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Aspergillus nidulans swo Mutants Show Defects in Polarity Establishment, Polarity Maintenance and Hyphal Morphogenesis
Michelle Momanya, Patrick J. Westfalla, and Gretel Abramowskyaa Department of Botany, University of Georgia, Athens, Georgia 30602
Corresponding author: Michelle Momany, Department of Botany, 2502 Plant Sciences, University of Georgia, Athens, GA 30602., momany{at}dogwood.botany.uga.edu (E-mail)
Communicating editor: P. J. PUKKILA
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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When the spores of filamentous fungi break dormancy, they grow isotropically, adding cell wall material uniformly in every direction. Later they switch to polarized growth, with new material added to the tip of an emerging germ tube. To identify genes involved in the synthesis and localization of cell wall material in filamentous fungi, we screened a collection of temperature-sensitive Aspergillus nidulans mutants for swollen cells. We have isolated mutants representing eight genes involved in polarity establishment, polarity maintenance, and hyphal morphogenesis. On the basis of the results of temperature-shift experiments, swo C, D, and F are required to establish polarity, while swoA is required to maintain polarity. swo B, E, G, and H are involved in later hyphal morphogenesis. Our results suggest that polarity establishment and polarity maintenance are genetically separate events and that a persistent signal is required for apical extension in A. nidulans.
ALL cells must organize areas of new growth to maintain their shape and function properly. Fungi employ distinctive patterns of new cell wall addition that ultimately lead to their growth as unicells, in the case of yeasts, or as hyphae, in the case of filamentous fungi. These distinctive patterns of cell wall deposition are the visible result of changes in cellular polarity. Many details of the polarity establishment that determines localization of new cell wall material are known for the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. In contrast, the processes of polarity establishment and subsequent new cell wall synthesis and localization are relatively unexplored in filamentous fungi.
The budding yeast S. cerevisiae shifts between isotropic and polarized growth modes (
The fission yeast S. pombe also switches between two distinct growth patterns (
Like yeast, filamentous fungi employ two distinct growth modes. When spores of filamentous fungi break dormancy, they first grow isotropically, adding new cell wall material uniformly in every direction. Later they switch to polarized growth, with new cell wall material forming an emerging germ tube (
Although the signal(s) responsible for polarity establishment in filamentous fungi is still unknown, several molecules implicated in subsequent hyphal extension and morphogenesis have recently been identified. In Neurospora crassa, deletion of the microtubule-dependent motor protein kinesin results in cells that are shorter and fatter than wild type (
To identify genes involved in the synthesis and localization of new cell wall material in filamentous fungi, we screened a collection of temperature-sensitive A. nidulans mutants for swollen cells. Defects in either cell wall localization or synthesis can presumably disrupt morphogenesis, giving rise to misshapen, swollen hyphae. Because cell wall localization ultimately depends upon cell polarity, we expected that at least some of our mutants would have polarity defects. We have isolated mutants representing eight genes involved in polarity establishment, polarity maintenance, and hyphal morphogenesis. Our results suggest that polarity establishment and polarity maintenance are separate events and that a persistent signal is required for apical extension.
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Aspergillus strains and growth methods:
Strains used in this study are listed in Table 1. Generation of the temperature-sensitive mutant collection has been previously described (
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Strain construction and genetic analysis were by standard A. nidulans techniques (
Staining and microscopy:
Examination of phenotypes in liquid medium has been previously described by
Localization of cell wall addition:
We initially attempted to label cell walls with the lectin wheat germ agglutinin coupled to fluorescein isothiocyanate (FITC; Sigma). In multiple experiments, the lectin did not label a band at the basal end of the germ tube. Therefore, we raised antibodies against total cell walls for use in labeling experiments. A. nidulans A28 was grown for 48 hr in complete liquid medium. Hyphae were homogenized and walls were isolated as previously described (
For data presented in Figure 3, conidia were inoculated onto coverslips in 10 ml of complete liquid medium and incubated at 30° for 4, 5, 6, or 7 hr. Coverslips with adhering germlings were removed from liquid medium and incubated with anticell wall antibody (diluted 1:1000 in phosphate buffered saline) at room temperature for 30 min. Coverslips with adhering hyphae were then washed three times in phosphate buffered saline, transferred to fresh complete liquid medium, and incubated for an additional hour at 30°. Coverslips with adhering germlings were then fixed, stained with FITC-coupled anti-mouse mouse antibody (Sigma), washed three times in phosphate buffered saline, stained with Calcofluor and Hoescht 33258, and placed on a microscope slide for viewing. In control experiments omitting the antibodies against cell walls (primary antibody), no staining was seen. In controls omitting the final hour of incubation, the entire germling was labeled. In controls delaying treatment with antibodies against cell walls until after the final hour of incubation, the entire germling was labeled. For data presented in Figure 3, 50 germlings were counted for each time point. Experiments were repeated three times with essentially identical results. A typical data set is shown.
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Temperature-shift experiments:
Temperature-shift experiments were carried out as described above (staining and microscopy) except for changes in incubation times and temperatures. For downshift experiments (Figure 4), conidia were inoculated to complete medium at 42°, incubated for 10 hr, and transferred to 30° for 2 hr prior to fixing and staining. For upshift experiments (Figure 5) conidia were inoculated to complete medium at 30°, incubated for 10 hr, and transferred to 42° for 2 hr prior to fixing and staining. Experiments were repeated three times with essentially identical results.
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Upshift experiments with localization of new growth (Figure 6) were carried out as described above with the following modifications. Conidia were incubated for 11.5 hr at 30°, treated with antibodies against cell walls for 30 min, transferred to fresh media prewarmed to 42°, and incubated for 4.5 hr at 42° prior to processing as described for localization of cell wall addition. When wild type was treated identically, growth was more rapid, making photography of an entire germling at high magnification difficult. For the wild-type control shown, incubation times were shortened to 10 hr at permissive temperature and 2 hr at restrictive temperature.
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| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Identification of swo mutants:
To identify genes important in cell wall synthesis and localization, we screened a preexisting collection of 1200 temperature-sensitive A. nidulans mutants (
Genetic characterization:
Because A. nidulans is haploid, single gene mutations are expected to segregate 1:1 in crosses with wild type. The 55 putative swo mutants were crossed to wild type and progeny were scored for temperature sensitivity and swelling. Nine mutants showed both 1:1 segregation and linkage of temperature sensitivity to the swollen cell phenotype (Table 2).
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To determine whether the swo mutations are dominant or recessive, stable diploids were constructed with wild-type strains. All diploids were wild type at restrictive temperature, indicating that the swo mutations are recessive (Table 2).
To determine if any of the nine swo mutations are allelic or tightly linked, crosses were made for every pairwise mutant combination using swo mutant strains containing reciprocal auxotrophic markers. The recovery of wild-type progeny from a cross was interpreted to mean that each parent strain had a lesion in a different swo gene. Wild-type progeny were recovered from every cross except those derived from ts6-90 by ts7-91 (data not shown). Stable diploid strains were constructed from fusion of ts6-90 and ts7-91 derivatives to determine whether they represented alleles or tightly linked genes. All ts6-90/ts7-91 diploids were temperature sensitive, indicating that the respective haploids are allelic. Ts6-90 and ts7-91 were designated swoA-1 and swoA-2, respectively. The seven other swo mutants were designated swoB–swoH (Table 1 and Table 2).
Phenotypic characterization:
The phenotypes of the swo mutants on solid medium were observed by inoculating to complete solid medium and incubating for 2 days at restrictive temperature. All mutants were able to send out germ tubes, although both alleles of swoA made only a few. Most of the swo mutants did not make the asexual spores (conidia) typically seen in wild-type strains after 2 days growth, although sparse conidiation was visible in cultures of swoB, swoD, and swoF. Many morphological mutants show wild-type growth when extra osmoticum is added to the medium. This restoration to the wild-type phenotype, known as osmotic remediality, is especially likely in the case of mutants where a weakened wall cannot resist internal turgor pressure. The swo mutants were tested for osmotic remediality on solid medium containing high levels of sucrose, sorbitol, or potassium chloride. Sucrose was the best osmotic stabilizer and so only those results are reported (Figure 1, Table 2, and data not shown). Five of the mutants (swoA-1, A-2, B, F, and G) were osmotically remedial at the restrictive temperature. Three (swoC, D, and E) were osmotically remedial at the semipermissive temperature. Only one mutant showed no osmotic remediality (swoH).
The dye Calcofluor binds to ß-linked glucans and chitin (
The phenotypes of the swo mutants in liquid were observed by inoculating on coverslips in complete medium and incubating at permissive or restrictive temperature (Figure 2). After 12–16 hr incubation, germlings were fixed and stained with Calcofluor and Hoescht 33258 to stain chitin and nuclei, respectively. At permissive temperature all swo mutants were indistinguishable from wild type, except for swoB. Only 26% of swoB germlings had septa after overnight growth at permissive temperature, compared to 100% in wild-type control cultures. At restrictive temperature, four of the swo mutants did not generally form germ tubes, instead showing isotropic or nonpolarized growth (swoA, C, D, and F; Figure 2, Table 4). The swoA-1 allele occasionally formed germ tubes, while swoA-2 never did. We postulate that swoA-1 is a leaky allele. The other mutants grew in a polar manner, but exhibited hyphal swelling or other morphological abnormalities (swoB, E, G, and H; Figure 2, Table 4).
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The switch from isotropic to polar growth in wild type:
When wild-type A. nidulans conidia germinate, they first expand uniformly in every direction and later grow by addition of new cell wall material at the tip of the germ tube. To define the timing of this switch from isotropic to polar growth relative to nuclear divisions, conidia of wild-type A. nidulans were inoculated onto coverslips in complete medium, grown for 4, 5, 6, or 7 hr, and incubated with polyclonal antibodies against cell walls for 30 min. Germlings were then washed, transferred to fresh medium without antibodies, and incubated for another hour. They were then fixed and stained with a fluorescently labeled secondary antibody (to label all growth prior to the final hour of incubation), Calcofluor (to label chitin), and Hoescht 33258 (to label nuclei). Cells that showed uniform antibody staining were scored as growing in a nonpolarized manner during the final hour of incubation. Cells that showed a localized unlabeled zone were scored as growing in a polarized manner during the final hour of incubation. Nuclear number and growth polarity were scored for each time point. As shown in Figure 3, the switch from isotropic to polar growth occurred at about 7 hr, around the time of the second nuclear division. Most cells with two nuclei grew isotropically, although occasionally a cell with only two nuclei grew in a polar manner. All cells with four nuclei grew in a polar manner. During the eighth hour of incubation, when most cells had eight nuclei, the germ tube grew by apical extension and the first septa were seen (data not shown). All of the swo mutants have at least four nuclei at restrictive temperature (Figure 2, Table 3) and so should be able to grow in a polar manner.
Temperature-shift experiments:
To determine the effect of the swo mutations on polarity establishment, conidia were inoculated onto coverslips in liquid medium, incubated at restrictive temperature for 10 hr, shifted to permissive temperature, and incubated for another 2 hr (Figure 4, Table 4). We thought that the defect in polarity establishment would also prevent germ tube extension and so expected that the mutants that do not show polarized growth at restrictive temperature (swoA, C, D, and F) would not be able to make germ tubes upon release from the temperature block. Indeed, swoC, D, and F behaved as expected: they did not make germ tubes within 2 hr of the shift to permissive temperature. The swoA mutant, however, did make germ tubes after the shift from restrictive to permissive temperature (Figure 4, Table 4). In fact, each cell made 3–4 normal looking germ tubes. Interestingly, these germ tubes were almost exclusively on one-half of the cell, rather than being equally spaced. Ninety-five percent of germ tubes formed in swoA-1 and 100 percent of germ tubes formed in swoA-2 after the downshift emerged from only one-half of the cell (Figure 4 and data not shown). As expected, the four swo mutants that showed polarized growth at restrictive temperature (swoB, E, G, and H) showed normal apical growth of hyphae after the shift from restrictive to permissive temperature (Figure 4, Table 4).
To determine the effect of the swo mutations on hyphal elongation, conidia were inoculated onto coverslips in complete medium, incubated at permissive temperature for 10 hr, shifted to restrictive temperature, and incubated for 2 hr. We expected that only the region of the hypha that grew after the shift to restrictive temperature (i.e., the apical region) would swell. Surprisingly, none of the swo mutants showed exclusively apical swelling after the shift to restrictive temperature (Figure 5, Table 4). Both swoA-1 and A-2 showed pronounced swelling along the whole hypha. SwoC and D showed slight basal swelling and apparently normal apical growth. SwoB showed basal swelling with normal apical growth, while swoE showed basal swelling and apical swelling at the tip. SwoG and H looked normal in both basal and apical regions.
To better distinguish growth that occurred at permissive temperature from growth that occurred after the shift to restrictive temperature, conidia from the nonpolar swo mutants were inoculated onto coverslips in complete medium, grown at permissive temperature for 11.5 hr, and incubated with polyclonal antibody against A. nidulans cell walls for 30 min. The germlings were then washed and transferred to fresh medium without antibodies, incubated for 4.5 hr at restrictive temperature, fixed, and stained with fluorescently labeled secondary antibody, Calcofluor, and Hoescht 33258 (Figure 6). SwoA-1, swoA-2, and swoF clearly showed swelling in the region of the hypha that had grown at permissive temperature (basal). In addition, swoA-1 (the presumed leaky allele) and swoF showed swollen growth in the region of the hypha that formed at restrictive temperature (apical). The swoA-2 allele showed no new apical extension after the shift to restrictive temperature. SwoC and D both showed normal apical extension after the shift to restrictive temperature.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Phenotypes of the swo mutants:
To identify genes involved in the synthesis and localization of new cell wall growth, we screened a collection of temperature-sensitive A. nidulans mutants for a swollen cell phenotype. Because the ultimate expression of polarity decisions is the localized deposition of new cell wall material, we expected that at least some of our swo mutants would have defects in polarity. We identified nine swo mutants representing eight genes. With the exception of swoH, the mutants show restoration of the wild-type phenotype by the addition of high osmoticum to the medium, hypersensitivity to the cell wall-binding dye Calcofluor, or both (Figure 1 and Table 2). These phenotypes are common among wall-related fungal mutants (
Nonpolar swo mutants show defects in polarity establishment and maintenance:
It seemed likely that the nonpolar swo mutants were defective in the transition from isotropic to polar growth. In time course experiments we found that the isotropic-to-polar switch occurred near the second nuclear division (Figure 3). This is consistent with the previous observation that the germ tube emerges concomitant with the second nuclear division in A. nidulans (
When incubated at restrictive temperature for 10 hr and then shifted to permissive temperature, swoA made germ tubes within 2 hr, while swoC, D, and F did not (Figure 4, Table 4). We interpret this to mean that swoC, D, and F are unable to establish polarity at restrictive temperature, while swoA is able to establish polarity but is blocked in the maintenance of polarity required for germ tube emergence. This result was surprising because there has been no previous evidence that polarity establishment can be separated from polarity maintenance in A. nidulans. We had assumed that the same signal would be responsible for both events, and so expected that none of the nonpolar swo mutants would be able to make germ tubes after release of the temperature block. An alternate interpretation is that both alleles of swoA are reversible. This seems unlikely because germ tubes can be seen emerging from swoA as early as 15 min after the shift from restrictive to permissive temperature (data not shown).
The pattern of germ tube emergence after release of the swoA temperature block was also a surprise. In wild-type A. nidulans, the first germ tube emerges and grows before a second germ tube emerges. This second germ tube is made 180° opposite the first (M. MOMANY, unpublished observations) in a pattern analogous to the bipolar budding pattern of diploid S. cerevisiae (reviewed by
When incubated at permissive temperature for 10 hr and shifted to restrictive temperature for 2 hr, swoA, C, D, and F showed varying levels of swelling in the basal region of the hypha (Figure 5, Table 4). Once more this result was a surprise. Most models of apical extension include the assumption that the cell wall in the basal region is set, that only the apical region is capable of growth. We expected that only the region of the hypha that formed at restrictive temperature (the apical region) would swell. Only swoF showed obvious swelling at the apex. Using antibodies against cell walls and longer incubation times, we were able to distinguish growth that occurred before and after the temperature shift more clearly (Figure 6). Our results showed that both alleles of swoA and swoF swelled in apical regions, with swoA-2 also ceasing apical extension completely at restrictive temperature. Both swoC and D showed only slight basal swelling and made normal germ tubes after the shift to restrictive temperature. We interpret these results to mean that a persistent signal is required for polarity maintenance in A. nidulans and that the swoA-2 mutant lacks this signal at restrictive temperature. The swoA-1 and swoF mutants appear to be partially defective in polarity maintenance, because they are capable of some apical extension at restrictive temperature. The swoC and D mutants, on the other hand, appear to have no defect in apical extension once polarity has been established.
Polar swo mutants show defects in hyphal morphogenesis:
The remaining swo mutants (swoB, E, G, and H) appear to be able to establish and maintain polarity at restrictive temperature despite defects in hyphal morphogenesis (Figure 2). The swoB mutant swells irregularly along the hypha and often ruptures, leaking cellular contents. This phenotype might indicate a defect in cell wall synthesis or assembly. The idea that swoB has a wall synthesis defect is consistent with its osmotic remediality and Calcofluor hypersensitivity (Figure 1, Table 2). The phenotype of the swoE mutant suggests a defect in branching and/or general hyphal patterning. Indeed, swoE has been isolated independently in screens for mutants with defects in cell patterning (hypA;
When incubated at restrictive temperature for 10 hr and then shifted to permissive temperature, all of the polar swo mutants showed swelling of the basal region and normal growth of the apical region, as expected if polarity establishment and maintenance are functioning (Figure 4, Table 4). When the mutants were incubated at permissive temperature for 10 hr and then shifted to restrictive temperature, the effects on them were more subtle than those seen on the nonpolar swo mutants (Figure 5, Table 4). SwoB gave the most dramatic result, with slight swelling and an abnormally high number of branches. This may indicate that swoB plays a role in branch formation. SwoE showed slight basal and apical swelling, while neither swoG nor swoH showed obvious abnormalities. The less-pronounced effect of the shift from permissive to restrictive temperature may indicate that the events that require swoG and H have been successfully completed before the shift to restrictive temperature. That is, they take place early in hyphal morphogenesis. However, in view of the phenotypes of swoG and H at restrictive temperature and their behavior in downshift experiments, it seems more likely that their effects are simply not seen within the 2-hr time period of growth at restrictive temperature.
Model for the roles of the swo genes:
We propose the following model for polarity establishment, polarity maintenance, and hyphal morphogenesis in A. nidulans (Figure 7):
- Close to the second nuclear division, the expanding conidium switches from isotropic to polar growth (Figure 3). This switch requires establishment of an axis of polarity that anticipates the location of germ tube emergence. The products of swoC, D, and F are all required to establish polarity based on the inability of these mutants to make germ tubes when released from the restrictive temperature in downshift experiments (Figure 4, Table 4). The swoC and D gene products are not required for germ tube emergence or apical extension based on the normal hyphae made by these mutants at restrictive temperature in upshift experiments (Figure 5 and Figure 6, Table 4). It should be noted that subsequent nuclear divisions are not dependent upon the establishment of polarity, i.e., there is no "polarity checkpoint" that affects nuclear division. If that were the case, the swo mutants would arrest with only two nuclei (Figure 2, Table 3).
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Figure 7. Model of polarity establishment, polarity maintenance, and hyphal morphogenesis. Sometime between the first and second nuclear divisions the conidium switches from isotropic to polar growth. Presumably, a molecular marker tags the site from which the germ tube will emerge (open triangle). A separate signal, or perhaps a modification of the polarity establishment marker, is sent to initiate germ tube emergence and apical extension (closed triangle). As the hypha matures, it forms septa and branches. See text for postulated roles of the swo gene products. - After polarity is established, a separate gene product is needed to maintain the axis of polarity so that the germ tube emerges. The product of the swoA gene is required for polarity maintenance, but not its establishment, based on the ability of the swoA mutant to make germ tubes rapidly upon release from restrictive temperature in downshift experiments and on its inability to maintain polarity in upshift experiments (Figure 4 and Figure 5, Table 4). Because of its association with apically extending tip cells, we speculate that the swoA gene product may interact with actin and/or the Spitzenkörper. The swoA protein may also show similarities to the tea1p or pom1p proteins that appear to organize polarity by marking the ends of S. pombe cells (
MATA and NURSE 1997 ;BAHLER and PRINGLE 1998 ). Future work will address these issues. - The polarity maintenance gene product required for germ tube emergence is also required for apical extension to continue. Even well after polarity has been established, the swoA mutant is not able to extend apically at restrictive temperature (Figure 6, Table 4). The swoF product also appears to play some role in polarity maintenance, in addition to its role in polarity establishment, on the basis of impaired apical extension in upshift experiments (Figure 5 and Figure 6, Table 4).
- Eventually the elongating hypha forms the branches and septa seen in mature fungal colonies. The products of swoB, E, G, and H all appear to be involved in establishing proper hyphal morphogenesis with postulated roles, including cell wall synthesis (swoB) and branch formation (swoG). Future work will examine these later events in hyphal morphogenesis more closely.
| ACKNOWLEDGMENTS |
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We thank John E. Hamer for generously providing the temperature-sensitive mutant collection, Jered Brown for technical assistance, and Debbie Haas for critical reading of the manuscript. This work was supported by a grant to M.M. from the Division of Energy Biosciences, U.S. Department of Energy. P.J.W. was supported by a predoctoral training grant in molecular and cellular mycology from the National Institutes of Health.
Manuscript received June 12, 1998; Accepted for publication October 15, 1998.
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 S. Konzack, P. E. Rischitor, C. Enke, and R. Fischer The Role of the Kinesin Motor KipA in Microtubule Organization and Polarized Growth of Aspergillus nidulans Mol. Biol. Cell, February 1, 2005; 16(2): 497 - 506. [Abstract] [Full Text] [PDF]
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M. Momany, R. Lindsey, T. W. Hill, E. A. Richardson, C. Momany, M. Pedreira, G. M. Guest, J. F. Fisher, R. B. Hessler, and K. A. Roberts The Aspergillus fumigatus cell wall is organized in domains that are remodelled during polarity establishment Microbiology, October 1, 2004; 150(10): 3261 - 3268. [Abstract] [Full Text] [PDF]
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T. Oka, T. Hamaguchi, Y. Sameshima, M. Goto, and K. Furukawa Molecular characterization of protein O-mannosyltransferase and its involvement in cell-wall synthesis in Aspergillus nidulans Microbiology, June 1, 2004; 150(6): 1973 - 1982. [Abstract] [Full Text] [PDF]
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X. Lin, C. Momany, and M. Momany SwoHp, a Nucleoside Diphosphate Kinase, Is Essential in Aspergillus nidulans Eukaryot. Cell, December 1, 2003; 2(6): 1169 - 1177. [Abstract] [Full Text] [PDF]
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S. Seiler and M. Plamann The Genetic Basis of Cellular Morphogenesis in the Filamentous Fungus Neurospora crassa Mol. Biol. Cell, November 1, 2003; 14(11): 4352 - 4364. [Abstract] [Full Text] [PDF]
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 X. Lin and M. Momany The Aspergillus nidulans swoC1 Mutant Shows Defects in Growth and Development Genetics, October 1, 2003; 165(2): 543 - 554. [Abstract] [Full Text] [PDF]
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P. Knechtle, F. Dietrich, and P. Philippsen Maximal Polar Growth Potential Depends on the Polarisome Component AgSpa2 in the Filamentous Fungus Ashbya gossypii Mol. Biol. Cell, October 1, 2003; 14(10): 4140 - 4154. [Abstract] [Full Text] [PDF]
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C. Bachewich, D. Y. Thomas, and M. Whiteway Depletion of a Polo-like Kinase in Candida albicans Activates Cyclase-dependent Hyphal-like Growth Mol. Biol. Cell, May 1, 2003; 14(5): 2163 - 2180. [Abstract] [Full Text] [PDF]
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 J. C. Bowman, P. S. Hicks, M. B. Kurtz, H. Rosen, D. M. Schmatz, P. A. Liberator, and C. M. Douglas The Antifungal Echinocandin Caspofungin Acetate Kills Growing Cells of Aspergillus fumigatus In Vitro Antimicrob. Agents Chemother., September 1, 2002; 46(9): 3001 - 3012. [Abstract] [Full Text] [PDF]
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