UmTea1, a Kelch and BAR domain-containing protein, acts at the cell cortex to regulate cell morphogenesis in the dimorphic fungus Ustilago maydis

Abstract

The spatial organization of a cell is crucial for distribution of cell components and for cell morphogenesis in all organisms. Ustilago maydis, a basidiomycete fungus, has a yeast-like and a filamentous form. The former buds once per cell cycle at one of the cell poles, and can use the same site repeatedly or choose a new site at the same pole or opposite pole. The filamentous form consists of a long apical cell with short septate basal compartments lacking cytoplasm. It grows at the apex and can reverse growth forming a new growth zone at the basal end. We are interested in understanding how these different morphologies are generated. Here we present identification and characterization of U. maydis Tea1, a homologue of the fission yeast cell end marker Tea1. We demonstrate that UmTea1, a Kelch domain protein, interacts with itself and is an important determinant of the site of polarized growth: tea1 mutants bud simultaneously from both cell poles and form bifurcate buds. UmTea1 also regulates septum positioning, cell wall deposition, cell and neck width, coordination of nuclear division and cell separation, and localization of sterol-rich membrane domains. Some of these functions are shared with UmTea4, another cell end marker. We show that Tea1::GFP localizes to sites of polarized or potential polarized growth and to the septation site in the yeast-like form. Additionally, localization of Tea1::GFP as rings along the filament suggests that the filament undergoes septation. We hypothesize that Tea1 may act as a scaffold for the assembly of proteins that determine the site of polarized growth.

Fungal plasma membrane domains

“…Indeed, in several fungal species it has been reported that sites of active membrane growth are enriched in sterols (Sterol-Rich Domains, SRDs), as seen using the fluorescent and 3'-β-sterol-binding filipin (Alvarez, Douglas and Konopka 2007;Malinsky et al 2013). Filipin-labelled SRDs have been observed at the bud tips and mating projections in S. cerevisiae (Bagnat and Simons 2002), the cell ends in S. pombe (Wachtler 2003), the hyphal tips of A. nidulans (Pearson et al 2004) and C. albicans (Martin and Konopka 2004), the places of septum formation in S. pombe (Wachtler 2003) and Ustilago maydis (Woraratanadharm, Kmosek and Banuett 2018) and the germling tips in N. crassa (Weichert et al 2016). In filamentous fungi in particular, the study of hyphal growth via the tip is a very active field of research and excellent recent reviews adequately cover the subject (Peñalva 2010;Steinberg et al 2017;Riquelme et al 2018).…”

The emerging role of septins in fungal pathogenesis

“…Another protein important for the site of polarised growth is Tea1; Δ tea1 mutants bud from both cell poles. Tea1 interacts with itself and localises to sites of polarised growth, where it may act as a scaffold for assembly of proteins such as septins that determine the site of polarised growth (Woraratanadharm et al, 2018 ), whereas the protein Mes1 is essential for strong polarised hyphal growth but not for yeast‐like growth. In Δ mes1 mutants the septin ring is absent from the bud tip but not the bud neck, suggesting that cell division is not affected whereas polarised growth is impacted (Cánovas, 2022 ).…”

The mitotic spindle mediates nuclear migration through an extremely narrow infection structure of the rice blast fungusMagnaporthe oryzae

“…In Ustilago maydis, nuclear division defects were found in Tea1 knockout mutants in the yeast-like cells (38). More research is needed to elucidate the mechanisms that guide the daughter bound SPB efficiently to the appressorial pore in M oryzae.…”