Maize smut caused by the fungus Ustilago maydis is a widespread disease characterized by the development of large plant tumours. U. maydis is a biotrophic pathogen that requires living plant tissue for its development and establishes an intimate interaction zone between fungal hyphae and the plant plasma membrane. U. maydis actively suppresses plant defence responses by secreted protein effectors. Its effector repertoire comprises at least 386 genes mostly encoding proteins of unknown function and expressed exclusively during the biotrophic stage. The U. maydis secretome also contains about 150 proteins with probable roles in fungal nutrition, fungal cell wall modification and host penetration as well as proteins unlikely to act in the fungal-host interface like a chorismate mutase. Chorismate mutases are key enzymes of the shikimate pathway and catalyse the conversion of chorismate to prephenate, the precursor for tyrosine and phenylalanine synthesis. Root-knot nematodes inject a secreted chorismate mutase into plant cells likely to affect development. Here we show that the chorismate mutase Cmu1 secreted by U. maydis is a virulence factor. The enzyme is taken up by plant cells, can spread to neighbouring cells and changes the metabolic status of these cells through metabolic priming. Secreted chorismate mutases are found in many plant-associated microbes and might serve as general tools for host manipulation.

Biotrophic pathogens, such as the related maize pathogenic fungi Ustilago maydis and Sporisorium reilianum, establish an intimate relationship with their hosts by secreting protein effectors. Because secreted effectors interacting with plant proteins should rapidly evolve, we identified variable genomic regions by sequencing the genome of S. reilianum and comparing it with the U. maydis genome. We detected 43 regions of low sequence conservation in otherwise well-conserved syntenic genomes. These regions primarily encode secreted effectors and include previously identified virulence clusters. By deletion analysis in U. maydis, we demonstrate a role in virulence for four previously unknown diversity regions. This highlights the power of comparative genomics of closely related species for identification of virulence determinants.

The maize pathogen Ustilago maydis has to undergo various morphological transitions for the completion of its sexual life cycle. For example, haploid cells respond to pheromone by forming conjugation tubes that fuse at their tips. The resulting dikaryon grows filamentously, expanding rapidly at the apex and inserting retraction septa at the basal pole. In this review, we present progress on the underlying mechanisms regulating such defined developmental programmes. The key findings of the postgenomic era are as follows: (1) endosomes function not only during receptor recycling, but also as multifunctional transport platforms; (2) a new transcriptional master regulator for pathogenicity is part of an intricate transcriptional network; (3) determinants for uniparental mitochondrial inheritance are encoded at the a2 mating-type locus; (4) microtubule-dependent mRNA transport is important in determining the axis of polarity; and (5) a battery of fungal effectors encoded in gene clusters is crucial for plant infection. Importantly, most processes are tightly controlled at the transcriptional, post-transcriptional and post-translational levels, resulting in a complex regulatory network. This intricate system is crucial for the timing of the correct order of developmental phases. Thus, new insights from all layers of regulation have substantially advanced our understanding of fungal development.