Skip to main content
Log in

Calmodulin concentrates at the apex of growing hyphae and localizes to the Spitzenkörper in Aspergillus nidulans

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary.

The calmodulin (CaM) localization pattern in the growing hyphal tip of Aspergillus nidulans was studied with the functional GFP::CaM fusion protein. A faint tip-high gradient of CaM was found in the growing hyphal tip, with CaM highly localized in the region corresponding to the Spitzenkörper forming a bright granule. The position of highly concentrated CaM in the extreme apex seemed to determine the orientation of the hypha. The normal pattern of CaM localization was also shown to be dependent on the integrated actin cytoskeleton. When the growth of the hyphal tip ceased, CaM failed to localize in the bright granule and was evenly distributed in the hyphal tip. These findings suggest that CaM may play an important role in establishing and maintaining apical organization, morphogenesis, and growth in Aspergillus nidulans.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • ED Allen R Aiuto AS Sussman (1980) ArticleTitleEffects of cytochalasins on Neurospora crassa. I. Growth and ultrastructure Protoplasma 102 63–75 Occurrence Handle6447315 Occurrence Handle1:CAS:528:DyaL3cXktVWgurk%3D Occurrence Handle10.1007/BF01276948

    Article  PubMed  CAS  Google Scholar 

  • S Bartnicki-García E Lippman (1969) ArticleTitleFungal morphogenesis: cell wall construction in Mucor rouxii Science 165 302–304 Occurrence Handle5787989

    PubMed  Google Scholar 

  • S Bartnicki-García F Hergert G Gierz (1989) ArticleTitleComputer simulation of fungal morphogenesis and the mathematical basis for hyphal tip growth Protoplasma 153 46–57 Occurrence Handle10.1007/BF01322464

    Article  Google Scholar 

  • Bracker CE, Murphy DJ, López-Franco R (1997) Laser microbeam manipulation of cell morphogenesis in growing fungal hyphae. In: Farkas DL, Tromberg BJ (eds) Functional imaging and optical manipulation of living cells. Proceedings of the SPIE, vol 2983. International Society for Optical Engineering, Bellingham, Wash, pp 67–80

  • SE Brockerhoff TN Davis (1992) ArticleTitleCalmodulin concentrates at regions of cell growth in Saccharomyces cerevisiae J Cell Biol 118 619–629 Occurrence Handle1639847 Occurrence Handle1:CAS:528:DyaK38XltVOrtbo%3D Occurrence Handle10.1083/jcb.118.3.619

    Article  PubMed  CAS  Google Scholar 

  • D Chin AR Means (2000) ArticleTitleCalmodulin: a prototypical calcium sensor Trends Cell Biol 10 322–328 Occurrence Handle10884684 Occurrence Handle1:CAS:528:DC%2BD3cXkvVyrtLw%3D Occurrence Handle10.1016/S0962-8924(00)01800-6

    Article  PubMed  CAS  Google Scholar 

  • DT Clarkson C Brownlee SM Ayling (1988) ArticleTitleCytoplasmic calcium measurements in intact higher plant cells: results from fluorescence ratio imaging of fura-2 J Cell Sci 91 71–80 Occurrence Handle1:CAS:528:DyaL1cXmt1Kjurk%3D

    CAS  Google Scholar 

  • TN Davis MS Urdea FR Masiarz J Thorner (1986) ArticleTitleIsolation of the yeast calmodulin gene: calmodulin is an essential protein Cell 47 423–431 Occurrence Handle3533275 Occurrence Handle1:CAS:528:DyaL2sXksVygtQ%3D%3D Occurrence Handle10.1016/0092-8674(86)90599-4

    Article  PubMed  CAS  Google Scholar 

  • A Geitmann AMC Emons (2000) ArticleTitleThe cytoskeleton in plant and fungal cell tip growth J Microsc 198 218–245 Occurrence Handle10849200 Occurrence Handle1:CAS:528:DC%2BD3cXkslygtro%3D Occurrence Handle10.1046/j.1365-2818.2000.00702.x

    Article  PubMed  CAS  Google Scholar 

  • I Haußer W Herth HD Reiss (1984) ArticleTitleCalmodulin in tip-growing plant cells, visualized by fluorescing calmodulin-binding phenothiazines Planta 162 33–39 Occurrence Handle10.1007/BF00397418

    Article  Google Scholar 

  • IB Heath (1990) ArticleTitleThe roles of actin in tip growth of fungi Int Rev Cytol 123 95–127 Occurrence Handle1:CAS:528:DyaK3MXktVGjtL0%3D

    CAS  Google Scholar 

  • IB Heath G Gupta S Bai (2000) ArticleTitlePlasma membrane-adjacent actin filaments, but not microtubules, are essential for both polarization and hyphal tip morphogenesis in Saprolegnia ferax and Neurospora crassa Fungal Genet Biol 30 45–62 Occurrence Handle10955907 Occurrence Handle1:CAS:528:DC%2BD3cXmtlekt70%3D Occurrence Handle10.1006/fgbi.2000.1203

    Article  PubMed  CAS  Google Scholar 

  • SS Hook AR Means (2001) ArticleTitleCa2+/CaM-dependent kinases: from activation to function Annu Rev Pharmacol Toxicol 41 471–505 Occurrence Handle11264466 Occurrence Handle1:CAS:528:DC%2BD3MXjsVaqt74%3D Occurrence Handle10.1146/annurev.pharmtox.41.1.471

    Article  PubMed  CAS  Google Scholar 

  • GJ Hyde IB Heath (1995) ArticleTitleCa2+-dependent polarization of axis establishment in the tip-growing organism, Saprolegnia ferax, by gradients of the ionophore A23187 Eur J Cell Biol 67 356–362 Occurrence Handle8521875 Occurrence Handle1:CAS:528:DyaK2MXosVaqsb4%3D

    PubMed  CAS  Google Scholar 

  • SL Jackson IB Heath (1993) ArticleTitleThe roles of calcium ions in hyphal tip growth Microbiol Rev 57 367–382 Occurrence Handle8336672 Occurrence Handle1:CAS:528:DyaK3sXlslOitbw%3D

    PubMed  CAS  Google Scholar 

  • JD Joseph AR Means (2002) ArticleTitleCalcium binding is required for calmodulin function in Aspergillus nidulans Eukaryot Cell 1 119–125 Occurrence Handle12455978 Occurrence Handle1:CAS:528:DC%2BD38XitVSlsL8%3D Occurrence Handle10.1128/EC.01.1.119-125.2002

    Article  PubMed  CAS  Google Scholar 

  • E Kafer (1977) ArticleTitleMeiotic and mitotic recombination in Aspergillus and its chromosomal aberrations Adv Genet 19 33–131 Occurrence Handle327767 Occurrence Handle1:CAS:528:DyaE2sXks1GjsLY%3D Occurrence Handle10.1016/S0065-2660(08)60245-X

    Article  PubMed  CAS  Google Scholar 

  • B Kost P Spielhofer NH Chua (1998) ArticleTitleA GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes Plant J 16 393–401 Occurrence Handle9881160 Occurrence Handle1:CAS:528:DyaK1MXhsVOquw%3D%3D Occurrence Handle10.1046/j.1365-313x.1998.00304.x

    Article  PubMed  CAS  Google Scholar 

  • CT Lin DY Sun GX Song (1986) ArticleTitleCalmodulin: localization in plant tissues J Histochem Cytochem 34 561–567 Occurrence Handle3084624 Occurrence Handle1:CAS:528:DyaL28Xit1aiurg%3D

    PubMed  CAS  Google Scholar 

  • B Liu NR Morris (2000) ArticleTitleA spindle pole body-associated protein, SNAD, affects septation and conidiation in Aspergillus nidulans Mol Gen Genet 263 375–387 Occurrence Handle10821171 Occurrence Handle1:CAS:528:DC%2BD3cXjsFeqtr0%3D Occurrence Handle10.1007/s004380051181

    Article  PubMed  CAS  Google Scholar 

  • KP Lu CD Rasmussen GS May AR Means (1992) ArticleTitleCooperative regulation of cell proliferation by calcium and calmodulin in Aspergillus nidulans Mol Endocrinol 6 365–374 Occurrence Handle1584213 Occurrence Handle1:CAS:528:DyaK38XitFSqu7o%3D Occurrence Handle10.1210/me.6.3.365

    Article  PubMed  CAS  Google Scholar 

  • L Lu YR Lee R Pan JN Maloof B Liu (2005) ArticleTitleAn internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis Mol Biol Cell 16 811–823 Occurrence Handle15574882 Occurrence Handle1:CAS:528:DC%2BD2MXhtVGitbY%3D Occurrence Handle10.1091/mbc.E04-05-0400

    Article  PubMed  CAS  Google Scholar 

  • CA McGoldrick C Gruver GS May (1995) ArticleTitleMyoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarised growth J Cell Biol 128 577–587 Occurrence Handle7860631 Occurrence Handle1:CAS:528:DyaK2MXjs1ehur0%3D Occurrence Handle10.1083/jcb.128.4.577

    Article  PubMed  CAS  Google Scholar 

  • DD Miller DA Callaham DJ Gross PK Hepler (1992) ArticleTitleFree Ca2+ gradient in growing pollen tubes of Lilium J Cell Sci 101 7–12 Occurrence Handle1:CAS:528:DyaK38XmtVyqu74%3D

    CAS  Google Scholar 

  • DD Miller SA Lancelle PK Hepler (1996) ArticleTitleActin microfilaments do not form a dense meshwork in Lilium longiflorum pollen tube tips Protoplasma 195 123–132 Occurrence Handle10.1007/BF01279191

    Article  Google Scholar 

  • SM Morris P Anaya X Xiang NR Morris (1997) ArticleTitleA prolactin-inducible T cell gene product is structurally similar to the Aspergillus nidulans nuclear movement protein NUDC Mol Endocrinol 11 229–236 Occurrence Handle9013770 Occurrence Handle1:CAS:528:DyaK2sXpsVOqtA%3D%3D Occurrence Handle10.1210/me.11.2.229

    Article  PubMed  CAS  Google Scholar 

  • MJ Moser MR Flory TN Davis (1997) ArticleTitleCalmodulin localizes to the spindle pole body of Schizosaccharomyces pombe and performs an essential function in chromosome segregation J Cell Sci 110 1805–1812 Occurrence Handle9264467 Occurrence Handle1:CAS:528:DyaK2sXlsFWrtLk%3D

    PubMed  CAS  Google Scholar 

  • A Moutinho J Love AJ Trewavas R Malhó (1998) ArticleTitleDistribution of calmodulin protein and mRNA in growing pollen tubes Sex Plant Reprod 11 131–139 Occurrence Handle1:CAS:528:DyaK1cXlsVSjtr0%3D Occurrence Handle10.1007/s004970050130

    Article  CAS  Google Scholar 

  • PTP Oliver (1973) ArticleTitleInfluence of cytochalasin B on hyphal morphogenesis of Aspergillus nidulans Protoplasma 76 279–281 Occurrence Handle4570045 Occurrence Handle1:CAS:528:DyaE3sXktlyrtL4%3D Occurrence Handle10.1007/BF01280703

    Article  PubMed  CAS  Google Scholar 

  • PR Ortega G Turin (1987) ArticleTitleCytomorphological defects produced by anticalmodulin agents in outgrowing germ tubes and elongation hyphae of Neurospora crassa Cytobios 49 137–145

    Google Scholar 

  • JM Picton MW Steer (1983) ArticleTitleEvidence for the role Ca2+ ions in tip extension in pollen tubes Protoplasma 115 11–17 Occurrence Handle1:CAS:528:DyaL3sXitFaqt7c%3D Occurrence Handle10.1007/BF01293575

    Article  CAS  Google Scholar 

  • ES Pierson DD Miller DA Callaham AM Shipley BA Rivers M Cresti PK Hepler (1994) ArticleTitlePollen 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 6 1815–1828 Occurrence Handle7866026 Occurrence Handle1:CAS:528:DyaK2MXivVWktLw%3D Occurrence Handle10.1105/tpc.6.12.1815

    Article  PubMed  CAS  Google Scholar 

  • CD Rasmussen RL Means KP Lu GS May AR Means (1990) ArticleTitleCharacterization and expression of the unique calmodulin gene of Aspergillus nidulans J Biol Chem 265 13767–13775 Occurrence Handle2199442 Occurrence Handle1:CAS:528:DyaK3cXmtVGrtL0%3D

    PubMed  CAS  Google Scholar 

  • K Rathore RJ Cork KR Robinson (1991) ArticleTitleA cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes Dev Biol 148 612–619 Occurrence Handle1743404 Occurrence Handle1:STN:280:DyaK38%2Fnslaruw%3D%3D Occurrence Handle10.1016/0012-1606(91)90278-B

    Article  PubMed  CAS  Google Scholar 

  • C Rato D Monteiro PK Hepler R Malho (2004) ArticleTitleCalmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes Plant J 38 887–897 Occurrence Handle15165182 Occurrence Handle1:CAS:528:DC%2BD2cXlslCntr0%3D Occurrence Handle10.1111/j.1365-313X.2004.02091.x

    Article  PubMed  CAS  Google Scholar 

  • JK Reissig SG Kiney (1983) ArticleTitleCalcium as a branching signal in Neurospora crassa J Bacteriol 154 1397–1402 Occurrence Handle6304014 Occurrence Handle1:CAS:528:DyaL3sXktlGqsro%3D

    PubMed  CAS  Google Scholar 

  • J Schmid FM Harold (1988) ArticleTitleDual roles for calcium ions in apical growth of Neurospora crassa J Gen Microbiol 134 2623–2631 Occurrence Handle2978297 Occurrence Handle1:CAS:528:DyaL1cXlvVOjt70%3D

    PubMed  CAS  Google Scholar 

  • S Srinivasan MM Vargas RW Roberson (1996) ArticleTitleFunctional, organizational, and biochemical analysis of actin in hyphal tip cells of Allomyces macrogynus Mycologia 88 57–70 Occurrence Handle1:CAS:528:DyaK28Xhslyhsbo%3D

    CAS  Google Scholar 

  • G Steinberg (1998) ArticleTitleOrganelle transport and molecular motors in fungi Fungal Genet Biol 24 161–177 Occurrence Handle9742200 Occurrence Handle1:CAS:528:DyaK1cXmslCitr8%3D Occurrence Handle10.1006/fgbi.1998.1058

    Article  PubMed  CAS  Google Scholar 

  • T Takeda M Yamamoto (1987) ArticleTitleAnalysis and in vivo disruption of the gene coding for calmodulin in Schizosaccharomyces pombe Proc Natl Acad Sci USA 84 3580–3584 Occurrence Handle3035538 Occurrence Handle1:CAS:528:DyaL2sXls12ktLs%3D Occurrence Handle10.1073/pnas.84.11.3580

    Article  PubMed  CAS  Google Scholar 

  • S Torralba M Raudaskoski AM Pedregosa F Laborda (1998) ArticleTitleEffect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nidulans Microbiology 144 45–53 Occurrence Handle9537763 Occurrence Handle1:CAS:528:DyaK1cXnsValtg%3D%3D Occurrence Handle10.1099/00221287-144-1-45

    Article  PubMed  CAS  Google Scholar 

  • S Yuan L Ling SB Xue (1995) ArticleTitleDistribution and role of calmodulin in tip growing hyphae of Saprolegnia ferax Cell Res 5 255–262

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Lu.

Additional information

Correspondence and reprints: Jiangsu Key Laboratory for Bioresource Technology, College of Life Science, Nanjing Normal University, Nanjing 210097, People’s Republic of China.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, G., Lu, L., Zhang, CY. et al. Calmodulin concentrates at the apex of growing hyphae and localizes to the Spitzenkörper in Aspergillus nidulans . Protoplasma 228, 159–166 (2006). https://doi.org/10.1007/s00709-006-0181-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-006-0181-3

Navigation