A novel transcription factor UvCGBP1 regulates development and virulence of rice false smut fungus Ustilaginoidea virens

References

• Sun WX, Fan J, Fang AF, et al. Ustilaginoidea virens: insights into an emerging rice pathogen. Annu Rev Phytopathol. 2020;58:1–23.
   PubMed Web of Science ®Google Scholar
• Guo XY, Li Y, Fan J, et al. Progress in the study of false smut disease in rice. J Agric Sci Technol. 2012;2:1211–1217.
   Google Scholar
• Koiso Y, Li Y, Iwasaki S, et al. Ustiloxins, antimitotic cyclic peptides from false smut balls on rice panicles caused by Ustilaginoidea virens. J Antibiot. 1994;47:765–773.
   PubMed Web of Science ®Google Scholar
• Miyazaki S, Matsumoto Y, Uchihara T, et al. High-performance liquid chromatographic determination of ustiloxin A in forage rice silage. J Vet Med Sci. 2009;71:239–241.
   PubMed Web of Science ®Google Scholar
• Ashizawa T, Takahashi M, Arai M, et al. Rice false smut pathogen, Ustilaginoidea virens, invades through small gap at the apex of a rice spikelet before heading. J Gen Plant Pathol. 2012;78:255–259.
   Web of Science ®Google Scholar
• Tang YX, Jin J, Hu DW, et al. Elucidation of the infection process of Ustilaginoidea virens (teleomorph: villosiclava virens) in rice spikelets. Plant Pathol. 2013;62:1–8.
   Web of Science ®Google Scholar
• Fan J, Liu J, Gong ZY, et al. The false smut pathogen Ustilaginoidea virens requires rice stamens for false smut ball formation. Environ Microbiol. 2020;2:646–659.
   Web of Science ®Google Scholar
• Song JH, Wei W, Lv B, et al. Rice false smut fungus hijacks the rice nutrients supply by blocking and mimicking the fertilization of rice ovary. Environ Microbiol. 2016;18:3840–3849.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang K, Fang AF, et al. Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nat Commun. 2014;5:3849.
   PubMed Web of Science ®Google Scholar
• Chen XY, Tang JT, Pei ZX, et al. The “pears and lemons” protein UvPal1 regulates development and virulence of Ustilaginoidea virens. Environ Microbiol. 2020;22:5414–5432.
   PubMed Web of Science ®Google Scholar
• Lv B, Zheng L, Liu H, et al. Use of random T-DNA mutagenesis in identification of gene UvPRO1, a regulator of conidiation, stress response, and virulence in Ustilaginoidea virens. Front Microbiol. 2016;7:2086.
   PubMed Web of Science ®Google Scholar
• Yu JJ, Yu MN, Song TQ, et al. A homeobox transcription factor UvHOX2 regulates chlamydospore formation, conidiogenesis and pathogenicity in Ustilaginoidea virens. Front Microbiol. 2019;10:1071.
   PubMed Web of Science ®Google Scholar
• Mt Z, Ding H, Huang L, et al. Low-affinity iron transport protein Uvt3277 is important for pathogenesis in the rice false smut fungus Ustilaginoidea virens. Curr Genet. 2017;63:131–144.
   PubMed Web of Science ®Google Scholar
• Fang AF, Gao H, Zhang N, et al. A novel effector gene SCRE2 contributes to full virulence of Ustilaginoidea virens to rice. Front Microbiol. 2019;10:845.
   PubMed Web of Science ®Google Scholar
• Xie SL, Wang YF, Wei W, et al. The Bax inhibitor UvBI-1, a negative regulator of mycelial growth and conidiation, mediates stress response and is critical for pathogenicity of the rice false smut fungus Ustilaginoidea virens. Curr Genet. 2019;65:1–13.
   PubMed Web of Science ®Google Scholar
• Guo WW, Gao YX, Yu ZM, et al. The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens. Fungal Genet Biol. 2019;129:65–73.
   PubMed Web of Science ®Google Scholar
• Tang JT, Bai J, Chen XY, et al. Two protein kinases UvPmk1 and UvCDC2 with significant functions in conidiation, stress response and pathogenicity of rice false smut fungus Ustilaginoidea virens. Curr Genet. 2019;66:409–420.
   PubMed Web of Science ®Google Scholar
• Chen XY, Hai D, Tang JT, et al. UvCom1 is an important regulator required for development and infection in the rice false smut fungus Ustilaginoidea virens. Phytopathology. 2020;110:483–493.
   PubMed Web of Science ®Google Scholar
• Meng S, Xiong M, Jagernath JS, et al. UvAtg8-mediated autophagy regulates fungal growth, stress responses, conidiation, and pathogenesis in Ustilaginoidea virens. Rice. 2020;13:56.
   PubMed Web of Science ®Google Scholar
• Chen XY, Li XB, Li PP, et al. Comprehensive identification of lysine 2-hydroxyisobutyrylated proteins in Ustilaginoidea virens reveals the involvement of lysine 2-hydroxyisobutyrylation in fungal virulence. J Integr Plant Biol. 2021;63:409–425.
   PubMed Web of Science ®Google Scholar
• Zhang N, Yang J, Fang AF, et al. The essential effector SCRE1 in Ustilaginoidea virens suppresses rice immunity via a small peptide region. Mol Plant Pathol. 2020;21:445–459.
   PubMed Web of Science ®Google Scholar
• Fan J, Du N, Li L, et al. A core effector UV_1261 promotes Ustilaginoidea virens infection via spatiotemporally suppressing plant defense. Phytopathol Res. 2019;1: 11.
   Google Scholar
• Chen XY, Pei ZX, Li PP, et al. Quantitative proteomics analysis reveals the function of the putative Ester Cyclase UvEC1 in the pathogenicity of the rice false smut fungus Ustilaginoidea virens. Int J Mol Sci. 2021;22:4069.
   PubMed Web of Science ®Google Scholar
• Lorito M, Mach RL, Sposato P, et al. Mycoparasitic interaction relieves binding of Cre1 carbon catabolite repressor protein to promoter sequence of ech-42 (endochitinase-encoding) gene of Trichoderma harzianum. Proc Natl Acad Sci USA. 1996;93:14868–14872.
   PubMed Web of Science ®Google Scholar
• De las Mercedes Dana M, Limon CM, Meijas R, et al. Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr Genet. 2000;38:335–342.
   Web of Science ®Google Scholar
• Kamper JT, Kamper U, Rogers LM, et al. Identification of regulatory elements in the cutinase promoter from Fusarium solani f. sp. pisi (Nectria haematococca). J Biol Chem. 1994;269:9195–9204.
   PubMed Web of Science ®Google Scholar
• Martinez-Pastor MT, Marchler G, Schuller C, et al. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress-response element (STRE). EMBO J. 1996;15:2227–2235.
   PubMed Web of Science ®Google Scholar
• Hurtado CA, Rachubinski RA. MHY1 encodes a C2H2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J Bacteriol. 1999;181:3051–3057.
   PubMed Web of Science ®Google Scholar
• Peterbauer C, Litscher D, Kubicek C. The Trichoderma atroviride seb1 (stress response element binding) gene encodes an AGGGG-binding protein which is involved in the response to high osmolarity stress. Mol Genet Genomics. 2002;268:223–231.
   PubMed Web of Science ®Google Scholar
• Jia Q, Lv B, Guo MY, et al. Effect of rice growth stage, temperature, relative humidity and wetness duration on infection of rice panicles by Villosiclava virens. EurJ Plant Pathol. 2015;141:15–25.
   Web of Science ®Google Scholar
• Wang YX, Chen JY, Li DW, et al. CgICUTl gene required for cutinase activity and pathogenicity of Colletotrichum gloeosporioides causing anthracnose of Camellia oleifera. EurJ Plant Pathol. 2017;147:103–114.
   Web of Science ®Google Scholar
• Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105–1111.
   PubMed Web of Science ®Google Scholar
• Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323.
   PubMed Web of Science ®Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140.
   PubMed Web of Science ®Google Scholar
• Xie C, Mao X, Huang J, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011;39:316–322.
   PubMed Web of Science ®Google Scholar
• Feng JX, Liu T, Qin B, et al. Identifying ChIP-seq enrichment using MACS. Nat Protoc. 2012;7:1728–1740.
   PubMed Web of Science ®Google Scholar
• Wang S, Sun HF, Ma J, et al. Target analysis by integration of transcriptome and ChIP-seq data with BETA. Nat Protoc. 2013;8:2502–2515.
   PubMed Web of Science ®Google Scholar
• Pepke S, Wold B, Mortazavi A. Computation for ChIP-seq and RNA-seq studies. Nat Methods. 2009;6:S22–S32.
   PubMed Web of Science ®Google Scholar
• Stephen GL, Georgi KM, Anshul K, et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 2012;22:1813–1831.
   PubMed Web of Science ®Google Scholar
• Wang Z, Zhang H, Liu C, et al. A deubiquitinating enzyme Ubp14 is required for development, stress response, nutrient utilization, and pathogenesis of Magnaporthe oryzae. Front Microbiol. 2018;9:769.
   PubMed Web of Science ®Google Scholar
• Tang JT, Chen XY, Yan YQ, et al. Comprehensive transcriptome profiling reveals abundant long non-coding RNAs associated with development of the rice false smut fungus, Ustilaginoidea virens. Environ Microbiol. 2021. DOI:10.1111/1462-2920.15432
   Web of Science ®Google Scholar
• Nikolaou E, Agrafioti I, Stumpf M, et al. Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol. 2009;9:44.
   PubMed Web of Science ®Google Scholar
• Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–399.
   PubMed Web of Science ®Google Scholar
• Chen S, Su L, Chen J, et al. Cutinase: characteristics, preparation, and application. Biotechnol Adv. 2013;31:1754–1767.
   PubMed Web of Science ®Google Scholar
• Kolattukudy PE, Li DX, Hwang CS, et al. Host signals in fungal gene-expression involved in penetration into the host. Can J Bot. 1995;73:1160–1168.
   Google Scholar
• Liu T, Hou J, Wang Y, et al. Genome-wide identification, classification and expression analysis in fungal-plant interactions of cutinase gene family and functional analysis of a putative ClCUT7 in Curvularia lunata. Mol Genet Genomics. 2016;291:1105–1115.
   PubMed Web of Science ®Google Scholar
• Sweigard JA, Chumley FG, Valent B. Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet. 1992;232:183–190.
   PubMedGoogle Scholar
• Skamnioti P, Gurr SJ. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell. 2007;19:2674–2689.
   PubMed Web of Science ®Google Scholar
• van Kan JAL, van’t Klooster JW, Wagemakers CAM, et al. Cutinase a of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol Plant Microbe Interact. 1997;10:30–38.
   PubMed Web of Science ®Google Scholar
• Li GT, Zhou XY, Xu JR. Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol. 2012;6:678–684.
   Web of Science ®Google Scholar
• Jiang C, Zhang X, Liu HQ, et al. Mitogen-activated protein kinase signalling in plant pathogenic fungi. PLoS Pathog. 2018;14:e1006875.
   PubMed Web of Science ®Google Scholar
• Li YB, Xu R, Liu CY, et al. Magnaporthe oryzae fimbrin organizes actin networks in the hyphal tip during polar growth and pathogenesis. PLoS Pathog. 2020;16(3):e1008437.
   PubMed Web of Science ®Google Scholar
• Machado AK, Brown NA, Urban M, et al. RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals. Pest Manag Sci. 2018;74(4):790–799.
   PubMed Web of Science ®Google Scholar
• Zhu X, Qi T, Yang Q, et al. Host-induced gene silencing of the MAPKK gene PsFUZ7 confers stable resistance to wheat stripe rust. Plant Physiol. 2017;175:1853–1863.
   PubMed Web of Science ®Google Scholar
• Wang MH, Wu L, Mei YZ, et al. Host-induced gene silencing of multiple genes of Fusarium graminearum enhances resistance to Fusarium head blight in wheat. Plant Biotechnol J. 2020;18:2373–2375.
   Google Scholar
• Koch A, Kumar N, Weber L, et al. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci USA. 2013;110:19324–19329.
   PubMed Web of Science ®Google Scholar
• Cheng W, Song XS, Li HP, et al. Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnol J. 2015;13:1335–1345.
   PubMed Web of Science ®Google Scholar
• Nowara D, Gay A, Lacomme C, et al. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell. 2010;22:3130–3141.
   PubMed Web of Science ®Google Scholar