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Ustilago maydis populations tracked maize through domestication and cultivation in the Americas.

ABSTRACT: The domestication of crops and the development of agricultural societies not only brought about major changes in human interactions with the environment but also in plants' interactions with the diseases that challenge them. We evaluated the impact of the domestication of maize from teosinte and the widespread cultivation of maize on the historical demography of Ustilago maydis, a fungal pathogen of maize. To determine the evolutionary response of the pathogen's populations, we obtained multilocus genotypes for 1088 U. maydis diploid individuals from two teosinte subspecies in Mexico and from maize in Mexico and throughout the Americas. Results identified five major U. maydis populations: two in Mexico; two in South America; and one in the United States. The two populations in Mexico diverged from the other populations at times comparable to those for the domestication of maize at 6000-10000 years before present. Maize domestication and agriculture enforced sweeping changes in U. maydis populations such that the standing variation in extant pathogen populations reflects evolution only since the time of the crop's domestication.

SUBMITTER: Munkacsi AB

PROVIDER: S-EPMC2366215 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Ustilago maydis reprograms cell proliferation in maize anthers.

Project description:The basidiomycete Ustilago maydis is a ubiquitous pathogen of maize (Zea mays), one of the world's most important cereal crops. Infection by this smut fungus triggers tumor formation in aerial plant parts within which the fungus sporulates. Using confocal microscopy to track U. maydis infection on corn anthers for 7 days post-injection, we found that U. maydis is located on the epidermis during the first 2 days, and has reached all anther lobe cell types by 3 days post-injection. Fungal infection alters cell-fate specification events, cell division patterns, host cell expansion and host cell senescence, depending on the developmental stage and cell type. Fungal effects on tassel and plant growth were also quantified. Transcriptome profiling using a dual organism microarray identified thousands of anther genes affected by fungal infection at 3 days post-injection during the cell-fate specification and rapid cell proliferation phases of anther development. In total, 4147 (17%) of anther-expressed genes were altered by infection, 2018 fungal genes were expressed in anthers, and 206 fungal secretome genes may be anther-specific. The results confirm that U. maydis deploys distinct genes to cause disease in specific maize organs, and suggest mechanisms by which the host plant is manipulated to generate a tumor.

| S-EPMC3769448 | biostudies-literature

Chloroplast-associated metabolic functions influence the susceptibility of maize to Ustilago maydis.

Project description:Biotrophic fungal pathogens must evade or suppress plant defence responses to establish a compatible interaction in living host tissue. In addition, metabolic changes during disease reflect both the impact of nutrient acquisition by the fungus to support proliferation and the integration of metabolism with the plant defence response. In this study, we used transcriptome analyses to predict that the chloroplast and associated functions are important for symptom formation by the biotrophic fungus Ustilago maydis on maize. We tested our prediction by examining the impact on disease of a genetic defect (whirly1) in chloroplast function. In addition, we examined whether disease was influenced by inhibition of glutamine synthetase by glufosinate (impacting amino acid biosynthesis) or inhibition of 3-phosphoshikimate 1-carboxyvinyltransferase by glyphosate (influencing secondary metabolism). All of these perturbations increased the severity of disease, thus suggesting a contribution to resistance. Overall, these findings provide a framework for understanding the components of host metabolism that benefit the plant versus the pathogen during a biotrophic interaction. They also reinforce the emerging importance of the chloroplast as a mediator of plant defence.

| S-EPMC6638283 | biostudies-literature

Early infection response of fungal biotroph <i>Ustilago maydis</i> in maize.

Project description:Common smut, caused by Ustilago maydis (DC.) Corda, is a destructive fungal disease of maize worldwide; it forms large tumors, reducing corn yield and quality. However, the molecular defense mechanism to common smut in maize remains unclear. The present study aimed to use a leading maize inbred line Ye478 to analyze the response to U. maydis inoculation. The histological and cytological analyses demonstrated that U. maydis grew gradually to the host cells 6 h post-inoculation (hpi). The samples collected at 0, 3, 6, and 12 hpi were analyzed to assess the maize transcriptomic changes in response to U. maydis. The results revealed differences in hormone signaling, glycometabolism, and photosynthesis after U. maydis infection; specific changes were detected in jasmonic acid (JA), salicylic acid (SA), ethylene (ET), and abscisic acid (ABA) signaling pathways, glycolysis/gluconeogenesis, and photosystems I and II, probably related to defense response. MapMan analysis demonstrated that the differentially expressed genes between the treatment and control groups were clustered into light reaction and photorespiration pathways. In addition, U. maydis inoculation induced chloroplast swelling and damage, suggesting a significant effect on the chloroplast activity and subsequent metabolic process, especially hexose metabolism. A further genetic study using wild-type and galactinol-sucrose galactosyltransferase (gsg) and yellow-green leaf-1 (ygl-1) mutants identified that these two U. maydis-induced genes negatively regulated defense against common smut in maize. Our measurements showed the pathogen early-invasion process, and the key pathways of both chlorophyll biosynthesis and sugar transportation were critical modified in the infected maize line, thereby throwing a light on the molecular mechanisms in the maize-U. maydis interaction.

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Acid pH Strategy Adaptation through NRG1 in Ustilago maydis.

Project description:The role of the Ustilago maydis putative homolog of the transcriptional repressor ScNRG1, previously described in Saccharomyces cerevisiae, Candida albicans and Cryptococcus neoformans, was analyzed by means of its mutation. In S. cerevisiae this gene regulates a set of stress-responsive genes, and in C. neoformans it is involved in pathogenesis. It was observed that the U. maydisNRG1 gene regulates several aspects of the cell response to acid pH, such as the production of mannosyl-erythritol lipids, inhibition of the expression of the siderophore cluster genes, filamentous growth, virulence and oxidative stress. A comparison of the gene expression pattern of the wild type strain versus the nrg1 mutant strain of the fungus, through RNA Seq analyses, showed that this transcriptional factor alters the expression of 368 genes when growing at acid pH (205 up-regulated, 163 down-regulated). The most relevant genes affected by NRG1 were those previously reported as the key ones for particular cellular stress responses, such as HOG1 for osmotic stress and RIM101 for alkaline pH. Four of the seven genes included WCO1 codifying PAS domain ( These has been shown as the key structural motif involved in protein-protein interactions of the circadian clock, and it is also a common motif found in signaling proteins, where it functions as a signaling sensor) domains sensors of blue light, two of the three previously reported to encode opsins, one vacuolar and non-pH-responsive, and another one whose role in the acid pH response was already known. It appears that all these light-reactive cell components are possibly involved in membrane potential equilibrium and as virulence sensors. Among previously described specific functions of this transcriptional regulator, it was found to be involved in glucose repression, metabolic adaptation to adverse conditions, cellular transport, cell rescue, defense and interaction with an acidic pH environment.

| S-EPMC7912220 | biostudies-literature

A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize.

Project description:The biotrophic fungus Ustilago maydis causes smut disease in maize with characteristic tumor formation and anthocyanin induction. Here, we show that anthocyanin biosynthesis is induced by the virulence promoting secreted effector protein Tin2. Tin2 protein functions inside plant cells where it interacts with maize protein kinase ZmTTK1. Tin2 masks a ubiquitin-proteasome degradation motif in ZmTTK1, thus stabilizing the active kinase. Active ZmTTK1 controls activation of genes in the anthocyanin biosynthesis pathway. Without Tin2, enhanced lignin biosynthesis is observed in infected tissue and vascular bundles show strong lignification. This is presumably limiting access of fungal hyphae to nutrients needed for massive proliferation. Consistent with this assertion, we observe that maize brown midrib mutants affected in lignin biosynthesis are hypersensitive to U. maydis infection. We speculate that Tin2 rewires metabolites into the anthocyanin pathway to lower their availability for other defense responses. DOI: http://dx.doi.org/10.7554/eLife.01355.001.

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Adaptation of Ustilago maydis to phenolic and alkaloid responsive metabolites in maize B73

Project description: Not available

| S-EPMC11294074 | biostudies-literature

Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors.

Project description:With the exception of Ustilago maydis, smut fungi infecting monocotyledonous hosts systemically colonize infected plants and cause symptoms exclusively in the inflorescences. Ustilago may disinfects primordia of all aerial organs of maize (Zea mays L.) and results in the formation of large plant tumours. Previously, we have found that U. maydis infection of seedling leaves, adult leaves and tassels causes organ-specific transcriptional changes in both the pathogen and the host. Of particular interest, U. may disgenes encoding secreted proteins are differentially expressed depending on the colonized maize organ. Therefore, we hypothesized that the fungus secretes virulence-related proteins (effectors)that act in an organ-specific manner. Here, we present the identification and functional characterization of 20 presumptive organ-specific U. maydis effector genes. Ustilago maydis deletion strains for these genes were generated and tested for infectivity of maize seedling leaves and tassels. This approach identified 11 effector genes required for the full virulence of U. maydis. In nine cases, virulence was only affected in one of the tested plant organs. These results demonstrate that individual fungal effector proteins contribute to fungal virulence in an organ-specific manner.

| S-EPMC6638905 | biostudies-literature

Maize gene expression during infection with Ustilago maydis

Project description:The fungal pathogen Ustilago maydis establishes a biotrophic relationship with its host plant maize. Hallmarks of the disease are large plant tumors in which fungal proliferation occurs. Plants have developed various defense pathways to cope with pathogens. We used microarrays to detail the global programme of gene expression during the infection process of Ustilago maydis in its host plant to get insights into the defense programs and the metabolic reprogramming needed to supply the fungus with nutrients. Keywords: time course

2008-03-01 | GSE10023 | GEO

Cell type specific transcriptional reprogramming of maize leaves during Ustilago maydis induced tumor formation.

Project description:Ustilago maydis is a biotrophic pathogen and well-established genetic model to understand the molecular basis of biotrophic interactions. U. maydis suppresses plant defense and induces tumors on all aerial parts of its host plant maize. In a previous study we found that U. maydis induced leaf tumor formation builds on two major processes: the induction of hypertrophy in the mesophyll and the induction of cell division (hyperplasia) in the bundle sheath. In this study we analyzed the cell-type specific transcriptome of maize leaves 4 days post infection. This analysis allowed identification of key features underlying the hypertrophic and hyperplasic cell identities derived from mesophyll and bundle sheath cells, respectively. We examined the differentially expressed (DE) genes with particular focus on maize cell cycle genes and found that three A-type cyclins, one B-, D- and T-type are upregulated in the hyperplasic tumorous cells, in which the U. maydis effector protein See1 promotes cell division. Additionally, most of the proteins involved in the formation of the pre-replication complex (pre-RC, that assure that each daughter cell receives identic DNA copies), the transcription factors E2F and DPa as well as several D-type cyclins are deregulated in the hypertrophic cells.

| S-EPMC6629649 | biostudies-literature

The core effector Cce1 is required for early infection of maize by Ustilago maydis.

Project description:The biotrophic pathogen Ustilago maydis, the causative agent of corn smut disease, infects one of the most important crops worldwide - Zea mays. To successfully colonize its host, U. maydis secretes proteins, known as effectors, that suppress plant defense responses and facilitate the establishment of biotrophy. In this work, we describe the U. maydis effector protein Cce1. Cce1 is essential for virulence and is upregulated during infection. Through microscopic analysis and in vitro assays, we show that Cce1 is secreted from hyphae during filamentous growth of the fungus. Strikingly, Δcce1 mutants are blocked at early stages of infection and induce callose deposition as a plant defense response. Cce1 is highly conserved among smut fungi and the Ustilago bromivora ortholog complemented the virulence defect of the SG200Δcce1 deletion strain. These data indicate that Cce1 is a core effector with apoplastic localization that is essential for U. maydis to infect its host.

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