Protoplasma

, Volume 193, Issue 1–4, pp 144–173 | Cite as

Pattern morphogenesis in cell walls of diatoms and pollen grains: a comparison

  • Anna -Maria M. Schmid
  • Roland K. Eberwein
  • Michael Hesse
Article
Received:
Accepted:

Summary

Mechanisms acting in pattern morphogenesis in the cell walls of two distant groups of plants, pollen of spermatophytes and diatoms, are compared in order to discriminate common principles from plant group- and wall material-specific features. The exinous wall in pollen is sequentially deposited on the exocellular side of the plasmalemma, while the siliceous wall in diatoms is formed intracellularly within an expanding silica deposition vesicle (SDV) which is attached to the internal face of the plasmalemma. Two levels of patterning occur in diatom and pollen walls: the overall pattern stabilises the wall mechanically and is apparently initiated in both groups by the parent cell, and a microtubule-dependent aperture and portula pattern created by the new mitotic (diatoms) or meiotic (pollen) cells. The parent wall in diatoms, and also the callosic wall in microspores, functions as anchor surfaces for transient, species-specific patterned adhesions of the plasmalemma to these walls, involved in pattern and shape creation. Patterned adhesion and exocytosis is blocked in pollen walls where the plasmalemma is shielded by the endoplasmic reticulum at the sites of the future apertures. In diatoms, wall patterning is uncoupled from the formation of a siliceous wall per se when the SDV and its wall is formed without contact to the the plasmalemma. Conversely, a blue-print pattern laid out in advance along the plasmalemma can be found in several diatoms. This highlights the key function of the plasmalemma and its associated membrane skeleton (fibrous lamina), and its orchestrated co-operation with elements of the radial filamentous cytoskeleton (actin?) in pattern formation. The role of microtubules during generation of the overall pattern may be primarily a transport and stabilizing function. Auxiliary organelles (spacer vesicles, endoplasmic reticulum, mitochondria) involved in diatoms for shaping the SDV, and a mechanism adhering and disconnecting this SDV together with spacer organelles in a species-specifically controlled sequence to and from the plasmalemma, are unnecessary for pollen wall patterning. The precise positioning of the portula pattern in diatom walls is discussed with respect to their role as permanent anchors of the cytoplasm to its wall, and in providing spatial information for nucelar migration and the next cell division, whereas apertures in pollen are for single use only.

Keywords

Adhesion Cell wall Diatoms Exine Plasmalemma Pollen Silica 

Abbreviations

AF

actin filaments

C/Ca

callose

CF

cleavage furrow

cPL

cleavage plasmalemma

DV

dense vesicles

ER

endoplasmic reticulum

ET

epitheca

HT

hypotheca

mPL

folded plasmalemma

MT

microtubules

MTOC

microtubule organising centre

PEV

primexine (matrix) vesicles

PL

plasmalemma

SDV

silica deposition vesicle

Si

silica

SL

SDV-membrane

SPV

spacer vesicles

This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barnes SH, Blackmore S (1986) Some functional features in pollen development. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press, London, pp. 71–80 (Linnean Society symposium series, vol 12)Google Scholar
  2. Bhandari NN (1984) The microsporangium. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin Heidelberg New York Tokyo, pp 53–121Google Scholar
  3. Blackmore S (1990) Sporoderm homologies and morphogenesis ofEchinops sphaerocephala (Compositae). Plant Syst Evol Suppl 5: 1–12Google Scholar
  4. —, Barnes SH (1987) Pollen wall morphogenesis inTragopogon porrifolius (Compositae: Lactuceae) and its taxonomic significance. Rev Palaeobot Palynol 52: 233–246Google Scholar
  5. — — (1988) Pollen ontogeny inCatananche caerulea L. (Compositae: Lactuceae) I. Premeiotic phase to establishment of tetrads. Ann Bot 62: 605–614Google Scholar
  6. — — (eds) (1991) Pollen and spores: patterns of diversification. Clarendon Press, Oxford, pp. 1–387 (The Systematics Association special volume 44)Google Scholar
  7. —, Ferguson IK (eds) (1986) Pollen and spores: form and function. Academic Press, London (Linnean Society symposium series, vol 12)Google Scholar
  8. —, Knox RB (eds) (1990) Microspores: evolution and ontogeny. Academic Press, LondonGoogle Scholar
  9. —, McConchie CA, Knox RB (1987) Phylogenetic analysis of the male ontogenetic program in aquatic and terrestrial monocotyledons. Cladistics 3: 333–347Google Scholar
  10. Brown RC, Lemmon BE (1987) Involvement of callose in determination of exine patterning in three hepatics of the subclass Jungermanniidae. Mem N Y Bot Garden 45: 11–121Google Scholar
  11. — — (1992) Control of division plane in normal and griseofulvin-treated microsporocytes ofMagnolia, J Cell Sci 103: 1031–1038Google Scholar
  12. Brugerolle G, Bricheux G (1984) Actin microfilaments are involved in scale formation of the chrysomonad cellSynura. Protoplasma 123: 203–212Google Scholar
  13. Buchen B, Sievers A (1981) Sporogenesis and pollen grain formation. In: Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 349–376 (Alfert M et al (eds) Cell biology monographs, vol 8)Google Scholar
  14. Crawford, RM, Hinz F (1995) The spines of the centric diatomCorethron criophilum: light microscopy of vegetative cell division. Eur J Phycol 30: 95–105Google Scholar
  15. Cresti M, Blackmore S, Went JL van (1992) Atlas of sexual reproduction in flowering plants. Springer, Berlin Heidelberg New York Tokyo, pp 1–249Google Scholar
  16. Dickinson HG (1970) Ultrastructural aspects of primexine formation in the microspore tetrad ofLilium longiflorum. Cytobiologie 1: 437–449Google Scholar
  17. — (1976) Common factors in exine deposition. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic Press, London, pp 27–38 (Linnean Society symposium series, vol 1)Google Scholar
  18. —, Bell PR (1970) The development of the sacci during pollen formation inPinus banksiana. Grana 10: 101–108Google Scholar
  19. —, Heslop-Harrison J (1977) Ribosomes, membranes and organelles during meiosis in angiosperms. Philos Trans R Soc Lond Biol 277: 327–342PubMedGoogle Scholar
  20. — — (1968) Common mode of deposition for the sporopollenin of sexine and nexine. Nature 220: 926–927PubMedGoogle Scholar
  21. —, Potter UJ (1976) The development of patterning in the alveolar sexine ofCosmos bipinnatus. New Phytol 76: 543–550Google Scholar
  22. —, Sheldon JM (1984) A radial system of microtubules extending between the nuclear envelope and the plasma membrane during early male haplophase in flowering plants. Planta 161: 86–90Google Scholar
  23. — — (1986) The generation of patterning at the plasma membrane of the young microspores inLilium. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press. London, pp 1–17 (Linnean Society symposium series, vol 12)Google Scholar
  24. — — (1990) The cell biological basis of exine formation inLilium sp. In: Blanca G, Diaz de la Guardia C, Fernandez MC, Garrido M, Rodriguez-Garcia MI, Romero Garcia AT (eds) Polen, esporas y sus aplicaciones. VII Simposio de Palinologia, Granada, 1988. Universidad de Granada, Granada, pp 17–29Google Scholar
  25. Drebes G (1974) Marines Phytoplankton. Eine Auswahl der Helgoländer Planktonalgen (Diatomeen, Peridineen). Thieme, StuttgartGoogle Scholar
  26. — (1976a, b)Attheya decora (Centrales). Vegetative Vermehrung und geschlechtliche Fortpflanzung, b/w 16mm cine films. Institut für Wissenschaftlichen Film, GöttingenGoogle Scholar
  27. Edgar L, Pickett-Heaps JD (1984) Valve morphogenesis in the pennate diatomNavicula cuspidata. J Phycol 20: 47–61Google Scholar
  28. Faegri K, Iversen J (1989) Textbook of pollen analysis, 4th edn. Wiley, ChichesterGoogle Scholar
  29. Feijó JA, Malhó R, Obermeyer G (1995) Ion dynamics and its possible role during in vitro germination and tube growth. Protoplasma 187: 155–167Google Scholar
  30. Franz SM, Schmid AM (1984) Cell-cycle and phenotypes ofBiddulphiopsis titiana. Diatom Res 9: 265–288Google Scholar
  31. French FW, Hargraves PE (1985) Spore formation in the life cycles of the diatomsChaetoceros diadema andLeptocylindrus danicus. J Phycol 21: 447–483Google Scholar
  32. Gabarayeva NI, Rowley JR (1994) Exine development inNymphaea colorata (Nymphaeaceae). Nord. J Bot 14: 671–691Google Scholar
  33. Gersonde R, Harwood DM (1990) Lower cretaceous diatoms from ODP LEG 113 site 693 (Weddel Sea). Part 1: Vegetative cells. In: Barker PF, Kennett JP (eds) Proceedings of the ocean drilling program, scientific results, vol 113. Texas A&M University, College Station, TX, pp 403–425Google Scholar
  34. Gilroy S, Trewavas A (1990) Signal sensing and signal transduction across the plasmamembrane. In: Larsson C, Moller IM (eds) The plant plasma membrane: structure, function and molecular biology. Springer, Berlin Heidelberg New York Tokyo, pp 203–232Google Scholar
  35. Gordon R, Brodland GW (1990) On square holes in pennate diatoms. Diatom Res 5: 409–413Google Scholar
  36. —, Drum RW (1994) The chemical basis of diatom morphogenesis. Int Rev Cytol 150: 243–372Google Scholar
  37. Graybosch RA, Palmer RG (1985a) Male sterility in soybean (Glycine max). I. Am J Bot 72: 1738–1750Google Scholar
  38. —, (1985b) Male sterility in soybean (Glycine max). II. Am J Bot 72: 1751–1764Google Scholar
  39. Halbritter H, Hesse M (1993) Sulcus morphology in some monocot families. Grana 32: 87–99Google Scholar
  40. Hay ED (1991) Cell biology of extracellular matrix. Plenum, New YorkGoogle Scholar
  41. Herth W, Schnepf E (1982) Chitin-fibril formation in algae. In: Brown RM (ed) Cellulose and other natural products. Plenum, New York, pp 185–206Google Scholar
  42. Heslop-Harrison J (1963) An ultrastructural study of pollen wall ontogeny inSilene pendula. Grana Palynol 4: 7–24Google Scholar
  43. — (1971a) Wall pattern formation in angiosperm microsporogenesis. Symp Soc Exp Biol 25: 277–300PubMedGoogle Scholar
  44. — (1971b) The pollen wall: structure and development. In: Heslop-Harrison J (ed) Pollen: development and physiology. Butterworth, London, pp 75–98Google Scholar
  45. Hesse M (1991) Cytology and morphogenesis of pollen and spores. Prog Bot 52: 19–34Google Scholar
  46. —, (1995) Cytology and morphogenesis of pollen and spores. Prog Bot 56: 33–55Google Scholar
  47. Horner HT, Pearson CB (1978) Pollen wall and aperture development inHelianthus annus (Compositae: Heliantheae). Am J Bot 65: 293–309Google Scholar
  48. Hynes RO (1992) Integrins: versatility, modulation, and signalling in cell adhesion. Cell 69: 11–25PubMedGoogle Scholar
  49. Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104: 613–627PubMedGoogle Scholar
  50. Kauss H (1996) Callose synthesis. In: Smallwood M, Knox P, Bowles DJ (eds) Membranes: specialized functions in plant cells. Bios Scientific Publishers, Oxford (in press)Google Scholar
  51. Knox RB (1984) The pollen grain. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin Heidelberg New York Tokyo, pp 197–271Google Scholar
  52. Lacalli TC (1981) Dissipative structures and morphogenetic pattern in unicellular algae. Philos Trans R Soc Lond Biol 294: 547–588Google Scholar
  53. Li CW, Volcani BE (1985) Studies on the biochemistry and fine structure of silica shell formation in diatoms. VII. Morphogenesis of the cell wall in a centric diatom,Ditylum brightwellii. Protoplasma 124: 10–29Google Scholar
  54. Luegmayr E (1994) Pollenmorphologische und pollenontogenetische Untersuchungen an ausgewählten Gesneriaceae. PhD thesis, Universität Wien, Vienna, AustriaGoogle Scholar
  55. McConnaughey T (1989) Biomineralization mechanisms. In: Crick RE (ed) Origin, evolution, and modern aspects of biomineralization in plants and animals. Plenum, New York, pp 57–73Google Scholar
  56. Mann S (1986) Biomineralization in lower plants and animals — chemical perspectives. In: Leadbeater BSC, Riding R (eds) Biomineralization in lower plants and animals. Clarendon Press, Oxford, pp 39–54 (Systematics Association special volume 30)Google Scholar
  57. Mayer C, Schmid AM (1995) Morphology, cell-cycle and growth rates ofOdontella regia. Diatom Res 10: 299–320Google Scholar
  58. Müller O (1906) Pleomorphismus, Auxosporen und Dauersporen bei Melosira-Arten. Jahrb Wiss Bot 43: 49–88Google Scholar
  59. Muñoz CA, Webster BD, Jernstedt JA (1995) Spatial congruence between exine pattern, microtubules and endomembranes inVigna pollen. Sex Plant Reprod 8: 147–151Google Scholar
  60. Obermeyer G, Bentrup FW (1996) Developmental physiology: regulation of polar cell growth and morphogenesis. Prog Bot 57: 54–67Google Scholar
  61. —, Blatt MR (1995) Electrical properties of intact pollen grains ofLilium longiflorum: characteristics of the non-germinating pollen grain. J Exp Bot 46: 803–813Google Scholar
  62. Oey JL, Schnepf E (1970) Über die Auslösung der Valvenbildung bei der DiatomeeCyclotella cryptica. Versuche mit Colchicin, Actinomycin-D, und Fluodesoxyuridin (FUDR). Arch Microbiol 17: 199–213Google Scholar
  63. Otto F (1982) Natürliche Konstruktionen. Deutsche Verlagsanstalt, StuttgartGoogle Scholar
  64. Owens SJ, Sheldon, JM, Dickinson HG (1990) The microtubular cytoskeleton during pollen development. Plant Syst Evol Suppl 5: 31–37Google Scholar
  65. Pacini E (1990) Harmomegathic characters of pteridophyta spores and spermatophyta pollen. Plant Syst Evol Suppl 5: 1–12Google Scholar
  66. Pérez-Muñoz CA, Jernstedt JA, Webster BD (1993a) Pollen wall development inVigna vexillata I. Characterization of wall layers. Am J Bot 80: 1183–1192Google Scholar
  67. — — — (1993b) Pollen wall development inVigna vexillata II. Ultrastructural studies. Am J Bot 80: 1193–1202Google Scholar
  68. Pickett-Heaps JD (1991) Post-mitotic cellular reorganisation in the diatomCymatopleura solea: the role of microtubules and the microtubule centre. Cell Motil Cytoskeleton 18: 279–292Google Scholar
  69. — (1996) Cell division in the centric diatomsOdontella (cf.mobiliensis) & O. sinensis. In: Pickett-Heaps JD, Pickett-Heaps J (eds) Diatoms: Cell division, motility and sexual reproduction. Video-disc. Cytographics Production, Sinauer, Sunderland, MA (in press)Google Scholar
  70. —, Tippit DH, Andreozzi JA (1979) Cell division in the pennate diatomPinnularia. IV. Valve morphogenesis. Biol Cell 35: 199–206Google Scholar
  71. —, Wetherbee R, Hill DRA (1988) Cell division and morphogenesis of the labiate process in the centric diatomDitylum brightwellii. Protoplasma 143: 139–149Google Scholar
  72. —, Schmid AM, Edgar L (1990) The cell biology of diatom valve formation. Prog Phycol Res 7: 1–168Google Scholar
  73. Porter EK, Parry D, Dickinson HG (1983) Changes in poly(A)+ RNA during male meiosis inLilium. J Cell Sci 62: 177–186PubMedGoogle Scholar
  74. Preisig HR (1994) Siliceous structures and silicification in flagellated protists. Protoplasma 181: 29–42Google Scholar
  75. —, Anderson OR, Corliss JO, Moestrup O, Powell MJ, Roberson RW, Wetherbee R (1994) Terminology and nomenclature of protist cell surface structures. Protoplasma 181: 1–28Google Scholar
  76. Punt W, Blackmore S, Nilsson S, LeThomas A (1994) Glossary of pollen and spore terminology. LPP Foundation, Utrecht (LPP contributions series, vol 1)Google Scholar
  77. Reuzeau C, Pont-Lezica RF (1995) Comparing plant and animal extracellular matrix cytoskeleton connections — are they alike? Protoplasma 186: 113–121Google Scholar
  78. Roberts K (1990) Structures at the plant cell surface. Curr Opin Cell Biol 2: 920–928PubMedGoogle Scholar
  79. — (1994) The plant extracellular matrix: in a new expansive mood. Curr Opin Cell Biol 6: 688–694PubMedGoogle Scholar
  80. Robinson DG, Depta H (1988) Coated vesicles. Annu Rev Plant Physiol Plant Mol Biol 39: 53–99Google Scholar
  81. —, Hillmer S (1990) Endocytosis in plants. Physiol Plant 79: 96–104Google Scholar
  82. Round FE, Crawford RM, Mann DG (1990) The diatoms: biology and morphology of the genera. Cambridge University Press, CambridgeGoogle Scholar
  83. Rowley JR, Dahl AO (1977) Pollen development inArtemisia vulgaris with special reference to glycocalyx material. Pollen Spores 19: 169–284Google Scholar
  84. —, Skvarla JJ (1975) The glycocalyx and initiation of exine spinules on microspores ofCanna. Am J Bot 62: 479–485Google Scholar
  85. Russel SD (1979) Fine structure of megagametophyte development inZea mays. Can J Bot 57: 1093–1110Google Scholar
  86. Schindler M (1993) Das neue Bild der Zellwand. Biologie Unserer Zeit 23: 113–120Google Scholar
  87. Schmid AM (1979) Influence of environmental factors on the development of the valve of diatoms. Protoplasma 99: 99–115Google Scholar
  88. Schmid AM (1980) Valve morphogenesis in diatoms: a pattern-related filamentous system in pennates and the effect of APM, colchicine and osmotic pressure. Nova Hedwigia 33: 811–847Google Scholar
  89. - (1984a) Wall morphogenesis inThalassiosira eccentrica: comparison of auxospore formation and the effect of MT-inhibitors. In: Mann DG (ed) Proceedings of the 7th International Symposium on Diatoms, Philadelphia, PA, 1982, pp 47–70Google Scholar
  90. - (1984b) Tricornate spines inThalassiosira eccentrica as a result of valve modelling. In: Mann DG (ed) Proceedings of the 7th International Symposium on Diatoms, Philadelphia, PA, 1982, pp 71–95Google Scholar
  91. — (1984c) Valve morphogenesis in diatoms. In: Bach K, Burckhardt B (eds) Diatoms I. Shells in nature and technics. Cramer, Stuttgart, pp 300–317 (Communications of the Institute of Lightweight Structures, vol 28)Google Scholar
  92. - (1986a) Organization and function of cell-structures in diatoms and their morphogenesis. In: Ricard M (eded) Proceedings of the 8th International Symposium on Diatoms, Paris, 1984, pp 271–292Google Scholar
  93. - (1986b) Wall morphogenesis inCoscinodiscus wailesii. II. Cytoplasmic events of valve morphogenesis. In: Ricard M (ed) Proceedings of the 8th International Symposium on Diatoms, Paris, 1984, pp 293–314Google Scholar
  94. — (1987a) Wall morphogenesis in centric diatoms. In: Wiessner W, Robinson D, Starr RC (eds) Algal development: molecular and cellular aspects. Springer, Berlin Heidelberg New York Tokyo, pp 34–41Google Scholar
  95. — (1987b) Morphogenetic forces in diatom wall formation. In: Bereiter-Hahn J, Anderson OR, Reif WE (eds) Cytomechanics: the mechanical basis of cell form and structure. Springer, Berlin Heidelberg New York Tokyo, pp 183–199Google Scholar
  96. — (1988) The special Golgi-ER-mitochondrium unit in the diatom genusCoscinodiscus. Plant Syst Evol 158: 211–223Google Scholar
  97. — (1994a) Aspects of morphogenesis and function of diatom cell walls with implications for taxonomy. Protoplasma 181: 43–60Google Scholar
  98. — (1994b) Slit scales in the auxospore scale case ofCoscinodiscus granii: the rudiments of rimoportulae? Diatom Res 9: 371–375Google Scholar
  99. - (1994c) Sexual reproduction inCoscinodiscus granii Gough in culture. In: Marino D (ed) Proceedings of the 13th International Symposium on Diatoms, Italy, 1994, pp 139–159Google Scholar
  100. —, Schulz D (1979) Wall morphogenesis in diatoms: deposition of silica by cytoplasmic vesicles. Protoplasma 100: 267–288Google Scholar
  101. —, Volcani BE (1983) Wall morphogenesis ofCoscinodiscus wailesii (Gran) Angst. I. Valve morphology and development of its architecture. J Phycol 19: 387–402Google Scholar
  102. —, Borowitzka MA, Volcani BE (1981) Morphogenesis and biochemistry of diatom cell walls. In: Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 63–97 [Alfert M et al (eds) Cell biology monographs, vol 8]Google Scholar
  103. Schnepf E (1984) The cytological viewpoint of functional compartmentation. In: Wiessner W, Robinson DG, Starr RC (eds) Compartments in algal cells and their interaction. Springer, Berlin Heidelberg New York Tokyo, pp 1–10Google Scholar
  104. —, Deichgräber G (1969) Über die Feinstruktur vonSynura petersenii unter besonderer Berücksichtigung der Morphogenese ihrer Kieselschuppen. Protoplasma 68: 85–106Google Scholar
  105. —, Drebes G (1980) Morphogenetic process inAttheya decora (Bacillariophyceae, Biddulphiinae). Plant Syst Evol 135: 265–277Google Scholar
  106. Scott RJ (1994) Pollen exine — the sporopollenin enigma and the physics of pattern. In: Scott RJ, Stead AD (eds) Molecular and cellular aspects of plant reproduction. Cambridge University Press, Cambridge, pp 49–82Google Scholar
  107. Sheldon JM, Dickinson, HG (1983) Determination of patterning in the pollen wall ofLilium henryi. J Cell Sci 63: 191–208PubMedGoogle Scholar
  108. —, (1986) Pollen wall formation inLilium: the effect of chaotropic agents, and the organization of the microtubluar cytoskeleton during pattern development. Planta 186: 11–23Google Scholar
  109. Shivanna KR, Johri BM (1985) The angiosperm pollen: structure and function. Wiley Eastern, New DelhiGoogle Scholar
  110. Simkiss K (1986) The process of biomineralization in lower plants and animals — an overview. In: Leadbeater BSC, Riding R (eds) Biomineralization in lower plants and animals. Clarendon Press, Oxford, pp 19–37 (Systematics Association special volume 30)Google Scholar
  111. Skvarla JJ, Rowley JR (1987) Ontogeny of pollen inPoinciana (Leguminosae). I. Development of exine template. Rev Palaeobot Palynol 50: 293–311Google Scholar
  112. Southworth D, Jernstedt JA (1995) Pollen exine development precedes microtubule rearrangement inVigna unguiculata (Fabaceae): a model for pollen wall patterning. Protoplasma 187: 79–87Google Scholar
  113. Steucek GL, Schmid AM (1989) Leight weight architecture of the diatomThalassiosira. In: Reiner R, Wirth H (eds) Contributions to the 1st International Symposium “Natürliche Konstruktionen: Leichtbau in Architektur und Natur”, SFB 230, Stuttgart, 1988, pp 195–203Google Scholar
  114. Stosch HA von (1982) On auxospore envelopes in diatoms. Bacillaria 5: 127–156Google Scholar
  115. —, Theil G, Kowallik K (1973) Entwicklungsgeschichtliche Untersuchungen an Diatomeen. V. Bau und Lebenszyklus vonChatoceros didymum, mit Beobachtungen über einige andere Arten der Gattung. Helgol Wiss Meeresunters 25: 384–445Google Scholar
  116. Takahashi M (1989a) Development of the echinate pollen wall inFarfugium japonicum (Compositae: Senecioneae). Bot Mag Tokyo 102: 219–234Google Scholar
  117. — (1989b) Pattern determination of the exine inCaesalpinia japonica (Leguminosae: Caesalpinioideae). Am J Bot 76: 1615–1626Google Scholar
  118. — (1992) Development of spinous exine inNuphar japonicum DeCandolle (Nymphaeaceae). Rev Palaeobot Palynol 75: 317–322Google Scholar
  119. — (1993) Exine initiation and substructure in pollen ofCaesalpinia japonica (Leguminosae: Caesalpinioideae). Am J Bot 80: 192–197Google Scholar
  120. — (1995a) Exine development inAucuba japonica Thunberg (Cornaceae). Rev Palaeobot Palynol 85: 199–205Google Scholar
  121. — (1995b) Three-dimensional aspects of exine initiation and development inLilium longiflorum (Liliaceae). Am J Bot 82: 847–854Google Scholar
  122. — (1995c) Development of structure-less pollen wall inCeratophyllum demersum L. (Ceratophyllaceae). J Plant Res 108: 205–208Google Scholar
  123. —, Kouchi J (1988) Ontogenetic development of spinous exine inHibiscus syriacus (Malvaceae). Am J Bot 75: 1549–1558Google Scholar
  124. —, Skvarla JJ (1991a) Exine pattern formation by plasma membrane inBougainvillea spectabilis Willd. (Nyctaginaceae). Am J Bot 78: 1063–1069Google Scholar
  125. — (1991b) Development of striate exine inIpomopsis rubura (Polemoniaceae). Am J Bot 78: 1724–1731Google Scholar
  126. Tiwari SC (1989) Cytoskeleton during pollen development inTradescantia virginiana: a study employing chemical fixation, freeze-substitution, immunofluorescence, and colchicine administration. Can J Bot 67: 1244–1253Google Scholar
  127. —, Gunning BES (1986) Colchicine inhibits plasmodium formation and disrupts pathways of sporopollenin secretion in the anther tapetum ofTradescantia virginiana L. Protoplasma 133: 115–128Google Scholar
  128. Traas JA (1990) The plasmamembrane associated cytoskeleton. In: Larson C, Moller IM (eds) The plant plasma membrane. Springer, Berlin Heidelberg New York Tokyo, pp 269–292Google Scholar
  129. Traverse A (1988) Paleopalynology. Unwin Hyman, BostonGoogle Scholar
  130. Ubera Jimenez JL, Hidalgo Fernandez P, Schlag MG, Hesse M (1996) Pollen and tapetum development in male fertileRosmarinus officinalis L. (Lamiaceae). Grana 34: 305–316Google Scholar
  131. Uehara K, Kurita S (1991) Ultrastructural study on spore wall morphogenesis inLycopodium clavatum (Lycopodiaceae). Am J Bot 78: 24–36Google Scholar
  132. Uffelen GA van (1991) The control of spore wall formation. In: Blackmore S, Barnes SH (eds) Pollen and spores: patterns of diversification. Clarendon Press, Oxford, pp 89–102 (The Systematics Association special volume 44)Google Scholar
  133. Wang C-S, Walling LL, Gu YQ, Ware CF. Lord EM (1994) Two classes of proteins and mRNAs inLilium longiflorum L. identified by human vitronectin probes. Plant Physiol. 104: 711–717PubMedGoogle Scholar
  134. Waterkeyn L. Bienfait A (1987) Localisation et rôle des β-1,3-glucanes (callose et chrysolaminarine) dans le genrePinnularia (diatomées). Cellule 74: 199–226Google Scholar
  135. Werner D (1977) Introduction with a note on taxonomy. In: Werner D (ed) The biology of diatoms. Bot Monogr 13: 1–17Google Scholar
  136. Wordemann L (1992) The cytoskeleton in diatoms. The mitotic spindle and the cell cycle dependent organization In: Menzel D (ed) The cytoskeleton of the algae. CRC Press, Boca Raton, pp 39–57Google Scholar
  137. Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microspore callose wall causes male sterility in transgenic tobacco. Plant Cell 4: 759–771PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Anna -Maria M. Schmid
    • 1
  • Roland K. Eberwein
    • 2
  • Michael Hesse
    • 2
  1. 1.Institut für PflanzenphysiologieUniversität SalzburgSalzburgAustria
  2. 2.Institut für BotanikUniversität WienVienna

Personalised recommendations