1887

Microbiology Society logo

Volume 150, Issue 10

Interspore bridges: a new feature of the spore wall Free

Abstract

The spore wall is a multilaminar coat that surrounds individual spores and protects them from environmental insult. Scanning electron microscopy reveals that the four spores of an ascus are connected by interspore bridges. Transmission electron microscopy of spores indicates that these bridges are continuous with the outer layers of the spore wall. In mutants, which lack the chitosan and dityrosine layers of the spore wall, bridges are absent. By contrast, in mutants, which lack only the dityrosine layer, bridges are present, suggesting that the bridges may be composed of chitosan. Interspore bridges are shown to be necessary to hold spores together after release from the ascus. A function for these bridges in the maintenance of heterozygous markers in a homothallic yeast population is proposed.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): SEM, scanning electron microscopy and TEM, transmission electron microscopy
© SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27253-0
2004-10-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/10/mic1503189.html?itemId=/content/journal/micro/10.1099/mic.0.27253-0&mimeType=html&fmt=ahah

References

  1. Briza, P., Winkler, G., Kalchhauser, H. & Breitenbach, M.(1986). Dityrosine is a prominent component of the yeast ascospore wall. A proof of its structure. J Biol Chem 261, 4288–4294. [Google Scholar]
  2. Briza, P., Ellinger, A., Winkler, G. & Breitenbach, M.(1988). Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan. J Biol Chem 263, 11569–11574. [Google Scholar]
  3. Briza, P., Ellinger, A., Winkler, G. & Breitenbach, M.(1990). Characterization of a dl-dityrosine-containing macromolecule from yeast ascospore walls. J Biol Chem 265, 15118–15123. [Google Scholar]
  4. Briza, P., Eckerstorfer, M. & Breitenbach, M.(1994). The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble ll-dityrosine-containing precursor of the yeast spore wall. Proc Natl Acad Sci U S A 91, 4524–4528.[CrossRef] [Google Scholar]
  5. Briza, P., Kalchhauser, H., Pittenauer, E., Allmaier, G. & Breitenbach, M.(1996).N,N′-Bisformyl dityrosine is an in vivo precursor of the yeast ascospore wall. Eur J Biochem 239, 124–131.[CrossRef] [Google Scholar]
  6. Christodoulidou, A., Bouriotis, V. & Thireos, G.(1996). Two sporulation-specific chitin deacetylase-encoding genes are required for the ascospore wall rigidity of Saccharomyces cerevisiae. J Biol Chem 271, 31420–31425.[CrossRef] [Google Scholar]
  7. Felder, T., Bogengruber, E., Tenreiro, S., Ellinger, A., Sa-Correia, I. & Briza, P.(2002). Dtrlp, a multidrug resistance transporter of the major facilitator superfamily, plays an essential role in spore wall maturation in Saccharomyces cerevisiae. Eukaryot Cell 1, 799–810.[CrossRef] [Google Scholar]
  8. Gutz, H., Heslot, H., Leupold, U. & Loprieno, N.(1974).Schizosaccharomyces pombe. In Handbook of Genetics, pp. 365–446. Edited by R. C. King. New York: Plenum.
  9. Herskowitz, I. & Jensen, R. E.(1991). Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol 194, 132–146. [Google Scholar]
  10. Kreger-Van Rij, N. J.(1978). Electron microscopy of germinating ascospores of Saccharomyces cerevisiae. Arch Microbiol 117, 73–77.[CrossRef] [Google Scholar]
  11. Kupiec, M., Byers, B., Esposito, R. E. & Mitchell, A. P.(1997). Meiosis and sporulation in Saccharomyces cerevisiae. In The Molecular Biology of the Yeast Saccharomyces. Cell Cycle and Biology, pp. 889–1036. Edited by J. R. Pringle, J. R. Broach & E. W. Jones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  12. Longtine, M. S., McKenzie, A. 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. & Pringle, J. R.(1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953–961.[CrossRef] [Google Scholar]
  13. Lynn, R. R. & Magee, P. T.(1970). Development of the spore wall during ascospore formation in Saccharomyces cerevisiae. J Cell Biol 44, 688–692.[CrossRef] [Google Scholar]
  14. Milton, J. B.(1997).Selection in Natural Populations. Oxford: Oxford University Press.
  15. Mishra, C., Semino, C. E., McCreath, K. J., de la Vega, H., Jones, B. J., Specht, C. A. & Robbins, P. W.(1997). Cloning and expression of two chitin deacetylase genes of Saccharomyces cerevisiae. Yeast 13, 327–336.[CrossRef] [Google Scholar]
  16. Moens, P. B.(1971). Fine structure of ascospore development in the yeast Saccharomyces cerevisiae. Can J Microbiol 17, 507–510.[CrossRef] [Google Scholar]
  17. Mortimer, R. K. & Hawthorne, D. C.(1969). Yeast genetics. In The Yeasts, pp. 386–453. Edited by A. H. Rose & J. S. Harrison. London: Academic Press.
  18. Nakamura, T., Abe, H., Hirata, A. & Shimoda, C.(2004). ADAM family protein Mde10 is essential for development of spore envelopes in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell 3, 27–39.[CrossRef] [Google Scholar]
  19. Neiman, A. M.(1998). Prospore membrane formation defines a developmentally regulated branch of the secretory pathway in yeast. J Cell Biol 140, 29–37.[CrossRef] [Google Scholar]
  20. Neiman, A. M., Katz, L. & Brennwald, P. J.(2000). Identification of domains required for developmentally regulated SNARE function in Saccharomyces cerevisiae. Genetics 155, 1643–1655. [Google Scholar]
  21. Orlean, P.(1997). Biogenesis of yeast wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Cell Cycle and Biology, pp. 229–262. Edited by J. R. Pringle, J. R. Broach & E. W. Jones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  22. Pammer, M., Briza, P., Ellinger, A., Schuster, T., Stucka, R., Feldmann, H. & Breitenbach, M.(1992).DIT101 (CSD2, CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls. Yeast 8, 1089–1099.[CrossRef] [Google Scholar]
  23. Rieder, S. E., Banta, L. M., Kohrer, K., McCaffery, J. M. & Emr, S. D.(1996). Multilamellar endosome-like compartments accumulate in the yeast vps28 vacuolar protein sorting mutant. Mol Biol Cell 7, 985–999.[CrossRef] [Google Scholar]
  24. Rose, M. D. & Fink, G. R.(1990).Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  25. Smits, G. J., van den Ende, H. & Klis, F. M.(2001). Differential regulation of cell wall biogenesis during growth and development in yeast. Microbiology 147, 781–794. [Google Scholar]
  26. Strathern, J. N. & Herskowitz, I.(1979). Asymmetry and directionality in production of new cell types during clonal growth: the switching pattern of homothallic yeast. Cell 17, 371–381.[CrossRef] [Google Scholar]
  27. Tachikawa, H., Bloecher, A., Tatchell, K. & Neiman, A. M.(2001). A Gip1p-Glc7p phosphatase complex regulates septin organization and spore wall formation. J Cell Biol 155, 797–808.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27253-0
Loading
Interspore bridges: a new feature of the Saccharomyces cerevisiae spore wall
Microbiology 150, 3189 (2004); https://doi.org/10.1099/mic.0.27253-0
/content/journal/micro/10.1099/mic.0.27253-0
/content/journal/micro/10.1099/mic.0.27253-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error