Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements

Plant Cell

Volumn 24, Issue 5, 2012, Pages 1733-1745

  Laurie, John D ^b,f   Ali, Shawkat ^a,g   Linning, Rob ^a   Mannhaupt, Gertrud ^b,c   Wong, Philip ^b   Güldener, Ulrich ^b   Münsterkötter, Martin ^a   Moore, Richard ^a,d   Kahmann, Regine ^c   Bakkeren, Guus ^a,f   Schirawski, Jan ^c,e  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^d CANADA'S MICHAEL SMITH GENOME SCIENCES CENTRE   (Canada)

^e RWTH AACHEN UNIVERSITY   (Germany)

^f UNIVERSITY OF ARIZONA   (United States)

^g UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; HORDEUM; HORDEUM VULGARE; SPORISORIUM REILIANUM; USTILAGO HORDEI; USTILAGO MAYDIS; ZEA MAYS;

EID: 84863095607     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.097261     Document Type: Article

References (70)

1. Abrusán, G., Grundmann, N., DeMester, L., and Makalowski, W. (2009). TEclass-A tool for automated classification of unknown eukaryotic transposable elements. Bioinformatics 25: 1329-1330.
2. Aguileta, G., Marthey, S., Chiapello, H., Lebrun, M.H., Rodolphe, F., Fournier, E., Gendrault-Jacquemard, A., and Giraud, T. (2008). Assessing the performance of single-copy genes for recovering robust phylogenies. Syst. Biol. 57: 613-627.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
4. Bakkeren, G. et al. (2006). Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet. Biol. 43: 655-666.
5. Bakkeren, G., Kämper, J., and Schirawski, J. (2008). Sex in smut fungi: Structure, function and evolution of mating-type complexes. Fungal Genet. Biol. 45 (suppl. 1): S15-S21.
6. Bakkeren, G., and Kronstad, J.W. (1994). Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc. Natl. Acad. Sci. USA 91: 7085-7089.
7. Basse, C.W., Kolb, S., and Kahmann, R. (2002). A maize-specifically expressed gene cluster in Ustilago maydis. Mol. Microbiol. 43: 75-93.
8. Baumgarten, A.M., Suresh, J., May, G., and Phillips, R.L. (2007). Mapping QTLs contributing to Ustilago maydis resistance in specific plant tissues of maize. Theor. Appl. Genet. 114: 1229-1238.
9. Baxter, L. et al. (2010). Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
10. Benson, G. (1999). Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Res. 27: 573-580.
11. Besemer, J., and Borodovsky, M. (2005). GeneMark: Web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res. 33(Web Server issue): W451-W454.
12. Blumenstiel, J.P. (2011). Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet. 27: 23-31.
13. Bölker, M., Urban, M., and Kahmann, R. (1992). The a mating type locus of U. maydis specifies cell signaling components. Cell 68: 441-450.
14. Cantu, D., Govindarajulu, M., Kozik, A., Wang, M., Chen, X., Kojima, K.K., Jurka, J., Michelmore, R.W., and Dubcovsky, J. (2011). Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS ONE 6: e24230.
15. Cerutti, H., and Casas-Mollano, J.A. (2006). On the origin and functions of RNA-mediated silencing: From protists to man. Curr. Genet. 50: 81-99.
16. Chen, E.S., Zhang, K., Nicolas, E., Cam, H.P., Zofall, M., and Grewal, S.I. (2008). Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451: 734-737.
17. Clutterbuck, A.J. (2011). Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet. Biol. 48: 306-326.
18. Dean, R.A. et al. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
19. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog. 5: e1000290.
20. Drinnenberg, I.A., Fink, G.R., and Bartel, D.P. (2011). Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333: 1592.
21. Drinnenberg, I.A., Weinberg, D.E., Xie, K.T., Mower, J.P., Wolfe, K. H., Fink, G.R., and Bartel, D.P. (2009). RNAi in budding yeast. Science 326: 544-550.
22. D'Souza, C.A. et al. (2011). Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. MBio. 2: e00342-e00410.
23. Duplessis, S. et al. (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl. Acad. Sci. USA 108: 9166-9171.
24. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2: 953-971.
25. Fischer, T., Cui, B., Dhakshnamoorthy, J., Zhou, M., Rubin, C., Zofall, M., Veenstra, T.D., and Grewal, S.I.S. (2009). Diverse roles of HP1 proteins in heterochromatin assembly and functions in fission yeast. Proc. Natl. Acad. Sci. USA 106: 8998-9003.
26. Freitag, M., Williams, R.L., Kothe, G.O., and Selker, E.U. (2002). A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc. Natl. Acad. Sci. USA 99: 8802-8807.
27. Galagan, J.E., and Selker, E.U. (2004). RIP: The evolutionary cost of genome defense. Trends Genet. 20: 417-423.
28. Gaudet, D.A., Wang, Y., Penniket, C., Lu, Z.X., Bakkeren, G., and Laroche, A. (2010). Morphological and molecular analyses of host and nonhost interactions involving barley and wheat and the covered smut pathogen Ustilago hordei. Mol. Plant Microbe Interact. 23: 1619-1634.
29. Grewal, T.S., Rossnagel, B.G., Bakkeren, G., and Scoles, G.J. (2008). Identification of resistance genes to barley covered smut and mapping of the Ruh1 gene using Ustilago hordei strains with defined avirulence genes. Can. J. Plant Pathol. 30: 277-284.
30. Haas, B.J. et al. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
31. Holloman, W.K., Schirawski, J., and Holliday, R. (2008). The homologous recombination system of Ustilago maydis. Fungal Genet. Biol. 45 (suppl. 1): S31-S39.
32. Hood, M.E., Katawczik, M., and Giraud, T. (2005). Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170: 1081-1089.
33. Horns, F., Petit, E., Yockteng, R., and Hood, M.E. (2012). Patterns of repeat-induced point mutation in transposable elements of basidiomycete fungi. Genome Biol. Evol. 4: 240-247.
34. Hu, G.G., Linning, R., and Bakkeren, G. (2002). Sporidial mating and infection process of the smut fungus, Ustilago hordei, in susceptible barley. Can. J. Bot. 80: 1103-1114.
35. Huang, X., and Madan, A. (1999). CAP3: A DNA sequence assembly program. Genome Res. 9: 868-877.
36. Janbon, G., Maeng, S., Yang, D.-H., Ko, Y.-J., Jung, K.-W., Moyrand, F., Floyd, A., Heitman, J., and Bahn, Y.-S. (2010). Characterizing the role of RNA silencing components in Cryptococcus neoformans. Fungal Genet. Biol. 47: 1070-1080.
37. Kämper, J. et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
38. Kämper, J., Reichmann, M., Romeis, T., Bölker, M., and Kahmann, R. (1995). Multiallelic recognition: Nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81: 73-83.
39. Kloc, A., and Martienssen, R. (2008). RNAi, heterochromatin and the cell cycle. Trends Genet. 24: 511-517.
40. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567-580.
41. Lauc, G., Ilic, I., and Heffer-Lauc, M. (1992). Entropies of coding and noncoding sequences of DNA and proteins. Biophys. Chem. 42: 7-11.
42. Laurie, J.D., Linning, R., and Bakkeren, G. (2008). Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr. Genet. 53: 49-58.
43. Lee, N., Bakkeren, G., Wong, K., Sherwood, J.E., and Kronstad, J.W. (1999). The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc. Natl. Acad. Sci. USA 96: 15026-15031.
44. Linning, R., Lin, D., Lee, N., Abdennadher, M., Gaudet, D., Thomas, P., Mills, D., Kronstad, J.W., and Bakkeren, G. (2004). Markerbased cloning of the region containing the UhAvr1 avirulence gene from the basidiomycete barley pathogen Ustilago hordei. Genetics 166: 99-111.
45. Lowe, T.M., and Eddy, S.R. (1997). tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
46. Lubberstedt, T., Klein, D., and Melchinger, A.E. (1998). Comparative QTL mapping of resistance to Ustilago maydis across four populations of European flint-maize. Theor. Appl. Genet. 97: 1321-1330.
47. Lubberstedt, T., Xia, X.C., Tan, G., Liu, X., and Melchinger, A.E. (1999). QTL mapping of resistance to Sporisorium reiliana in maize. Theor. Appl. Genet. 99: 593-598.
48. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., and de Vries, R.P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol. 45 (suppl. 1): S63-S70.
49. Nakayashiki, H., Kadotani, N., and Mayama, S. (2006). Evolution and diversification of RNA silencing proteins in fungi. J. Mol. Evol. 63: 127-135.
50. Parra, G., Bradnam, K., Ning, Z., Keane, T., and Korf, I. (2009). Assessing the gene space in draft genomes. Nucleic Acids Res. 37: 289-297.
51. Pearson, W.R., Wood, T., Zhang, Z., and Miller, W. (1997). Comparison of DNA sequences with protein sequences. Genomics 46: 24-36.
52. Raffaele, S. et al. (2010). Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540-1543.
53. Rattei, T., Tischler, P., Götz, S., Jehl, M.A., Hoser, J., Arnold, R., Conesa, A., and Mewes, H.W. (2010). SIMAP-A comprehensive database of pre-calculated protein sequence similarities, domains, annotations and clusters. Nucleic Acids Res. 38(Database issue): D223-D226.
54. Schirawski, J., Heinze, B., Wagenknecht, M., and Kahmann, R. (2005). Mating type loci of Sporisorium reilianum: Novel pattern with three a and multiple b specificities. Eukaryot. Cell 4: 1317-1327.
55. Schirawski, J. et al. (2010). Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330: 1546-1548.
56. Selker, E.U., and Stevens, J.N. (1985). DNA methylation at asymmetric sites is associated with numerous transitionmutations. Proc. Natl. Acad. Sci. USA 82: 8114-8118.
57. Shabalina, S.A., and Koonin, E.V. (2008). Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. (Amst.) 23: 578-587.
58. Slotkin, R.K., and Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8: 272-285.
59. Smith, E., and Shilatifard, A. (2007). The A, B, Gs of silencing. Genes Dev. 21: 1141-1144.
60. Spanu, P.D. et al. (2010). Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
61. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
62. Ter-Hovhannisyan, V., Lomsadze, A., Chernoff, Y.O., and Borodovsky, M. (2008). Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18: 1979-1990.
63. Wang, X., Hsueh, Y.-P., Li, W., Floyd, A., Skalsky, R., and Heitman, J. (2010). Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev. 24: 2566-2582.
64. Wicker, T., Schlagenhauf, E., Graner, A., Close, T.J., Keller, B., and Stein, N. (2006). 454 sequencing put to the test using the complex genome of barley. BMC Genomics 7: 275.
65. Woodhouse, M.R., Schnable, J.C., Pedersen, B.S., Lyons, E., Lisch, D., Subramaniam, S., and Freeling, M. (2010). Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol. 8: e1000409.
66. Wootton, J.C., and Federhen, S. (1993). Statistics of local complexity in amino acid sequences and sequence databases. Comput. Chem. 17: 149-163.
67. Xu, J. et al. (2007). Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc. Natl. Acad. Sci. USA 104: 18730-18735.
68. Zemach, A., McDaniel, I.E., Silva, P., and Zilberman, D. (2010). Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919.
69. Zofall, M., and Grewal, S.I. (2006). Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol. Cell 22: 681-692.
70. Zuckerkandl, E., and Pauling, L. (1965). Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins, V. Bryson and H.J. Vogel, eds (New York: Academic Press), pp. 97-166.