The General Transcriptional Repressor Tup1 Is Required for Dimorphism and Virulence in a Fungal Plant Pathogen

Abstract

A critical step in the life cycle of many fungal pathogens is the transition between yeast-like growth and the formation of filamentous structures, a process known as dimorphism. This morphological shift, typically triggered by multiple environmental signals, is tightly controlled by complex genetic pathways to ensure successful pathogenic development. In animal pathogenic fungi, one of the best known regulators of dimorphism is the general transcriptional repressor, Tup1. However, the role of Tup1 in fungal dimorphism is completely unknown in plant pathogens. Here we show that Tup1 plays a key role in orchestrating the yeast to hypha transition in the maize pathogen Ustilago maydis. Deletion of the tup1 gene causes a drastic reduction in the mating and filamentation capacity of the fungus, in turn leading to a reduced virulence phenotype. In U. maydis, these processes are controlled by the a and b mating-type loci, whose expression depends on the Prf1 transcription factor. Interestingly, Δtup1 strains show a critical reduction in the expression of prf1 and that of Prf1 target genes at both loci. Moreover, we observed that Tup1 appears to regulate Prf1 activity by controlling the expression of the prf1 transcriptional activators, rop1 and hap2. Additionally, we describe a putative novel prf1 repressor, named Pac2, which seems to be an important target of Tup1 in the control of dimorphism and virulence. Furthermore, we show that Tup1 is required for full pathogenic development since tup1 deletion mutants are unable to complete the sexual cycle. Our findings establish Tup1 as a key factor coordinating dimorphism in the phytopathogen U. maydis and support a conserved role for Tup1 in the control of hypha-specific genes among animal and plant fungal pathogens.

Strategies for Wheat Stripe Rust Pathogenicity Identified by Transcriptome Sequencing

“…The change in morphology between yeast-like growth and a filamentous state in response to environmental signals is frequently associated with virulence in plant pathogenic fungi [106]. TUP1 plays a central role in controlling the expression of the genes implicated in the genetic control of mating, filamentation, and pathogenic development of Ustilago maydis [108]. Analyzing the function of TUP1 in rust fungi could provide a better understand of how it acts within the unique biological context in which these pathogens develop.…”

The Transcriptional Repressor TupA in Aspergillus niger Is Involved in Controlling Gene Expression Related to Cell Wall Biosynthesis, Development, and Nitrogen Source Availability

“…The important role of Tup1/TupA in pathogenic fungi has received further attention because of its important role in dimorphism and pathogenicity. Although the role of Tup1 in fungal dimorphism is conserved, the way it controls the switch differs between fungi [12], [31]–[33].…”

TheCoprinopsis cinereaTup1 homologue Cag1 is required for gill formation during fruiting body morphogenesis

“…Tup1 homologues have also been studied in filamentous fungi and are implicated in switching of cell growth, conidiation and pathogenesis in Neurospora crassa (Yamashiro et al, 1996), Candida albicans (Braun and Johnson, 1997, 2000), Aspergillus nidulans (Hicks et al, 2001), Penicillium marneffei (Todd et al, 2003), Cryptococcus neoformans (Lee et al, 2005, 2009) and Ustilago maydis (Elías-Villalobos et al, 2011). These studies on some phenotypes suggested that Tup1 homologues activate the expression of certain genes.…”

“…Tup1 homologues are conserved throughout eukaryotes (Courey and Jia, 2001) and have been demonstrated to regulate gene expression in a wide variety of cellular processes, including metabolic change, asexual and sexual development, responses to environmental signals and developmental switching (Elías-Villalobos et al, 2011; Hicks et al, 2001; Long et al, 2006; Todd et al, 2003; Yamashiro et al, 1996). …”