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In previous work, we have shown that the transcription factor Nit2 plays a major role in the utilisation of non‐favoured nitrogen sources like nitrate, minor amino acids or nucleobases in saprotrophic sporidia of the basidiomycete corn smut fungus Ustilago maydis. Addressing the knowledge gap regarding how filamentous phytopathogens adapt to nitrogen limitation in the host plant, we employed Δnit2 mutants in the natural FB1 × FB2 background to identify Nit2‐regulated genes during biotrophy. We further investigated the impact of Nit2 on the physiology of leaf galls in nitrogen‐replete versus nitrogen‐limited host plants by comparative RNA‐Seq and metabolic steady state analysis. About one third of the fungal genes affected by Nit2 during biotrophy were involved in nitrogen metabolism and transport, only showing minor overlap to saprotrophic sporidia. Induction of the nitrate assimilation cluster was completely dependent on Nit2 during biotrophy. In nitrogen‐limited host plants, Δnit2 leaf galls accumulated nitrate and showed reduced accumulation of the nitrogen‐rich phloem transport amino acids asparagine and glutamine compared to wild‐type galls. However, total protein content in galls and pathogenicity were comparable between fungal genotypes in both nitrogen regimes. The findings of our physiological and transcriptomic analysis demonstrate that nitrate utilisation is dispensable for U. maydis during biotrophy and can likely be actively compensated by increased utilisation of abundant organic nitrogen sources, like asparagine, GABA and glutamine in a partially Nit2‐dependent fashion. The transcription factor Nit2 of the smut Ustilago maydis controls nitrate utilisation during biotrophy and affects steady state nitrate and amino acid contents in maize leaf galls under nitrogen depletion.

Corn smut fungus (Ustilago maydis [DC.] Corda) is a globally widespread pathogen affecting both forage and sweet maize hybrids, with higher significance in sweet maize. Remote sensing technologies demonstrated favorable results for disease monitoring on the field scale. The study focused on the changes in vegetation index (VI) values influenced by the pathogen. In this study, four hybrids, two forage maize and two sweet maize hybrids were examined. Artificial infection was carried out at three different doses: a low (2500 sporidium number/mL), medium (5000 sporidium number/mL) and high dose (10,000 sporidium number/mL) with a non-infected control plot for each hybrid. The experimental plots were monitored using a multispectral UAV sensor of five monochrome channels on three different dates, i.e., 7, 14 and 21 days after infection. Five different indices (NDVI, GNDVI, ENDVI, LCI, and NDRE) were determined in Quantum GIS 3.20. The obtained results demonstrated that the infection had a significant effect on the VI values in sweet maize hybrids. A high-dose infection in the Dessert R 73 hybrid resulted in significantly lower values compared to the non-infected hybrids in three indices (NDVI, LCI and GNDVI). In the case of the NOA hybrids, GNDVI and ENDVI were able to show significant differences between the values of the infection levels.

More political and public awareness of the plight of the world’s crops when it comes to fungal disease is crucial to stave off a major threat to global food security. More political and public awareness of the plight of the world’s crops when it comes to fungal disease is crucial to stave off a major threat to global food security. A dark cloud of dust from smut surrounds a machine harvesting crops on a sunny day

Ustilago maydis is a pathogenic fungus that causes corn smut. Because of its easy cultivation and genetic transformation, U. maydis has become an important model organism for plant‐pathogenic basidiomycetes. U. maydis is able to infect maize by producing effectors and secreted proteins as well as surfactant‐like metabolites. In addition, the production of melanin and iron carriers is also associated with its pathogenicity. Here, advances in our understanding of the pathogenicity of U. maydis, the metabolites involved in the pathogenic process, and the biosynthesis of these metabolites, are reviewed and discussed. This summary will provide new insights into the pathogenicity of U. maydis and the functions of associated metabolites, as well as new clues for deciphering the biosynthesis of metabolites. Ustilago maydis is a common biotrophic plant‐pathogenic fungus that causes serious economic losses. We summarize the research on maize pathogenesis, and the metabolites related to U. maydis infection and their biosynthesis.

Smut fungi comprise one of the largest groups of fungal plant pathogens causing disease in all cereal crops. They directly penetrate host tissues and establish a biotrophic interaction. To do so, smut fungi secrete a wide range of effector proteins, which suppress plant immunity and modulate cellular functions as well as development of the host, thereby determining the pathogen’s lifestyle and virulence potential. The conserved effector Erc1 (enzyme required for cell-to-cell extension) contributes to virulence of the corn smut Ustilago maydis in maize leaves but not on the tassel. Erc1 binds to host cell wall components and displays 1,3-β-glucanase activity, which is required to attenuate β-glucan-induced defense responses. Here we show that Erc1 has a cell type-specific virulence function, being necessary for fungal cell-to-cell extension in the plant bundle sheath and this function is fully conserved in the Erc1 orthologue of the barley pathogen Ustilago hordei . Smut fungi secrete effector proteins that suppress host plant immunity. Here the authors show that the corn smut effector Erc1 has 1,3-β-glucanase activity and promotes virulence in maize leaves by attenuating β-glucan-induced defense responses.

Peroxisome‐localized oxo‐phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12‐OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non‐JA producing OPRs remain largely unknown. Here, we generated Mutator‐insertional mutants of the maize OPR2 gene and tested its role in resistance to pathogens with distinct lifestyles. Functional analyses showed that the opr2 mutants were more susceptible to the (hemi)biotrophic pathogens Colletotrichum graminicola and Ustilago maydis, but were more resistant to the necrotrophic fungus Cochliobolus heterostrophus. Hormone profiling revealed that increased susceptibility to C. graminicola was associated with decreased salicylic acid (SA) but increased JA levels. Mutation of the JA‐producing lipoxygenase 10 (LOX10) reversed this phenotype in the opr2 mutant background, corroborating the notion that JA promotes susceptibility to this pathogen. Exogenous SA did not rescue normal resistance levels in opr2 mutants, suggesting that this SA‐inducible gene is the key downstream component of the SA‐mediated defences against C. graminicola. Disease assays of the single and double opr2 and lox10 mutants and the JA‐deficient opr7opr8 mutants showed that OPR2 negatively regulates JA biosynthesis, and that JA is required for resistance against C. heterostrophus. Overall, this study uncovers a novel function of a non‐JA producing OPR as a major negative regulator of JA biosynthesis during pathogen infection, a function that leads to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle. ZmOPR2 functions as a key component of salicylic acid‐mediated defences via suppressing jasmonic acid biosynthesis during pathogen infection, leading to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle.

Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. The secreted effector protein Pit2 is an inhibitor of papain-like cysteine proteases (PLCPs) essential for virulence. Pit2 inhibitory function relies on a conserved 14 amino acids motif (PID14). Here we show that synthetic PID14 peptides act more efficiently as PLCP inhibitors than the full-length Pit2 effector. Mass spectrometry shows processing of Pit2 by maize PLCPs, which releases an inhibitory core motif from the PID14 sequence. Mutational analysis demonstrates that two conserved residues are essential for Pit2 function. We propose that the Pit2 effector functions as a substrate mimicking molecule: Pit2 is a suitable substrate for apoplastic PLCPs and its processing releases the embedded inhibitor peptide, which in turn blocks PLCPs to modulate host immunity. Remarkably, the PID14 core motif is present in several plant associated fungi and bacteria, indicating the existence of a conserved microbial inhibitor of proteases (cMIP). Pit2 is a secreted Ustilago maydis effector that contributes to corn smut disease by inhibiting papain-like cysteine proteases (PLCPs) in maize. Here Misas Villamil et al. show that Pit2 mimics PLCP substrates, and is cleaved to release a peptide that blocks PLCP activity and represses host immunity.

Fungal pathogenesis depends on accurate secretion and location of virulence factors which drive host colonization. Protein glycosylation is a common posttranslational modification of cell wall components and other secreted factors, typically required for correct protein localization, secretion and function. Thus, the absence of glycosylation is associated with animal and plant pathogen avirulence. While the relevance of protein glycosylation for pathogenesis has been well established, the main glycoproteins responsible for the loss of virulence observed in glycosylation-defective fungi have not been identified. Here, we devise a proteomics approach to identify such proteins and use it to demonstrate a role for the highly conserved protein disulfide isomerase Pdi1 in virulence. We show that efficient Pdi1 N-glycosylation, which promotes folding into the correct protein conformation, is required for full pathogenic development of the corn smut fungus Ustilago maydis. Remarkably, the observed virulence defects are reminiscent of those seen in glycosylation-defective cells suggesting that the N-glycosylation of Pdi1 is necessary for the full secretion of virulence factors. All these observations, together with the fact that Pdi1 protein and RNA expression levels rise upon virulence program induction, suggest that Pdi1 glycosylation is important for normal pathogenic development in U. maydis. Our results provide new insights into the role of glycosylation in fungal pathogenesis.

The basidiomycete Ustilago maydis is a biotrophic organism responsible for corn smut disease. In recent years, it has become one of the most promising models for biochemical and biotechnological research due to advantages, such as rapid growth, and easy genetic manipulation. In some aspects, this yeast is more similar to complex eukaryotes, such as humans, compared to standard laboratory yeast models. U. maydis can be employed as a tool to explore physiological processes with more versatility than other fungi. Previously, U. maydis was only considered as a phytopathogenic fungus, but different studies have shown its potential as a research model. Therefore, numerous promising studies have focused on deepening our understanding of the natural interactions, enzyme production, and biotechnological capacity. In this review, we explore general characteristics of U. maydis, both as pathogenic and “innocuous” basidiomycete. Additionally, a comparison with other yeast models focusing on genetic, biochemical, and biotechnological research are analyzed, to emphasize the versatility, dynamism, and novelty that U. maydis has as a research model. In this review, we highlight the applications of the yeast form of the fungus; however, since the filamentous form is also of relevance, it is addressed in the present work, as well.

The common smut of corn, caused by Ustilago maydis, reduces the yield and quality of maize forage. When heavy infestations of corn smut occur, grain yields can be so severely decreased that the most viable economic alternative may be to harvest and ensile the crop. Only a couple of studies have attempted to investigate the influence of aerobic exposure on the nutritive value and aerobic stability of silage, which is prepared from smut-infected maize. In this study, individual whole corn plants were harvested by hand. The plants were distributed into three treatments: 0% infected, 50% infected, and 100% infected. The fresh forage was ensiled in triplicate for a 90-day period. Aerobic exposure lasted for 28 days. Samples were taken on the day of opening and on the 3rd, 7th, 14th, and 28th days. Near infrared spectroscopy (NIRS) calibration equations were used for the prediction of qualitative indicators. Silage prepared from 100% smut-infected maize had comparatively poor quality with dry matter loss, increasing pH and the low amount of starch. It was also distinguished with significant temperature increases from days 15 to 18 of aerobic exposure. Silage prepared from 50% smut-infected maize did not show significant quality changes over the period of the experiment, although it had inferior quality compared to the silage prepared from smut-free maize. While silage prepared from smut-infected maize had an overall worse quality than silage prepared from non-infected maize, it should not have an adverse effect on livestock health or production.