Dokument

Summary:
The genome of the fungal wheat pathogen Zymoseptoria tritici consists of thirteen essential chromosomes and several so-called dispensable chromosomes. These dispensable chromosomes encode only 6% of the protein coding genes of Z. tritici. To date no genes involved in pathogenicity are described on the dispensable chromosomes which can be lost after meiosis or mitotic cell division without any apparent effect on fitness. To investigate the underlying molecular basis of instability of the dispensable chromosomes, the epigenetic components of both the essential and dispensable chromosomes were characterized here. Chromatin immunoprecipitation and sequencing of DNA associated with the centromere specific histone (CenH3) was conducted to identify the centromeres of Z. tritici. It was shown that the centromeres of Z. tritici are small, sequence independent and lack any conserved motif. The centromeres are AT-rich, but not located in the most abundant AT-rich region of the chromosomes, and the centromeric organization is similar for both essential and dispensable chromosomes. To study centromere dynamic, parental and progeny strains derived from a meiotic cross were included in the study. The centromeres of these strains were shown to be conserved among Z. tritici strains. The deletion of the centromere of the dispensable chromosome 14 resulted in several strains were chromosome 14 was completely lost, while only a single strain was identified with a neocentromere on chromosome 14. The chromatin content of both types of chromosomes was also investigated. Three histone modifications specific for either euchromatin or heterochromatin were characterized. The essential chromosomes are enriched with euchromatin while the dispensable chromosomes are mainly heterochromatic. Several repeat rich regions with low gene density were also enriched with heterochromatin on the essential chromosomes. One particularly large region of 780 kb of the essential chromosome 7 was in addition found to be enriched with facultative heterochromatin. Genes in this region are silenced both during axenic and infectious growth. Based on the obtained results, it can be concluded that the difference between the essential and dispensable chromosomes cannot be associated with the centromeres. However, differences in the chromatin states is a main difference between the two types of chromosomes. To investigate the hemibiotrophic lifestyle switch in Z. tritici the epigenetic component of infectious growth was studied with a focus on RNA interference (RNAi). Five mutant strains of several proteins involved in the RNAi pathway were created. It could be demonstrated that Dicer and Argonaute genes play a role during the formation of asexual fruiting bodies called pycnidia. In contrast to the Dicer gene, the Argonaute genes show an unusual degree of sequence variation among Z. tritici strains. Collectively, the work presented here underlines the importance of epigenetics in both genome stability as well as pathogenicity in the fungal pathogen Z. tritici.

Bibliographie / References

1. Galagan, J.E., Calvo, S.E., Borkovich, K. a, Selker, E.U., Read, N.D., Jaffe, D., FitzHugh, W., Ma, L.-J., Smirnov, S., Purcell, S., et al. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859–868.
2. Cumberledge, S., and Carbon, J. (1987). Saccharomyces cerevisiae. Genetics 117, 203–212.
3. Adams, M.D. (2000). The Genome Sequence of Drosophila melanogaster. Science. 287, 2185– 2195.
4. Westwood, J.H., Roney, J.K., Khatibi, P.A., and Stromberg, V.K. (2009). RNA translocation between parasitic plants and their hosts. Pest Manag. Sci. 65, 533–539.
5. Gu, W., Claycomb, J.M., Batista, P.J., Mello, C.C., and Conte, D. (2011). Cloning Argonaute- Associated Small RNAs from Caenorhabditis elegans. In Argonaute Proteins: Methods and Protocols, T.C. Hobman, and T.F. Duchaine, eds. (Totowa, NJ: Humana Press), pp. 251–280.
6. Dang, Y., Zhang, Z., and Liu, Y. (2014). Small RNA-Mediated Gene Silencing in Neurospora. In Fungal RNA Biology, A. Sesma, and T. von der Haar, eds. (Cham: Springer International Publishing), pp. 269–289.
7. Freitag, M. (2014). Fungal Chromatin and Its Role in Regulation of Gene Expression. In Fungal Genomics, M. Nowrousian, ed. (Springer-Verlag Berlin Heidelberg),.
8. McDonald, B.A., and Martinez, J.P. (1991). Chromosome length polymorphisms in a Septoria tritici population. Curr. Genet. 19, 265–271.
9. Jones, K. (1998). Robertsonian Fusion and Centric Fission in Karyotype Evolution of Higher Plants. Bot. Rev. 64, 273–289.
10. VanEtten, H.D., Jorgensen, S., Enkerli, J., and Covert, S.F. (1998). Inducing the loss of conditionally dispensable chromosomes in Nectria haematococca during vegetative growth. Curr. Genet. 33, 299–303.
11. Covert, S.F. (1998). Supernumerary chromosomes in filamentous fungi. Curr. Genet. 33, 311–319. References 129
12. Dhar, M.K., Friebe, B., Koul, A.K., and Gill, B.S. (2002). Origin of an apparent B chromosome by mutation, chromosome fragmentation and specific DNA sequence amplification. Chromosoma 111, 332–340.
13. Lamb, J.C., Kato, A., and Birchler, J.A. (2005). Sequences associated with A chromosome centromeres are present throughout the maize B chromosome. Chromosoma 113, 337–349.
14. Mishra, P.K., Baum, M., and Carbon, J. (2007). Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol. Genet. Genomics 278, 455–465.
15. Zhou, J., Fu, Y., Xie, J., Li, B., Jiang, D., Li, G., and Cheng, J. (2012). Identification of microRNA- like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol. Genet. Genomics 287, 275–282.
16. Marschner, S., Kumke, K., and Houben, A. (2007). B chromosomes of B. dichromosomatica show a reduced level of euchromatic histone H3 methylation marks. Chromosom. Res. 15, 215–222.
17. Gupta, O.P., Permar, V., Koundal, V., Singh, U.D., and Praveen, S. (2012). MicroRNA regulated defense responses in Triticum aestivum L. during Puccinia graminis f.sp. tritici infection. Mol. Biol. Rep. 39, 817–824.
18. Yin, W., Birchler, J. a., and Han, F. (2011). Maize centromeres: where sequence meets epigenetics. Front. Biol. (Beijing). 6, 102–108.
19. Functional selection and analysis of Yeast Centromeric DNA. Cell 42, 913–921.
20. Stimpson, K.M., and Sullivan, B.A. (2010). Epigenomics of centromere assembly and function.
21. Gullerova, M., and Proudfoot, N.J. (2008). Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132, 983–995.
22. Obbard, D.J., Jiggins, F.M., Halligan, D.L., and Little, T.J. (2006). Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr. Biol. 16, 580–585.
23. Vagnarelli, P., Ribeiro, S.A., and Earnshaw, W.C. (2008). Centromeres: old tales and new tools. FEBS Lett. 582, 1950–1959.
24. Riddle, N.C., and Birchler, J.A. (2003). Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Genet. 19, 593–597.
25. Galagan, J.E., and Selker, E.U. (2004). RIP: the evolutionary cost of genome defense. Trends Genet. 20, 417–423.
26. Duncan, K.E., and Howard, R.J. (2000). Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycol. Res. 104, 1074–1082.
27. Pumplin, N., and Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol. 11, 745–760.
28. Tsutsumi, A., Kawamata, T., Izumi, N., Seitz, H., and Tomari, Y. (2011). Recognition of the pre- miRNA structure by Drosophila Dicer-1. Nat. Struct. Mol. Biol. 18, 1153–1158.
29. Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
30. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078– 2079.
31. Ellendorff, U., Fradin, E.F., de Jonge, R., and Thomma, B.P.H.J. (2009). RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60, 591–602.
32. Stukenbrock, E.H., Banke, S., Javan-Nikkhah, M., and McDonald, B.A. (2007). Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol. Biol. Evol. 24, 398–411.
33. Gouy, M., Guindon, S., and Gascuel, O. (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221–224.
34. Nicolas, F.E., Moxon, S., de Haro, J.P., Calo, S., Grigoriev, I. V., Torres-Martínez, S., Moulton, V., Ruiz-Vázquez, R.M., and Dalmay, T. (2010). Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides. Nucleic Acids Res. 38, 5535–5541.
35. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321.
36. De Wit, E., and de Laat, W. (2012). A decade of 3C technologies : insights into nuclear organization. Genes Dev. 21, 11–24.
37. Honda, S., Lewis, Z.A., Huarte, M., Cho, L.Y., David, L.L., Shi, Y., and Selker, E.U. (2010). The DMM complex prevents spreading of DNA methylation from transposons to nearby genes in Neurospora crassa. Genes Dev. 24, 443–454.
38. 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.
39. Rudd, M.K., Endicott, R.M., Friedman, C., Walker, M., Young, J.M., Osoegawa, K., de Jong, P.J., Green, E.D., and Trask, B.J. (2009). Comparative sequence analysis of primate subtelomeres originating from a chromosome fission event. Genome Res. 19, 33–41.
40. Lewis, Z.A., Honda, S., Khlafallah, T.K., Jeffress, J.K., Freitag, M., Mohn, F., Schübeler, D., and Selker, E.U. (2009). Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 19, 427–437.
41. Stukenbrock, E.H., Bataillon, T., Dutheil, J.Y., Hansen, T.T., Li, R., Zala, M., McDonald, B.A., Jun, W., and Schierup, M.H. (2011). The making of a new pathogen: Insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21, 2157–2166.
42. Thakur, J., and Sanyal, K. (2013). Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res. 638–652.
43. Genomics in C. elegans: so many genes, such a little worm. Genome Res. 15, 1651–1660.
44. Ahn, J., and Walton, J.D. (1996). Chromssomal Organization of TOx2, a Complex Locus Controlling Host-Selective Toxin Biosynthesis in Cochliobolus carbonum. Plant Cell 8, 887–897.
45. Bowler, J., Scott, E., Tailor, R., Scalliet, G., Ray, J., and Csukai, M. (2010). New capabilities for Mycosphaerella graminicola Research. Mol. Plant Pathol. 11, 691–704.
46. Vetukuri, R.R., Avrova, A.O., Grenville-briggs, L.J., van West, P., Söderbom, F., Savenkov, E.I., Whisson, S.C., and Dixelius, C. (2011). Evidence for involvement of Dicer-like, Argonaute and histone deacetylase proteins in gene silencing in Phytophthora infestans. Mol. Plant Pathol. 12, 772–785.
47. Lu, S., Sun, Y.-H., Amerson, H., and Chiang, V.L. (2007). MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J. 51, 1077–1098.
48. Henikoff, S., Ahmad, K., and Malik, H.S. (2001). The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 293, 1098–1102.
49. Schueler, M.G., Higgins, A.W., Rudd, M.K., Gustashaw, K., and Willard, H.F. (2001). Genomic and genetic definition of a functional human centromere. Science. 294, 109–115.
50. Chang, S.-S., Zhang, Z., and Liu, Y. (2012). RNA Interference Pathways in Fungi: Mechanisms and Functions. Annu. Rev. Microbiol. 305–323.
51. Campos, E.I., and Reinberg, D. (2009). Histones: annotating chromatin. Annu. Rev. Genet. 43, 559– 599.
52. Van der Burgt, A., Karimi Jashni, M., Bahkali, A.H., and de Wit, P.J.G.M. (2014). Pseudogenization in pathogenic fungi with different host plants and lifestyles might reflect their evolutionary past. Mol. Plant Pathol. 15, 133–144.
53. Mehrabi, R., Taga, M., and Kema, G.H.J. (2007). Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range. Mycologia 99, 868–876.
54. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S.L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
55. Luijsterburg, M.S., Dinant, C., Lans, H., Stap, J., Wiernasz, E., Lagerwerf, S., Warmerdam, D.O., Lindh, M., Brink, M.C., Dobrucki, J.W., et al. (2009). Heterochromatin protein 1 is recruited to various types of DNA damage. J. Cell Biol. 185, 577–586.
56. Coleman, J.J., Rounsley, S.D., Rodriguez-Carres, M., Kuo, A., Wasmann, C.C., Grimwood, J., Schmutz, J., Taga, M., White, G.J., Zhou, S., et al. (2009). The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5, e1000618.
57. Ma, L.-J., Van Der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.-J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., et al. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367–373.
58. De Wit, P.J.G.M., van der Burgt, A., Ökmen, B., Stergiopoulos, I., Abd-Elsalam, K.A., Aerts, A.L., Bahkali, A.H., Beenen, H.G., Chettri, P., Cox, M.P., et al. (2012). The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. 8, e1003088.
59. Schmidt, S.M., Houterman, P.M., Schreiver, I., Ma, L., Amyotte, S., Chellappan, B., Boeren, S., Takken, F.L.W., and Rep, M. (2013). MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. BMC Genomics 14, 119.
60. Goodwin, S.B., Waalwijk, C., and Kema, G.H.J. (2004). Genetics and genomics of Mycosphaerella graminicola A model for the dothideales. In Applied Mycology and Biotechnology, pp. 315–330.
61. Masumoto, H., Nakano, M., and Ohzeki, J.-I. (2004). The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres. Chromosom. Res. 12, 543– 556.
62. Candida albicans Dicer (CaDcr1) is required for efficient ribosomal and spliceosomal RNA maturation. Proc. Natl. Acad. Sci. U. S. A. 109, 523–528.
63. Centromeric Sequence: Evidence for an Evolutionary Relationship With the B Chromosome Centromere. Genetics 159, 291–302.
64. Weiberg, A., Wang, M., Lin, F.-M., Zhao, H., Zhang, Z., Kaloshian, I., Huang, H.-D., and Jin, H. (2013). Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways. Science. 342, 118–123.
65. Grewal, S.I.S., and Jia, S. (2007). Heterochromatin revisited. Nat. Rev. Genet. 8, 35–46.
66. Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007). High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837.
67. Human Parasite Toxoplasma gondii. PLoS Pathog. 6, e1000920.
68. Clarke, L., and Carbon, J. (1980). Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287, 504–509.
69. Napoli, C., Lemieux, C., and Jorgensen, R. (1990). lntroduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes Ín trans. Plant Cell 2, 279–289.
70. Wilson, R.C., and Doudna, J.A. (2013). Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 42, 217–239.
71. Hammond, T.M., Xiao, H., Boone, E.C., Decker, L.M., Lee, S.A., Perdue, T.D., Pukkila, P.J., and Shiu, P.K.T. (2013). Novel proteins required for meiotic silencing by unpaired DNA and siRNA generation in Neurospora crassa. Genetics 194, 91–100.
72. Kadotani, N., Nakayashiki, H., Tosa, Y., and Mayama, S. (2004). One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-triggered RNA silencing and related small interfering RNA accumulation. J. Biol. Chem. 279, 44467–44474.
73. Houben, A., and Carchilan, M. (2012). Plant B Chromosomes: What Makes Them Different? In Plant Cytogenetics, Plant Genetics and Genomics: Crops and Models 4, H.W. Bass, and J.A. Birchler, eds. (New York, NY: Springer New York), pp. 59–77.
74. Romano, N., and Macino, G. (1992). Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol. 6, 3343–3353.
75. Padmanabhan, S., Thakur, J., Siddharthan, R., and Sanyal, K. (2008). Rapid evolution of Cse4p-rich centromeric DNA sequences in closely related pathogenic yeasts, Candida albicans and Candida References 134 dubliniensis. Proc. Natl. Acad. Sci. U. S. A. 105, 19797–19802.
76. Regulation of Heterochromatic Silencing and Histone H3 Lysine-9 Methylation by RNAi. Science. 297, 1833–1837.
77. Billmyre, R.B., Calo, S., Feretzaki, M., Wang, X., and Heitman, J. (2013). RNAi function, diversity, and loss in the fungal kingdom. Chromosom. Res. 21, 561–572.
78. Ponomarenko, A., Goodwin, S.B., and Kema, G.H.J. (2011). Septoria tritici blotch ( STB ) of wheat. Plant Heal. Instr. 1–8.
79. Collas, P. (2010). The current state of chromatin immunoprecipitation. Mol. Biotechnol. 45, 87– 100.
80. Schübeler, D., MacAlpine, D.M., Scalzo, D., Wirbelauer, C., Kooperberg, C., van Leeuwen, F., Gottschling, D.E., O'Neill, L.P., Turner, B.M., Delrow, J., et al. (2004). The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote.
81. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797.
82. Mallory, A., and Vaucheret, H. (2010). Form, function, and regulation of Argonaute proteins. Plant References 133
83. Rouxel, T., Grandaubert, J., Hane, J.K., Hoede, C., van de Wouw, A.P., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., et al. (2011). Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat. Commun. 2, 202. References 135
84. Soyer, J.L., El Ghalid, M., Glaser, N., Ollivier, B., Linglin, J., Grandaubert, J., Balesdent, M.-H., Connolly, L.R., Freitag, M., Rouxel, T., et al. (2014). Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet. 10, e1004227.
85. Balesdent, M.-H., Fudal, I., Ollivier, B., Bally, P., Grandaubert, J., Eber, F., Chèvre, A.-M., Leflon, M., and Rouxel, T. (2013). The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol. 198, 887–898.
86. Volpe, T.A., Schramke, V., Hamilton, G.L., White, S.A., Teng, G., Martienssen, R.A., and Allshire, R.C. (2003). RNA interference is required for normal centromere function in fission yeast. Chromosom. Res. 11, 137–146.
87. Martienssen, R.A., Zaratiegui, M., and Goto, D.B. (2005). RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet. 21, 450–456.
88. Goodwin, S.B., Barek, S.B.M., Dhillon, B., Wittenberg, A.H.J., Crane, C.F., Hane, J.K., Foster, A.J., van der Lee, T.A.J., Grimwood, J., Aerts, A., et al. (2011). Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis. PLoS Genet. 7, e1002070.
89. Ishii, K., Ogiyama, Y., Chikashige, Y., Soejima, S., Masuda, F., Kakuma, T., Hiraoka, Y., and Takahashi, K. (2008). Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science. 321, 1088–1091.
90. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806– 811.
91. Nunes, C.C., Gowda, M., Sailsbery, J., Xue, M., Chen, F., Brown, D.E., Oh, Y., Mitchell, T.K., and Dean, R.A. (2011). Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genomics 12, 288–308.
92. Raman, V., Simon, S.A., Romag, A., Demirci, F., Mathioni, S.M., Zhai, J., Meyers, B.C., and Donofrio, N.M. (2013). Physiological stressors and invasive plant infections alter the small RNA transcriptome of the rice blast fungus, Magnaporthe oryzae. BMC Genomics 14, 326.
93. Hu, Y., Stenlid, J., Elfstrand, M., and Olson, A. (2013). Evolution of RNA interference proteins dicer and argonaute in Basidiomycota. Mycologia 105, 1489–1498.
94. Lee, H.-C., Chang, S., Choudhary, S., Aalto, A.P., Maiti, M., Bamford, D.H., and Liu, Y. (2009). qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459, 274–277.
95. Formation of de novo centromeres and constructution of first-generation human artificial References 131 micochromosomes. Nat. Genet. 15.
96. Rodríguez-Paredes, M., and Esteller, M. (2011). Cancer epigenetics reaches mainstream oncology. Nat. Med. 17, 330–339.
97. Gaszner, M., and Felsenfeld, G. (2006). Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 7, 703–713.
98. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol. Evol.
99. Pfaffl, M.W., Horgan, G.W., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
100. Han, F., Lamb, J.C., and Birchler, J.A. (2006). High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc. Natl. Acad. Sci. U. S. A. 103, 3238–3243.
101. Malik, H.S., and Henikoff, S. (2001). Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157, 1293–1298.
102. Liu, H., Cottrell, T.R., Pierini, L.M., Goldman, W.E., and Doering, T.L. (2002). RNA Interference in the Pathogenic Fungus Cryptococcus neoformans. Genetics 160, 463–470.
103. Baum, M., Sanyal, K., Mishra, P.K., Thaler, N., and Carbon, J. (2006). Formation of functional centromeric chromatin is specified epigenetically in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 103, 14877–14882.
104. Castillo, A.G., Mellone, B.G., Partridge, J.F., Richardson, W., Hamilton, G.L., Allshire, R.C., and Pidoux, A.L. (2007). Plasticity of fission yeast CENP-A chromatin driven by relative levels of histone H3 and H4. PLoS Genet. 3, e121.
105. Bensasson, D., Zarowiecki, M., Burt, A., and Koufopanou, V. (2008). Rapid evolution of yeast centromeres in the absence of drive. Genetics 178, 2161–2167.
106. Bártová, E., Krejcí, J., Harnicarová, A., Galiová, G., and Kozubek, S. (2008). Histone modifications and nuclear architecture: a review. J. Histochem. Cytochem. 56, 711–721.
107. Zhang, P., Li, W., Friebe, B., and Gill, B.S. (2008). The origin of a " zebra " chromosome in wheat suggests nonhomologous recombination as a novel mechanism for new chromosome evolution and step changes in chromosome number. Genetics 179, 1169–1177.
108. Allshire, R.C., and Karpen, G.H. (2008). Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923–937.
109. Folco, H.D., Pidoux, A.L., Urano, T., and Allshire, R.C. (2008). Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science. 319, 94–97.
110. Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 106, 2688–2693.
111. Ketel, C., Wang, H.S.W., McClellan, M., Bouchonville, K., Selmecki, A., Lahav, T., Gerami-Nejad, M., and Berman, J. (2009). Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet. 5, e1000400. References 132
112. Carthew, R.W., and Sontheimer, E.J. (2009). Origins and Mechanisms of miRNAs and siRNAs. Cell 136, 642–655.
113. Wittenberg, A.H.J., van Der Lee, T.A.J., Ben M'barek, S., Ware, S.B., Goodwin, S.B., Kilian, A., Visser, R.G.F., Kema, G.H.J., and Schouten, H.J. (2009). Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4, e5863.
114. Ghildiyal, M., and Zamore, P.D. (2009). Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94–108.
115. Wang, Z., Zang, C., Rosenfeld, J.A., Schones, D.E., Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Peng, W., Zhang, M.Q., et al. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897–903.
116. Dinant, C., and Luijsterburg, M.S. (2009). The emerging role of HP1 in the DNA damage response. Mol. Cell. Biol. 29, 6335–6340.
117. Malone, C.D., and Hannon, G.J. (2009). Small RNAs as guardians of the genome. Cell 136, 656– 668.
118. Peng, J.C., and Karpen, G.H. (2008). Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 18, 204–211.
119. Braun, L., Cannella, D., Ortet, P., Barakat, M., Sautel, C.F., Kieffer, S., Garin, J., Bastien, O., Voinnet, O., and Hakimi, M.-A. (2010). A Complex Small RNA Repertoire Is Generated by a Plant/Fungal-Like Machinery and Effected by a Metazoan-Like Argonaute in the Single-Cell References 128
120. Lee, H.-C., Li, L., Gu, W., Xue, Z., Crosthwaite, S.K., Pertsemlidis, A., Lewis, Z.A., Freitag, M., Selker, E.U., Mello, C.C., et al. (2010). Diverse pathways generate microRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Mol. Cell 38, 803–814.
121. Palmer, J.M., and Keller, N.P. (2010). Secondary metabolism in fungi: does chromosomal location matter? Curr. Opin. Microbiol. 13, 431–436.
122. Langmead, B. (2010). Aligning short sequencing reads with Bowtie. Curr Protoc Bioinforma. 1–24.
123. Halic, M., and Moazed, D. (2010). Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140, 504–516.
124. Zaratiegui, M., Vaughn, M.W., Irvine, D. V., Goto, D., Watt, S., Bähler, J., Arcangioli, B., and Martienssen, R.A. (2011). CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469, 112–115.
125. Zhang, X., Zhao, H., Gao, S., Wang, W.-C., Katiyar-Agarwal, S., Huang, H.-D., Raikhel, N., and Jin, H. (2011). Arabidopsis Argonaute 2 regulates innate immunity via miRNA393( * )-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 42, 356–366.
126. Rhind, N., Chen, Z., Yassour, M., Thompson, D.A., Haas, B.J., Habib, N., Wapinski, I., Roy, S., Lin, M.F., Heiman, D.I., et al. (2011). Comparative Functional Genomics of the Fission Yeasts. Science. 930, 930–936.
127. Heterochromatin is required for normal distribution of Neurospora CenH3. Mol. Cell. Biol. 31, 2528–2542.
128. Bannister, A.J., and Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Res. 21, 381–395.
129. Roy, B., and Sanyal, K. (2011). Diversity in requirement of genetic and epigenetic factors for centromere function in fungi. Eukaryot. Cell 10, 1384–1395.
130. Rando, O.J., and Winston, F. (2012). Chromatin and transcription in yeast. Genetics 190, 351–387.
131. Smith, K.M., Galazka, J.M., Phatale, P.A., Connolly, L.R., and Freitag, M. (2012). Centromeres of filamentous fungi. Chromosom. Res. 20, 635–656.
132. Burrack, L.S., and Berman, J. (2012). Neocentromeres and epigenetically inherited features of centromeres. Chromosom. Res. 20, 607–619.
133. Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti. PLoS One 7, e44198.
134. Vetukuri, R.R., Åsman, A.K.M., Tellgren-Roth, C., Jahan, S.N., Reimegård, J., Fogelqvist, J., Savenkov, E., Söderbom, F., Avrova, A.O., Whisson, S.C., et al. (2012). Evidence for Small RNAs Homologous to Effector-Encoding Genes and Transposable Elements in the Oomycete Phytophthora infestans. PLoS One 7, e51399.
135. Jiang, N., Yang, Y., Janbon, G., Pan, J., and Zhu, X. (2012). Identification and functional demonstration of miRNAs in the fungus Cryptococcus neoformans. PLoS One 7, e52734.
136. Lefrançois, P., Auerbach, R.K., Yellman, C.M., Roeder, G.S., and Snyder, M. (2013). Centromere- Like Regions in the Budding Yeast Genome. PLoS Genet. 9, e1003209.
137. Nicolás, F.E., Torres-Martínez, S., and Ruiz-Vázquez, R.M. (2013). Loss and retention of RNA interference in fungi and parasites. PLoS Pathog. 9, e1003089.
138. Catalanotto, C., Pallotta, M., Refalo, P., Sachs, M.S., Vayssie, L., Macino, G., and Cogoni, C. (2004). Redundancy of the Two Dicer Genes in Transgene-Induced Posttranscriptional Gene Silencing in Neurospora crassa. Mol. Cell. Biol. 24, 2536–2545.
139. Jamieson, K., Rountree, M.R., Lewis, Z.A., Stajich, J.E., and Selker, E.U. (2013). Regional control of histone H3 lysine 27 methylation in Neurospora. Proc. Natl. Acad. Sci. U. S. A. 55, 1–6.
140. Ng, R., and Carbon, J. (1987). Mutational and In Vitro Protein-Binding Studies on Centromere DNA from Saccharomyces cerevisiae. Mol. Cell. Biol. 7.
141. Croll, D., Zala, M., and McDonald, B.A. (2013). Breakage-fusion-bridge Cycles and Large Insertions Contribute to the Rapid Evolution of Accessory Chromosomes in a Fungal Pathogen.
142. Katiyar-Agarwal, S., and Jin, H. (2010). Role of Small RNAs in Host-Microbe Interactions. Annu. Rev. Phytopathol. 48, 225–246.
143. Dang, Y., Li, L., Guo, W., Xue, Z., and Liu, Y. (2013). Convergent Transcription Induces Dynamic DNA Methylation at disiRNA Loci. PLoS Genet. 9, e1003761.
144. 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.
145. Drinnenberg, I.A., Fink, G.R., and Bartel, D.P. (2011). Compatibility with killer explains the rise of RNAi-deficient fungi. Science. 333, 1592.
146. Connolly, L.R., Smith, K.M., and Freitag, M. (2013). The Fusarium graminearum Histone H3 K27 Methyltransferase KMT6 Regulates Development and Expression of Secondary Metabolite Gene Clusters. PLoS Genet. 9, e1003916.
147. Clarke, L., Amstutz, H., Fishel, B., and Carbon, J. (1986). Analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. U. S. A. 83, 8253–8257.
148. Sanyal, K., Baum, M., and Carbon, J. (2004). Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc. Natl. Acad. Sci. U. S. A. 101, 11374–11379.
149. Wood, V., Gwilliam, R., Rajandream, M., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S., et al. (2002). Genome sequence of Schizosaccharomyces pombe. Tanpakushitsu Kakusan Koso. 47, 1215–1220.

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