The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis

Abstract

The corn smut fungus Ustilago maydis is a model organism for elucidating host colonization strategies of biotrophic fungi. Here we performed an in depth transcriptional profiling of the entire plant-associated development of U. maydis wild-type strains. In our analysis we focused on fungal metabolism, nutritional strategies, secreted effectors and regulatory networks. Secreted proteins were enriched in three distinct expression modules corresponding to stages on the plant surface, establishment of biotrophy and induction of tumors. These modules are likely the key determinants for U. maydis virulence. With respect to nutrient utilization, we observed that expression of several nutrient transporters was tied to these virulence modules rather than being controlled by nutrient availability. We show that oligopeptide transporters likely involved in nitrogen assimilation are important virulence factors. By measuring the intramodular connectivity of transcription factors, we identified the potential drivers for the virulence modules. While known components of the b-mating type cascade emerged as inducers for the plant surface and biotrophy module, we identified a set of yet uncharacterized transcription factors as likely responsible for expression of the tumor module. We demonstrate a crucial role for leaf tumor formation and effector gene expression for one of these transcription factors.

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

“…S5). The abundance of T. thlaspeos reads in infected samples was low (0.18–0.28%), which is in agreement with the early phase of maize infection by U. maydis , when the fungal hyphae have not started proliferating and the coverage is < 0.5% (Lanver et al ., ). U. maydis then proliferates massively at the local infection site, while T. thlaspeos grows along the vasculature, resulting in relatively low levels of fungal biomass.…”

“…Subsequently, fungal hyphae proliferate inside the apoplast and/or grow through host cells, establishing an intimate contact zone for the exchange of nutrients and proteins. Functional genomic analyses of the grass smut fungi U. maydis, Sporisorium reilianum and U. hordei have greatly contributed to our understanding of smut infection and the associated host responses (K€ amper et al, 2006;Brefort et al, 2009;Ghareeb et al, 2015;Lanver et al, 2018). In short, these studies have revealed different repertoires of conserved and host-adapted effector proteins (Okmen & Doehlemann, 2014;Lanver et al, 2017).…”

Advances in understanding obligate biotrophy in rust fungi

“…The oligopeptide transporter (OPT) genes are more numerous in rust fungi than in other basidiomycetes and have been shown to be highly expressed during host infection and in haustoria of rust fungi (Duplessis et al, 2011a;Garnica et al, 2013). Recently, OPT genes were associated with virulence in the smut fungus Ustilago maydis, suggesting that extracellular peptides represent an important source of nutrients for the fungus (Lanver et al, 2018). So far, no functional characterization of OPT has been conducted in rust fungi.…”

The insertion of a mitochondrial selfish element into the nuclear genome and its consequences

“…To shed light on the functional implication of the translocation of the HEG and subsequent mutations we (i) assessed the expression profile of these genes and (ii) generated a deletion strain and phenotyped it. For the expression analysis we relied on a previously published RNASeq data set (Lanver et al 2018), from which we extracted the expression profiles of genes in the telomeric region of chromosome 9 ( Figure 5A). While the expression of UMAG_11064 remained close to zero in the three replicates, expression of UMAG_11065 increased during plant infection.…”