Septins from the Phytopathogenic Fungus Ustilago maydis Are Required for Proper Morphogenesis but Dispensable for Virulence

Abstract

BackgroundSeptins are a highly conserved family of GTP-binding proteins involved in multiple cellular functions, including cell division and morphogenesis. Studies of septins in fungal cells underpin a clear correlation between septin-based structures and fungal morphology, providing clues to understand the molecular frame behind the varied morphologies found in fungal world.Methodology/Principal Findings Ustilago maydis genome has the ability to encode four septins. Here, using loss-of-function as well as GFP-tagged alleles of these septin genes, we investigated the roles of septins in the morphogenesis of this basidiomycete fungus. We described that septins in U. maydis could assemble into at least three different structures coexisting in the same cell: bud neck collars, band-like structures at the growing tip, and long septin fibers that run from pole to pole near the cell cortex. We also found that in the absence of septins, U. maydis cells lost their elongated shape, became wider at the central region and ended up losing their polarity, pointing to an important role of septins in the morphogenesis of this fungus. These morphological defects were alleviated in the presence of an osmotic stabilizer suggesting that absence of septins affected the proper formation of the cell wall, which was coherent with a higher sensitivity of septin defective cells to drugs that affect cell wall construction as well as exocytosis. As U. maydis is a phytopathogen, we analyzed the role of septins in virulence and found that in spite of the described morphological defects, septin mutants were virulent in corn plants.Conclusions/SignificanceOur results indicated a major role of septins in morphogenesis in U. maydis. However, in contrast to studies in other fungal pathogens, in which septins were reported to be necessary during the infection process, we found a minor role of septins during corn infection by U. maydis.

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

“…However, since yeast septin mutants do not display the simultaneous emergence of multiple buds, AspB also appears to have a role in restricting new growth foci not seen in S. cerevisiae. A. nidulans ⌬aspA and ⌬aspC strains also show the emergence of extra germ tubes and branches, as does a septin deletion mutant in another filamentous fungus, U. maydis (1,38). Thus, the restriction of new growth foci might be a common function for septins in other filamentous fungi.…”

“…In A. gossypii, a series of short bars has been observed to form the mature septin ring (15). In U. maydis the Cdc10 filaments extend from pole to pole in the budding stage and in A. fumigatus AspD and AspE septins form visible filaments (1,32).…”

“…In addition, Cdc10 and Cdc3 were occasionally observed to form filaments in hyphae. 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).…”

Endosomal assembly and transport of heteromeric septin complexes promote septin cytoskeleton formation

“…Its genome encodes the core septins Cdc3, Cdc10, Cdc11 and Cdc12 (UMAG_10503, UMAG_10644, UMAG_03449 and UMAG_03599, respectively). However, a clear Shs1 orthologue is missing (Alvarez-Tabares and Perez-Martin, 2010;Böhmer et al, 2009). A prerequisite for infection is the switch from yeast to hyphal growth (Vollmeister et al, 2012).…”

Fungal pathogens are platforms for discovering novel and conserved septin properties

“…Interestingly, as a point of contrast, septins in several other fungal pathogens localize somewhat independently of one another and/or form additional assemblies. In the plant pathogen Ustilago maydis , septins collectively localize to a variety of structures, from collars at the bud-neck to filaments concentrated at growing cell tips that can span the length of the cell [30,31]. Interestingly, Um Sep4 (a Cdc10 ortholog), the only septin protein lacking a C-terminal coiled-coil domain, forms fibers running along the length of the cell that partially co-localize with microtubules yet do not depend on microtubules for localization (Figure 1b) [30].…”