Smut Fungi 2.0

A special issue of Journal of Fungi (ISSN 2309-608X).

Deadline for manuscript submissions: closed (15 August 2022) | Viewed by 48334

Special Issue Editors


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Guest Editor
Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, KY, USA
Interests: host–pathogen interactions; smut fungi (Microbotryum violaceum, Ustilago maydis, Sporisorium reilianum); dimorphism in fungi; control of mitochondrial inheritance
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Forensic Science, Master of Science Forensic Science, and Environmental and Life Sciences Graduate Programs, Trent University, Peterborough, ON, Canada
Interests: Ustilago maydis; Sporisorium reilianum; fungal hybridization and pathogenesis; teliospore development and germination; transcriptome analysis; natural antisense transcripts and lncRNAs
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Matthias-Schleiden Institut/Genetik, Friedrich-Schiller-Universität Jena, Jena, Germany
Interests: Sporisorium reilianum; Ustilago maydis; control of host specificity; control of symptom specificity; control of mitochondrial inheritance; genome comparison; transcriptome analysis; fluorescence microscopy; gene functional analysis
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Smut fungi are a large, diverse, and non-monophyletic group of plant pathogens. They include several species that have gained prominence as models for plant pathogenic fungi due to (1) their facility of manipulation and extensive molecular genetic toolkits (e.g., Ustilago maydis, U. hordei, Sporisorium reilianum), (2) their economic and international diplomatic impacts (e.g., Tilletia caries, T. contraversa, Thecaphora solani), and (3) their use in ecological/population genetics/evolutionary studies and as paradigms for emerging infectious diseases through host shifts (e.g., the Microbotryum violaceum species complex). More recently, tool development for other smut fungi has enabled enhanced investigation of pathogen–plant interactions (e.g., U. bromivora), and of distinct crops and diseases (e.g., U. esculenta, S. scitamineum). Nevertheless, many other species have been poorly studied or have only recently been recognized for their interesting and unique properties. In this Special Issue, we aim to combine both original research works and review articles with particular emphasis on molecular genetic approaches that together feature a wide range, and unravel important characteristics, of smut species, thereby advancing our understanding of this important group of plant pathogens.

Prof. Dr. Michael H. Perlin
Prof. Dr. Barry J. Saville
Prof. Dr. Jan Schirawski
Guest Editors

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Keywords

  • smut fungi
  • host/pathogen interactions
  • phytopathogens
  • Ustilago
  • Sporisorium
  • Microbotryum
  • Tilletia

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Published Papers (16 papers)

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16 pages, 2721 KiB  
Article
Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen Ustilaginoidea virens from Jiangsu, China, Molecular Mechanisms, and Fitness Stability
by Jiehui Song, Zhiying Wang, Yan Wang, Sijie Zhang, Tengyu Lei, You Liang, Qigen Dai, Zhongyang Huo, Ke Xu and Shuning Chen
J. Fungi 2022, 8(12), 1311; https://doi.org/10.3390/jof8121311 - 16 Dec 2022
Cited by 6 | Viewed by 1548
Abstract
Rice false smut (RFS), caused by Ustilaginoidea virens, is an important fungal disease of rice. In China, Methyl Benzimidazole Carbamates (MBCs), including carbendazim, are common fungicides used to control RFS and other rice diseases. In this study, resistance of U. virens to [...] Read more.
Rice false smut (RFS), caused by Ustilaginoidea virens, is an important fungal disease of rice. In China, Methyl Benzimidazole Carbamates (MBCs), including carbendazim, are common fungicides used to control RFS and other rice diseases. In this study, resistance of U. virens to carbendazim was monitored for three consecutive years during 2018 to 2020. A total of 321 U. virens isolates collected from Jiangsu Province of China were tested for their sensitivity to carbendazim on PSA. The concentration at which mycelial growth is inhibited by 50% (EC50) of the carbendazim-sensitive isolates was 0.11 to 1.38 µg/mL, with a mean EC50 value of 0.66 μg/mL. High level of resistance to carbendazim was detected in 14 out of 321 isolates. The resistance was stable but associated with a fitness penalty. There was a statistically significant and moderate negative correlation (r= −0.74, p < 0.001) in sensitivity between carbendazim and diethofencarb. Analysis of the U. virens genome revealed two potential MBC targets, Uvβ1Tub and Uvβ2Tub, that putatively encode β-tubulin gene. The two β-tubulin genes in U. virens share 78% amino acid sequence identity, but their function in MBC sensitivity has been unclear. Both genes were identified and sequenced from U. virens sensitive and resistant isolates. It is known that mutations in the β2-tubulin gene have been shown to confer resistance to carbendazim in other fungi. However, no mutation was found in the Uvβ2Tub gene in either resistant or sensitive isolates. Variations including point mutations, non-sense mutations, codon mutations, and frameshift mutations were found in the Uvβ1Tub gene from the 14 carbendazim-resistant isolates, which have not been reported in other fungi before. Thus, these results indicated that variations of Uvβ1Tub result in the resistance to carbendazim in field isolates of Ustilaginoidea virens. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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14 pages, 3871 KiB  
Article
β-Xylosidase SRBX1 Activity from Sporisorium reilianum and Its Synergism with Xylanase SRXL1 in Xylose Release from Corn Hemicellulose
by Yuridia Mercado-Flores, Alejandro Téllez-Jurado, Carlos Iván Lopéz-Gil and Miguel Angel Anducho-Reyes
J. Fungi 2022, 8(12), 1295; https://doi.org/10.3390/jof8121295 - 13 Dec 2022
Cited by 3 | Viewed by 1701
Abstract
Sposisorium reilianum is the causal agent of corn ear smut disease. Eleven genes have been identified in its genome that code for enzymes that could constitute its hemicellulosic system, three of which have been associated with two Endo-β-1,4-xylanases and one with α-L-arabinofuranosidase activity. [...] Read more.
Sposisorium reilianum is the causal agent of corn ear smut disease. Eleven genes have been identified in its genome that code for enzymes that could constitute its hemicellulosic system, three of which have been associated with two Endo-β-1,4-xylanases and one with α-L-arabinofuranosidase activity. In this study, the native protein extracellular with β-xylosidase activity, called SRBX1, produced by this basidiomycete was analyzed by performing production kinetics and its subsequent purification by gel filtration. The enzyme was characterized biochemically and sequenced. Finally, its synergism with Xylanase SRXL1 was determined. Its activity was higher in a medium with corn hemicellulose and glucose as carbon sources. The purified protein was a monomer associated with the sr16700 gene, with a molecular weight of 117 kDa and optimal activity at 60 °C in a pH range of 4–7, which had the ability to hydrolyze the ρ-nitrophenyl β-D-xylanopyranoside and ρ-Nitrophenyl α-L-arabinofuranoside substrates. Its activity was strongly inhibited by silver ions and presented Km and Vmax values of 2.5 mM and 0.2 μmol/min/mg, respectively, using ρ-nitrophenyl β-D-xylanopyranoside as a substrate. The enzyme degrades corn hemicellulose and birch xylan in combination and in sequential synergism with the xylanase SRXL1. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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17 pages, 3808 KiB  
Article
Improved Itaconate Production with Ustilago cynodontis via Co-Metabolism of CO2-Derived Formate
by Lena Ullmann, Nils Guntermann, Philipp Kohl, Gereon Schröders, Andreas Müsgens, Giancarlo Franciò, Walter Leitner and Lars M. Blank
J. Fungi 2022, 8(12), 1277; https://doi.org/10.3390/jof8121277 - 5 Dec 2022
Cited by 1 | Viewed by 1722
Abstract
In recent years, it was shown that itaconic acid can be produced from glucose with Ustilago strains at up to maximum theoretical yield. The use of acetate and formate as co-feedstocks can boost the efficiency of itaconate production with Ustilaginaceae wild-type strains by [...] Read more.
In recent years, it was shown that itaconic acid can be produced from glucose with Ustilago strains at up to maximum theoretical yield. The use of acetate and formate as co-feedstocks can boost the efficiency of itaconate production with Ustilaginaceae wild-type strains by reducing the glucose amount and thus the agricultural land required for the biotechnological production of this chemical. Metabolically engineered strains (U. cynodontis Δfuz7 Δcyp3 ↑Pria1 and U. cynodontis Δfuz7 Δcyp3 PetefmttA ↑Pria1) were applied in itaconate production, obtaining a titer of 56.1 g L−1 and a yield of 0.55 gitaconate per gsubstrate. Both improved titer and yield (increase of 5.2 g L−1 and 0.04 gitaconate per gsubstrate, respectively) were achieved when using sodium formate as an auxiliary substrate. By applying the design-of-experiments (DoE) methodology, cultivation parameters (glucose, sodium formate and ammonium chloride concentrations) were optimized, resulting in two empirical models predicting itaconate titer and yield for U. cynodontis Δfuz7 Δcyp3 PetefmttA ↑Pria1. Thereby, an almost doubled itaconate titer of 138 g L−1 was obtained and a yield of 0.62 gitaconate per gsubstrate was reached during confirmation experiments corresponding to 86% of the theoretical maximum. In order to close the carbon cycle by production of the co-feed via a “power-to-X” route, the biphasic Ru-catalysed hydrogenation of CO2 to formate could be integrated into the bioprocess directly using the obtained aqueous solution of formates as co-feedstock without any purification steps, demonstrating the (bio)compatibility of the two processes. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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13 pages, 2244 KiB  
Article
The Toxicity of Salicylhydroxamic Acid and Its Effect on the Sensitivity of Ustilaginoidea virens to Azoxystrobin and Pyraclostrobin
by Jiehui Song, Zhiying Wang, Sijie Zhang, Yan Wang, You Liang, Qigen Dai, Zhongyang Huo and Ke Xu
J. Fungi 2022, 8(11), 1231; https://doi.org/10.3390/jof8111231 - 21 Nov 2022
Cited by 2 | Viewed by 1579
Abstract
Rice false smut (RFS) caused by Ustilaginoidea virens has been one of the most severe rice diseases. Fungicide-based chemical control is a significant measure to control RFS. In the sensitivity determination of quinone outside inhibitor (QoI) fungicide in vitro, salicylhydroxamic acid (SHAM) has [...] Read more.
Rice false smut (RFS) caused by Ustilaginoidea virens has been one of the most severe rice diseases. Fungicide-based chemical control is a significant measure to control RFS. In the sensitivity determination of quinone outside inhibitor (QoI) fungicide in vitro, salicylhydroxamic acid (SHAM) has been commonly added to artificial culture media in order to inhibit alternative oxidase of phytopathogenic fungi. However, some studies showed that artificial media should not include SHAM due to its toxicity. Whether SHAM should be added in the assay of U. virens sensitivity to QoI fungicide remains unknown. In this study, two appropriate media, potato sucrose agar (PSA) and minimal medium (MM), were selected to test SHAM toxicity and sensitivity of U. virens to azoxystrobin and pyraclostrobin. The mycelial growth and sensitivity to azoxystrobin and pyraclostrobin had no significant difference between on PSA and MM. SHAM could significantly inhibit mycelial growth, conidial germination, peroxidase (POD) and esterase activity of U. virens. Average effective concentration for inhibiting 50% (EC50) values of SHAM against mycelial growth of ten U. virens were 27.41 and 12.75 μg/mL on PSA and MM, respectively. The EC50 values of SHAM against conidial germination of isolates HWD and JS60 were 70.36 and 44.69 μg/mL, respectively. SHAM at 30 μg/mL significantly inhibited POD and esterase activity of isolates HWD and JS60, and even SHAM at 10 μg/mL significantly inhibited POD activity of isolate HWD. In addition, SHAM significantly reduced EC50 values and EC90 values of azoxystrobin and pyraclostrobin on both PSA and MM. Even in the presence of SHAM at 10 μg/mL, average EC50 values of ten U. virens isolates for azoxystrobin decreased 1.7-fold on PSA and 4.8-fold on MM, and for pyraclostrobin that decreased 2.8-fold on PSA and 4.8-fold on MM. Therefore, these results suggest that SHAM should not be included in artificial media in the assay of U. virens sensitivity to QoI fungicides. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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16 pages, 8845 KiB  
Article
Kinase Hog1 and Adr1 Opposingly Regulate Haploid Cell Morphology by Controlling Vacuole Size in Sporisorium scitamineum
by Enping Cai, Meixin Yan, Xian Sun, Rong Zeng, Wenqiang Zheng, Yizhen Deng, Zide Jiang and Changqing Chang
J. Fungi 2022, 8(8), 865; https://doi.org/10.3390/jof8080865 - 17 Aug 2022
Cited by 3 | Viewed by 1509
Abstract
Morphogenesis is a strictly regulated efficient system in eukaryotes for adapting to environmental changes. However, the morphogenesis regulatory mechanism in smut fungi is not clear. This study reports a relationship between MAP kinase Hog1 and cAMP-dependent protein kinase A catalytic subunit (Adr1) for [...] Read more.
Morphogenesis is a strictly regulated efficient system in eukaryotes for adapting to environmental changes. However, the morphogenesis regulatory mechanism in smut fungi is not clear. This study reports a relationship between MAP kinase Hog1 and cAMP-dependent protein kinase A catalytic subunit (Adr1) for the morphological regulation in the sugarcane pathogen Sporisorium scitamineum. The results demonstrated that MAP kinase Hog1 and cAMP/PKA signaling pathways are essential for the morphological development of S. scitamineum. Interestingly, MAP kinase Hog1 and cAMP/PKA signaling pathways’ defective mutants exhibit an opposite morphological phenotype. The morphology of cAMP/PKA defective mutants is recovered by deleting the SsHOG1 gene. However, MAP kinase Hog1 and cAMP-dependent protein kinase catalytic subunit Adr1 do not interfere with each other. Further investigations showed that kinase Hog1 and Adr1 antagonistically regulates the vacuolar size, which contributes to the cell size and determines the cellular elongation rates. Kinase Hog1 and Adr1 also antagonistically balanced the cell wall integrity and permeability. Taken together, kinase Hog1- and Adr1-based opposing morphogenesis regulation of S. scitamineum by controlling the vacuolar size and cell wall permeability is established during the study. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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15 pages, 2643 KiB  
Article
Functional Analysis of the Plasma Membrane H+-ATPases of Ustilago maydis
by Melissa Vázquez-Carrada, Michael Feldbrügge, Dario Rafael Olicón-Hernández, Guadalupe Guerra-Sánchez and Juan Pablo Pardo
J. Fungi 2022, 8(6), 550; https://doi.org/10.3390/jof8060550 - 24 May 2022
Cited by 3 | Viewed by 2430
Abstract
Plasma membrane H+-ATPases of fungi, yeasts, and plants act as proton pumps to generate an electrochemical gradient, which is essential for secondary transport and intracellular pH maintenance. Saccharomyces cerevisiae has two genes (PMA1 and PMA2) encoding H+-ATPases. In contrast, [...] Read more.
Plasma membrane H+-ATPases of fungi, yeasts, and plants act as proton pumps to generate an electrochemical gradient, which is essential for secondary transport and intracellular pH maintenance. Saccharomyces cerevisiae has two genes (PMA1 and PMA2) encoding H+-ATPases. In contrast, plants have a larger number of genes for H+-ATPases. In Ustilago maydis, a biotrophic basidiomycete that infects corn and teosinte, the presence of two H+-ATPase-encoding genes has been described, one with high identity to the fungal enzymes (pma1, UMAG_02851), and the other similar to the plant H+-ATPases (pma2, UMAG_01205). Unlike S. cerevisiae, these two genes are expressed jointly in U. maydis sporidia. In the present work, mutants lacking one of these genes (Δpma1 and Δpma2) were used to characterize the role of each one of these enzymes in U. maydis physiology and to obtain some of their kinetic parameters. To approach this goal, classical biochemical assays were performed. The absence of any of these H+-ATPases did not affect the growth or fungal basal metabolism. Membrane potential tests showed that the activity of a single H+-ATPase was enough to maintain the proton-motive force. Our results indicated that in U. maydis, both H+-ATPases work jointly in the generation of the electrochemical proton gradient, which is important for secondary transport of metabolites and regulation of intracellular pH. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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12 pages, 1522 KiB  
Article
Ustilago maydis Metabolic Characterization and Growth Quantification with a Genome-Scale Metabolic Model
by Ulf W. Liebal, Lena Ullmann, Christian Lieven, Philipp Kohl, Daniel Wibberg, Thiemo Zambanini and Lars M. Blank
J. Fungi 2022, 8(5), 524; https://doi.org/10.3390/jof8050524 - 20 May 2022
Cited by 6 | Viewed by 2733
Abstract
Ustilago maydis is an important plant pathogen that causes corn smut disease and serves as an effective biotechnological production host. The lack of a comprehensive metabolic overview hinders a full understanding of the organism’s environmental adaptation and a full use of its metabolic [...] Read more.
Ustilago maydis is an important plant pathogen that causes corn smut disease and serves as an effective biotechnological production host. The lack of a comprehensive metabolic overview hinders a full understanding of the organism’s environmental adaptation and a full use of its metabolic potential. Here, we report the first genome-scale metabolic model (GSMM) of Ustilago maydis (iUma22) for the simulation of metabolic activities. iUma22 was reconstructed from sequencing and annotation using PathwayTools, and the biomass equation was derived from literature values and from the codon composition. The final model contains over 25% annotated genes (6909) in the sequenced genome. Substrate utilization was corrected by BIOLOG phenotype arrays, and exponential batch cultivations were used to test growth predictions. The growth data revealed a decrease in glucose uptake rate with rising glucose concentration. A pangenome of four different U. maydis strains highlighted missing metabolic pathways in iUma22. The new model allows for studies of metabolic adaptations to different environmental niches as well as for biotechnological applications. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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24 pages, 6159 KiB  
Article
The Sporisorium reilianum Effector Vag2 Promotes Head Smut Disease via Suppression of Plant Defense Responses
by Yulei Zhao, Nisha Agrawal, Hassan Ghareeb, Mohammad Tanbir Habib, Sascha Dickmeis, Jens Schwachtje, Tim E. Iven, Joachim Kopka, Ivo Feussner and Jan Schirawski
J. Fungi 2022, 8(5), 498; https://doi.org/10.3390/jof8050498 - 11 May 2022
Cited by 2 | Viewed by 2711
Abstract
Genome comparison between the maize pathogens Ustilago maydis and Sporisorium reilianum revealed a large diversity region (19-1) containing nearly 30 effector gene candidates, whose deletion severely hampers virulence of both fungi. Dissection of the S. reilianum gene cluster resulted in the identification of [...] Read more.
Genome comparison between the maize pathogens Ustilago maydis and Sporisorium reilianum revealed a large diversity region (19-1) containing nearly 30 effector gene candidates, whose deletion severely hampers virulence of both fungi. Dissection of the S. reilianum gene cluster resulted in the identification of one major contributor to virulence, virulence-associated gene 2 (vag2; sr10050). Quantitative reverse-transcriptase polymerase chain reaction (qRT-PCR) experiments revealed high expression of vag2 during biotrophic growth of S. reilianum. Using the yeast secretion trap assay, we confirmed the existence of a functional signal peptide allowing protein secretion via the conventional secretory pathway. We identified the cytoplasmic maize chorismate mutase ZmCM2 by yeast two-hybrid screening as a possible interaction partner of Vag2. Interaction of the two proteins in planta was confirmed by bimolecular fluorescence complementation. qRT-PCR experiments revealed vag2-dependent downregulation of salicylic acid (SA)-induced genes, which correlated with higher SA levels in plant tissues colonized by Δvag2 deletion strains relative to S. reilianum wildtype strains. Metabolite analysis suggested rewiring of pathogen-induced SA biosynthesis by preferential conversion of the SA precursor chorismate into the aromatic amino acid precursor prephenate by ZmCM2 in the presence of Vag2. Possibly, the binding of Vag2 to ZmCM2 inhibits the back reaction of the ZmCM2-catalyzed interconversion of chorismate and prephenate, thus contributing to fungal virulence by lowering the plant SA-induced defenses. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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18 pages, 14503 KiB  
Article
Squalene Monooxygenase Gene SsCI80130 Regulates Sporisorium scitamineum Mating/Filamentation and Pathogenicity
by Yichang Cai, Yi Zhang, Han Bao, Jiaoyun Chen, Jianwen Chen and Wankuan Shen
J. Fungi 2022, 8(5), 470; https://doi.org/10.3390/jof8050470 - 30 Apr 2022
Cited by 2 | Viewed by 1944
Abstract
Sugarcane is an important sugar crop and energy crop worldwide. Sugarcane smut caused by Sporisorium scitamineum is a serious fungal disease that occurs worldwide, seriously affecting the yield and quality of sugarcane. It is essential to reveal the molecular pathogenesis of S. scitamineum [...] Read more.
Sugarcane is an important sugar crop and energy crop worldwide. Sugarcane smut caused by Sporisorium scitamineum is a serious fungal disease that occurs worldwide, seriously affecting the yield and quality of sugarcane. It is essential to reveal the molecular pathogenesis of S. scitamineum to explore a new control strategy of sugarcane smut. Based on transcriptome sequencing data of two S. scitamineum strains Ss16 and Ss47, each with a different pathogenicity, our laboratory screened out the SsCI80130 gene predicted to encode squalene monooxygenase. In this study, we obtained the knockout mutants (ΔSs80130+ and ΔSs80130) and complementary mutants (COM80130+ and COM80130) of this gene by the polyethylene glycol-mediated (PEG-mediated) protoplast transformation technology, and then performed a functional analysis of the gene. The results showed that the deletion of the SsCI80130 gene resulted in the increased content of squalene (substrate for squalene monooxygenase) and decreased content of ergosterol (the final product of the ergosterol synthesis pathway) in S. scitamineum. Meanwhile, the sporidial growth rate of the knockout mutants was significantly slower than that of the wild type and complementary mutants; under cell-wall stress or oxidative stress, the growth of the knockout mutants was significantly inhibited. In addition, the sexual mating ability and pathogenicity of knockout mutants were significantly weakened, while the sexual mating ability could be restored by adding exogenous small-molecular signal substance cAMP (cyclic adenosine monophosphate) or tryptophol. It is speculated that the SsCI80130 gene was involved in the ergosterol biosynthesis in S. scitamineum and played an important role in the sporidial growth, stress response to different abiotic stresses (including cell wall stress and oxidative stress), sexual mating/filamentation and pathogenicity. Moreover, the SsCI80130 gene may affect the sexual mating and pathogenicity of S. scitamineum by regulating the ergosterol synthesis and the synthesis of the small-molecular signal substance cAMP or tryptophol required for sexual mating. This study reveals for the first time that the gene encoding squalene monooxygenase is involved in regulating the sexual mating and pathogenicity of S. scitamineum, providing a basis for the molecular pathogenic mechanism of S. scitamineum. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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20 pages, 7274 KiB  
Article
Seventeen Ustilaginaceae High-Quality Genome Sequences Allow Phylogenomic Analysis and Provide Insights into Secondary Metabolite Synthesis
by Lena Ullmann, Daniel Wibberg, Tobias Busche, Christian Rückert, Andreas Müsgens, Jörn Kalinowski and Lars M. Blank
J. Fungi 2022, 8(3), 269; https://doi.org/10.3390/jof8030269 - 8 Mar 2022
Cited by 8 | Viewed by 3566
Abstract
The family of Ustilaginaceae belongs to the order of Basidiomycetes. Despite their plant pathogenicity causing, e.g., corn smut disease, they are also known as natural producers of value-added chemicals such as extracellular glycolipids, organic acids, and polyols. Here, we present 17 high-quality draft [...] Read more.
The family of Ustilaginaceae belongs to the order of Basidiomycetes. Despite their plant pathogenicity causing, e.g., corn smut disease, they are also known as natural producers of value-added chemicals such as extracellular glycolipids, organic acids, and polyols. Here, we present 17 high-quality draft genome sequences (N50 > 1 Mb) combining third-generation nanopore and second-generation Illumina sequencing. The data were analyzed with taxonomical genome-based bioinformatics methods such as Percentage of Conserved Proteins (POCP), Average Nucleotide Identity (ANI), and Average Amino Acid Identity (AAI) analyses indicating that a reclassification of the Ustilaginaceae family might be required. Further, conserved core genes were determined to calculate a phylogenomic core genome tree of the Ustilaginaceae that also supported the results of the other phylogenomic analysis. In addition, to genomic comparisons, secondary metabolite clusters (e.g., itaconic acid, mannosylerythritol lipids, and ustilagic acid) of biotechnological interest were analyzed, whereas the sheer number of clusters did not differ much between species. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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14 pages, 5875 KiB  
Article
Identification and Functional Characterization of a Putative Alternative Oxidase (Aox) in Sporisorium reilianum f. sp. zeae
by Hector Mendoza, Caroline D. Culver, Emma A. Lamb, Luke A. Schroeder, Sunita Khanal, Christian Müller, Jan Schirawski and Michael H. Perlin
J. Fungi 2022, 8(2), 148; https://doi.org/10.3390/jof8020148 (registering DOI) - 31 Jan 2022
Cited by 3 | Viewed by 3449
Abstract
The mitochondrial electron transport chain consists of the classical protein complexes (I–IV) that facilitate the flow of electrons and coupled oxidative phosphorylation to produce metabolic energy. The canonical route of electron transport may diverge by the presence of alternative components to the electron [...] Read more.
The mitochondrial electron transport chain consists of the classical protein complexes (I–IV) that facilitate the flow of electrons and coupled oxidative phosphorylation to produce metabolic energy. The canonical route of electron transport may diverge by the presence of alternative components to the electron transport chain. The following study comprises the bioinformatic identification and functional characterization of a putative alternative oxidase in the smut fungus Sporisorium reilianum f. sp. zeae. This alternative respiratory component has been previously identified in other eukaryotes and is essential for alternative respiration as a response to environmental and chemical stressors, as well as for developmental transitionaoxs during the life cycle of an organism. A growth inhibition assay, using specific mitochondrial inhibitors, functionally confirmed the presence of an antimycin-resistant/salicylhydroxamic acid (SHAM)-sensitive alternative oxidase in the respirasome of S. reilianum. Gene disruption experiments revealed that this enzyme is involved in the pathogenic stage of the fungus, with its absence effectively reducing overall disease incidence in infected maize plants. Furthermore, gene expression analysis revealed that alternative oxidase plays a prominent role in the teliospore developmental stage, in agreement with favoring alternative respiration during quiescent stages of an organism’s life cycle. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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19 pages, 3416 KiB  
Article
Ustilago maydis Secreted Endo-Xylanases Are Involved in Fungal Filamentation and Proliferation on and Inside Plants
by Ismael Moreno-Sánchez, María Dolores Pejenaute-Ochoa, Blanca Navarrete, Ramón R. Barrales and José I. Ibeas
J. Fungi 2021, 7(12), 1081; https://doi.org/10.3390/jof7121081 - 15 Dec 2021
Cited by 7 | Viewed by 3287
Abstract
Plant pathogenic fungi must be able to degrade host cell walls in order to penetrate and invade plant tissues. Among the plant cell wall degrading enzymes (PCWDEs) produced, xylanases are of special interest since its degradation target, xylan, is one of the main [...] Read more.
Plant pathogenic fungi must be able to degrade host cell walls in order to penetrate and invade plant tissues. Among the plant cell wall degrading enzymes (PCWDEs) produced, xylanases are of special interest since its degradation target, xylan, is one of the main structural polysaccharides in plant cell walls. In the biotrophic fungus Ustilago maydis, attempts to characterize PCWDEs required for virulence have been unsuccessful, most likely due to functional redundancy. In previous high-throughput screening, we found one xylanase to be important for U. maydis infection. Here, we characterize the entire U. maydis endo-xylanase family, comprising two enzymes from the glycoside hydrolase (GH) 10 family, Xyn1 and Xyn2, one from GH11, Xyn11A, and one from GH43, Xyn3. We show that all endo-xylanases except Xyn3 are secreted and involved in infection in a non-redundant manner, suggesting different roles for each xylanase in this process. Taking a closer look inside the plant during the pathogenic process, we observed that all secreted xylanases were necessary for fungal proliferation. Finally, we found that at least Xyn11A accumulated in the apoplast of the infected plant after three days, highlighting the role of these enzymes as important secreted proteins during fungal proliferation inside plant tissues. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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28 pages, 7755 KiB  
Article
Fungal Pathogen Emergence: Investigations with an Ustilago maydis × Sporisorium reilianum Hybrid
by Emilee R. M. Storfie and Barry J. Saville
J. Fungi 2021, 7(8), 672; https://doi.org/10.3390/jof7080672 - 20 Aug 2021
Cited by 3 | Viewed by 2672
Abstract
The emergence of new fungal pathogens threatens sustainable crop production worldwide. One mechanism by which new pathogens may arise is hybridization. To investigate hybridization, the related smut fungi, Ustilago maydis and Sporisorium reilianum, were selected because they both infect Zea mays [...] Read more.
The emergence of new fungal pathogens threatens sustainable crop production worldwide. One mechanism by which new pathogens may arise is hybridization. To investigate hybridization, the related smut fungi, Ustilago maydis and Sporisorium reilianum, were selected because they both infect Zea mays, can hybridize, and tools are available for their analysis. The hybrid dikaryons of these fungi grew as filaments on plates but their colonization and virulence in Z. mays were reduced compared to the parental dikaryons. The anthocyanin induction caused by the hybrid dikaryon infections was distinct, suggesting its interaction with the host was different from that of the parental dikaryons. Selected virulence genes previously characterized in U. maydis and their predicted S. reilianum orthologs had altered transcript levels during hybrid infection of Z. mays. The downregulated U. maydis effectors, tin2, pit2, and cce1, and transcription factors, rbf1, hdp2, and nlt1, were constitutively expressed in the hybrid. Little impact was observed with increased effector expression; however, increased expression of rbf1 and hdp2, which regulate early pathogenic development by U. maydis, increased the hybrid’s capacity to induce symptoms including the rare induction of small leaf tumors. These results establish a base for investigating molecular aspects of smut fungal hybrid pathogen emergence. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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20 pages, 6920 KiB  
Article
Histidine Kinase Sln1 and cAMP/PKA Signaling Pathways Antagonistically Regulate Sporisorium scitamineum Mating and Virulence via Transcription Factor Prf1
by Enping Cai, Shuquan Sun, Yizhen Deng, Peishen Huang, Xian Sun, Yuting Wang, Changqing Chang and Zide Jiang
J. Fungi 2021, 7(8), 610; https://doi.org/10.3390/jof7080610 - 28 Jul 2021
Cited by 11 | Viewed by 2394
Abstract
Many prokaryotes and eukaryotes utilize two-component signaling pathways to counter environmental stress and regulate virulence genes associated with infection. In this study, we identified and characterized a conserved histidine kinase (SsSln1), which is the sensor of the two-component system of Sln1–Ypd1–Ssk1 in Sporisorium [...] Read more.
Many prokaryotes and eukaryotes utilize two-component signaling pathways to counter environmental stress and regulate virulence genes associated with infection. In this study, we identified and characterized a conserved histidine kinase (SsSln1), which is the sensor of the two-component system of Sln1–Ypd1–Ssk1 in Sporisorium scitamineum. SsSln1 null mutant exhibited enhanced mating and virulence capabilities in S. scitamineum, which is opposite to what has been reported in Candida albicans. Further investigations revealed that the deletion of SsSLN1 enhanced SsHog1 phosphorylation and nuclear localization and thus promoted S. scitamineum mating. Interestingly, SsSln1 and cAMP/PKA signaling pathways antagonistically regulated the transcription of pheromone-responsive transcription factor SsPrf1, for regulating S. scitamineum mating and virulence. In short, the study depicts a novel mechanism in which the cross-talk between SsSln1 and cAMP/PKA pathways antagonistically regulates mating and virulence by balancing the transcription of the SsPRF1 gene in S. scitamineum. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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15 pages, 11524 KiB  
Article
A Novel Core Effector Vp1 Promotes Fungal Colonization and Virulence of Ustilago maydis
by Cuong V. Hoang, Chibbhi K. Bhaskar and Lay-Sun Ma
J. Fungi 2021, 7(8), 589; https://doi.org/10.3390/jof7080589 - 23 Jul 2021
Cited by 6 | Viewed by 4096
Abstract
The biotrophic fungus Ustilago maydis secretes a plethora of uncharacterized effector proteins and causes smut disease in maize. Among the effector genes that are up-regulated during the biotrophic growth in maize, we identified vp1 (virulence promoting 1), which has an expression [...] Read more.
The biotrophic fungus Ustilago maydis secretes a plethora of uncharacterized effector proteins and causes smut disease in maize. Among the effector genes that are up-regulated during the biotrophic growth in maize, we identified vp1 (virulence promoting 1), which has an expression that was up-regulated and maintained at a high level throughout the life cycle of the fungus. We characterized Vp1 by applying in silico analysis, reverse genetics, phenotypic assessment, microscopy, and protein localization and provided a fundamental understanding of the Vp1 protein in U. maydis. The reduction in fungal virulence and colonization in the vp1 mutant suggests the virulence-promoting function of Vp1. The deletion studies on the NLS (nuclear localization signal) sequence and the protein localization study revealed that the C-terminus of Vp1 is processed after secretion in plant apoplast and could localize to the plant nucleus. The Ustilago hordei ortholog UhVp1 lacks NLS localized in the plant cytoplasm, suggesting that the orthologs might have a distinct subcellular localization. Further complementation studies of the Vp1 orthologs in related smut fungi revealed that none of them could complement the virulence function of U. maydis Vp1, suggesting that UmVp1 could acquire a specialized function via sequence divergence. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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Review

Jump to: Research

20 pages, 931 KiB  
Review
Sugarcane Smut: Current Knowledge and the Way Forward for Management
by Muhammad Aslam Rajput, Nasir Ahmed Rajput, Rehana Naz Syed, Abdul Mubeen Lodhi and Youxiong Que
J. Fungi 2021, 7(12), 1095; https://doi.org/10.3390/jof7121095 - 19 Dec 2021
Cited by 35 | Viewed by 8685
Abstract
Whip smut of sugarcane is the most serious and widely spread disease of sugarcane and causes a significant reduction in cane quantity and quality. The severity of this disease often depends on the pathogen races, environmental conditions, cultivar genotype and the interaction among [...] Read more.
Whip smut of sugarcane is the most serious and widely spread disease of sugarcane and causes a significant reduction in cane quantity and quality. The severity of this disease often depends on the pathogen races, environmental conditions, cultivar genotype and the interaction among these three factors. Under optimum climatic conditions, this disease has the potential to cause total crop failure. Resistance screening is an ongoing process due to the variability among smut pathogen isolates. Multiple races and mutation ability of smut pathogen makes the breeding task more complex. A number of studies on various aspects of the disease epidemiology and management have been published. Due to many overlapping characteristics within the species complex, there is a dearth of information on early detection and strategies to control the smut pathogen. Furthermore, there is a need to coordinate these findings to expedite its research and control. In this paper, we summarize the disease etiology, especially disease impact on the qualitative and quantitative parameters of sugarcane. We also gathered research progress on molecular-based detection and available information on genetic variability in S.scitamineum. The research on the set of management options needed to effectively cope with the disease are reviewed herein. The present review is expected to be helpful for the further investigation on smut resistance in sugarcane. Full article
(This article belongs to the Special Issue Smut Fungi 2.0)
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