Guanyl Nucleotide Exchange Factor Sql2 and Ras2 Regulate Filamentous Growth in Ustilago maydis

Abstract

The cyclic AMP (cAMP)-signaling pathway regulates cell morphology and plays a crucial role during pathogenic development of the plant-pathogenic fungus Ustilago maydis. Strains lacking components of this signaling pathway, such as the G␣-subunit Gpa3 or the adenylyl cyclase Uac1, are nonpathogenic and grow filamentously. On the other hand, strains exhibiting an activated cAMP pathway due to a dominant-active allele of gpa3 display a glossy colony phenotype and are unable to proliferate in plant tumors. Here we present the identification of sql2 as a suppressor of the glossy colony phenotype of a gpa3 Q206L strain. sql2 encodes a protein with similarity to CDC25-like guanine nucleotide exchange factors, which are known to act on Ras proteins. Overexpression of sql2 leads to filamentous growth that cannot be suppressed by exogenous cAMP, suggesting that Sql2 does not act upstream of Uac1. To gain more insight in signaling processes regulated by Sql2, we isolated two genes encoding Ras proteins. Expression of dominant active alleles of ras1 and ras2 showed that Ras2 induces filamentous growth while Ras1 does not affect cell morphology but elevates pheromone gene expression. These results indicate that Ras1 and Ras2 fulfill different functions in U. maydis. Moreover, observed similarities between the filaments induced by sql2 and ras2 suggest that Sql2 is an activator of Ras2. Interestingly, sql2 deletion mutants are affected in pathogenic development but not in mating, indicating a specific function of sql2 during pathogenesis.

QTL mapping of temperature sensitivity reveals candidate genes for thermal adaptation and growth morphology in the plant pathogenic fungus Zymoseptoria tritici

“…Among these, gene 56742 encodes a guanine nucleotide exchange factor, a family of proteins involved in various intracellular signaling pathways. In a previous study in Ustilago maydis, a guanine nucleotide exchange factor was shown to be involved in dimorphism (Muller et al, 2003), hence we consider this the most likely candidate gene explaining this QTL.…”

Basidiomycete Mating Type Genes and Pheromone Signaling

“…neoformans, Ras1 is involved in regulation of early stages of mating, and it is necessary for pheromone production (115), while the cAMP production and Pka pathway are controlled by Gpa1 (118). In U. maydis, dominant/constitutively active Ras2 changed the growth pattern from yeast-like to filamentous, while dominant active Ras1 elevated pheromone expression, probably via increased cAMP levels (52,64). Also, the expression of both Ras proteins varies.…”

“…The function of Ras proteins encoded by two different genes, Ras1 and Ras2, has been extensively analyzed in S. cerevisiae (108), Cr. neoformans (68,69,114,115,118), and U. maydis (52,64). Several aspects complicate the understanding of the function of Ras proteins, as Ras gene expression is often controlled by nutritional and environmental factors.…”

Mitogen-Activated Protein Kinase Signaling in Plant-Interacting Fungi: Distinct Messages from Conserved Messengers

“…Thus, expression of a dominant active ras2 allele promotes pseudohyphal growth in a manner dependent on the Kss1-1 MAPK cascade. One possible activator of Ras2 is the GEF protein Sql2 (Figure 5; Müller et al, 2003a). However, unlike ras2 mutants, sql2 knockouts are defective in plant infection but not in mating.…”