1887

Abstract

is an obligate biotrophic parasite of the wildflower species . This dikaryotic fungus, commonly known as an anther smut, requires that haploid, yeast-like sporidia of opposite mating types fuse and differentiate into dikaryotic hyphae that penetrate host tissue as part of the fungal life cycle. Mating occurs under conditions of cool temperatures and limited nutrients. Further development requires host cues or chemical mimics, including a variety of lipids, e.g. phytols. To identify global changes in transcription associated with developmental shifts, RNA-Seq was conducted at several stages of fungal propagation, i.e. haploid cells grown independently on rich and nutrient-limited media, mated cells on nutrient-limited media as well as a time course of such mated cells exposed to phytol. Comparison of haploid cells grown under rich and nutrient-limited conditions identified classes of genes probably associated with general nutrient availability, including components of the RNAi machinery. Some gene enrichment patterns comparing the nutrient-limited and mated transcriptomes suggested gene expression changes associated with the mating programme (e.g. homeodomain binding proteins, secreted proteins, proteins unique to ¸ multicopper oxidases and RhoGEFs). Analysis for phytol treatment compared with mated cells alone allowed identification of genes likely to be involved in the dikaryotic switch (e.g. oligopeptide transporters). Gene categories of particular note in all three conditions included those in the major facilitator superfamily, proteins containing PFAM domains of the secretory lipase family as well as proteins predicted to be secreted, many of which have the hallmarks of fungal effectors with potential roles in pathogenicity.

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2017-03-01
2021-10-18
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References

  1. Refrégier G, Le Gac M, Jabbour F, Widmer A, Shykoff JA et al. Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation. BMC Evol Biol 2008; 8:100 [View Article][PubMed]
    [Google Scholar]
  2. Hood ME, Antonovics J. Two-celled promycelia and mating-type segregation in Ustilago violacea (Microbotryum violaceum). Int J Plant Sci 1998; 159:199–205 [View Article]
    [Google Scholar]
  3. Badouin H, Hood ME, Gouzy J, Aguileta G, Siguenza S et al. Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus Microbotryum lychnidis-dioicae. Genetics 2015; 200:1275–1284 [View Article][PubMed]
    [Google Scholar]
  4. Perlin MH, Amselem J, Fontanillas E, Toh SS, Chen Z et al. Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus. BMC Genomics 2015; 16:461 [View Article][PubMed]
    [Google Scholar]
  5. Fontanillas E, Hood ME, Badouin H, Petit E, Barbe V et al. Degeneration of the nonrecombining regions in the mating-type chromosomes of the anther-smut fungi. Mol Biol Evol 2015; 32:928–943 [View Article][PubMed]
    [Google Scholar]
  6. Hood ME, Antonovics J, Koskella B. Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms. Genetics 2004; 168:141–146 [View Article][PubMed]
    [Google Scholar]
  7. Billiard S, López-Villavicencio M, Devier B, Hood ME, Fairhead C et al. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev Camb Philos Soc 2011; 86:421–442 [View Article][PubMed]
    [Google Scholar]
  8. Day AW. Communication through fimbriae during conjugation in a fungus. Nature 1976; 262:583–584 [View Article][PubMed]
    [Google Scholar]
  9. Xu L, Petit E, Hood ME. Variation in mate-recognition pheromones of the fungal genus Microbotryum. Heredity 2016; 116:44–51 [View Article][PubMed]
    [Google Scholar]
  10. Wilch G, Ward S, Castle A. Transmission of mitochondrial DNA in Ustilago violacea. Curr Genet 1992; 22:135–140 [View Article][PubMed]
    [Google Scholar]
  11. Gauthier GM. Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog 2015; 11:e1004608 [View Article][PubMed]
    [Google Scholar]
  12. Lengeler KB, Davidson RC, D'Souza C, Harashima T, Shen W-C et al. Signal transduction cascades regulating fungal development and virulence. Microbiol Biol Rev 2000; 64:746–785 [View Article]
    [Google Scholar]
  13. Sánchez-Martínez C, Pérez-Martín J. Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis – similar inputs, different outputs. Curr Opin Microbiol 2001; 4:214–221 [View Article][PubMed]
    [Google Scholar]
  14. Martínez-Soto D, Ruiz-Herrera J. Transcriptomic analysis of the dimorphic transition of Ustilago maydis induced in vitro by a change in pH. Fungal Genet Biol 2013; 58–59:116–125 [View Article][PubMed]
    [Google Scholar]
  15. Paul JA, Barati MT, Cooper M, Perlin MH. Physical and genetic interaction between ammonium transporters and the signaling protein Rho1 in the plant pathogen Ustilago maydis. Eukaryot Cell 2014; 13:1328–1336 [View Article][PubMed]
    [Google Scholar]
  16. Smith DG, Garcia-Pedrajas MD, Gold SE, Perlin MH. Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Mol Microbiol 2003; 50:259–275 [View Article][PubMed]
    [Google Scholar]
  17. Castle AJ. Isolation and identification of α-tocopherol as an inducer of the parasitic phase of Ustilago violacea. Phytopathology 1984; 74:1194–1200 [View Article]
    [Google Scholar]
  18. Antonovics J, Hood M, Partain J. The ecology and genetics of a host shift: microbotryum as a model system. Am Nat 2002; 160:S40–S53 [View Article][PubMed]
    [Google Scholar]
  19. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA et al. Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 2010; 7:709–715 [View Article][PubMed]
    [Google Scholar]
  20. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L et al. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 2009; 37:e123 [View Article][PubMed]
    [Google Scholar]
  21. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644–652 [View Article][PubMed]
    [Google Scholar]
  22. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 2013; 8:1494–1512 [View Article][PubMed]
    [Google Scholar]
  23. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25 [View Article][PubMed]
    [Google Scholar]
  24. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011; 12:323 [View Article][PubMed]
    [Google Scholar]
  25. Kadota K, Nishiyama T, Shimizu K. A normalization strategy for comparing tag count data. Algorithms Mol Biol 2012; 7:5 [View Article][PubMed]
    [Google Scholar]
  26. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article][PubMed]
    [Google Scholar]
  27. Oliveros JC. VENNY. An Interactive Tool for Comparing Lists with Venn's Diagrams, 2.0 ed. 2007–2015
    [Google Scholar]
  28. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34:267–273 [View Article][PubMed]
    [Google Scholar]
  29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102:15545–15550 [View Article][PubMed]
    [Google Scholar]
  30. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005; 21:3674–3676 [View Article][PubMed]
    [Google Scholar]
  31. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016; 44:D457–D462 [View Article][PubMed]
    [Google Scholar]
  32. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P et al. GenePattern 2.0. Nat Genet 2006; 38:500–501 [View Article][PubMed]
    [Google Scholar]
  33. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article][PubMed]
    [Google Scholar]
  34. Kurzynska-Kokorniak A, Koralewska N, Pokornowska M, Urbanowicz A, Tworak A et al. The many faces of Dicer: the complexity of the mechanisms regulating Dicer gene expression and enzyme activities. Nucleic Acids Res 2015; 43:4365–4380 [View Article][PubMed]
    [Google Scholar]
  35. Potenza N, Papa U, Russo A. Differential expression of Dicer and Argonaute genes during the differentiation of human neuroblastoma cells. Cell Biol Int 2009; 33:734–738 [View Article][PubMed]
    [Google Scholar]
  36. Lau SK, Chow WN, Wong AY, Yeung JM, Bao J et al. Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLoS Negl Trop Dis 2013; 7:e2398 [View Article][PubMed]
    [Google Scholar]
  37. Kim HK, Jo SM, Kim GY, Kim DW, Kim YK et al. A large-scale functional analysis of putative target genes of mating-type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum. PLoS Genet 2015; 11:e1005486 [View Article][PubMed]
    [Google Scholar]
  38. Dunkel N, Hertlein T, Franz R, Reuß O, Sasse C et al. Roles of different peptide transporters in nutrient acquisition in Candida albicans. Eukaryot Cell 2013; 12:520–528 [View Article][PubMed]
    [Google Scholar]
  39. Toh SS, Perlin MH. Size does matter: staging of Silene latifolia floral buds for transcriptome studies. Int J Mol Sci 2015; 16:22027–22045 [View Article][PubMed]
    [Google Scholar]
  40. Kües U, Rühl M. Multiple multi-copper oxidase gene families in basidiomycetes—what for?. Curr Genomics 2011; 12:72–94 [View Article][PubMed]
    [Google Scholar]
  41. Jones SK Jr, Bennett RJ. Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 2011; 48:668–676 [View Article][PubMed]
    [Google Scholar]
  42. Rutherford JC, Lin X, Nielsen K, Heitman J. Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcus neoformans. Eukaryot Cell 2008; 7:237–246 [View Article][PubMed]
    [Google Scholar]
  43. Petit E, Giraud T, De Vienne DM, Coelho MA, Aguileta G et al. Linkage to the mating-type locus across the genus Microbotryum: insights into nonrecombining chromosomes. Evolution 2012; 66:3519–3533 [View Article][PubMed]
    [Google Scholar]
  44. Feldbrügge M, Kämper J, Steinberg G, Kahmann R. Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 2004; 7:666–672 [View Article][PubMed]
    [Google Scholar]
  45. Bakkeren G, Kämper J, Schirawski J. Sex in smut fungi: structure, function and evolution of mating-type complexes. Fungal Genet Biol 2008; 45:S15–S21 [View Article][PubMed]
    [Google Scholar]
  46. Heimel K, Scherer M, Schuler D, Kämper J. The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 2010; 22:2908–2922 [View Article][PubMed]
    [Google Scholar]
  47. Pöggeler S, Nowrousian M, Ringelberg C, Loros JJ, Dunlap JC et al. Microarray and real-time PCR analyses reveal mating type-dependent gene expression in a homothallic fungus. Mol Genet Genomics 2006; 275:492–503 [View Article][PubMed]
    [Google Scholar]
  48. Becker K, Beer C, Freitag M, Kück U. Genome-wide identification of target genes of a mating-type α-domain transcription factor reveals functions beyond sexual development. Mol Microbiol 2015; 96:1002–1022 [View Article]
    [Google Scholar]
  49. Ait Benkhali J, Coppin E, Brun S, Peraza-Reyes L, Martin T et al. A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina. PLoS Genet 2013; 9:e1003642 [View Article][PubMed]
    [Google Scholar]
  50. Jewell JB, Browse J. Epidermal jasmonate perception is sufficient for all aspects of jasmonate-mediated male fertility in Arabidopsis. Plant J 2016; 85:634–647 [View Article][PubMed]
    [Google Scholar]
  51. Yuan Z, Zhang D. Roles of jasmonate signalling in plant inflorescence and flower development. Curr Opin Plant Biol 2015; 27:44–51 [View Article][PubMed]
    [Google Scholar]
  52. Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G et al. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol Ecol 2014; 23:753–773 [View Article][PubMed]
    [Google Scholar]
  53. Klose J, De Sá MM, Kronstad JW. Lipid-induced filamentous growth in Ustilago maydis. Mol Microbiol 2004; 52:823–835 [View Article][PubMed]
    [Google Scholar]
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