| BMC Genomics | |
| Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus | |
| Christina A. Cuomo2  David J. Schultz8  Michael E. Hood4  Tatiana Giraud1  Hadi Quesneville5  Toni Gabaldón1,10  Dominique Razeeq8  Jared Andrews8  Helene Badouin1  Elsa Petit6  Gabriela Aguileta3  Qiandong Zeng2  Sarah Young2  Bernard Henrissat6  Sebastien Duplessis9  Jonathan Goldberg2  Zehua Chen2  Su San Toh8  Eric Fontanillas1  Joelle Amselem7  Michael H Perlin8  | |
| [1] CNRS, Orsay, F-91405, France;Broad Institute of MIT and Harvard, Cambridge 02142, MA, USA;Centre for Genomic Regulation (CRG), Barcelona, Spain;Department of Biology, Amherst College, Amherst 01002, MA, USA;Institut National de la Recherche Agronomique (INRA), Unité de Recherche Génomique Info (URGI), Versailles, France;Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, Marseille, 13288, France;Institut National de la Recherche Agronomique (INRA), Biologie et gestion des risques en agriculture (BIOGER), Thiverval-Grignon, France;Department of Biology, Program on Disease Evolution, University of Louisville, Louisville 40292, KY, USA;UMR 1136, Université de Lorraine, Interactions Arbres-Microorganismes, Vandoeuvre-lès-Nancy, France;Institució Catalana d’Estudis Avançats (ICREA), Barcelona, Spain | |
| 关键词: Pathogen alteration of host development; Mating-type chromosomes; Transposable elements; CAZymes; Anther smuts; Microbotryum violaceum; | |
| Others : 1216173 DOI : 10.1186/s12864-015-1660-8 |
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| received in 2014-12-18, accepted in 2015-05-28, 发布年份 2015 | |
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【 摘 要 】
Background
The genus Microbotryum includes plant pathogenic fungi afflicting a wide variety of hosts with anther smut disease. Microbotryum lychnidis-dioicae infects Silene latifolia and replaces host pollen with fungal spores, exhibiting biotrophy and necrosis associated with altering plant development.
Results
We determined the haploid genome sequence for M. lychnidis-dioicae and analyzed whole transcriptome data from plant infections and other stages of the fungal lifecycle, revealing the inventory and expression level of genes that facilitate pathogenic growth. Compared to related fungi, an expanded number of major facilitator superfamily transporters and secretory lipases were detected; lipase gene expression was found to be altered by exposure to lipid compounds, which signaled a switch to dikaryotic, pathogenic growth. In addition, while enzymes to digest cellulose, xylan, xyloglucan, and highly substituted forms of pectin were absent, along with depletion of peroxidases and superoxide dismutases that protect the fungus from oxidative stress, the repertoire of glycosyltransferases and of enzymes that could manipulate host development has expanded. A total of 14 % of the genome was categorized as repetitive sequences. Transposable elements have accumulated in mating-type chromosomal regions and were also associated across the genome with gene clusters of small secreted proteins, which may mediate host interactions.
Conclusions
The unique absence of enzyme classes for plant cell wall degradation and maintenance of enzymes that break down components of pollen tubes and flowers provides a striking example of biotrophic host adaptation.
【 授权许可】
2015 Perlin et al.
【 预 览 】
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【 参考文献 】
- [1]Kemler M, Lutz M, Göker M, Oberwinkler F, Begerow D. Hidden diversity in the non-caryophyllaceous plant parasite members of Microbotryum (Pucciniomycotina: Microbotryales). Syst Biodivers. 2009; 7:297-306.
- [2]De Vienne DM, Hood ME, Giraud T. Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol. 2009; 22:2532-2541.
- [3]Le Gac M, Hood ME, Fournier E, Giraud T. Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evol Int J Org Evol. 2007; 61:15-26.
- [4]Le Gac M, Hood ME, Giraud T. Evolution of reproductive isolation within a parasitic fungal species complex. Evol Int J Org Evol. 2007; 61:1781-1787.
- [5]De Vienne DM, Refregier G, Hood ME, Guigue A, Devier B, Vercken E, Smadja C, Deseille A, Giraud T. Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. J Evol Biol. 2009; 22:683-698.
- [6]Giraud T, Yockteng R, Lopez-Villavicencio M, Refregier G, Hood ME. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell. 2008; 7:765-775.
- [7]Gibson AK, Hood ME, Giraud T. Sibling competition arena: selfing and a competition arena can combine to constitute a barrier to gene flow in sympatry. Evol Int J Org Evol. 2012; 66:1917-1930.
- [8]Alexander HM. An experimental field study of anther-smut disease of Silene alba caused by Ustilago violacea: genotypic variation and disease incidence. Evolution. 1989; 43:835-847.
- [9]Antonovics J, Hood ME, Partain J. The ecology and genetics of host shift: Microbotryum as a model system. Am Nat. 2002; 160:S40-S53.
- [10]Refrégier G, Le Gac M, Jabbour F, Widmer A, Shykoff JA, Yockteng R, Hood ME, Giraud T. 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.
- [11]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.
- [12]Hood ME, Petit E, Giraud T. Extensive divergence between mating-type chromosomes of the anther-smut fungus. Genetics. 2013; 193:309-315.
- [13]Hughes CF, Perlin MH. Differential expression of mepA, mepC and smtE during growth and development of Microbotryum violaceum. Mycologia. 2005; 97:605-611.
- [14]Roche BM, Alexander HM, Maltby AD. Dispersal and disease gradients of anther-smut infection of Silene Alba at different life stages. Ecology. 1995; 76:1863-1871.
- [15]Jennersten O. Butterfly visitors as vectors of Ustilago violacea spores between caryophyllaceous plants. Oikos. 1983; 40:125-130.
- [16]Akhter S, Antonovics J. Use of internal transcribed spacer primers and fungicide treatments to study the anther-smut disease, Microbotryum violaceum (=Ustilago violacea), of white campion Silene alba (=Silene latifolia). Int J Plant Sci. 1999; 160:1171-1176.
- [17]Kokontis J, Ruddat M. Promotion of Hyphal growth in Ustilago-Violacea by host factors from Silene-Alba. Arch Microbiol. 1986; 144:302-306.
- [18]Kokontis JM, Ruddat M. Enzymatic hydrolysis of Hyphal growth factors for Ustilago violacea isolated from the host plant Silene alba. Bot Gaz. 1989; 150:439-444.
- [19]Scutt CP, Kamisugi Y, Sakai F, Gilmartin PM. Laser isolation of plant sex chromosomes: studies on the DNA composition of the X and Y sex chromosomes of Silene latifolia. Genome Natl Res Counc Can Genome Cons Natl Rech Can. 1997; 40:705-715.
- [20]Alexander HM, Antonovics J. Spread of anther-smut disease (Ustilago violacea) and character correlations in a genetically variable experimental population of Silene alba. J Ecol. 1995; 83:783-794.
- [21]Robertson SE, Li Y, Scutt CP, Willis ME, Gilmartin PM. Spatial expression dynamics of Men-9 delineate the third floral whorl in male and female flowers of dioecious Silene latifolia. Plant J Cell Mol Biol. 1997; 12:155-168.
- [22]Kazama Y, Koizumi A, Uchida W, Ageez A, Kawano S. Expression of the floral B-function gene SLM2 in female flowers of Silene latifolia infected with the smut fungus Microbotryum violaceum. Plant Cell Physiol. 2005; 46:806-811.
- [23]Billiard S, López-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T. 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.
- [24]Billiard S, López-Villavicencio M, Hood ME, Giraud T. Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J Evol Biol. 2012; 25:1020-1038.
- [25]Fraser JA, Heitman J. Evolution of fungal sex chromosomes. Mol Microbiol. 2004; 51:299-306.
- [26]Fraser JA, Hsueh YP, Findley KM, Heitman J. Evolution of the Mating-Type Locus: The Basidiomycetes. In: Sex in Fungi. Heitman J, Kronstad J, Taylor J, Casselton L, editors. ASM Press, Washington, D.C; 2007: p.19-34.
- [27]Menkis A, Jacobson DJ, Gustafsson T, Johannesson H. The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet. 2008; 4: Article ID e1000030
- [28]Hood ME. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics. 2002; 160:457-461.
- [29]Hood ME, Antonovics J. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea). Heredity. 2000; 85(Pt 3):231-241.
- [30]Hood ME. Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica. 2005; 124:1-10.
- [31]Whittle CA, Sun Y, Johannesson H. Degeneration in codon usage within the region of suppressed recombination in the mating-type chromosomes of Neurospora tetrasperma. Eukaryot Cell. 2011; 10:594-603.
- [32]Whittle CA, Johannesson H. Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma. Heredity. 2011; 107:305-314.
- [33]Fontanillas E, Hood ME, Badouin H, Petit E, Barbe V, Gouzy J, de Vienne DM, Aguileta G, Poulain J, Wincker P, Chen Z, Toh SS, Cuomo CA, Perlin MH, Gladieux P, Giraud T. Degeneration of the non-recombining regions in the mating-type chromosomes of the anther-smut fungi. Mol Biol Evol. 2014; 32(4):928-943.
- [34]Farbos I, Oliveira M, Negrutiu I, Mouras A. Sex organ determination and differentiation in the dioecious plant Melandrium album (Silene latifolia): a cytological and histological analysis. Sex Plant Reprod. 1997; 10:155-167.
- [35]Grant S, Hunkirchen B, Saedler H. Developmental differences between male and female flowers in the dioecious plant Silene latifolia. Plant J. 1994; 6:471-480.
- [36]Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinforma Oxf Engl. 2007; 23:1061-1067.
- [37]Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciuffetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GHJ, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW et al.. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun. 2011; 2:202.
- [38]Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet. 2009; 10:285-311.
- [39]Duplessis S, Cuomo CA, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M et al.. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci. 2011; 108:9166-9171.
- [40]Yockteng R, Marthey S, Chiapello H, Gendrault A, Hood ME, Rodolphe F, Devier B, Wincker P, Dossat C, Giraud T. Expressed sequences tags of the anther smut fungus, Microbotryum violaceum, identify mating and pathogenicity genes. BMC Genomics. 2007; 8:272.
- [41]Kapitonov VV, Jurka J. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 2001; 98:8714-8719.
- [42]Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AM, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JI, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N et al.. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009; 461:393-398.
- [43]Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, de la Vega RC R, Branco S, Giraud T. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol Ecol. 2014; 23:753-773.
- [44]Hood ME, Katawczik M, Giraud T. Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics. 2005; 170:1081-1089.
- [45]Horns F, Petit E, Yockteng R, Hood ME. Patterns of repeat-induced point mutation in transposable elements of basidiomycete fungi. Genome Biol Evol. 2012; 4:240-247.
- [46]Cambareri EB, Jensen BC, Schabtach E, Selker EU. Repeat-induced G-C to A-T mutations in Neurospora. Science. 1989; 244:1571-1575.
- [47]Selker EU, Cambareri EB, Jensen BC, Haack KR. Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell. 1987; 51:741-752.
- [48]Walser J-C, Furano AV. The mutational spectrum of non-CpG DNA varies with CpG content. Genome Res. 2010; 20(7):875-882.
- [49]Fryxell KJ, Moon W-J. CpG mutation rates in the human genome are highly dependent on local GC content. Mol Biol Evol. 2005; 22:650-658.
- [50]Jiang C, Zhao Z. Directionality of point mutation and 5-methylcytosine deamination rates in the chimpanzee genome. BMC Genomics. 2006; 7:316.
- [51]Morton BR, Bi IV, McMullen MD, Gaut BS. Variation in mutation dynamics across the maize genome as a function of regional and flanking base composition. Genetics. 2006; 172:569-577.
- [52]Amselem J, Lebrun M-H, Quesneville H. Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes. BMC Genomics. 2015; 16:141.
- [53]Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010; 328:916-919.
- [54]Nicolás FE, Torres-Martínez S, Ruiz-Vázquez RM. Loss and retention of RNA interference in fungi and parasites. PLoS Pathog. 2013; 9: Article ID e1003089
- [55]Petit E, Giraud T, de Vienne DM, Coelho MA, Aguileta G, Amselem J, Kreplak J, Poulain J, Gavory F, Wincker P, Young SK, Cuomo C, Perlin MH, Hood ME. Linkage to the mating-type locus across the genus Microbotryum: insights into nonrecombining chromosomes. Evol Int J Org Evol. 2012; 66:3519-3533.
- [56]Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bölker M, Kahmann R. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell. 1992; 68:647-657.
- [57]Devier B, Aguileta G, Hood ME, Giraud T. Ancient trans-specific polymorphism at pheromone receptor genes in basidiomycetes. Genetics. 2009; 181:209-223.
- [58]Votintseva AA, Filatov DA. Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics. 2009; 182:1391-1396.
- [59]Bachtrog D. Accumulation of Spock and Worf, two novel non-LTR retrotransposons, on the neo-Y chromosome of Drosophila miranda. Mol Biol Evol. 2003; 20:173-181.
- [60]Elhaik E, Landan G, Braur D. Can GC content at third-codon positions be used as a proxy for isochore composition? Mol Biol Evol. 2009; 26:1829-1833.
- [61]Klose J, de Sá MM, Kronstad JW. Lipid-induced filamentous growth in Ustilago maydis. Mol Microbiol. 2004; 52:823-835.
- [62]Castle AJ. Isolation and Identification of α -Tocopherol as an Inducer of the Parasitic Phase of Ustilago violacea. Phytopathology. 1984; 74:1194.
- [63]Suh MC, Samuels AL, Jetter R, Kunst L, Pollard M, Ohlrogge J, Beisson F. Cuticular lipid composition, surface structure, and gene expression in arabidopsis stem epidermis. Plant Physiol. 2005; 139:1649-1665.
- [64]Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014; 42(Database issue):D490-D495.
- [65]Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009; 37(Database issue):D233-D238.
- [66]Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist EA, Sun H, LaButti KM, Schmutz J, Jabbour D, Luo H, Baker SE, Pisabarro AG, Walton JD, Blanchette RA, Henrissat B, Martin F, Cullen D, Hibbett DS, Grigoriev IV. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A. 2014; 111:9923-9928.
- [67]Prillinger H, Deml G, Dörfler C, Laaser G, Lockau W. A contribution to the systematics and evolution of higher fungi - yeast-types in the basidiomycetes, part II: microbotryum-type. Bot Acta. 1991; 104:5-17.
- [68]Roeijmans H, Prillinger H, Umile C, Sugiyama J, Nakase T, Boekhout T (1998) Analysis of carbohydrate composition of cell walls and extracellular carbohydrates. In: Kurtzman C, Fell JW, Boekhout T (ed) The Yeasts - A Taxonomic Study. Volume 1. 5th edition. Elsevier, p. 103–105.
- [69]Liepman AH, Nairn CJ, Willats WGT, Sørensen I, Roberts AW, Keegstra K. Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants. Plant Physiol. 2007; 143:1881-1893.
- [70]Alexander NJ, McCormick SP, Hohn TM. TRI12, a trichothecene efflux pump from Fusarium sporotrichioides: gene isolation and expression in yeast. Mol Gen Genet. 1999; 261:977-984.
- [71]Wahl R, Wippel K, Goos S, Kämper J, Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 2010; 8: Article ID e1000303
- [72]Voegele RT, Struck C, Hahn M, Mendgen K. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci U S A. 2001; 98:8133-8138.
- [73]Moccia MD, Oger-Desfeux C, Marais GA, Widmer A. A White Campion (Silene latifolia) floral expressed sequence tag (EST) library: annotation, EST-SSR characterization, transferability, and utility for comparative mapping. BMC Genomics. 2009; 10:243.
- [74]Veneault-Fourrey C, Commun C, Kohler A, Morin E, Balestrini R, Plett J, Danchin E, Coutinho P, Wiebenga A, de Vries RP, Henrissat B, Martin F. Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet Biol FG B. 2014; 72:168-181.
- [75]Antoniw JF, Ritter CE, Pierpoint WS, Loon LCV. Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J Gen Virol. 1980; 47:79-87.
- [76]Baldrian P. Fungal laccases - occurrence and properties. FEMS Microbiol Rev. 2006; 30:215-242.
- [77]Takahashi T, Kakehi J-I. Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot. 2010; 105:1-6.
- [78]Brose N, Betz A, Wegmeyer H. Divergent and convergent signaling by the diacylglycerol second messenger pathway in mammals. Curr Opin Neurobiol. 2004; 14:328-340.
- [79]Dong W, Lv H, Xia G, Wang M. Does diacylglycerol serve as a signaling molecule in plants? Plant Signal Behav. 2012; 7:472-475.
- [80]Stergiopoulos I, de Wit PJGM. Fungal effector proteins. Annu Rev Phytopathol. 2009; 47:233-263.
- [81]Bauer R, Oberwinkler F, Vanky K. Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot. 1997; 75:1273-1314.
- [82]Palmieri G, Bianco C, Cennamo G, Giardina P, Marino G, Monti M, Sannia G. Purification, characterization, and functional role of a novel extracellular protease from Pleurotus ostreatus. Appl Environ Microbiol. 2001; 67:2754-2759.
- [83]Palmieri G, Cennamo G, Faraco V, Amoresano A, Sannia G, Giardina P. Atypical laccase isoenzymes from copper supplemented Pleurotus ostreatus cultures. Enzyme Microb Technol. 2003; 33:220-230.
- [84]Whittaker MM, Kersten PJ, Cullen D, Whittaker JW. Identification of catalytic residues in glyoxal oxidase by targeted mutagenesis. J Biol Chem. 1999; 274:36226-36232.
- [85]Luttrell ES. Tissue replacement diseases caused by fungi. Annu Rev Phytopathol. 1981; 19:373-389.
- [86]Cashion NL, Luttrell ES. Host parasite relationships in Karnal bunt of wheat. Phytopathology. 1988; 78:75-84.
- [87]Schäfer AM, Kemler M, Bauer R, Begerow D. The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Botany. 2010; 88:875-885.
- [88]Eisikowitch D, Lachance MA, Kevan PG, Willis S, Collins-Thompson DL. The effect of the natural assemblage of microorganisms and selected strains of the yeast Metschnikowia reukaufii in controlling the germination of pollen of the common milkweed Asclepias syriaca. Can J Bot. 1990; 68:1163-1165.
- [89]Biémont C. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics. 2010; 186:1085-1093.
- [90]Schmidt SM, Houterman PM, Schreiver I, Ma L, Amyotte S, Chellappan B, Boeren S, Takken FLW, Rep M. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. BMC Genomics. 2013; 14:119.
- [91]Otto SP, Pannell JR, Peichel CL, Ashman T-L, Charlesworth D, Chippindale AK, Delph LF, Guerrero RF, Scarpino SV, McAllister BF. About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet TIG. 2011; 27:358-367.
- [92]Luo H, Perlin MH. The gamma-tubulin-encoding gene from the basidiomycete fungus, Ustilago violacea, has a long 5′-untranslated region. Gene. 1993; 137:187-194.
- [93]Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A. Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods. 2010; 7:709-715.
- [94]Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res. 2009; 37: Article ID e123
- [95]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29:644-652.
- [96]Borodovsky M, Lomsadze A, Ivanov N, Mills R. Eukaryotic gene prediction using GeneMark.hmm. Curr Protoc Bioinforma. 2003; Chapter 4:Unit4 6.
- [97]Stanke M, Steinkamp R, Waack S, Morgenstern B. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 2004; 32(Web Server issue):W309-W312.
- [98]Majoros WH, Pertea M, Salzberg SL. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinforma Oxf Engl. 2004; 20:2878-2879.
- [99]Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 2008; 9:R7.
- [100]Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res. 2004; 14:988-995.
- [101]Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013; 8:1494-1512.
- [102]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.
- [103]Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323.
- [104]Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26:139-140.
- [105]Kadota K, Nishiyama T, Shimizu K. A normalization strategy for comparing tag count data. Algorithms Mol Biol AMB. 2012; 7:5.
- [106]Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995; 57:289-300.
- [107]Flutre T, Duprat E, Feuillet C, Quesneville H. Considering transposable element diversification in de novo annotation approaches. PLoS ONE. 2011; 6: Article ID e16526
- [108]Edgar RC, Myers EW. PILER: identification and classification of genomic repeats. Bioinformatics. 2005; 21 Suppl 1:i152-i158.
- [109]Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, Ashburner M, Anxolabehere D. Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol. 2005; 1:166-175.
- [110]Bao Z, Eddy SR. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 2002; 12:1269-1276.
- [111]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005; 110:462-467.
- [112]Hane JK, Oliver RP. RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics. 2008; 9:478.
- [113]Zytnicki M, Quesneville H. S-MART, a software toolbox to aid RNA-seq data analysis. PLoS ONE. 2011; 6: Article ID e25988
- [114]Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc. 2007; 2:953-971.
- [115]Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004; 340:783-795.
- [116]Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011; 8:785-786.
- [117]Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305:567-580.
- [118]Pierleoni A, Martelli PL, Casadio R. PredGPI: a GPI-anchor predictor. BMC Bioinformatics. 2008; 9:392.
- [119]Käll L, Krogh A, Sonnhammer ELL. Advantages of combined transmembrane topology and signal peptide prediction–the Phobius web server. Nucleic Acids Res. 2007; 35(Web Server issue):W429-W432.
- [120]Brameier M, Krings A, MacCallum RM. NucPred–predicting nuclear localization of proteins. Bioinformatics. 2007; 23:1159-1160.
- [121]Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 2010; 38(Database issue):D161-D166.
- [122]Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007; 35(Web Server issue):W585-W587.
- [123]Ongoing and future developments at the Universal Protein Resource. Nucleic Acids Res. 2011; 39(Database issue):D214-D219.
- [124]Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2012; 40(Database issue):D71-D75.
- [125]Lum G, Min XJ. FunSecKB: the Fungal Secretome KnowledgeBase. Database J Biol Databases Curation. 2011; 2011:bar001.
- [126]Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003; 13:2178-2189.
- [127]Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011; 7: Article ID e1002195
- [128]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21:3674-3676.
- [129]Huerta-Cepas J, Capella-Gutierrez S, Pryszcz LP, Denisov I, Kormes D, Marcet-Houben M, Gabaldón T. PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucleic Acids Res. 2011; 39(Database issue):D556-D560.
- [130]Huerta-Cepas J, Gabaldón T. Assigning duplication events to relative temporal scales in genome-wide studies. Bioinforma Oxf Engl. 2011; 27:38-45.
- [131]Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GHJ, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJGM, Zhong S, Goodwin SB, Grigoriev IV. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog. 2012; 8: Article ID e1003037
- [132]Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P et al.. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012; 336:1715-1719.
- [133]Holliday R. Ustilago Maydis. In: Handbook of Genetics. King RC, editor. Plenum Press, New York; 1974: p.575-595.
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