Skip to main content
Genetics logoLink to Genetics
. 1998 Feb;148(2):669–680. doi: 10.1093/genetics/148.2.669

hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans.

S G Kaminskyj 1, J E Hamer 1
PMCID: PMC1459825  PMID: 9504915

Abstract

Aspergillus nidulans grows by apical extension of multinucleate cells called hyphae that are subdivided by the insertion of crosswalls called septa. Apical cells vary in length and number of nuclei, whereas subapical cells are typically 40 microm long with three to four nuclei. Apical cells have active mitotic cycles, whereas subapical cells are arrested for growth and mitosis until branch formation reinitiates tip growth and nuclear divisions. This multicellular growth pattern requires coordination between localized growth, nuclear division, and septation. We searched a temperature-sensitive mutant collection for strains with conditional defects in growth patterning and identified six mutants (designated hyp for hypercellular). The identified hyp mutations are nonlethal, recessive defects in five unlinked genes (hypA-hypE). Phenotypic analyses showed that these hyp mutants have aberrant patterns of septation and show defects in polarity establishment and tip growth, but they have normal nuclear division cycles and can complete the asexual growth cycle at restrictive temperature. Temperature shift analysis revealed that hypD and hypE play general roles in hyphal morphogenesis, since inactivation of these genes resulted in a general widening of apical and subapical cells. Interestingly, loss of hypA or hypB function lead to a cessation of apical cell growth but activated isotropic growth and mitosis in subapical cells. The inferred functions of hypA and hypB suggest a mechanism for coordinating apical growth, subapical cell arrest, and mitosis in A. nidulans.

Full Text

The Full Text of this article is available as a PDF (328.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ayscough K. R., Drubin D. G. ACTIN: general principles from studies in yeast. Annu Rev Cell Dev Biol. 1996;12:129–160. doi: 10.1146/annurev.cellbio.12.1.129. [DOI] [PubMed] [Google Scholar]
  2. Bergen L. G., Morris N. R. Kinetics of the nuclear division cycle of Aspergillus nidulans. J Bacteriol. 1983 Oct;156(1):155–160. doi: 10.1128/jb.156.1.155-160.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borgia P. T., Dodge C. L. Characterization of Aspergillus nidulans mutants deficient in cell wall chitin or glucan. J Bacteriol. 1992 Jan;174(2):377–383. doi: 10.1128/jb.174.2.377-383.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Borgia P. T., Iartchouk N., Riggle P. J., Winter K. R., Koltin Y., Bulawa C. E. The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet Biol. 1996 Sep;20(3):193–203. doi: 10.1006/fgbi.1996.0035. [DOI] [PubMed] [Google Scholar]
  5. Borgia P. T., Miao Y., Dodge C. L. The orlA gene from Aspergillus nidulans encodes a trehalose-6-phosphate phosphatase necessary for normal growth and chitin synthesis at elevated temperatures. Mol Microbiol. 1996 Jun;20(6):1287–1296. doi: 10.1111/j.1365-2958.1996.tb02647.x. [DOI] [PubMed] [Google Scholar]
  6. Bruno K. S., Aramayo R., Minke P. F., Metzenberg R. L., Plamann M. Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J. 1996 Nov 1;15(21):5772–5782. [PMC free article] [PubMed] [Google Scholar]
  7. Clutterbuck A. J. A mutational analysis of conidial development in Aspergillus nidulans. Genetics. 1969 Oct;63(2):317–327. doi: 10.1093/genetics/63.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cunningham K. W., Fink G. R. Ca2+ transport in Saccharomyces cerevisiae. J Exp Biol. 1994 Nov;196:157–166. doi: 10.1242/jeb.196.1.157. [DOI] [PubMed] [Google Scholar]
  9. Cunningham K. W., Fink G. R. Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol. 1996 May;16(5):2226–2237. doi: 10.1128/mcb.16.5.2226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dayton J. S., Means A. R. Ca(2+)/calmodulin-dependent kinase is essential for both growth and nuclear division in Aspergillus nidulans. Mol Biol Cell. 1996 Oct;7(10):1511–1519. doi: 10.1091/mbc.7.10.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doonan J. H. Cell division in Aspergillus. J Cell Sci. 1992 Nov;103(Pt 3):599–611. doi: 10.1242/jcs.103.3.599. [DOI] [PubMed] [Google Scholar]
  12. Drubin D. G., Nelson W. J. Origins of cell polarity. Cell. 1996 Feb 9;84(3):335–344. doi: 10.1016/s0092-8674(00)81278-7. [DOI] [PubMed] [Google Scholar]
  13. Duffy J. B., Perrimon N. Recent advances in understanding signal transduction pathways in worms and flies. Curr Opin Cell Biol. 1996 Apr;8(2):231–238. doi: 10.1016/s0955-0674(96)80070-6. [DOI] [PubMed] [Google Scholar]
  14. Fiddy C., Trinci A. P. Mitosis, septation, branching and the duplication cycle in Aspergillus nidulans. J Gen Microbiol. 1976 Dec;97(2):169–184. doi: 10.1099/00221287-97-2-169. [DOI] [PubMed] [Google Scholar]
  15. Hammerschmidt M., Brook A., McMahon A. P. The world according to hedgehog. Trends Genet. 1997 Jan;13(1):14–21. doi: 10.1016/s0168-9525(96)10051-2. [DOI] [PubMed] [Google Scholar]
  16. Harris S. D., Morrell J. L., Hamer J. E. Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics. 1994 Feb;136(2):517–532. doi: 10.1093/genetics/136.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hastie A. C. Benlate-induced instability of Aspergillus diploids. Nature. 1970 May 23;226(5247):771–771. doi: 10.1038/226771a0. [DOI] [PubMed] [Google Scholar]
  18. Jackson S. L., Heath I. B. Roles of calcium ions in hyphal tip growth. Microbiol Rev. 1993 Jun;57(2):367–382. doi: 10.1128/mr.57.2.367-382.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kore-eda S., Murayama T., Uno I. Isolation and characterization of the adenylate cyclase structural gene of Neurospora crassa. Jpn J Genet. 1991 Jun;66(3):317–334. doi: 10.1266/jjg.66.317. [DOI] [PubMed] [Google Scholar]
  20. Kron S. J., Gow N. A. Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle. Curr Opin Cell Biol. 1995 Dec;7(6):845–855. doi: 10.1016/0955-0674(95)80069-7. [DOI] [PubMed] [Google Scholar]
  21. Kropf D. L., Henry C. A., Gibbon B. C. Measurement and manipulation of cytosolic pH in polarizing zygotes. Eur J Cell Biol. 1995 Nov;68(3):297–305. [PubMed] [Google Scholar]
  22. Käfer E. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet. 1977;19:33–131. doi: 10.1016/s0065-2660(08)60245-x. [DOI] [PubMed] [Google Scholar]
  23. Levina N. N., Lew R. R., Heath I. B. Cytoskeletal regulation of ion channel distribution in the tip-growing organism Saprolegnia ferax. J Cell Sci. 1994 Jan;107(Pt 1):127–134. doi: 10.1242/jcs.107.1.127. [DOI] [PubMed] [Google Scholar]
  24. McGoldrick C. A., Gruver C., May G. S. myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J Cell Biol. 1995 Feb;128(4):577–587. doi: 10.1083/jcb.128.4.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McKenney J. M., Proctor J. D., Harris S., Chinchili V. M. A comparison of the efficacy and toxic effects of sustained- vs immediate-release niacin in hypercholesterolemic patients. JAMA. 1994 Mar 2;271(9):672–677. [PubMed] [Google Scholar]
  26. Meyerowitz E. M. Genetic control of cell division patterns in developing plants. Cell. 1997 Feb 7;88(3):299–308. doi: 10.1016/s0092-8674(00)81868-1. [DOI] [PubMed] [Google Scholar]
  27. Morris N. R. Mitotic mutants of Aspergillus nidulans. Genet Res. 1975 Dec;26(3):237–254. doi: 10.1017/s0016672300016049. [DOI] [PubMed] [Google Scholar]
  28. Motoyama T., Fujiwara M., Kojima N., Horiuchi H., Ohta A., Takagi M. The Aspergillus nidulans genes chsA and chsD encode chitin synthases which have redundant functions in conidia formation [corrected and republished article originally appeared in Mol Gen Genet 1996 Jun; 251(4):442-50]. Mol Gen Genet. 1997 Jan 27;253(4):520–528. doi: 10.1007/s004380050353. [DOI] [PubMed] [Google Scholar]
  29. Motoyama T., Kojima N., Horiuchi H., Ohta A., Takagi M. Isolation of a chitin synthase gene (chsC) of Aspergillus nidulans. Biosci Biotechnol Biochem. 1994 Dec;58(12):2254–2257. doi: 10.1271/bbb.58.2254. [DOI] [PubMed] [Google Scholar]
  30. Mösch H. U., Roberts R. L., Fink G. R. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5352–5356. doi: 10.1073/pnas.93.11.5352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Osmani A. H., van Peij N., Mischke M., O'Connell M. J., Osmani S. A. A single p34cdc2 protein kinase (encoded by nimXcdc2) is required at G1 and G2 in Aspergillus nidulans. J Cell Sci. 1994 Jun;107(Pt 6):1519–1528. doi: 10.1242/jcs.107.6.1519. [DOI] [PubMed] [Google Scholar]
  32. Pierson E. S., Miller D. D., Callaham D. A., Shipley A. M., Rivers B. A., Cresti M., Hepler P. K. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell. 1994 Dec;6(12):1815–1828. doi: 10.1105/tpc.6.12.1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pringle J. R., Bi E., Harkins H. A., Zahner J. E., De Virgilio C., Chant J., Corrado K., Fares H. Establishment of cell polarity in yeast. Cold Spring Harb Symp Quant Biol. 1995;60:729–744. doi: 10.1101/sqb.1995.060.01.079. [DOI] [PubMed] [Google Scholar]
  34. Rasmussen C., Garen C., Brining S., Kincaid R. L., Means R. L., Means A. R. The calmodulin-dependent protein phosphatase catalytic subunit (calcineurin A) is an essential gene in Aspergillus nidulans. EMBO J. 1994 Aug 15;13(16):3917–3924. doi: 10.1002/j.1460-2075.1994.tb06703.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Reichle R. E., Alexander J. V. MULTIPERFORATE SEPTATIONS, WORONIN BODIES, AND SEPTAL PLUGS IN FUSARIUM. J Cell Biol. 1965 Mar 1;24(3):489–496. doi: 10.1083/jcb.24.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Robinow C. F., Caten C. E. Mitosis in Aspergillus nidulans. J Cell Sci. 1969 Sep;5(2):403–431. doi: 10.1242/jcs.5.2.403. [DOI] [PubMed] [Google Scholar]
  37. Rosenberger R. F., Kessel M. Synchrony of nuclear replication in individual hyphae of Aspergillus nidulans. J Bacteriol. 1967 Nov;94(5):1464–1469. doi: 10.1128/jb.94.5.1464-1469.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Smith D. J., Payton M. A. Hyphal tip extension in Aspergillus nidulans requires the manA gene, which encodes phosphomannose isomerase. Mol Cell Biol. 1994 Sep;14(9):6030–6038. doi: 10.1128/mcb.14.9.6030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Som T., Kolaparthi V. S. Developmental decisions in Aspergillus nidulans are modulated by Ras activity. Mol Cell Biol. 1994 Aug;14(8):5333–5348. doi: 10.1128/mcb.14.8.5333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Specht C. A., Liu Y., Robbins P. W., Bulawa C. E., Iartchouk N., Winter K. R., Riggle P. J., Rhodes J. C., Dodge C. L., Culp D. W. The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis. Fungal Genet Biol. 1996 Jun;20(2):153–167. doi: 10.1006/fgbi.1996.0030. [DOI] [PubMed] [Google Scholar]
  41. Ward M. P., Gimeno C. J., Fink G. R., Garrett S. SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol Cell Biol. 1995 Dec;15(12):6854–6863. doi: 10.1128/mcb.15.12.6854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wieser J., Lee B. N., Fondon J. w., 3rd, Adams T. H. Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet. 1994 Dec;27(1):62–69. doi: 10.1007/BF00326580. [DOI] [PubMed] [Google Scholar]
  43. Wolkow T. D., Harris S. D., Hamer J. E. Cytokinesis in Aspergillus nidulans is controlled by cell size, nuclear positioning and mitosis. J Cell Sci. 1996 Aug;109(Pt 8):2179–2188. doi: 10.1242/jcs.109.8.2179. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES