Organic acids and glucose prime late-stage fungal biotrophy in maize

Abstract

Many plant-associated fungi are obligate biotrophs that depend on living hosts to proliferate. However, little is known about the molecular basis of the biotrophic lifestyle, despite the impact of fungi on the environment and food security. In this work, we show that combinations of organic acids and glucose trigger phenotypes that are associated with the late stage of biotrophy for the maize pathogen Ustilago maydis . These phenotypes include the expression of a set of effectors normally observed only during biotrophic development, as well as the formation of melanin associated with sporulation in plant tumors. U. maydis and other hemibiotrophic fungi also respond to a combination of carbon sources with enhanced proliferation. Thus, the response to combinations of nutrients from the host may be a conserved feature of fungal biotrophy.

The Maize Pathogen Ustilago maydis Secretes Glycoside Hydrolases and Carbohydrate Oxidases Directed toward Components of the Fungal Cell Wall

“…Of note, a similar hypothesis has been recently proposed for another U. maydis b-1,3 glucanase (Erc1) whose activity toward laminarihexaose has been shown to suppress laminarihexaoseinduced ROS burst in plant leaves (35). All in all, it is clear that the fate and role of FCW/PCW-derived oxidized products released by fungal oxidative enzymes is an emerging matter of utmost importance (38,(44)(45)(46)(47). Conclusions.…”

The Monothiol Glutaredoxin Grx4 Influences Iron Homeostasis and Virulence in Ustilago maydis

“…Interestingly, there is increasing evidence that Grx4 is also connected to oxygen sensing and regulation via sterol binding transcription factors such as SrbA and the transcription factor AtrR in A. fumigatus [35]. In U. maydis, we previously showed that cultures with the combination of glucose and malate form melanin and are hypoxic, and we determined that tumor tissues in leaves and stems during biotrophy are also reduced in oxygen levels [5]. It is tempting to speculate that oxygen sensing via an unknow transcription factor together with Grx4/Urbs1 regulates iron homeostasis, mitochondrial functions (electron transport and the TCA cycle), ergosterol synthesis, and heme-related functions, and integrates central metabolism with the mating pathway to influence virulence and biotrophy.…”

“…The salt solution was prepared without FeCl 3 . All other components of the low iron MM are identical to regular MM [1,5]. Glucose and arabinose were used at 1%.…”

“…The fungus induces chlorotic tumors on all aerial parts of the host plant, and the tumors become filled with masses of melanized resting spores (teliospores) that facilitate the dormancy and dissemination of the fungus. U. maydis has emerged as a useful model to investigate mechanisms of fungal biotrophy, including adaptation to the host nutritional environment and the activities of a plethora of effector proteins delivered during colonization [2][3][4][5]. The utility of U. maydis as a model is particularly important because many biotrophic plant pathogens, such as the rust fungi, cause devastating crop losses but are difficult to study in the laboratory.…”

The interplay between electron transport chain function and iron regulatory factors influences melanin formation inCryptococcus neoformans

“…Mitochondria play a central role in respiratory metabolism for fungal pathogens of plants and animals, and support the ability of fungi to sense environmental and host conditions (1)(2)(3)(4)(5). The importance of mitochondrial functions in pathogenesis has been demonstrated for a number of fungal pathogens of humans including Cryptococcus neoformans and the related species C. gattii (1,(6)(7)(8).…”