, Volume 198, Issue 1–2, pp 53–65 | Cite as

A comparative ultrastructural analysis of exine pattern development in wild-typeArabidopsis and a mutant defective in pattern formation

  • D. M. Paxson-Sowders
  • H. A. Owen
  • C. A. Makaroff


In order to identify factors necessary for the establishment of the reticulate pollen wall pattern, we have characterized a T-DNA tagged mutant ofArabidopsis thaliana that is defective in pattern formation. This study reports the results of an ultrastructural comparison of pollen wall formation in the mutant to wall development in wild-type plants. Pollen wall development in the mutant parallels that of wild-type until the early tetrad stage. At this point in wild-type plants, the microspore plasma membrane assumes a regular pattern of ridges and valleys. Initial sporopollenin deposition occurs on the ridges marking the beginning of probacula formation. In contrast, the plasma membrane in the mutant appears irregular with flattened protuberances and rare invaginations. As a result, the wild-type regular pattern of ridges and valleys is not formed. Sporopollenin is randomly deposited on the plasma membrane and aggregates on the locule wall; it is not anchored to the membrane. Our finding that the mutation blocks the normal invagination of the plasma membrane and disrupts the proper deposition of sporopollenin during wall formation suggests that the mutation could be in a gene responsible for pattern formation. These results also provide direct evidence that the plasma membrane plays a critical role in the establishment of the pollen wall pattern.


Arabidopsis thaliana Exine patterning Male-sterile mutants Plasma membrane Pollen development Sporopollenin 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Cutter EG (1971) Plant anatomy: experiment and interpretation. Addison-Wesley, Reading, MAGoogle Scholar
  2. Dahl AO (1986) Observation on pollen development inArabidopsis under gravitationally controlled environments. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press, London, pp 49–60Google Scholar
  3. Dickinson HG (1970) Ultrastructural aspects of primexine formation in the microspore tetrad ofLilium longiflorum. Cytobiologie 4: 437–449Google Scholar
  4. —, Sheldon JM (1986) The generation of patterning at the plasma membrane of the young microspore ofLilium. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press, London, p 1–17Google Scholar
  5. Erdtman G (1952) Pollen morphology and plant taxonomy: an introduction to palynology. Almqvist and Wiksell, StockholmGoogle Scholar
  6. — (1969) Handbook of palynology: an introduction to the study of pollen grains and spores. Hafner, New YorkGoogle Scholar
  7. Feldmann KA (1991) T-DNA insertion mutagenesis inArabidopsis: mutational spectrum. Plant J 1: 71–82Google Scholar
  8. Fitzgerald MA, Knox RB (1995) Initiation of primexine in freeze-substituted microspores ofBrassica campestris. Sex Plant Reprod 8: 99–104Google Scholar
  9. —, Barnes SH, Blackmore S, Calder DM, Knox RB (1994) Exine formation in the pollinium ofDendrobium. Protoplasma 179: 121–130Google Scholar
  10. Godwin H (1968) The origin of the exine. New Phytol 67: 667–676Google Scholar
  11. Heslop-Harrison J (1963) An ultrastructural study of pollen wall ontogeny inSilene pendula. Grana Palynol 4: 7–24Google Scholar
  12. — (1971a) The pollen wall: structure and development. In: Heslop-Harrison J (ed) Pollen: development and physiology. Butterworths, London, pp 75–98Google Scholar
  13. (1971b) Wall pattern formation in angiosperm microsporogenesis. Symp Soc Exp Biol 25: 277–300Google Scholar
  14. Hoefert LL (1968) Polychromatic stains for the thin sections ofBeta embedded in epoxy resin. Stain Tectmol 43: 145–151Google Scholar
  15. Ingber I (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. I Cell Sci 104: 613–627Google Scholar
  16. Kuang A, Musgrave ME (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation inArabidopsis thaliana. Protoplasma 194: 81–90PubMedGoogle Scholar
  17. Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis inArabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185: 7–21Google Scholar
  18. Peirson BN, Owen HA, Feldmann KA, Makaroff CA (1996) Characterization of three male-sterile mutants ofArabidopsis thaliana exhibiting alterations in meiosis. Sex Plant Reprod 9: 1–16Google Scholar
  19. Pérez-Muñoz CA, Jernstedt JA, Webster BD (1993) Pollen wall development inVigna vexillata II. Ultrastructural studies. Am J Bot 80: 1193–1202Google Scholar
  20. —, Webster BD, Jernstedt JA (1995) Spatial congruence between exine pattern, microtubules and endomembranes inVigna pollen. Sex Plant Reprod 8: 147–151Google Scholar
  21. Scott RJ (1994) Pollen exine — the sporopollenin enigma and the physics of pattern. In: Scott RJ, Stead MA (eds) Molecular and cellular aspects of plant reproduction. Cambridge University Press, Cambridge, pp 49–81Google Scholar
  22. Sheldon JM, Dickinson HG (1983) Determination of patterning in the pollen wall ofLilium henryi. J Cell Sci 63: 191–208PubMedGoogle Scholar
  23. — — (1986) Pollen wall formation inLilium: the effect of chaotropic agents, and the organisation of the microtubular cytoskeleton during pattern development. Planta 168: 11–23Google Scholar
  24. Skvarla JJ, Larson DA (1966) Fine structural studies ofZea mays pollen I. Cell membranes and exine ontogeny. Am J Bot 53: 1112–1125Google Scholar
  25. —, Rowley JR (1987) Ontogeny of pollen inPoinciana (Leguminoseae). I. Development of exine template. Rev Palaeobot Palynol 50: 293–311Google Scholar
  26. Smith MM, McCully ME (1978) A critical evaluation of the specificity of aniline blue induced fluorescence. Protoplasma 95: 229–254Google Scholar
  27. 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
  28. Stanley RG, Linskens HF (1974) Pollen: biology, biochemistry, management. Springer, New York Berlin HeidelbergGoogle Scholar
  29. Sutherland J, McCully ME (1976) A note on the structural changes in the walls of pericycle cells initiating lateral root meristems inZea mays. Can J Bot 54: 2083–2087Google Scholar
  30. Takahashi M (1989) Pattern determination of the exine inCaesalpinia japonica (Leguminosae: Caesalpinioideae). Am J Bot 76: 1615–1626Google Scholar
  31. Takahashi M, Skvarla JJ (1991) Exine pattern formation by plasma membrane inBougainvillea spectabilis Willd. (Nyctaginaceae). Am J Bot 78: 1063–1069Google Scholar
  32. Waterkeyn L, Bienfait A (1970) On a possible function of the callosic special wall inIpomoea purpurea (L) Roth. Grana 10: 13–20Google Scholar
  33. Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4: 759–771PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1997

Authors and Affiliations

  • D. M. Paxson-Sowders
    • 1
  • H. A. Owen
    • 2
  • C. A. Makaroff
    • 1
  1. 1.Department of ChemistryMiami UniversityOxfordUSA
  2. 2.Department of Biological SciencesUniversity of Wisconsin-MilwaukeeMilwaukee

Personalised recommendations