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Modulation of Host Immunity and Development by Ustilago maydis

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Plant Relationships

Part of the book series: The Mycota ((MYCOTA,volume 5))

Abstract

Fungal pathogens are an enormous threat to plants, causing tremendous losses in worldwide crop production. A mechanistic understanding of fungal virulence is crucial to developing novel plant protection strategies in sustainable agriculture. Biotrophic pathogens colonize living plant tissue and reprogram their hosts to stimulate proliferation and development of fungal infection structures. To promote infection, fungal pathogens secrete sets of virulence proteins termed “effectors” which interfere with host metabolism and cellular function.

The maize smut pathogen, Ustilago maydis, has been established for decades as a prime model system for understanding the genetics, cell biology and pathology of biotrophic fungi. U. maydis colonizes primordia of all aerial parts of the maize plant resulting in a comprehensive reprogramming of organ development and host physiology. The most prominent symptoms of maize smut disease are large galls/tumors, which develop within a week at infection sites and contain the teliospores that in nature are the predominant dispersal stage of U. maydis.

Within this chapter, we summarize the current knowledge on the pathogenic development of U. maydis with an emphasis on its effector repertoire and how it interferes with the host plant during infection. We discuss evolution and transcriptional activation of the fungal effectome, as well as the known molecular mechanisms of virulence by fungal effectors and the plant processes they modulate. We also highlight gaps in current knowledge, discuss limitations of the system, and provide an outlook on possible strategies to address unsolved research questions.

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References

  • Alcantara A, Bosch J, Nazari F, Hoffmann G, Gallei M, Uhse S, Darino MA, Olukayode T, Reumann D, Baggaley L, Djamei A (2019) Systematic Y2H screening reveals extensive effector-complex formation. Front Plant Sci 10:1437

    Article  Google Scholar 

  • Allen A, Islamovic E, Kaur J, Gold S, Shah D, Smith TJ (2013) The virally encoded killer proteins from Ustilago maydis. Fungal Biol Rev 26:166–173

    Article  Google Scholar 

  • Altegoer F, Weiland P, Giammarinaro PI, Freibert S-A, Binnebesel L, Han X, Lepak A, Kahmann R, Lechner M, Bange G (2020) The two paralogous kiwellin proteins KWL1 and KWL1-b from maize are structurally related and have overlapping functions in plant defense. J Biol Chem 295:7816–7825

    Article  CAS  Google Scholar 

  • Altmann M, Altmann S, Rodriguez PA, Weller B, Elorduy Vergara L, Palme J, Marín-de la rosa N, Sauer M, Wenig M, Villaécija-Aguilar JA, Sales J, Lin C-W, Pandiarajan R, Young V, Strobel A, Gross L, Carbonnel S, Kugler KG, Garcia-Molina A, Bassel GW, Falter C, Mayer KFX, Gutjahr C, Vlot AC, Grill E, Falter-Braun P (2020) Extensive signal integration by the phytohormone protein network. Nature 583:271–276

    Article  CAS  Google Scholar 

  • Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080

    Article  CAS  Google Scholar 

  • Azevedo C, Betsuyaku S, Peart J, Takahashi A, Noël L, Sadanandom A, Casais C, Parker J, Shirasu K (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J 25:2007–2016

    Article  CAS  Google Scholar 

  • Bauer R, Begerow D, Oberwinkler E, Piepenbring M, Berbee ML (2001) Ustilaginomycetes. Systematics and evolution. Springer, New York

    Google Scholar 

  • Baumgarten AM, Suresh J, May G, Phillips RL (2007) Mapping QTLs contributing to Ustilago maydis resistance in specific plant tissues of maize. Theor Appl Genet 114:1229–1238

    Article  Google Scholar 

  • Bauters L, Stojilković B, Gheysen G (2021) Pathogens pulling the strings: effectors manipulating salicylic acid and phenylpropanoid biosynthesis in plants. Mol Plant Pathol 22:1436–1448

    Article  CAS  Google Scholar 

  • Benevenuto J, Teixeira-Silva NS, Kuramae EE, Croll D, Monteiro-Vitorello CB (2018) Comparative genomics of smut pathogens: insights from orphans and positively selected genes into host specialization. Front Microbiol 9

    Google Scholar 

  • Bindics J, Khan M, Uhse S, Kogelmann B, Baggely L, Reumann D, Ingole KD, Stirnberg A, Rybecky A, Darino M, Navarrete F, Doehlemann G, Djamei A (2022) Many ways to TOPLESS – manipulation of plant auxin signalling by a cluster of fungal effectors. New Phytol 236(4):1455–1470. https://doi.org/10.1111/nph.18315

    Article  Google Scholar 

  • Bleau JR, Spoel SH (2021) Selective redox signaling shapes plant-pathogen interactions. Plant Physiol 186:53–65

    Article  CAS  Google Scholar 

  • Bölker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68:9

    Article  Google Scholar 

  • Bosch J, Czedik-Eysenberg A, Hastreiter M, Khan M, Güldener U, Djamei A (2019) Two is better than one: studying Ustilago bromivora–Brachypodium compatibility by using a hybrid pathogen. Mol Plant Microbe Interact 32:1623–1634

    Article  CAS  Google Scholar 

  • Brachmann A, Weinzierl G, Kämper J, Kahmann R (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42:1047–1063

    Article  CAS  Google Scholar 

  • Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445

    Article  CAS  Google Scholar 

  • Brefort T, Tanaka S, Neidig N, Doehlemann G, Vincon V, Kahmann R (2014) Characterization of the largest effector gene cluster of Ustilago maydis. PLoS Pathog 10:e1003866

    Article  Google Scholar 

  • Carella P, Evangelisti E, Schornack S (2018) Sticking to it: phytopathogen effector molecules may converge on evolutionarily conserved host targets in green plants. Curr Opin Plant Biol 44:175–180

    Article  CAS  Google Scholar 

  • Castanheira S, Mielnichuk N, Perez-Martin J (2014) Programmed cell cycle arrest is required for infection of corn plants by the fungus Ustilago maydis. Development 141:4817–4826

    Article  CAS  Google Scholar 

  • Cheung HYK, Donaldson ME, Storfie ERM, Spence KL, Fetsch JLO, Harrison MC, Saville BJ (2021) Zfp1, a putative Zn(II)2Cys6 transcription factor, influences Ustilago maydis pathogenesis at multiple stages. Plant Pathol 70:1626–1639

    Article  CAS  Google Scholar 

  • Croll D, McDonald BA (2012) The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog 8:e1002608

    Article  CAS  Google Scholar 

  • Darino M, Chia K-S, Marques J, Aleksza D, Soto-Jiménez LM, Saado I, Uhse S, Borg M, Betz R, Bindics J, Zienkiewicz K, Feussner I, Petit-Houdenot Y, Djamei A (2021) Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling. New Phytol 229:3393–3407

    Article  CAS  Google Scholar 

  • Depotter JRL, Doehlemann G (2020) Target the core: durable plant resistance against filamentous plant pathogens through effector recognition. Pest Manag Sci 76:426–431

    Article  CAS  Google Scholar 

  • Depotter JR, Seidl MF, Wood TA, Thomma BP (2016) Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Curr Opin Microbiol 32:7–13

    Article  CAS  Google Scholar 

  • Depotter JRL, Van Beveren F, Rodriguez-Moreno L, Kramer HM, Chavarro Carrero EA, Fiorin GL, Van Den Berg GCM, Wood TA, Thomma B, Seidl MF (2021a) The interspecific fungal hybrid Verticillium longisporum displays subgenome-specific gene expression. mBio 12:e0149621

    Article  Google Scholar 

  • Depotter JRL, Zuo W, Hansen M, Zhang B, Xu M, Doehlemann G (2021b) Effectors with different gears: divergence of Ustilago maydis effector genes is associated with their temporal expression pattern during plant infection. J Fungi 7:16

    Article  CAS  Google Scholar 

  • Depotter JRL, Misas Villamil JC, Doehlemann G (2022) Maize immune signalling peptide ZIP1 evolved de novo from a retrotransposon. bioRxiv. https://doi.org/10.1101/2022.05.18.492421

  • Djamei A, Kahmann R (2012) Ustilago maydis: dissecting the molecular Interface between pathogen and plant. PLoS Pathog 8:e1002955

    Article  CAS  Google Scholar 

  • Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R (2011) Metabolic priming by a secreted fungal effector. Nature 478:395–398

    Article  CAS  Google Scholar 

  • Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kuhnemann J, Sonnewald U, Kahmann R, Kamper J (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195

    Article  CAS  Google Scholar 

  • Doehlemann G, Van Der Linde K, Assmann D, Schwammbach D, HOF A, Mohanty A, Jackson D, Kahmann R (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5:e1000290

    Article  Google Scholar 

  • Doehlemann G, Reissmann S, Aßmann D, Fleckenstein M, Kahmann R (2011) Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol Microbiol 81:751–766

    Article  CAS  Google Scholar 

  • Dong S, Raffaele S, Kamoun S (2015) The two-speed genomes of filamentous pathogens: waltz with plants. Curr Opin Genet Dev 35:57–65

    Article  CAS  Google Scholar 

  • Dürrenberger F, Wong K, Kronstad JW (1998) Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. Proc Natl Acad Sci 95:5684–5689

    Article  Google Scholar 

  • Dutheil JY, Mannhaupt G, Schweizer G, Sieber C, Münsterkötter M, Güldener U, Schirawski J, Kahmann R (2016) A tale of genome compartmentalization: the evolution of virulence clusters in smut fungi. Genome Biol Evol 8:681–704

    Article  Google Scholar 

  • Eitzen K, Sengupta P, Kroll S, Kemen E, Doehlemann G (2021) A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme. elife 10

    Google Scholar 

  • Erchinger P (2017) Functional characterization of the Ustilago maydis effector protein Ten1. Dissertation:125

    Google Scholar 

  • Fedler M, Luh KS, Stelter K, Nieto-Jacobo F, Basse CW (2009) The a2 mating-type locus genes lga2 and rga2 direct uniparental mitochondrial DNA (mtDNA) inheritance and constrain mtDNA recombination during sexual development of Ustilago maydis. Genetics 181:847–860

    Article  Google Scholar 

  • Fernández-Álvarez A, Marín-Menguiano M, Lanver D, Jiménez-Martín A, Elías-Villalobos A, Pérez-Pulido AJ, Kahmann R, Ibeas JI (2012) Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog 8:e1002563

    Article  Google Scholar 

  • Fernández-Álvarez A, Elías-Villalobos A, Jiménez-Martín A, Marín-Menguiano M, Ibeas JI (2013) Endoplasmic reticulum glucosidases and protein quality control factors cooperate to establish biotrophy in Ustilago maydis. Plant Cell 25:4676–4690

    Article  Google Scholar 

  • Flor-Parra I, Vranes M, Kämper JR, Pérez-Martín J (2006) Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 18:2369–2387

    Article  CAS  Google Scholar 

  • Fukada F, Rössel N, Münch K, Glatter T, Kahmann R (2021) A small Ustilago maydis effector acts as a novel adhesin for hyphal aggregation in plant tumors. New Phytol 231:416–431

    Article  CAS  Google Scholar 

  • Gage MJ, Bruenn J, Fischer M, Sanders D, Smith TJ (2001) KP4 fungal toxin inhibits growth in Ustilago maydis by blocking calcium uptake. Mol Microbiol 41:775–785

    Article  CAS  Google Scholar 

  • Gage MJ, Rane SG, Hockerman GH, Smith TJ (2002) The virally encoded fungal toxin KP4 specifically blocks L-type voltage-gated calcium channels. Mol Pharmacol 61:936–944

    Article  CAS  Google Scholar 

  • Gao L, Kelliher T, Nguyen L, Walbot V (2013) Ustilago maydis reprograms cell proliferation in maize anthers. Plant J 75:903–914

    Article  CAS  Google Scholar 

  • Gillissen BJ, Sandmann C, Schroeer B, Bölker M, Kahmann R (1992) A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 21:10

    Google Scholar 

  • Goodwin S, McPherson JD, Mccombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351

    Article  CAS  Google Scholar 

  • Gupta P, Ravi I, Sharma V (2013) Induction of β-1,3-glucanase and chitinase activity in the defense response of Eruca sativa plants against the fungal pathogen Alternaria brassicicola. J Plant Interact 8:155–161

    Article  CAS  Google Scholar 

  • Hampel M, Jakobi M, Schmitz L, Meyer U, Finkernagel F, Doehlemann G, Heimel K (2016) Unfolded protein response (UPR) regulator Cib1 controls expression of genes encoding secreted virulence factors in Ustilago maydis. PLoS One 11:e0153861

    Article  Google Scholar 

  • Han X, Altegoer F, Steinchen W, Binnebesel L, Schuhmacher J, Glatter T, Giammarinaro PI, Djamei A, Rensing SA, Reissmann S, Kahmann R, Bange G (2019) A kiwellin disarms the metabolic activity of a secreted fungal virulence factor. Nature 565:650–653

    Article  CAS  Google Scholar 

  • Haskins R, Thorn J (2011) Biochemistry of the Ustilaginales. VII. Antibiotic activity of ustilagic acid. Can J Bot 29:585–592

    Article  Google Scholar 

  • Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58

    Article  Google Scholar 

  • Heimel K, Scherer M, Vranes M, Wahl R, Pothiratana C, Schuler D, Vincon V, Finkernagel F, Flor-Parra I, Kamper J (2010) The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog 6:e1001035

    Article  Google Scholar 

  • Heimel K, Freitag J, Hampel M, Ast J, Bölker M, Kämper J (2013) Crosstalk between the unfolded protein response and pathways that regulate pathogenic development in Ustilago maydis. Plant Cell 25:4262–4277

    Article  CAS  Google Scholar 

  • Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G (2012) The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8:e1002684

    Article  CAS  Google Scholar 

  • Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G, Kumlehn J, Mishra B, Sharma R, Thines M, Hückelhoven R, Doehlemann G (2015) The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol 206:1116–1126

    Article  CAS  Google Scholar 

  • Hewald S, Linne U, Scherer M, Marahiel MA, Kämper J, Bölker M (2006) Identification of a gene cluster for biosynthesis of Mannosylerythritol lipids in the Basidiomycetous fungus Ustilago maydis. Appl Environ Microbiol 72:5469–5477

    Article  CAS  Google Scholar 

  • Hof A, Zechmann B, Schwammbach D, Hückelhoven R, Doehlemann G (2014) Alternative cell death mechanisms determine epidermal resistance in incompatible barley-Ustilago interactions. Mol Plant-Microbe Interact 27:403–414

    Article  CAS  Google Scholar 

  • Holliday R (1964) A mechanism for gene conversion in fungi. Genet Res 5:282–304

    Article  Google Scholar 

  • Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kamper J, Sonnewald U, Voll LM (2009) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol 152:293–308

    Article  Google Scholar 

  • Jonkers W, Estrada AER, Lee K, Breakspear A, May G, Kistler HC (2012) Metabolome and transcriptome of the interaction between Ustilago maydis and fusarium verticillioides in vitro. Appl Environ Microbiol 78:3656–3667

    Article  CAS  Google Scholar 

  • Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589

    Article  CAS  Google Scholar 

  • Kaffarnik F, Müller P, Leibundgut M, Kahmann R, Feldbrügge M (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22:5817–5826

    Article  CAS  Google Scholar 

  • Kamper J, Reichmann M, Romeis T, Bolker M, Kahmann R (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:73–83

    Article  CAS  Google Scholar 

  • Kamper J, Kahmann R, Bolker M, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, De Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, Decaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

    Article  Google Scholar 

  • Kellner R, Vollmeister E, Feldbrügge M, Begerow D (2011) Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system. PLoS Genet 7:e1002436

    Article  CAS  Google Scholar 

  • Kitagawa K, Skowyra D, Elledge SJ, Harper JW, Hieter P (1999) SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 4:21–33

    Article  CAS  Google Scholar 

  • Koltin Y, Day PR (1976) Inheritance of killer phenotypes and double-stranded RNA in Ustilago maydis. Proc Natl Acad Sci U S A 73:5

    Article  Google Scholar 

  • Krijger J-J, Thon MR, Deising HB, Wirsel SGR (2014) Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation. BMC Genomics 15:722

    Article  Google Scholar 

  • Kronstad JW, Leong SA (1989) Isolation of two alleles of the b locus of Ustilago maydis. Proc Natl Acad Sci U S A 86:978–982

    Article  CAS  Google Scholar 

  • Kwon S, Rupp O, Brachmann A, Blum CF, Kraege A, Goesmann A, Feldbrugge M (2021) mRNA inventory of extracellular vesicles from Ustilago maydis. J Fungi (Basel) 7

    Google Scholar 

  • Lanver D, Berndt P, Tollot M, Naik V, Vranes M, Warmann T, Münch K, Rössel N, Kahmann R (2014) Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog 10:e1004272

    Article  Google Scholar 

  • Lanver D, Tollot M, Schweizer G, Lo Presti L, Reissmann S, Schuster M, Tanaka S, Liang L, Ludwig N, Kahmann R (2017) Ustilago maydis effectors and their impact on virulence. Nat Rev Microbiol 15:409–421

    Article  CAS  Google Scholar 

  • Lanver D, Muller AN, Happel P, Schweizer G, Haas FB, Franitza M, Pellegrin C, Reissmann S, Altmuller J, Rensing SA, Kahmann R (2018) The biotrophic development of Ustilago maydis studied by RNA-Seq analysis. Plant Cell 30:300–323

    Article  CAS  Google Scholar 

  • Lefebvre F, Joly DL, Labbé C, Teichmann B, Linning R, Belzile F, Bakkeren G, Bélanger RR (2013) The transition from a phytopathogenic smut ancestor to an anamorphic biocontrol agent deciphered by comparative whole-genome analysis. Plant Cell 25:1946–1959

    Article  CAS  Google Scholar 

  • Liang L (2012) The role of Stp1, a secreted effector, in the biotrophic interaction of Ustilago maydis and its host plant maize. Dissertation 100

    Google Scholar 

  • Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, Zhang M, Gu L, Zhang B, Dou D (2014) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 5:4686

    Article  CAS  Google Scholar 

  • Lo Presti L, Zechmann B, Kumlehn J, Liang L, Lanver D, Tanaka S, Bock R, Kahmann R (2017) An assay for entry of secreted fungal effectors into plant cells. New Phytol 213:956–964

    Article  CAS  Google Scholar 

  • Lu S, Faris JD (2019) Fusarium graminearum KP4-like proteins possess root growth-inhibiting activity against wheat and potentially contribute to fungal virulence in seedling rot. Fungal Genet Biol 123:1–13

    Article  CAS  Google Scholar 

  • Ludwig N, Reissmann S, Schipper K, Gonzalez C, Assmann D, Glatter T, Moretti M, Rexer K-H, Snetselaar K, Kahmann R (2021) A cell surface-exposed protein complex with an essential virulence function in Ustilago maydis. Nat Microbiol 6:722–730

    Article  CAS  Google Scholar 

  • Ma Z, Zhu L, Song T, Wang Y, Zhang Q, Xia Y, Qiu M, Lin Y, Li H, Kong L, Fang Y, Ye W, Dong S, Zheng X, Tyler BM (2017) A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355:710–714

    Article  CAS  Google Scholar 

  • Ma L-S, Wang L, Trippel C, Mendoza-Mendoza A, Ullmann S, Moretti M, Carsten A, Kahnt J, Reissmann S, Zechmann B, Bange G, Kahmann R (2018) The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins. Nat Commun 9:1711

    Article  Google Scholar 

  • Marcon C, Altrogge L, Win YN, Stöcker T, Gardiner JM, Portwood JL II, Opitz N, Kortz A, Baldauf JA, Hunter CT, McCarty DR, Koch KE, Schoof H, Hochholdinger F (2020) BonnMu: a sequence-indexed resource of transposon-induced maize mutations for functional genomics studies. Plant Physiol 184:620–631

    Article  CAS  Google Scholar 

  • Marín-Menguiano M, Moreno-Sánchez I, Barrales RR, Fernández-Álvarez A, Ibeas JI (2019) N-glycosylation of the protein disulfide isomerase Pdi1 ensures full Ustilago maydis virulence. PLoS Pathog 15:e1007687

    Article  Google Scholar 

  • Martínez-Espinoza AD, García-Pedrajas MAD, Gold SE (2002) The Ustilaginales as plant pests and model systems. Fungal Genet Biol 35:1–20

    Article  Google Scholar 

  • Matei A, Ernst C, Gunl M, Thiele B, Altmuller J, Walbot V, Usadel B, Doehlemann G (2018) How to make a tumour: cell type specific dissection of Ustilago maydis-induced tumour development in maize leaves. New Phytol 217:1681–1695

    Article  Google Scholar 

  • Mendoza-Mendoza A, Berndt P, Djamei A, Weise C, Linne U, Marahiel MA, Vranfa M, Kämper J, Kahmann R (2009) Physical chemical plant derived signals induce differentiation in Ustilago maydis. Mol Microbiol 71:895

    Article  CAS  Google Scholar 

  • Milisavljevic M, Petkovic J, Samardzic J, Kojic M (2018) Bioavailability of nutritional resources from cells killed by oxidation supports expansion of survivors in Ustilago maydis populations. Front Microbiol 9

    Google Scholar 

  • Misas Villamil JC, Mueller AN, Demir F, Meyer U, Ökmen B, Schulze Hüynck J, Breuer M, Dauben H, Win J, Huesgen PF, Doehlemann G (2019) A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif. Nat Commun 10:1576

    Article  Google Scholar 

  • Misas-Villamil JC, Van Der Hoorn RA, Doehlemann G (2016) Papain-like cysteine proteases as hubs in plant immunity. New Phytol 212:902–907

    Article  CAS  Google Scholar 

  • Morrison EN, Emery RJN, Saville BJ (2017) Fungal derived cytokinins are necessary for normal Ustilago maydis infection of maize. Plant Pathol 66:726–742

    Article  CAS  Google Scholar 

  • Mueller O, Kahmann R, Aguilar G, Trejo-Aguilar B, Wu A, De Vries RP (2008) The secretome of the maize pathogen Ustilago maydis. Fungal Genet Biol 45:S63–S70

    Article  CAS  Google Scholar 

  • Mueller AN, Ziemann S, Treitschke S, Aßmann D, Doehlemann G (2013) Compatibility in the Ustilago maydis–maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog 9:e1003177

    Article  CAS  Google Scholar 

  • Nakano M, Ichinose Y, Mukaihara T (2020) Ralstonia solanacearum type III effector RipAC targets SGT1 to suppress effector-triggered immunity. Plant Cell Physiol 61:2067–2076

    Article  CAS  Google Scholar 

  • Navarrete F, Gallei M, Kornienko AE, Saado I, Chia K-S, Darino MA, Khan M, Bindics J, Djamei A (2021a) TOPLESS promotes plant immunity by repressing auxin signaling and is targeted by the fungal effector Naked1. Plant Commun 3(2):100269

    Article  Google Scholar 

  • Navarrete F, Grujic N, Stirnberg A, Saado I, Aleksza D, Gallei M, Adi H, Alcantara A, Khan M, Bindics J, Trujillo M, Djamei A (2021b) The Pleiades are a cluster of fungal effectors that inhibit host defenses. PLoS Pathog 17:e1009641

    Article  CAS  Google Scholar 

  • Ökmen B, Kemmerich B, Hilbig D, Wemhöner R, Aschenbroich J, Perrar A, Huesgen PF, Schipper K, Doehlemann G (2018) Dual function of a secreted fungalysin metalloprotease in Ustilago maydis. New Phytol 220:249–261

    Article  Google Scholar 

  • Ökmen B, Schwammbach D, Bakkeren G, Neumann U, Doehlemann G (2021) The Ustilago hordei-barley interaction is a versatile system for characterization of fungal effectors. J Fungi (Basel) 7

    Google Scholar 

  • Park CM, Bruenn JA, Ganesa C, Flurkey WF, Bozarth RF, Koltin Y (1994) Structure and heterologous expression of the Ustilago maydis viral toxin KP4. Mol Microbiol 11:155–164

    Article  CAS  Google Scholar 

  • Park C-M, Banerjee N, Koltin Y, Bruenn JA (1996) The Ustilago maydis virally encoded KP1 killer toxin. Mol Microbiol 20:957–963

    Article  CAS  Google Scholar 

  • Pathi KM, Rink P, Budhagatapalli N, Betz R, Saado I, Hiekel S, Becker M, Djamei A, Kumlehn J (2020) Engineering smut resistance in maize by site-directed mutagenesis of LIPOXYGENASE 3. Front Plant Sci 11:543895

    Article  Google Scholar 

  • Paulus JK, Van Der Hoorn RAL (2018) Tricked or trapped—two decoy mechanisms in host–pathogen interactions. PLoS Pathog 14:e1006761

    Article  Google Scholar 

  • Puhalla JE (1968) Compatibility reactions on solid medium and interstrain inhibition in Ustilago maydis. Genetics 60:461–474

    Article  CAS  Google Scholar 

  • Pusztahelyi T (2018) Chitin and chitin-related compounds in plant-fungal interactions. Mycology 9:189–201

    Article  CAS  Google Scholar 

  • Qi J, Wang J, Gong Z, Zhou JM (2017) Apoplastic ROS signaling in plant immunity. Curr Opin Plant Biol 38:92–100

    Article  CAS  Google Scholar 

  • Rabe F, Bosch J, Stirnberg A, Guse T, Bauer L, Seitner D, Rabanal FA, Czedik-Eysenberg A, Uhse S, Bindics J, Genenncher B, Navarrete F, Kellner R, Ekker H, Kumlehn J, Vogel JP, Gordon SP, Marcel TC, Munsterkotter M, Walter MC, Sieber CM, Mannhaupt G, Guldener U, Kahmann R, Djamei A (2016a) A complete toolset for the study of Ustilago bromivora and Brachypodium sp. as a fungal-temperate grass pathosystem. elife 5

    Google Scholar 

  • Rabe F, Seitner D, Bauer L, Navarrete F, Czedik-Eysenberg A, Rabanal FA, Djamei A (2016b) Phytohormone sensing in the biotrophic fungus Ustilago maydis - the dual role of the transcription factor Rss1. Mol Microbiol 102:290–305

    Article  CAS  Google Scholar 

  • Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10:417–430

    Article  CAS  Google Scholar 

  • Redkar A, Hoser R, Schilling L, Zechmann B, Krzymowska M, Walbot V, Doehlemann G (2015) A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell 27:1332–1351

    Article  CAS  Google Scholar 

  • Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355

    Article  CAS  Google Scholar 

  • Reyes-Fernández EZ, Shi Y-M, Grün P, Bode HB, Bölker M, Druzhinina IS (2021) An unconventional melanin biosynthesis pathway in Ustilago maydis. Appl Environ Microbiol 87:e01510–e01520

    Article  Google Scholar 

  • Saado I, Chia K-S, Betz R, Alcântara A, Pettkó-Szandtner A, Navarrete F, D’Auria JC, Kolomiets MV, Melzer M, Feussner I, Djamei A (2022) Effector-mediated relocalization of a maize lipoxygenase protein triggers susceptibility to Ustilago maydis. Plant Cell 34(7):2785–2805

    Article  Google Scholar 

  • Sánchez-Vallet A, Fouché S, Fudal I, Hartmann FE, Soyer JL, Tellier A, Croll D (2018) The genome biology of effector gene evolution in filamentous plant pathogens. Annu Rev Phytopathol 56:21–40

    Article  Google Scholar 

  • Sánchez-Vallet A, Tian H, Rodriguez-Moreno L, Valkenburg D-J, Saleem-Batcha R, Wawra S, Kombrink A, Verhage L, De Jonge R, Van Esse HP, Zuccaro A, Croll D, Mesters JR, Thomma BPHJ (2020) A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization. PLoS Pathog 16:e1008652

    Article  Google Scholar 

  • Schilling L, Matei A, Redkar A, Walbot V, Doehlemann G (2014) Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol Plant Pathol 15:780–789

    Article  CAS  Google Scholar 

  • Schirawski J, Böhnert HU, Steinberg G, Snetselaar K, Adamikowa L, Kahmann R (2005) Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis [W]. Plant Cell 17:3532–3543

    Article  CAS  Google Scholar 

  • Schurack S, Depotter JRL, Gupta D, Thines M, Doehlemann G (2021) Comparative transcriptome profiling identifies maize line specificity of fungal effectors in the maize-Ustilago maydis interaction. Plant J 106:733–752

    Article  CAS  Google Scholar 

  • Schuster M, Schweizer G, Kahmann R (2018a) Comparative analyses of secreted proteins in plant pathogenic smut fungi and related basidiomycetes. Fungal Genet Biol 112:21–30

    Article  CAS  Google Scholar 

  • Schuster M, Trippel C, Happel P, Lanver D, Reissmann S, Kahmann R (2018b) Single and multiplexed gene editing in Ustilago maydis using CRISPR-Cas9. Bio Protoc 8:e2928

    Article  CAS  Google Scholar 

  • Schweizer G, Haider MB, Barroso GV, Rössel N, Münch K, Kahmann R, Dutheil JY (2021) Population genomics of the maize pathogen Ustilago maydis: demographic history and role of virulence clusters in adaptation. Genome Biol Evol 13

    Google Scholar 

  • Seitner D, Uhse S, Gallei M, Djamei A (2018) The core effector Cce1 is required for early infection of maize by Ustilago maydis. Mol Plant Pathol 19:2277–2287

    Article  CAS  Google Scholar 

  • Seong K, Krasileva KV (2022) Comparative computational structural genomics highlights divergent evolution of fungal effectors. bioRxiv. https://doi.org/10.1101/2022.05.02.490317

  • Sharma R, Mishra B, Runge F, Thines M (2014) Gene loss rather than gene gain is associated with a host jump from monocots to dicots in the smut fungus Melanopsichium pennsylvanicum. Genome Biol Evol 6:2034–2049

    Article  CAS  Google Scholar 

  • Sharma R, Ökmen B, Doehlemann G, Thines M (2019) Saprotrophic yeasts formerly classified as Pseudozyma have retained a large effector arsenal, including functional Pep1 orthologs. Mycol Prog 18:763–768

    Article  Google Scholar 

  • Skibbe DS, Doehlemann G, Fernandes J, Walbot V (2010) Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89–92

    Article  CAS  Google Scholar 

  • Snelders NC, Rovenich H, Petti GC, Rocafort M, Van Den Berg GCM, Vorholt JA, Mesters JR, Seidl MF, Nijland R, Thomma BPHJ (2020) Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nat Plants 6:1365–1374

    Article  CAS  Google Scholar 

  • Sperschneider J, Dodds PN (2022) EffectorP 3.0: prediction of apoplastic and cytoplasmic effectors in fungi and oomycetes. Mol Plant-Microbe Interact 35:146–156

    Article  CAS  Google Scholar 

  • Steinlauf R, Peery T, Koltin Y, Bruenn J (1988) The Ustilago maydis virus-encoded toxin—effect of KP6 on sensitive cells and spheroplasts. Exp Mycol 12:264–274

    Article  CAS  Google Scholar 

  • Stergiopoulos I, Wit PJGMD (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263

    Article  CAS  Google Scholar 

  • Stirnberg A, Djamei A (2016) Characterization of ApB73, a virulence factor important for colonization of Zea mays by the smut Ustilago maydis. Mol Plant Pathol 17:1467–1479

    Article  CAS  Google Scholar 

  • Storfie ERM, Saville BJ (2021) Fungal pathogen emergence: investigations with an Ustilago maydis × Sporisorium reilianum hybrid. J Fungi 7:672

    Article  CAS  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    Article  CAS  Google Scholar 

  • Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J, Vermerris W, Koenig S, Feussner K, Feussner I, Kahmann R (2014) A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. elife 3:e01355

    Article  Google Scholar 

  • Tanaka S, Schweizer G, Rössel N, Fukada F, Thines M, Kahmann R (2019) Neofunctionalization of the secreted Tin2 effector in the fungal pathogen Ustilago maydis. Nat Microbiol 4:251–257

    Article  CAS  Google Scholar 

  • Tanaka S, Gollin I, Rössel N, Kahmann R (2020) The functionally conserved effector Sta1 is a fungal cell wall protein required for virulence in Ustilago maydis. New Phytol 227:185–199

    Article  CAS  Google Scholar 

  • Taniguti LM, Schaker PD, Benevenuto J, Peters LP, Carvalho G, Palhares A, Quecine MC, Nunes FR, Kmit MC, Wai A, Hausner G, Aitken KS, Berkman PJ, Fraser JA, Moolhuijzen PM, Coutinho LL, Creste S, Vieira ML, Kitajima JP, Monteiro-Vitorello CB (2015) Complete genome sequence of Sporisorium scitamineum and biotrophic interaction transcriptome with sugarcane. PLoS One 10:e0129318

    Article  Google Scholar 

  • Tao J, Ginsberg I, Banerjee N, Held W, Koltin Y, Bruenn JA (1990) Ustilago maydis KP6 killer toxin: structure, expression in Saccharomyces cerevisiae, and relationship to other cellular toxins. Mol Cell Biol 10:1373–1381

    CAS  Google Scholar 

  • Teichmann B, Linne U, Hewald S, Marahiel MA, Bölker M (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66:525–533

    Article  CAS  Google Scholar 

  • Teichmann B, Liu L, Schink KO, Bölker M (2010) Activation of the Ustilagic acid biosynthesis gene cluster in Ustilago maydis by the C2H2 zinc finger transcription factor Rua1. Appl Environ Microbiol 76:2633–2640

    Article  CAS  Google Scholar 

  • Thines M (2019) An evolutionary framework for host shifts – jumping ships for survival. New Phytol 224:605–617

    Article  Google Scholar 

  • Thomas P (1989) Barley smuts in the prairie provinces of Canada, 1983-88. Can J Plant Pathol 11:133–136

    Article  Google Scholar 

  • Tollot M, Assmann D, Becker C, Altmüller J, Dutheil JY, Wegner C-E, Kahmann R (2016) The WOPR protein Ros1 is a master regulator of Sporogenesis and late effector gene expression in the maize pathogen Ustilago maydis. PLoS Pathog 12:e1005697

    Article  Google Scholar 

  • Trione E (1982) Dwarf bunt of wheat and its importance in international wheat trade [Tilletia controversa, history, epidemiology, United States, China]. Plant Dis 66:1083–1088

    Article  Google Scholar 

  • Uhse S, Djamei A (2018) Effectors of plant-colonizing fungi and beyond. PLoS Pathog 14:e1006992

    Article  Google Scholar 

  • Uhse S, Pflug FG, Stirnberg A, Ehrlinger K, Von Haeseler A, Djamei A (2018) In vivo insertion pool sequencing identifies virulence factors in a complex fungal-host interaction. PLoS Biol 16:e2005129

    Article  Google Scholar 

  • Valverde ME, Paredes-López O, Pataky JK, Guevara-Lara F, Pineda T (1995) Huitlacoche (Ustilago maydis) as a food source—biology, composition, and production. Crit Rev Food Sci Nutr 35:191–229

    Article  CAS  Google Scholar 

  • Van Der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    Article  Google Scholar 

  • Van Der Linde K, Mueller AN, Hemetsberger C, Kashani F, Van Der Hoorn RA, Doehlemann G (2012) The maize cystatin CC9 interacts with apoplastic cysteine proteases. Plant Signal Behav 7:1397–1401

    Article  Google Scholar 

  • Van Der Linde K, Timofejeva L, Egger RL, Ilau B, Hammond R, Teng C, Meyers BC, Doehlemann G, Walbot V (2018) Pathogen Trojan horse delivers bioactive host protein to Alter maize anther cell behavior in situ. Plant Cell 30:528–542

    Article  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  Google Scholar 

  • Wagner-Vogel G, Lämmer F, Kämper J, Basse CW (2015) Uniparental mitochondrial DNA inheritance is not affected in Ustilago maydis Δatg11 mutants blocked in mitophagy. BMC Microbiol 15:23

    Article  Google Scholar 

  • Wu JQ, Song L, Ding Y, Dong C, Hasan M, Park RF (2021) A chromosome-scale assembly of the wheat leaf rust pathogen Puccinia triticina provides insights into structural variations and genetic relationships with haplotype resolution. Front Microbiol 12:704253

    Article  Google Scholar 

  • Yu G, Xian L, Xue H, Yu W, Rufian JS, Sang Y, Morcillo RJL, Wang Y, Macho AP (2020) A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity. PLoS Pathog 16:e1008933

    Article  CAS  Google Scholar 

  • Zahiri A, Heimel K, Wahl R, Rath M, Kämper J (2010) The Ustilago maydis Forkhead transcription factor Fox1 is involved in the regulation of genes required for the attenuation of plant defenses during pathogenic development. Mol Plant Microbe Interact 23:1118–1129

    Article  CAS  Google Scholar 

  • Zheng Y, Kief J, Auffarth K, Farfsing JW, Mahlert M, Nieto F, Basse CW (2008) The Ustilago maydis Cys2His2-type zinc finger transcription factor Mzr1 regulates fungal gene expression during the biotrophic growth stage. Mol Microbiol 68:1450–1470

    Article  CAS  Google Scholar 

  • Zhou JM, Zhang Y (2020) Plant immunity: danger perception and signaling. Cell 181:978–989

    Article  CAS  Google Scholar 

  • Zuo W, Ökmen B, Depotter JRL, Ebert MK, Redkar A, Villamil JM, Doehlemann G (2019) Molecular interactions between smut fungi and their host plants. Annu Rev Phytopathol 57:411–430

    Article  CAS  Google Scholar 

  • Zuo W, Depotter JR, Doehlemann G (2020) Cas9HF1 enhanced specificity in Ustilago maydis. Fungal Biol 124:228–234

    Article  CAS  Google Scholar 

  • Zuo W, Depotter JR, Gupta DK, Thines M, Doehlemann G (2021) Cross-species analysis between the maize smut fungi Ustilago maydis and Sporisorium reilianum highlights the role of transcriptional change of effector orthologs for virulence and disease. New Phytol

    Google Scholar 

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Authors and Affiliations

  1. Department of Plant Pathology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany

    Armin Djamei, Maxim Prokchorchik & Natalia De Sousa Teixeira E. Silva

  2. Institute for Plant Sciences and Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne, Germany

    Jasper Depotter, Georgios Saridis, Sina Barghahn, Weiliang Zuo, Johana Misas Villamil & Gunther Doehlemann

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  1. Armin Djamei
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  4. Maxim Prokchorchik
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Correspondence to Armin Djamei or Gunther Doehlemann .

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  1. School of Natural Sciences, Massey University, Palmerston North, New Zealand

    Barry Scott

  2. School of Agriculture and Environment, Massey University, Palmerston North, New Zealand

    Carl Mesarich

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Djamei, A. et al. (2023). Modulation of Host Immunity and Development by Ustilago maydis. In: Scott, B., Mesarich, C. (eds) Plant Relationships. The Mycota, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-031-16503-0_1

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