The germinal centre kinase Don3 triggers the dynamic rearrangement of higher‐order septin structures during cytokinesis in <i>Ustilago maydis</i>

Böhmer, Christian; Ripp, Caroline; Bölker, Michael

doi:10.1111/j.1365-2958.2009.06948.x

Cited by 39 publications

(49 citation statements)

References 73 publications

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“…This scaffolding is thought to provide rigidity to the emerging infection peg. In U. maydis , septins (Alvarez-Tabarés and Pérez-Martín, 2010; Böhmer et al, 2009) as well as Tea4 (this work) and Tea1 (a cell end marker) (Woraratanadharm and Banuett, unpublished) localize to the neck region in the yeast-like cell. It is possible that UmTea1 may have a similar role at the neck as Tea1 in the M. oryzae appressorium pore.…”

Section: Discussionmentioning

confidence: 81%

The cell end marker Tea4 regulates morphogenesis and pathogenicity in the basidiomycete fungus Ustilago maydis

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Woraratanadharm

et al. 2014

Fungal Genetics and Biology

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Positional cues localized to distinct cell domains are critical for the generation of cell polarity and cell morphogenesis. These cues lead to assembly of protein complexes that organize the cytoskeleton resulting in delivery of vesicles to sites of polarized growth. Tea4, an SH3 domain protein, was first identified in fission yeast, and is a critical determinant of the axis of polarized growth, a role conserved among ascomycete fungi. Ustilago maydis is a badiomycete fungus that exhibits a yeast-like form that is nonpathogenic and a filamentous form that is pathogenic on maize and teozintle. We are interested in understanding how positional cues contribute to generation and maintenance of these two forms, and their role in pathogenicity. We identified a homologue of fission yeast tea4 in a genetic screen for mutants with altered colony and cell morphology and present here analysis of Tea4 for the first time in a basidiomycete fungus. We demonstrate that Tea4 is an important positional marker for polarized growth and septum location in both forms. We uncover roles for Tea4 in maintenance of cell and neck width, cell separation, and cell wall deposition in the yeast-like form, and in growth rate, formation of retraction septa, growth reversal, and inhibition of budding in the filamentous form. We show that Tea4∷GFP localizes to sites of polarized or potential polarized growth in both forms, as observed in ascomycete fungi. We demonstrate an essential role of Tea4 in pathogencity in the absence of cell fusion. Basidiomycete and ascomycete Tea4 homologues share SH3 and Glc7 domains. Tea4 in basidiomycetes has additional domains, which has led us to hypothesize that Tea4 has novel functions in this group of fungi.

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Section: Discussionmentioning

confidence: 81%

The cell end marker Tea4 regulates morphogenesis and pathogenicity in the basidiomycete fungus Ustilago maydis

Valinluck

Woraratanadharm

et al. 2014

Fungal Genetics and Biology

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“…Notably, as Clp1-interacting proteins (see Supplemental Table 1 online), we identified Cdc15, a protein required for cytokinesis and nuclear distribution in U. maydis (Bö hmer et al, 2009) and, in addition, the orthologs of BZZ1, Mob1, and CDC36, which were shown to be involved in septum formation, polar growth, and cell cycle control in various fungal species (Hartwell et al, 1970;Reed, 1980;Breter et al, 1983;Luca and Winey, 1998;Luca et al, 2001;Soulard et al, 2002;Weiss et al, 2002;Song et al, 2008;Maerz et al, 2009). A possible role for these proteins during in planta development of U. maydis has not been investigated yet and thus remains speculative.…”

Section: Role Of the Clp1-rbf1 Interaction In Pathogenic Developmentmentioning

confidence: 99%

TheUstilago maydisClp1 Protein Orchestrates Pheromone andb-Dependent Signaling Pathways to Coordinate the Cell Cycle and Pathogenic Development

et al. 2010

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Regulation of the cell cycle and morphogenetic switching during pathogenic and sexual development in Ustilago maydis is orchestrated by a concerted action of the a and b mating-type loci. Activation of either mating-type locus triggers the G2 cell cycle arrest that is a prerequisite for the formation of the infectious dikaryon; this cell cycle arrest is released only after penetration of the host plant. Here, we show that bW, one of the two homeodomain transcription factors encoded by the b mating-type locus, and the zinc-finger transcription factor Rbf1, a master regulator for pathogenic development, interact with Clp1 (clampless 1), a protein required for the distribution of nuclei during cell division of the dikaryon. In addition, we identify Cib1, a previously undiscovered bZIP transcription factor required for pathogenic development, as a Clp1-interacting protein. Clp1 interaction with bW blocks b-dependent functions, such as the b-dependent G2 cell cycle arrest and dimorphic switching. The interaction of Clp1 with Rbf1 results in the repression of the a-dependent pheromone pathway, conjugation tube formation, and the a-induced G2 cell cycle arrest. The concerted interaction of Clp1 with Rbf1 and bW coordinates a-and b-dependent cell cycle control and ensures cell cycle release and progression at the onset of biotrophic development.

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“…In the dimorphic basidiomycete Ustilago maydis, septins are not essential but are required for normal growth and morphology and localize to the yeast neck and as a band at the growing hyphal tip (1,8). In addition, Sep4 (Cdc10) uniquely formed septin fibers along the cell cortex (1), and septins underwent dynamic rearrangements from hourglass collars into ring structures during septation (7,10). In the rice blast fungus Magnaporthe oryzae, septins form rings that anticipate the site of the appressorium septum (54).…”

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confidence: 99%

The Septin AspB in Aspergillus nidulans Forms Bars and Filaments and Plays Roles in Growth Emergence and Conidiation

2012

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In yeast, septins form rings at the mother-bud neck and function as diffusion barriers. In animals, septins form filaments that can colocalize with other cytoskeletal elements. In the filamentous fungus Aspergillus nidulans there are five septin genes, aspA (an ortholog of Saccharomyces cerevisiae CDC11), aspB (an ortholog of S. cerevisiae CDC3), aspC (an ortholog of S. cerevisiae CDC12), aspD (an ortholog of S. cerevisiae CDC10), and aspE (found only in filamentous fungi). The aspB gene was previously reported to be the most highly expressed Aspergillus nidulans septin and to be essential. Using improved gene targeting techniques, we found that deletion of aspB is not lethal but results in delayed septation, increased emergence of germ tubes and branches, and greatly reduced conidiation. We also found that AspB-green fluorescent protein (GFP) localizes as rings and collars at septa, branches, and emerging layers of the conidiophore and as bars and filaments in conidia and hyphae. Bars are found in dormant and isotropically expanding conidia and in subapical nongrowing regions of hyphae and display fast movements. Filaments form as the germ tube emerges, localize to hyphal and branch tips, and display slower movements. All visible AspB-GFP structures are retained in ⌬aspD and lost in ⌬aspA and ⌬aspC strains. Interestingly, in the ⌬aspE mutant, AspB-GFP rings, bars, and filaments are visible in early growth, but AspB-GFP rods and filaments disappear after septum formation. AspE orthologs are only found in filamentous fungi, suggesting that this class of septins might be required for stability of septin bars and filaments in highly polar cells. Septins are evolutionarily conserved GTP binding proteins that form complexes and are increasingly viewed as cytoskeletal elements (62). Septins are found in all eukaryotes except higher plants (20,52) and are involved in a variety of cellular processes including cytokinesis, vesicle trafficking, cytoskeleton organization, polarity, and formation of diffusion barriers (35,39,44,53,62). Perhaps, not surprisingly given their roles in such critical processes, septin defects have been associated with many human diseases (29).The septins were first discovered in the budding yeast Saccharomyces cerevisiae as temperature-sensitive cell cycle mutants defective in cytokinesis (31, 41). Early in the yeast cell cycle, septins localize as a cap at the future site of bud emergence. As the bud emerges, septins localize first as a ring at the mother/bud neck and later as an hourglass structure as the bud develops (25,26,37). At cytokinesis, the hourglass structure converts into two rings. Septins at the neck form diffusion barriers that keep the cellular machinery necessary for growth and cytokinesis properly localized (16,18,22,49,50,60). In addition, septins are part of the morphogenesis checkpoint that coordinates nuclear division with bud formation (37).In S. cerevisiae septins organize into hetero-oligomeric octamers that associate end to end to form nonpolar filaments (6). Electron ...

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The germinal centre kinase Don3 triggers the dynamic rearrangement of higher‐order septin structures during cytokinesis in Ustilago maydis

Cited by 39 publications

References 73 publications

The cell end marker Tea4 regulates morphogenesis and pathogenicity in the basidiomycete fungus Ustilago maydis

The cell end marker Tea4 regulates morphogenesis and pathogenicity in the basidiomycete fungus Ustilago maydis

TheUstilago maydisClp1 Protein Orchestrates Pheromone andb-Dependent Signaling Pathways to Coordinate the Cell Cycle and Pathogenic Development

The Septin AspB in Aspergillus nidulans Forms Bars and Filaments and Plays Roles in Growth Emergence and Conidiation

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