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Teliospores of smut fungi teliospore walls and the development of ornamentation studied by electron microscopy

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Summary

The walls of mature teliospores and the development of ornamentation, as seen by transmission electron microscopy, are described for 37 genera of smut fungi, based on observations of ca. 120 species and on literature. Structural diversity of mature teliospore walls is due to differences in spore wall layers forming the spore wall (endosporium, middle layer, exosporium, ornamentation) and to different elements forming the ornamentation (exosporium, ornaments, sheath, hyphal wall, adjacent fungal cells, material of the host). During teliosporogenesis the outer layers are usually deposited first. At the beginning of the formation of the ornamentation the plasma membrane may be smooth or undulated carrying the developing ornaments on its tips or in its depressions. The ornamentation of some genera appears similar when seen by scanning electron microscopy, but can be the product of different developmental patterns (e.g., warts of species ofFarysia, Tilletia, andUstilago), however, warty and reticulate ornamentation can both be produced by similar developmental processes (shown, e.g., for species ofCintractia andTilletia). Typical structures of the mature teliospore wall and developmental patterns based on homologous similarities are described for the following groups of genera or species:Macalpinomyces, Melanopsichium, Sporisorium, andUstilago infecting members of the family Poaceae;Kuntzeomyces, Testicularia, andTrichocintractia; Anthracoidea, Cintractia, Heterotolyposporium piluliforme, andTolyposporium junci; Glomosporium, Sorosporium, andThecaphora; Conidiosporomyces, Erratomyces, Ingoldiomyces, Neovossia, Oberwinkleria, andTilletia; Entyloma, and genera of the Doassansia group;Liroa, Microbotryum, Sphacelotheca, Ustilago infecting dicotyledons, andZundeliomyces; Aurantiosporium, Fulvisporium, andUstilentyloma. Special characteristics of the teliospore wall were observed for the generaDermatosorus, Doassinga, Entorrhha, Farysia, Mycosyrinx, Rhamphospora, and some species ofTolyposporium.

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References

  • Allen JV, Hess WM, Weber DJ (1971) Ultrastructural investigations of dormantTilletia caries teliospores. Mycologia 63: 144–156

    PubMed  Google Scholar 

  • Amerson HV, Van Dyke CG (1978) The ontogeny of echinulation (spines) in uredospores ofPuccinia sparganioides. Exp Mycol 2: 41–50

    Google Scholar 

  • Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 75: 1273–1314

    Google Scholar 

  • Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on nuclear LSU rDNA sequences of smut fungi and related taxa. Can J Bot 75: 2045–2056

    Google Scholar 

  • Berndt R (1993) Untersuchungen zur Ultrastruktur und Anatomie der Melampsoraceen (Uredinales, Basidiomycetes). PhD thesis, University of Tübingen, Tübingen, Federal Republic of Germany

    Google Scholar 

  • Deml G, Oberwinkler F (1981) Studies in Heterobasidiomycetes, part 4: investigations onEntorrhiza casparyana by light and electron microscopy. Mycologia 73: 392–398

    Google Scholar 

  • ——, Bauer R (1985) Studies in Heterobasidiomycetes, part 38:Sphacelotheca polygoni-persicariae G. Deml & Oberw. spec. nov. Phytopathol Z 113: 231–242

    Google Scholar 

  • Döbbeler P (1997) Biodiversity of bryophilous ascomycetes. Biodiv Conserv 6: 721–738

    Google Scholar 

  • Durán R (1982) The species ofThecaphora on Compositae in North America. Can J Bot 60: 1512–1522

    Google Scholar 

  • —, Fischer GW (1961) The genusTilletia. Washington State University, Washington

    Google Scholar 

  • Durrieu G, Rajeriarison C (1968) L'ornementation sporale desUstilago parasites des Polygonacées (observations en microscopie électronique). C R Hebd Séances Acad Sci D 267: 1940–1942

    Google Scholar 

  • Fineran BA (1993) A lamellated striated layer in the spore wall of the smut fungusEntorrhiza (Ustilaginales). Protoplasma 173: 58–69

    Google Scholar 

  • — (1994) Hot fixation of fungal spores for transmission electron microscopy: application to thick-walled spores of the smut fungusEntorrhiza. Mycol Res 98: 799–809

    Google Scholar 

  • —, Fineran JM (1984) Teliospores ofEntorrhiza casparyana (Ustilaginales): a correlated thin-sectioning and freeze-fracture study of endogenously dormant spores. Can J Bot 62: 2525–2539

    Google Scholar 

  • — — (1992) Teliospore wall structure inEntorrhiza (Tilletiaceae) and its relationship to taxonomy of the genus. Can J Bot 70: 1964–1983

    Google Scholar 

  • Fineran JM (1980) The structure of galls induced byEntorrhiza C. Weber (Ustilaginales) on roots of the Cyperaceae and Juncaceae. Nova Hedwigia 32: 265–284

    Google Scholar 

  • Fitt BDL, McCartney HA, Walklate PJ (1989) The role of rain in dispersal of pathogen inoculum. Annu Rev Phytopathol 27: 241–270

    Google Scholar 

  • Gardner JS, Allen JV, Hess WM (1975) Fixation of dormantTilletia teliospores for thin sectioning. Stain Technol 50: 347–350

    PubMed  Google Scholar 

  • — — —, Tripathi RK (1983a) Sheath structure ofTilletia indica teliospores. Mycologia 75: 333–336

    Google Scholar 

  • —, Hess WM, Tripathi RK (1983b) Surface rodlets ofTilletia indica teliospores. J Bacteriol 154: 502–504

    PubMed  Google Scholar 

  • Gäumann E (1964) Die Pilze: Grundzüge ihrer Entwicklungsgeschichte und Morphologie. Birkhäuser, Basel

    Google Scholar 

  • Graham SO (1959) The effects of various reagents, mounting media, and dyes on the teliospore walls ofTilletia contraversa Kühn. Mycologia 51: 477–491

    Google Scholar 

  • — (1960) The morphology and a chemical analysis of the teliospore of the dwarf bunt fungus,Tilletia contraversa. Mycologia 52: 97–118

    Google Scholar 

  • Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J Bot 38: 125–174

    Google Scholar 

  • Hashioka Y, Ikegami H, Horino O (1966) Fine structure of the rice false smut chlamydospores in comparison with that of the cereal smut spores. Res Bull Fac Agric Gifu Univ 22: 40–44

    Google Scholar 

  • Henry CE (1984) A scanning electron microscope study of the surface structure of teliospores of ten species in the Ustilaginales. Bot Gaz 145: 452–460

    Google Scholar 

  • Hess WM, Gardner JS (1983) Development and nature of the partition layer inTilletia caries teliospore walls. J Bacteriol 154: 499–501

    PubMed  Google Scholar 

  • —, Trione EJ (1986) Use of electron microscopy to characterize teliospores ofTilletia caries andT. controversa. Plant Dis 70: 458–460

    Google Scholar 

  • —, Weber DJ (1976) Form and function in basidiomycete spores. In: Weber DJ, Hess WM (eds) The fungal spore: form and function. Wiley Interscience, New York, pp 643–713

    Google Scholar 

  • Hille M, Brandes J (1956) Elektronenmikroskopische Untersuchung der Sporenoberfläche einigerUstilago-Arten. Phytopathol Z 28: 104–109

    Google Scholar 

  • Hiura M (1975) On the hydrolyzate of zeagallan, a new glucan from corn smut galls. J Agric Chem Soc Japan 49: 185–187

    Google Scholar 

  • — (1976) On the acetolyzate and o-methylate of zeagallan, a new glucan from corn smut galls. J Agric Chem Soc Japan 50: 121–126

    Google Scholar 

  • —, Hiura M (1977) On gelatinized hyphal aggregates in corn smut galls. Ann Phytopathol Soc Japan 43: 304–305

    Google Scholar 

  • Huang H-Q, Nielsen J (1984) Hybridization of the seedling-infectingUstilago spp. pathogenic on barley and oats, and a study of the genotypes conditioning the morphology of their spore walls. Can J Bot 62: 603–608

    Google Scholar 

  • Ingold CT (1959) Jelly as a water-reserve in fungi. Trans Br Mycol Soc 42: 475–478

    Google Scholar 

  • Jones D (1968) Surface features of fungal spores as revealed in a scanning electron microscope. Trans Br Mycol Soc 51: 608–610

    Google Scholar 

  • Kakishima M (1980) Smut spores of the Ustilaginales classified by surface structure. Trans Mycol Soc Japan 21: 423–433

    Google Scholar 

  • Khanna A, Payak MM (1968) Teliospore morphology of some smut fungi II: light microscopy. Mycologia 60: 655–662

    Google Scholar 

  • — — (1971) Fine structure of some graminaceous smut spores. J Ultrastruct Res 37: 254

    Google Scholar 

  • — — (1972) Teliospore morphology of some smut fungi IV:Sphacelotheca reiliana. Nova Hedwigia 23: 907–913

    Google Scholar 

  • — —, Mehta SC (1966) Teliospore morphology of some smut fungi I: electron microscopy. Mycologia 58: 562–569

    Google Scholar 

  • — —, Prakash N (1971) Teliospore morphology of some smut fungi III:Ustilago nuda. Ind Phytopathol 24: 481–486

    Google Scholar 

  • Kukkonen I (1964) Taxonomic studies on the species of the section Echinosporae ofAnthracoidea. Ann Bot Fenn 1: 161–177

    Google Scholar 

  • — (1965) Preservation and germination experiments with someAnthracoidea spores. Ann Bot Fenn 2: 113–126

    Google Scholar 

  • —, Vaissalo T (1964) An electron microscope study on spore formation in a smut. Ann Bot Fenn 1: 236–249

    Google Scholar 

  • Langdon RFN, Fullerton RA (1975) Sorus ontogeny and sporogenesis in some smut fungi. Austr J Bot 23: 915–930

    Google Scholar 

  • — — (1977)Macalpinomyces, a new genus of smut fungi. Trans Br Mycol Soc 68: 27–30

    Google Scholar 

  • — — (1978) The genusSphacelotheca (Ustilaginales): criteria for its delimitation and the consequences thereof. Mycotaxon 51: 421–456

    Google Scholar 

  • Laseter JL, Hess WM, Weete JD, Stocks DL, Weber DJ (1968) Chemotaxonomic and ultrastructural studies on three species ofTilletia occurring on wheat. Can J Microbiol 14: 1149–1154

    PubMed  Google Scholar 

  • Ling L, Stevenson JA (1949) A note on the genusKuntzeomyces. Mycologia 41: 87–89

    Google Scholar 

  • Littlefield LJ, Bracker CE (1971) Ultrastructure and development of urediospore ornamentation inMelampsora lini. Can J Bot 49: 2067–2073

    Google Scholar 

  • McCartney HA (1994) Dispersal of spores and pollen from crops. Grana 33: 76–80

    Google Scholar 

  • Mims CW, Snetselaar KM (1991) Teliospore maturation in the smut fungusSporisorium sorghi: an ultrastructural study using freeze substitution fixation. Bot Gaz 152: 1–7

    Google Scholar 

  • — —, Richardson EA (1992) Ultrastructure of the leaf stripe smut fungusUstilago striiformis: host-pathogen relationship and teliospore development. Int J Plant Sci 153: 289–300

    Google Scholar 

  • Mordue JEM (1986) Ustilospore ornamentation in the European genera of smut fungi. Trans Br Mycol Soc 87: 407–431

    Google Scholar 

  • Nagler A (1986) Untersuchungen zur Gattungsabgrenzung vonGinanniella Ciferri undUrocystis Rabenhorst sowie zur Ontogenie vonThecaphora seminis-convolvuli (Desm.) Ito. PhD thesis, University of Tübingen, Tübingen, Federal Republic of Germany

    Google Scholar 

  • Nawaz MS, Hess WM (1987) Ultrastructure ofNeovossia horrida teliospores. Mycologia 79: 173–179

    Google Scholar 

  • Nielsen J (1968) The inheritance of spore wall characteristics inUstilago avenae andU. kolleri. Can J Bot 46: 497–500

    Google Scholar 

  • Nyffeler R (1997) Stem anatomy ofUebelmannia (Cactaceae): with special reference toUebelmannia gummifera. Bot Acta 110: 489–495

    Google Scholar 

  • Ohta R (1966) Electron microscopical observations on spore-wall of some species of Ustilago. Trans Mycol Soc Japan 7: 259–263

    Google Scholar 

  • Paine WA, Hess WM (1984) Ultrastructure of germinating sugarcane smut (Ustilago scitaminea) teliospores. Trans Br Mycol Soc 82: 385–395

    Google Scholar 

  • Payak MM (1964) Palynology of fungi. In: Nair PKK (ed) Recent advances in palynology. National Botanic Gardens, Lucknow, pp 27–55

    Google Scholar 

  • Piepenbring M (1994) Brandpilze (Ustilaginales und Tilletiales) von Costa Rica: Ökologie, Morphologie, Ultrastruktur und Systematik. PhD thesis, University of Tübingen, Tübingen, Federal Republic of Germany

    Google Scholar 

  • — (1995a) Taxonomic studies on Ustilaginales from Costa Rica. Mycol Res 99: 783–788

    Google Scholar 

  • — (1995b)Trichocintractia, a new genus forCintractia utriculicola (Ustilaginales). Can J Bot 73: 1089–1096

    Google Scholar 

  • — (1996) Smut fungi (Ustilaginales and Tilletiales) in Costa Rica. Nova Hedwigia Beih 113: 1–155

    Google Scholar 

  • —, Bauer R (1997)Erratomyces, a new genus of Tilletiales with species on Leguminosae. Mycologia 89: 924–936

    Google Scholar 

  • —, Vánky K, Oberwinkler F (1996)Aurantiosporium, a new genus forUstilago subnitens (Ustilaginales). Plant Syst Evol 199: 53–64

    Google Scholar 

  • —, Bauer R, Oberwinkler F (1998a) Teliospores of smut fungi: general aspects of teliospore walls and sporogenesis. Protoplasma 204: 155–218

    Google Scholar 

  • —, Bauer R, Oberwinkler F (1998b) Teliospores of smut fungi: teliospore connections, appendages, and germ pores studied by electron microscopy; phylogenetic discussion of characteristics of teliospores. Protoplasma 204: 202–218

    Google Scholar 

  • - Hagedorn G, Oberwinkler F (1998c) Spore liberation and dispersal in smut fungi. Bot Acta (in press)

  • Ramberg JE, McLaughlin DJ (1980) Ultrastructural study of promycelial development and basidiospore initiation inUstilago maydis. Can J Bot 58: 1548–1561

    Google Scholar 

  • Robb J (1972) Ultrastructure ofUstilago hordei I: pregermination development of hydrating teliospores. Can J Bot 50: 1253–1261

    Google Scholar 

  • Roberson RW, Luttrell ES (1987) Ultrastructure of teliospore ontogeny inTilletia indica. Mycologia 79: 753–763

    Google Scholar 

  • — —, Fuller MS (1990) Mycoparasitism of teliospores ofUstilago bullata by an oomycete. Can J Bot 68: 2415–2421

    Google Scholar 

  • Savile DBO (1954) Cellular mechanics, taxonomy and evolution in the Uredinales and Ustilaginales. Mycologia 46: 736–761

    Google Scholar 

  • Schwinn FJ (1969) Die Darstellung von Pilzsporen im Raster-Elektronenmikroskop. Phytopathol Z 64: 376–379

    Google Scholar 

  • Swinburne TR, Matthews HI (1963) The surface structure of chlamydospores ofTilletia caries. Trans Br Mycol Soc 46: 245–248

    Google Scholar 

  • Tibell L (1984) A reappraisal of the taxonomy of Caliciales. Nova Hedwigia Beih 79: 597–713

    Google Scholar 

  • Trione EJ, Hess WM, Stockwell VO (1989) Growth and sporulation of the dikaryons of the dwarf bunt fungus in wheat plants and in culture. Can J Bot 67: 1671–1680

    Google Scholar 

  • Vánky K (1987a) Illustrated genera of smut fungi. Gustav Fischer, Stuttgart

    Google Scholar 

  • — (1987b) The genusDermatosorus (Ustilaginales). Trans Br Mycol Soc 89: 61–65

    Google Scholar 

  • — (1987c)Zundeliomyces, a new genus of Ustilaginales. Trans Br Mycol Soc 89: 477–482

    Google Scholar 

  • — (1991) Spore morphology in the taxonomy of Ustilaginales. Trans Mycol Soc Japan 32: 381–400

    Google Scholar 

  • — (1994) European smut fungi. Gustav Fischer, Stuttgart

    Google Scholar 

  • — (1995a) Taxonomical studies on Ustilaginales XII. Mycotaxon 54: 215–238

    Google Scholar 

  • — (1995b) Ustilaginales ofSchoenus (Cyperaceae). Mycotaxon 56: 217–229

    Google Scholar 

  • — (1996)Mycosyrinx and other pair-spored Ustilaginales. Mycoscience 37: 173–185

    Google Scholar 

  • — (1997)Heterotolyposporium, a new genus of Ustilaginales. Mycotaxon 63: 143–154

    Google Scholar 

  • —, Bauer R (1992)Conidiosporomyces, a new genus of Ustilaginales. Mycotaxon 43: 426–435

    Google Scholar 

  • — — (1995)Oberwinkleria, a new genus of Ustilaginales. Mycotaxon 53: 361–368

    Google Scholar 

  • — — (1996)Ingoldiomyces, a new genus of Ustilaginales. Mycotaxon 59: 277–287

    Google Scholar 

  • —, Bauer R, Begerow D (1997)Fulvisporium, a new genus of Ustilaginales. Mycotaxon 64: 57–66

    Google Scholar 

  • - - - (1998)Doassinga, a new genus of Doassansiales (Ustilaginomycetes). Mycologia 190 (in press)

  • Weete JD, Laseter JL, Weber DJ, Hess WM, Stocks DL (1969) Hydrocarbons, fatty acids, and ultrastructure of smut spores. Phytopathology 59: 545–548

    Google Scholar 

  • Zambettakis C (1970) Les caractères qui régissent la classification des Ustilaginales. Rev Mycol (Paris) 34: 399–415

    Google Scholar 

  • Zogg H, Schwinn FJ (1971) Surface structures of spores of the Ustilaginales. Trans Br Mycol Soc 57: 403–410

    Google Scholar 

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  1. Lehrstuhl Spezielle Botanik/Mykologie, Botanisches Institut, Universität Tübingen, Auf der Morgenstelle 1, D-72076, Tübingen, Federal Republic of Germany

    M. Piepenbring, R. Bauer & F. Oberwinkler

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  1. M. Piepenbring
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  2. R. Bauer
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  3. F. Oberwinkler
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Part 165 in the series “Studies in Heterobasidiomycetes” from the Botanical Institute, University of Tübingen

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Piepenbring, M., Bauer, R. & Oberwinkler, F. Teliospores of smut fungi teliospore walls and the development of ornamentation studied by electron microscopy. Protoplasma 204, 170–201 (1998). https://doi.org/10.1007/BF01280323

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