The Novel Effector Ue943 Is Essential for Host Plant Colonization by Ustilago esculenta.

The smut fungus Ustilago esculenta obligately parasitizes Zizania latifolia and induces smut galls at the stem tips of host plants. Previous research identified a putative secreted protein, Ue943, which is required for the biotrophic phase of U. esculenta but not for the saprophytic phase. Here, we studied the role of Ue943 during the infection process. Conserved homologs of Ue943 were found in smut fungi. Ue943 can be secreted by U. esculenta and localized to the biotrophic interface between fungi and plants. It is required at the early stage of colonization. The Ue943 deletion mutant caused reactive oxygen species (ROS) production and callose deposition in the host plant at 1 and 5 days post inoculation, which led to failed colonization. The virulence deficiency was restored by overexpressing gene Ue943 or Ue943:GFP. Transcriptome analysis further showed a series of changes in plant hormones following ROS production when the host plant was exposed to ΔUe943. We hypothesize that Ue943 might be responsible for ROS suppression or avoidance of recognition by the plant immune system. The mechanism underlying Ue943 requires further study to provide more insights into the virulence of smut fungi.

[1]  B. Thomma,et al.  Structural and functional analysis of the cerato‐platanin‐like protein Cpl1 suggests diverging functions in smut fungi , 2023, Molecular plant pathology.

[2]  ShiYu Li,et al.  Transcriptome Comparison between Two Strains of Ustilago esculenta during the Mating , 2022, Journal of fungi.

[3]  Lihu Wang,et al.  The interaction of ABA and ROS in plant growth and stress resistances , 2022, Frontiers in Plant Science.

[4]  Nurul Arneida Husin.  Transcriptome analysis during fruit developmental stages in durian (Durio zibethinus Murr.) var. D24 , 2022, bioRxiv.

[5]  ShiYu Li,et al.  An Endoglucanase Secreted by Ustilago esculenta Promotes Fungal Proliferation , 2022, Journal of fungi.

[6]  I. Dubery,et al.  The presence of oxygenated lipids in plant defense in response to biotic stress: a metabolomics appraisal , 2021, Plant signaling & behavior.

[7]  B. Saville,et al.  Fungal Pathogen Emergence: Investigations with an Ustilago maydis × Sporisorium reilianum Hybrid , 2021, Journal of fungi.

[8]  R. Funada,et al.  Direct fluorescence imaging of lignocellulosic and suberized cell walls in roots and stems , 2020, AoB PLANTS.

[9]  Marco Milanesi,et al.  PANEV: an R package for a pathway-based network visualization , 2020, BMC Bioinformatics.

[10]  Min Wu,et al.  Cloning and disruption of the UeArginase in Ustilago esculenta: evidence for a role of arginine in its dimorphic transition , 2019, BMC Microbiology.

[11]  Leili Shahriyari,et al.  Effect of normalization methods on the performance of supervised learning algorithms applied to HTSeq-FPKM-UQ data sets: 7SK RNA expression as a predictor of survival in patients with colon adenocarcinoma , 2019, Briefings Bioinform..

[12]  M. Thines,et al.  Saprotrophic yeasts formerly classified as Pseudozyma have retained a large effector arsenal, including functional Pep1 orthologs , 2019, Mycological Progress.

[13]  R. Kahmann,et al.  Neofunctionalization of the secreted Tin2 effector in the fungal pathogen Ustilago maydis , 2018, Nature Microbiology.

[14]  Urs Lahrmann,et al.  Mining the effector repertoire of the biotrophic fungal pathogen Ustilago hordei during host and non-host infection. , 2018, Molecular plant pathology.

[15]  Pitter F. Huesgen,et al.  Dual function of a secreted fungalysin metalloprotease in Ustilago maydis. , 2018, The New phytologist.

[16]  Lei Wang,et al.  The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins , 2018, Nature Communications.

[17]  Ping Liu,et al.  Transcriptome analysis of PCOS arrested 2-cell embryos , 2018, Cell cycle.

[18]  V. Walbot,et al.  How to make a tumour: cell type specific dissection of Ustilago maydis-induced tumour development in maize leaves. , 2018, The New phytologist.

[19]  Yafen Zhang,et al.  Investigation on the differentiation of two Ustilago esculenta strains - implications of a relationship with the host phenotypes appearing in the fields , 2017, BMC Microbiology.

[20]  J. Zhang,et al.  RNA-seq analysis provides insight into reprogramming of culm development in Zizania latifolia induced by Ustilago esculenta , 2017, Plant Molecular Biology.

[21]  S. Reissmann,et al.  Ustilago maydis effectors and their impact on virulence , 2017, Nature Reviews Microbiology.

[22]  A. Holzinger,et al.  Aniline blue and Calcofluor white staining of callose and cellulose in the streptophyte green algae Zygnema and Klebsormidium. , 2016, Bio-protocol.

[23]  G. Doehlemann,et al.  Conservation of the Ustilago maydis effector See1 in related smuts , 2015, Plant signaling & behavior.

[24]  Yafen Zhang,et al.  An efficient genetic manipulation protocol for Ustilago esculenta. , 2015, FEMS microbiology letters.

[25]  V. Seidl-Seiboth,et al.  Cerato-platanins: elicitors and effectors. , 2014, Plant science : an international journal of experimental plant biology.

[26]  M. Thines,et al.  Gene Loss Rather Than Gene Gain Is Associated with a Host Jump from Monocots to Dicots in the Smut Fungus Melanopsichium pennsylvanicum , 2014, Genome biology and evolution.

[27]  S. Molinari,et al.  Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. , 2014, Molecular plant pathology.

[28]  I. Feussner,et al.  A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize , 2014, eLife.

[29]  G. Doehlemann,et al.  Compatibility in the Ustilago maydis–Maize Interaction Requires Inhibition of Host Cysteine Proteases by the Fungal Effector Pit2 , 2013, PLoS pathogens.

[30]  WenLi Chen,et al.  Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana , 2011, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[31]  Chung-Mo Park,et al.  MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. , 2010, The New phytologist.

[32]  M. Torres.  ROS in biotic interactions. , 2010, Physiologia plantarum.

[33]  A. Mohanty,et al.  Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells , 2009, PLoS pathogens.

[34]  Karolina M. Pajerowska-Mukhtar,et al.  Salicylic Acid Inhibits Pathogen Growth in Plants through Repression of the Auxin Signaling Pathway , 2007, Current Biology.

[35]  P. Schreier,et al.  Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis , 2007, Molecular Genetics and Genomics.

[36]  O. Matsuda,et al.  Role of chloroplast trienoic fatty acids in plant disease defense responses. , 2004, The Plant journal : for cell and molecular biology.

[37]  G. Braus,et al.  Establishing a versatile Golden Gate cloning system for genetic engineering in fungi. , 2014, Fungal genetics and biology : FG & B.

[38]  Jiana Li,et al.  Horizontal gene transfer in plants , 2013, Functional & Integrative Genomics.

[39]  N. Jambunathan.  Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. , 2010, Methods in molecular biology.