2008) The Gene Ontology (GO) project in 2008. Nucleic Acids Res 36:D440–D444Google Scholar
  56. Giberson RT, Demaree RS Jr (1995) Microwave fixation: understanding the variables to achieve rapid reproducible results. Microsc Res Tech 32:246–254PubMedGoogle Scholar
  57. Giberson RT, Demaree RS, Nordhausen RW (1997) Four-hour processing of clinical/diagnostic specimens for electron microscopy. J Vet Diagn Invest 9:61–67PubMedGoogle Scholar
  58. Giddings TH (2003) Freeze-substitution protocols for improved visualization of membranes in high-pressure frozen samples. J Microsc 212:53–61PubMedGoogle Scholar
  59. Gilkey JC, Staehelin LA (1986) Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J Electron Micr Tech 3:177–210Google Scholar
  60. Giner JL, Zhao H, Beach DH, Parish EJ, Jayasimhulu K, Kaneshiro ES (2002) Comprehensive and definitive structural identities of Pneumocystis carinii sterols. J Lipid Res 43:1114–1124PubMedGoogle Scholar
  61. Girbardt M (1957) Der Spitzenkörper von Polystictus versicolor. Planta 50:47–59Google Scholar
  62. Girbardt M (1969) Die Ultrastruktur der Apikalregion von Pilzhyphen. Protoplasma 67:413–441Google Scholar
  63. Glauert AM (1991) Fixation, dehydration and embedding of biological specimens. North-Holland, AmsterdamGoogle Scholar
  64. Gold JJ, Heath IB, Bauchop T (1988) Ultrastructural description of a new chytrid genus of caecum anaerobe, Caecomyces equi gen. nov, sp. nov., assigned to the Neocallimasticaceae. Biosystems 21:403–415Google Scholar
  65. Grandmougin-Ferjani A, Dalpé Y, Hartmann MA, Laruelle F, Sancholle M (1999) Sterol distribution in arbuscular mycorrhizal fungi. Phytochemistry 50:1027–1031Google Scholar
  66. Grove SN, Bracker CE (1970) Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkörper. J Bacteriol 104:989–1009PubMedCentralPubMedGoogle Scholar
  67. Harding MW, Stutz JC, Roberson RW (1999) Host-parasite relationships in bean cultivars of varying susceptibility to bean rust. Can J Bot 77:1551–1559Google Scholar
  68. Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M (2004) Spitzenkörper meets polarisome: microscopy, genetics, and genomics converge. Eukaryot Cell 4:225–229Google Scholar
  69. Hawker LE (1965) Fine structure of fungi as revealed by electron microscopy. Biol Rev Camb Philos Soc 40:52–92PubMedGoogle Scholar
  70. Healy RA, Kumar TKA, Hewitt DA, McLaughlin DJ (2013) Functional and phylogenetic implications of septal pore ultrastructure in the ascoma of Neolecta vitellina. Mycologia 105:802–813. doi: 10.3852/12-347 PubMedGoogle Scholar
  71. Heath IB (1980) Variant mitoses in lower eukaryotes: indicators of evolution of mitosis? Int Rev Cytol 64:1–80PubMedGoogle Scholar
  72. Heath IB (1986) Nuclear division: a marker for protist phylogeny. Prog Protistol 1:115–162Google Scholar
  73. Heath IB, Rethoret K (1982) Mitosis in the fungus Zygorhynchus moelleri: evidence for stage specific enhancement of microtubule preservation by freeze substitution. European J Cell Biol 28:180–189Google Scholar
  74. Heath IB, Bauchop T, Skipp RA (1983) Assignment of the rumen anaerobe Neovcallimastix frontalis to the Spizellomycetales (Chytridiomycota) on the basis of its polyflagellate zoospore ultrastructure. Can J Bot 61:295–307Google Scholar
  75. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James TY, Kirk PM, Lucking R, Lumbsch HT, Lutzoni FL, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljag U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schußler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547PubMedGoogle Scholar
  76. Hoch HC (1986) Freeze-substitution of fungi. In: Aldrich HC, Todd WJ (eds) Ultrastructural techniques for microorganisms. Plenum, New York, NY, pp 183–212Google Scholar
  77. Hoch HC, Fuller MS (1977) Mycoparasitic relationships I. Morphological features of interaction between Pythium acanthicum and several fungal hosts. Arch Microbiol 111:207–224Google Scholar
  78. Hoch HC, Howard RJ (1980) Ultrastructure of freeze substituted hyphae of the basidiomycete Laetisaria arvalis. Protoplasma 103:281–297Google Scholar
  79. Hoch HC, Howard RJ (1981) Conventional chemical fixations induce artifactual swelling of dolipore septa. J Exp Mycol 5:167–172Google Scholar
  80. Hoch HC, Staples RC (1983) Ultrastructural organization of the non-differentiated uredospore germling of Uromyces phaseoli variety typica. Mycologia 75:795–824Google Scholar
  81. Hohmann-Marriott MF, Uchida M, van de Meene AML, Garret M, Hjelm BE, Kokoori S, Roberson RW (2006) Electron tomography and its application to revealing fungal ultrastructure: Tansley review. New Phytol 172:208–220PubMedGoogle Scholar
  82. Howard RJ (1981) Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze substitution. J Cell Sci 48:89–103PubMedGoogle Scholar
  83. Howard RJ, Aist JR (1979) Hyphal tip cell ultrastructure of the fungus Fusarium: improved preservation by freeze-substitution. J Ultrastruct Res 66:224–234PubMedGoogle Scholar
  84. Howard RJ, Aist JR (1980) Cytoplasmic microtubules and fungal morphogenesis: ultrastructure effects of methyl benzimidazole-2-ylcarbamate determined by freeze-substitution of hyphal tip cells. J Cell Biol 87:55–64PubMedGoogle Scholar
  85. Howard RJ, O’Donnell KL (1987) Freeze substitution of fungi for cytological analysis. Exp Mycol 11:250–269Google Scholar
  86. Hughes LM, Bao J, Hu Z-L, Honavar V, Reecy JM (2008) Animal trait ontology: the importance of a unified trait vocabulary for animal species. J Anim Sci 86:1485–1491PubMedCentralPubMedGoogle Scholar
  87. Hutchison LJ, Summerbell RC (1990) Studies on the systematics of ectomycorrhizal fungi in axenic culture. Reactions of mycelia to diazonium blue B stain. Mycologia 82:36–42Google Scholar
  88. James TY, Kauff F, Schoch C, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüssler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DH, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006a) Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443:818–822PubMedGoogle Scholar
  89. James TY, Letcher PM, Longcore JE, Mozley-Standridge SE, Porter D, Powell MJ, Griffith GW, Vilgalys R (2006b) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and a proposal for a new phylum (Blastocladiomycota). Mycologia 98:860–871PubMedGoogle Scholar
  90. Jenkinson TS, Celio GJ, Padamsee M, Dentinger BTM, Meyer ML, McLaughlin DJ (2008) Conservation of cytoplasmic organization in the cystidia of Suillus species. Mycologia 100:539–547PubMedGoogle Scholar
  91. Joffrion TM, Cushion MT (2010) Sterol biosynthesis and sterol uptake in the fungal pathogen Pneumocystis carinii. FEMS Microbiol Lett 311:1–9PubMedGoogle Scholar
  92. Kaneshiro ES (2002) Sterol biosynthesis in Pneumocystis: unique steps that define unique targets. Drug Resist Updat 5:259–268PubMedGoogle Scholar
  93. Kimbrough JW (1994) Septal ultrastructure and ascomycete systematics. In: Hawksworth DL (ed) Ascomycete systematics: problems and perspectives in the nineties. Plenum, New York, NY, pp 127–141Google Scholar
  94. Kleven NL, McLaughlin DJ (1989) A light and electron microscopic study of the developmental cycle in the basidiomycete Pachnocybe ferruginea. Can J Bot 67:1336–1348Google Scholar
  95. Köhli M, Galati V, Boudier V, Roberson RW, Philippsen P (2008) Growth-speed correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. J Cell Sci 121:3803–3814Google Scholar
  96. Kumar TKA, Crow JA, Wennblom TJ, Abril M, Letcher PM, Blackwell M, Roberson RW, McLaughlin DJ (2011) An ontology of fungal subcellular traits. Am J Bot 98:1504–1510PubMedGoogle Scholar
  97. Kumar TKA, Healy R, Spatafora JW, Blackwell M, McLaughlin DJ (2012) Orbilia ultrastructure, character evolution and phylogeny of Pezizomycotina. Mycologia 104:462–476. doi: 10.3852/11-213 PubMedGoogle Scholar
  98. Kumar TKA, Blackwell M, Letcher PM, Roberson RW, McLaughlin DJ (2013) Research and teaching with the AFTOL SBD: an informatics resource for fungal subcellular and biochemical data. IMA Fungus 4:259–263. doi: 10.5598/imafungus.2013.04.02.11 Google Scholar
  99. Kuo M (2006) Using a microscope: equipment. MushroomExpert.Com website. http://www.mushroomexpert.com/microscope_equipment.html
  100. Kurtzman CP, Fell JW, Boekhout T (eds) (2011) The yeasts: a taxonomic study, 5th edn. Amsterdam, ElsevierGoogle Scholar
  101. Lange L, Olson LW (1978) The zoospore of Olpidium radicale. Trans Brit Mycol Soc 71:43–55Google Scholar
  102. Letcher PM, Powell MJ (2005) Kappamyces, a new genus in the Chytridiales. Nova Hedwigia 80:115–133Google Scholar
  103. Letcher PM, Powell MJ, Churchill PF, Chambers JG (2006) Ultrastructural and molecular delineation of a new order, the Rhizophydiales. Mycol Res 110:898–915PubMedGoogle Scholar
  104. Letcher PM, Powell MJ, Viusent MC (2008) Rediscovery of an unusual chytridiaceous fungus new to the order Rhizophydiales. Mycologia 100:325–334PubMedGoogle Scholar
  105. Lewis PR, Knight DP (1977) Staining methods for sectioned material. North-Holland, AmsterdamGoogle Scholar
  106. Li J, Heath IB (1991) The development and zoospore ultrastructure of a polycentric chytridiomycete gut fungus, Orpinomyces joyonii comb. nov. Can J Bot 69:580–589Google Scholar
  107. Linnaeus C (1753) Species plantarum. Laurentius Salvius, StockholmGoogle Scholar
  108. Longcore JE, Simmons DR (2012) The Polychytriales ord. nov. contains chitinophilic members of the rhizophlyctoid alliance. Mycologia 104:276–294PubMedGoogle Scholar
  109. López-Franco R, Bracker CE (1996) Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195:90–111Google Scholar
  110. Lü HS, McLaughlin DJ (1991) Ultrastructure of the septal pore apparatus and early septum initiation in Auricularia auricula-judae. Mycologia 83:322–334Google Scholar
  111. Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung G-H, Lücking R, Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim Y-W, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R (2004) Where are we in assembling the fungal tree of life, classifying the fungi, and understanding the evolution of their subcellular traits? Am J Bot 91:1446–1480PubMedGoogle Scholar
  112. Maddison WP, Maddison DR (2000) MacClade, version 4, Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MAGoogle Scholar
  113. Maddison WP, Maddison DR (2007) Mesquite: a modular system for evolutionary analysis, version 2.0. http://mesquiteproject.org
  114. Martin GW (1955) Are fungi plants? Mycologia 47:779–792Google Scholar
  115. McCracken DA, Dodd JL (1971) Molecular structure of starch-type polysaccharides from Hericium ramosum and Hericium coralloides. Science 174:419PubMedGoogle Scholar
  116. McDaniel DP, Roberson RW (2000) Intracellular motility and mechanisms of control during hyphal tip growth in Allomyces. Fungal Genet Biol 31:223–234Google Scholar
  117. McLaughlin DJ (1990) A new cytoplasmic structure in the basidiomycete Helicogloea: the microscala. Exp Mycol 14:331–338Google Scholar
  118. McLaughlin DJ, Beckett A, Yoon KS (1985) Ultrastructure and evolution of ballistosporic basidiospores. Bot J Linn Soc 91:253–271Google Scholar
  119. McLaughlin DJ, Berres ME, Szabo LJ (1995a) Molecules and morphology in basidiomycete phylogeny. Can J Bot 73(Suppl 1):S684–S692Google Scholar
  120. McLaughlin DJ, Frieders EM, Lü HS (1995b) A microscopist’s view of heterobasidiomycete phylogeny. Stud Mycol 38:91–109Google Scholar
  121. McLaughlin DJ, Frieders EM, Berres ME, Doublès JC, Wick SM (1996) Immunofluorescence analysis of the microtubule cytoskeleton in the yeast phase of the basidiomycete Kriegeria eriophori with a brief note on the yeast phase of Septobasidium carestianum. Mycologia 88:339–349Google Scholar
  122. McLaughlin DJ, McLaughlin EG, Lemke PA (eds) (2001) The mycota. Systematics and evolution, vol 7A, B. Springer, BerlinGoogle Scholar
  123. McLaughlin DJ, Celio GJ, Padamsee M, Dentinger BTM (2008) Cystidial structure in two genera of the Russulales. Botany 86:545–550Google Scholar
  124. McLaughlin DJ, Hibbett DS, Lutzoni F, Spatafora JW, Vilgalys R (2009) The search for the Fungal Tree of Life. Trends Microbiol 17:488–497PubMedGoogle Scholar
  125. Melzer MV (1924) L’ornementation des spores de Russules. Bull Soc Myc de Fr 40:78–81Google Scholar
  126. Mendgen K, Welter K, Scheffold F, Knauf-Beiter G (1991) High pressure freezing of rust infected leaves. In: Mendgen K, Leseman DE (eds) Electron microscopy of plant pathogens. Springer, Berlin, pp 31–42Google Scholar
  127. Miller SL (1988) Early basidiospore formation in Lactarius lignyotellus. Mycologia 80:99–107Google Scholar
  128. Mims CW, Richardson EA (2005) Light and electron microscopy of teliospores and teliospore germination in the rust fungus Coleosporium ipomoeae. Can J Bot 83:451–458Google Scholar
  129. Mims CW, Roberson RW, Richardson EA (1988) Ultrastructure of freeze-substituted and chemically fixed basidiospores of Gymnosporangium juniperi-virginianae. Mycologia 80:356–364Google Scholar
  130. Mims CW, Richardson EA, Kimbrough JW (1990) Ultrasturcture of ascopore delimitation in freeze substituted samples of Ascodesmis nigricans (Pezizales). Protoplasma 156:94–102Google Scholar
  131. Mims CW, Rodriguez-Lother C, Richardson EA (2002) Ultrastructure of the host–pathogen interface in daylily leaves infected by the rust fungus Puccinia hemerocallidis. Protoplasma 219:221–226PubMedGoogle Scholar
  132. 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. Microsc Microanal Proc 9:522–531Google Scholar
  133. Moor H (1987) Theory and practice of high pressure freezing. In: Steinbrecht RA, Ziehold K (eds) Cryotechniques in biological electron microscopy. Springer, New York, NY, pp 175–191Google Scholar
  134. Moore RT, McAlear JR (1962) Fine structure of Mycota 7. Am J Bot 49:86–94Google Scholar
  135. Mozley-Standridge SE, Letcher PM, Longcore JE, Porter D, Simmons DR (2009) Cladochytriales - a new order in Chytridiomycota. Mycol Res 113:498–507PubMedGoogle Scholar
  136. Newhouse JR, Hoch HC, MacDonald WL (1983) The ultrastructure of Endothia parasitica. Comparison of a virulent with a hyphovirulent isolate. Can J Bot 61:389–399Google Scholar
  137. Nylander W (1865) Ad historiam reactionis iodi apud Lichenes et Fungos notula. Flora 48:465–468Google Scholar
  138. Nylander W (1867) Hypochlorite of lime and hydrate of potash, two new criteria in the study of lichens. J Linn Soc Bot 9:358–365, Translated and communicated by LeightonGoogle Scholar
  139. O’Donnell KL, McLaughlin DJ (1981) Ultrastructure of meiosis in the hollyhock fungus, Puccinia malvacearum I. Prophase I – prometaphase I. Protoplasma 108:225–244Google Scholar
  140. O’Donnell KL, McLaughlin DJ (1984) Ultrastructure of meiosis in Ustilago maydis. Mycologia 76:468–485Google Scholar
  141. Oberwinkler F, Bauer R (1989) The systematics of gasteroid, auricularioid heterobasidiomycetes. Sydowia 41:224–256Google Scholar
  142. Oberwinkler F, Kirschner R, Arenal F, Villarreal M, Rubio V, Bergerow D, Bauer R (2006) Two new pycnidial members of the Atractiellales: Basidiopycnis hyalina and Proceropycnis pinicola. Mycologia 98:637–649PubMedGoogle Scholar
  143. Padamsee M, Celio GJ, McLaughlin DJ (2008) Reciprocal illumination: using phylogeny and ultrastructure to study cystidia of two Psathyrella species. Botany 86:1–9Google Scholar
  144. Padamsee M, Kumar TKA, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K, Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC (2012) The common food contaminant Wallemia sebi has a small genome and reveals mechanisms for surviving an osmotically stressful environment. Fungal Genet Biol 49:217–226PubMedGoogle Scholar
  145. Pereira J (1854) The elements of materia medica and therapeutics. Blanchard and Lea, Philadelphia, PAGoogle Scholar
  146. Pfister DH, Kimbrough JW (2001) Discomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota, vol 7A, Systematics and evolution. Springer, Berlin, pp 257–281Google Scholar
  147. Picard KT, Letcher PM, Powell MJ (2009) Rhizidium phycophilum, a new species in Chytridiales. Mycologia 101:696–706PubMedGoogle Scholar
  148. Poon NH, Day AW (1976) Somatic nuclear division in the sporidia of Ustilago violacea. IV. Microtubules and spindle pole body. Can J Microbiol 22:507–522PubMedGoogle Scholar
  149. Powell MJ, Letcher PM, Longcore JE (2011) Operculomyces is a new genus in the order Rhizophydiales. Mycologia 103:854–862PubMedGoogle Scholar
  150. Prillinger H, Dörfler C, Laaser G, Hauska G (1990) A contribution to the systematics and evolution of higher fungi: yeast-types in the basidiomycetes. Part III: Ustilago-type. Z Mycol 56:251–278Google Scholar
  151. Prillinger H, Oberwinkler F, Umile C, Tlachac K, Bauer R, Dörfler C, Taufratzhofer E (1993) Analysis of cell wall carbohydrates (neutral sugars) from ascomycetous and basidiomycetous yeasts with and without derivatization. J Gen Appl Microbiol 39:1–34Google Scholar
  152. Prillinger H, Lopandic K, Schweigkofler W, Deak R, Henk J, Aarts HJM, Bauer R, Sterflinger K, Kraus GF, Maraz A (2002) Phylogeny and systematics of the fungi with special reference to the Ascomycota and Basidiomycota. In: Breitenbach M, Crameri R, Lehrer SB (eds) Fungal allergy and pathogenicity, vol 81, Chem Immunol. Karger, Basel, pp 207–295Google Scholar
  153. Reichle RE, Lichtwardt RW (1972) Fine structure of the trichomycete, Harpella melusinae, from black-fly guts. Arch Mikrobiol 81:103–125Google Scholar
  154. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212PubMedCentralPubMedGoogle Scholar
  155. Rezaeian M, Beakes GW, Parker DS (2004) Methods for the isolation, culture and assessment of the status of anaerobic rumen chytrids in both in vitro and in vivo systems. Mycol Res 34:1215–1226Google Scholar
  156. Riquelme M, McDaniel D, Roberson RW, Bartnicki-García S (2002) The effect of ropy-1 mutation on cytoplasmic organization in mature hyphae of Neurospora crassa. Fungal Genet Biol 37:171–179PubMedGoogle Scholar
  157. Roberson RW (1993) Cryofixation and freeze substitution of teliospores of Gymnosporangium clavipes: an ultrastructural investigation. Mycol Res 97:195–204Google Scholar
  158. Roberson RW, Fuller MS (1988) Ultrastructural aspects of the hyphal tip of Sclerotium rolfsii preserved by freeze substitution. Protoplasma 146:143–149Google Scholar
  159. Roberson RW, Fuller MS (1990) Effects of the sterol biosynthesis inhibitor cyproconazole on hyphal tip cells of Sclerotium rolfsii. II. An electron microscopic study. Exp Mycol 14:124–135Google Scholar
  160. Roberson RW, Luttrell ES (1987) Ultrastructure of teliospore ontogeny in Tilletia indica. Mycologia 79:753–763Google Scholar
  161. Roberson RW, Vargas M (1994) The tubulin cytoskeleton and its sites of nucleation in Allomyces macrogynus. Protoplasma 182:19–31Google Scholar
  162. Roberson RW, Luttrell ES, Fuller MS (1990) Mycoparasitisum of teliospores of the smut fungus Ustilago bullata by an oomycete. Can J Bot 68:2415–2421Google Scholar
  163. Roberson RW, Abril M, Blackwell M, Letcher P, McLaughlin DJ, Mouriño-Pérez RR, Riquelme M, Uchida M (2010) Hyphal structure. In: Borkovich K, Ebbole D (eds) Cellular and molecular biology of filamentous fungi. ASM Press, Washington, DC, pp 8–24Google Scholar
  164. Roberson RW, Saucedo B, MacLean D, Propster J, Unger B, O’Neil TA, Parvanehgohar K, Cavanaugh C, Lowry D (2011) The hyphal tip structure of Basidiobolus sp.: a zygomycete fungus of uncertain phylogeny. Fungal Biol 115:485–492PubMedGoogle Scholar
  165. Rolland L (1887) De la coloration en bleu développée par l’iode sur divers champignons. Bull Soc Myc de Fr 3:134–137Google Scholar
  166. Shields JP, Fuller MS (1996) Ultrastructure of chytridiomycete and oomycete zoopores using spray-freeze fixation. Protoplasma 191:84–95Google Scholar
  167. Silva MT, Guerra FC, Magalhães MM (1968) The fixative action of uranyl acetate in electron microscopy. Experientia 24:1074PubMedGoogle Scholar
  168. Simmons RD, James TY, Meyer AF, Longcore JE (2009) Lobulomycetales, a new order in the Chytridiomycota. Mycol Res 113:450–460PubMedGoogle Scholar
  169. Srijayanthi S, Vargas M, Roberson RW (1996) Functional, organizational, and biochemical analysis of actin in the hyphal tip cells of Allomyces macrogynus. Mycologia 88:57–80Google Scholar
  170. Stajich JE, Berbee ML, Blackwell M, Hibbett DS, James TY, Spatafora JW, Taylor JW (2009) The fungi. Curr Biol 19:R840–R845PubMedCentralPubMedGoogle Scholar
  171. Swann EC, Frieders EM, McLaughlin DJ (1999) Microbotryum, Kriegeria, and the changing paradigm in basidiomycete classification. Mycologia 91:51–66Google Scholar
  172. Swofford DL (2002) PAUP*, Phylogenetic analysis using parsimony (*and other methods), version 4.0. Sinauer Associates, Sunderland, MAGoogle Scholar
  173. Taylor JW (1984) Correlative light and electron microscopy with fluorescent stains. Mycologia 76:462–467Google Scholar
  174. Taylor J, Mims CW (1990) Fungal development and host cell responses in the rust fungus Puccinia substriata var. indica in seedlings of mature leaves of susceptible and resistant pearl millet. Can J Bot 69:1207–1219Google Scholar
  175. Tevayanond R (1981) On the nature of the reaction of diazonium blue B with basidiomycetous yeasts. PhD Thesis, University of California, DavisGoogle Scholar
  176. Torruella G, Suga H, Riutort M, Pereto J, Ruiz-Trillo I (2009) The evolutionary history of lysine biosynthesis pathways within eukaryotes. J Mol Evol 69:240–248PubMedGoogle Scholar
  177. Urbina H, Blackwell M (2012) Multilocus phylogenetic study of the Scheffersomyces yeast clade and characterization of the N-terminal region of xylose reductase gene. PLoS ONE 7(6):e39128PubMedCentralPubMedGoogle Scholar
  178. Van Driel KGA, van Peer AF, Grijpstra J, Wösten HAB, Verkleij AJ, Muller WH, Boekhout T (2008) Septal pore cap protein SPC18, isolated from the basidiomycetous fungus Rhizoctonia solani, also resides in pore plugs. Eukaryot Cell 7:1865–1873PubMedCentralPubMedGoogle Scholar
  179. Van Driel KGA, Humbel BM, Verkleij AJ, Stalpers J, Müller WH, Boekhout T (2009) Septal pore complex morphology in the Agaricomycotina (Basidiomycota) with emphasis on the Cantharellales and Hymenochaetales. Mycol Res 113:559–576PubMedGoogle Scholar
  180. Van Peer AF, Wang F, van Driel KGA, de Jong JF, van Donselaar EG, Müller WH, Boekhout T, Lugones LG, Wösten HAB (2010) The septal pore cap is an organelle that functions in vegetative growth and mushroom formation of the wood-rot fungus Schizophyllum commune. Environ Microbiol 12:833–884PubMedGoogle Scholar
  181. Vargas M, Aronson JM, Roberson RW (1993) Cytological organization of hyphal tip cells of Allomyces macrogynus. Protoplasma 176:43–52Google Scholar
  182. Vélez CG, Letcher PM, Schultz S, Powell MJ, Churchill PF (2011) Molecular phylogenetic and zoospore ultrastructural analyses of Chytridium olla establish the limits of a monophyletic Chytridiales. Mycologia 103:118–130PubMedGoogle Scholar
  183. Vogel HJ (1960) Two modes of lysine synthesis among lower fungi: evolutionary significance. Biochim Biophys Acta 41:172–173Google Scholar
  184. Vogel HJ (1965) Lysine biosynthesis and evolution: fungi, gymnosperms and angiosperms. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic, New York, NY, pp 25–40Google Scholar
  185. Webster P (2007) Microwave-assisted processing and embedding for transmission electron microscopy. In: Kuo J (ed) Electron microscopy methods and protocols. Humana Press, Totowa, NJ, pp 47–65Google Scholar
  186. Weete JD, Abril M, Blackwell M (2010) Phylogenetic distribution of fungal sterols. PLoS One 5(5):e10899. doi: 10.1371/journal.pone.0010899 PubMedCentralPubMedGoogle Scholar
  187. Weiss M, Bauer R, Bergerow D (2004) Spotlights on heterobasidiomycetes. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in basidiomycete mycology. IHW, Eching, pp 7–48Google Scholar
  188. White MM, James TY, O’Donnell K, Cafaro MJ, Tanabe Y, Sugiyama J (2006) Phylogeny of the Zygomycota based on nuclear ribosomal sequence data. Mycologia 98:872–884PubMedGoogle Scholar
  189. Winey M, Mamay CL, O’Toole ET, Mastronarde DN, Giddings TH, McDonald KL, McIntosh JR (1995) Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J Cell Biol 129:1601–1615PubMedGoogle Scholar
  190. Yoon KS, McLaughlin DJ (1986) Basidiosporogenesis in Boletus rubinellus II. Late spore development. Mycologia 8:185–197Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • David J. McLaughlin
    • 1
  • T. K. Arun Kumar
    • 2
  • Meredith Blackwell
    • 3
    • 4
  • Peter M. Letcher
    • 5
  • Robert W. Roberson
    • 6
  1. 1.Department of Plant BiologyUniversity of MinnesotaSt. PaulUSA
  2. 2.Department of BotanyThe Zamorin’s Guruvayurappan CollegeCalicutIndia
  3. 3.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  4. 4.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA
  5. 5.Department of Biological SciencesUniversity of AlabamaTuscaloosaUSA
  6. 6.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations