期刊论文详细信息
BMC Genomics
Genome sequence and virulence variation-related transcriptome profiles of Curvularia lunata, an important maize pathogenic fungus
Jie Chen1  Yingying Li1  Kehe Fu1  Yujuan Suo1  Jinxin Gao1  Yaqian Li1  Shigang Gao1 
[1] Ministry of Agriculture Key Laboratory of Urban Agriculture (South), Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai 200240, P. R. China
关键词: Pathogenicity variation;    RNA-seq;    Genome sequencing;    Curvularia lunata;   
Others  :  1216399
DOI  :  10.1186/1471-2164-15-627
 received in 2014-03-02, accepted in 2014-07-17,  发布年份 2014
PDF
【 摘 要 】

Background

Curvularia lunata is an important maize foliar fungal pathogen that distributes widely in maize growing area in China. Genome sequencing of the pathogen will provide important information for globally understanding its virulence mechanism.

Results

We report the genome sequences of a highly virulent C. lunata strain. Phylogenomic analysis indicates that C. lunata was evolved from Bipolaris maydis (Cochliobolus heterostrophus). The highly virulent strain has a high potential to evolve into other pathogenic stains based on analyses on transposases and repeat-induced point mutations. C. lunata has a smaller proportion of secreted proteins as well as B. maydis than entomopathogenic fungi. C. lunata and B. maydis have a similar proportion of protein-encoding genes highly homologous to experimentally proven pathogenic genes from pathogen-host interaction database. However, relative to B. maydis, C. lunata possesses not only many expanded protein families including MFS transporters, G-protein coupled receptors, protein kinases and proteases for transport, signal transduction or degradation, but also many contracted families including cytochrome P450, lipases, glycoside hydrolases and polyketide synthases for detoxification, hydrolysis or secondary metabolites biosynthesis, which are expected to be crucial for the fungal survival in varied stress environments. Comparative transcriptome analysis between a lowly virulent C. lunata strain and its virulence-increased variant induced by resistant host selection reveals that the virulence increase of the pathogen is related to pathways of toxin and melanin biosynthesis in stress environments, and that the two pathways probably have some overlaps.

Conclusions

The data will facilitate a full revelation of pathogenic mechanism and a better understanding of virulence differentiation of C. lunata.

【 授权许可】

   
2014 Gao et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150630103437556.pdf 2521KB PDF download
Figure 7. 192KB Image download
Figure 6. 63KB Image download
Figure 5. 88KB Image download
Figure 4. 83KB Image download
Figure 3. 125KB Image download
Figure 2. 50KB Image download
Figure 1. 109KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】
  • [1]Dai FC, Gao WD, Wu RJ, Jin XH: A noticeable corn disease: Curvularia leaf spot. ACTA Phytopathologica Sinica 1995, 25:330.
  • [2]Dai FC, Wang XM, Zhu ZD, Gao WD, Huo NX: Curvularia leaf spot of maize: pathogens and varietal resistance. ACTA Phytopathologica Sinica 1998, 2:123-129.
  • [3]Macri F, Lenna P: Leaf corn blight incited by Curvularia lunata (Wakk.) Boed. J Plant Pathol 1974, 10:27-35.
  • [4]Gao S, Liu T, Li Y, Wu Q, Fu K, Chen J: Understanding resistant germplasm-induced virulence variation through analysis of proteomics and suppression subtractive hybridization in a maize pathogen Curvularia lunata. Proteomics 2012, 12:3524-3535.
  • [5]Feng J, Gao Z, Xue C, Zhuang J, Chen J, Bai S: The pathogenesis of the cell-degrading enzymes produced by Curvularia lunata. Rain Fed Crops 2002, 22:164-167.
  • [6]Liu T, Liu L, Jiang X, Huang X, Chen J: A new furanoid toxin produced by Curvularia lunata, the causal agent of maize Curvularia leaf spot. Can J Plant Pathol 2009, 31:22-27.
  • [7]Xu SF, Chen J, Liu LX, Wang XF, Huang XL, Zhai YH: Proteomics associated with virulence differentiation of Curvularia lunata in maize in China. J Integr Plant Biol 2007, 49:487-496.
  • [8]Liu T, Xu S, Liu L, Zhou F, Hou J, Chen J: Cloning and characteristics of Brn1 gene in Curvularia lunata causing leaf spot in maize. Eur J Plant Pathol 2011, 131:211-219.
  • [9]Gao SG, Zhou FH, Liu T, Li YY, Chen J: A MAP kinase gene, Clk1, is required for conidiation and pathogenicity in the phytopathogenic fungus Curvularia lunata. J Basic Microbiol 2012, 53:214-223.
  • [10]Wang JY, Chen J: Cloning and functional analysis of Clm1 in Curvularia lunata. Acta Phytopathologica Sinica 2011, 41:464-472.
  • [11]Biggins JB, Ternei MA, Brady SF: Malleilactone, a polyketide synthase-derived virulence factor encoded by the cryptic secondary metabolome of Burkholderia pseudomallei group pathogens. J Am Chem Soc 2012, 134:13192-13195.
  • [12]Baker SE, Kroken S, Inderbitzin P, Asvarak T, Li BY, Shi L, Yoder OC, Turgeon BG: Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol Plant Microbe Interact 2006, 19:139-149.
  • [13]Liu T, Liu LX, Liu ZC, Hou JM, Gao SG, Zhou FH, Chen J: Construction and characterization of a norm a lized full-length cDNA library of Curvularia lunata. Acta Phytopathol Sinica 2010, 40:250-257.
  • [14]Jing J, Liu T, Chen J: Construction and characterization of yeast two hybrid cDNA library of Curvularia lunata. Acta Phytopathol Sinica 2012, 42:93-96.
  • [15]Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH: VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 2008, 320:1504-1506.
  • [16]Condon BJ, Leng Y, Wu D, Bushley KE, Ohm RA, Otillar R, Martin J, Schackwitz W, Grimwood J, MohdZainudin N: Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens. PLoS Genet 2013, 9:e1003233.
  • [17]Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang YL, Decaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes HW, Mitterbauer R, Muehlbauer G, et al.: The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
  • [18]Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ: The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
  • [19]Zheng P, Xia Y, Xiao G, Xiong C, Hu X, Zhang S, Zheng H, Huang Y, Zhou Y, Wang S, Zhao GP, Liu X, St Leger RJ, Wang C: Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 2011, 12:R116.
  • [20]Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang B, Fang W, Wang S, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia Y, Wang C: Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 2011, 7:e1001264.
  • [21]Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, et al.: Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 2008, 4:e1000046.
  • [22]McElwain JC, Punyasena SW: Mass extinction events and the plant fossil record. Trends Ecol Evol 2007, 22:548-557.
  • [23]Winnenburg R, Baldwin TK, Urban M, Rawlings C, Kohler J, Hammond-Kosack KE: PHI-base: a new database for pathogen host interactions. Nucleic Acids Res 2006, 34:D459-D464.
  • [24]Kang S, Lebrun MH, Farrall L, Valent B: Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol Plant Microbe Interact 2001, 14:671-674.
  • [25]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.
  • [26]Galagan JE, Selker EU: RIP: the evolutionary cost of genome defense. Trends Genet 2004, 20:417-423.
  • [27]Dangl JL, Jones JD: Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
  • [28]Dimroth P: Primary sodium ion translocating enzymes. Biochim Biophys Acta 1997, 1318:11-51.
  • [29]Paulsen IT, Brown MH, Skurray RA: Proton-dependent multidrug efflux systems. Microbiol Rev 1996, 60:575-608.
  • [30]de Waard MA: Significance of ABC transporters in fungicide sensitivity and resistance. Pestic Sci 1997, 51:271-275.
  • [31]Roohparvar R, De Waard MA, Kema GH, Zwiers LH: MgMfs1, a major facilitator superfamily transporter from the fungal wheat pathogen Mycosphaerella graminicola, is a strong protectant against natural toxic compounds and fungicides. Fungal Genet Biol 2007, 44:378-388.
  • [32]Crešnar B, Petrič S: Cytochrome P450 enzymes in the fungal kingdom. Biochimica et Biophysica Acta (BBA)-Proteins & Proteomics 2011, 1814:29-35.
  • [33]Nelson DR: The cytochrome p450 homepage. Hum Genomics 2009, 4:59-65.
  • [34]Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M: Molecular and genetic studies of fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 2007, 71:2105-2123.
  • [35]Butchko RA, Plattner RD, Proctor RH: Deletion analysis of FUM genes involved in tricarballylic ester formation during fumonisin biosynthesis. J Agric Food Chem 2006, 54:9398-9404.
  • [36]Bojja RS, Cerny RL, Proctor RH, Du L: Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J Agr Food Chem 2004, 52:2855-2860.
  • [37]Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB: The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003, 63:1256-1272.
  • [38]DeZwaan TM, Carroll AM, Valent B, Sweigard JA: Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. The Plant Cell Online 1999, 11:2013-2030.
  • [39]Preininger AM, Hamm HE: G protein signaling: insights from new structures. Sci STKE 2004, 2004:re3.
  • [40]Svoboda P, Teisinger J, Novotny J, Bourova L, Drmota T, Hejnova L, Moravcova Z, Lisy V, Rudajev V, Stohr J, Vokurkova A, Svandova I, Durchankova D: Biochemistry of transmembrane signaling mediated by trimeric G proteins. Physiol Res 2004, 53(Suppl 1):S141-S152.
  • [41]Yu HY, Seo JA, Kim JE, Han KH, Shim WB, Yun SH, Lee YW: Functional analyses of heterotrimeric G protein G alpha and G beta subunits in Gibberella zeae. Microbiology 2008, 154:392-401.
  • [42]Chen RE, Thorner J: Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 2007, 1773:1311-1340.
  • [43]Xu JR: Map kinases in fungal pathogens. Fungal Genet Biol 2000, 31:137-152.
  • [44]Pierce KL, Premont RT, Lefkowitz RJ: Seven-transmembrane receptors. Nat Rev Mol Cell Biol 2002, 3:639-650.
  • [45]Xu J-R, Hamer JE: MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 1996, 10:2696-2706.
  • [46]Oide S, Liu J, Yun SH, Wu D, Michev A, Choi MY, Horwitz BA, Turgeon BG: Histidine kinase two-component response regulator proteins regulate reproductive development, virulence, and stress responses of the fungal cereal pathogens Cochliobolus heterostrophus and Gibberella zeae. Eukaryot Cell 2010, 9:1867-1880.
  • [47]Ochiai N, Tokai T, Nishiuchi T, Takahashi-Ando N, Fujimura M, Kimura M: Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem Biophys Res Commun 2007, 363:639-644.
  • [48]Torosantucci A, Chiani P, De Bernardis F, Cassone A, Calera JA, Calderone R: Deletion of the two-component histidine kinase gene (CHK1) of Candida albicans contributes to enhanced growth inhibition and killing by human neutrophils in vitro. Infect Immun 2002, 70:985-987.
  • [49]Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM, Dekker HL, de Koster CG, Cornelissen BJ: A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 2004, 53:1373-1383.
  • [50]Lauge R, Goodwin PH, de Wit PJ, Joosten MH: Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants. Plant J 2000, 23:735-745.
  • [51]Westerink N, Brandwagt BF, de Wit PJ, Joosten MH: Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E ) by secretion of a stable avr4E isoform. Mol Microbiol 2004, 54:533-545.
  • [52]van den Burg HA, Westerink N, Francoijs KJ, Roth R, Woestenenk E, Boeren S, de Wit PJ, Joosten MH, Vervoort J: Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J Biol Chem 2003, 278:27340-27346.
  • [53]van den Burg HA, Spronk CA, Boeren S, Kennedy MA, Vissers JP, Vuister GW, de Wit PJ, Vervoort J: Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions: the chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J Biol Chem 2004, 279:16786-16796.
  • [54]Stephenson SA, Hatfield J, Rusu AG, Maclean DJ, Manners JM: CgDN3: an essential pathogenicity gene of colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol Plant Microbe Interact 2000, 13:929-941.
  • [55]Marx F: Small, basic antifungal proteins secreted from filamentous ascomycetes: a comparative study regarding expression, structure, function and potential application. Appl Microbiol Biotechnol 2004, 65:133-142.
  • [56]Mygind PH, Fischer RL, Schnorr KM, Hansen MT, Sönksen CP, Ludvigsen S, Raventós D, Buskov S, Christensen B, De Maria L: Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 2005, 437:975-980.
  • [57]Marcet-Houben M, Ballester AR, de la Fuente B, Harries E, Marcos JF, Gonzalez-Candelas L, Gabaldon T: Genome sequence of the necrotrophic fungus Penicillium digitatum, the main postharvest pathogen of citrus. BMC Genomics 2012, 13:646.
  • [58]De Wit PJ, Mehrabi R, Van den Burg HA, Stergiopoulos I: Fungal effector proteins: past, present and future. Mol Plant Pathol 2009, 10:735-747.
  • [59]de Jonge R, Thomma BP: Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 2009, 17:151-157.
  • [60]Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, Stulemeijer IJ, van den Berg GC, Borras-Hidalgo O, Dekker HL, de Koster CG, de Wit PJ, Joosten MH, Thomma BP: The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 2008, 69:119-136.
  • [61]Muller O, Schreier PH, Uhrig JF: Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 2008, 279:27-39.
  • [62]Kim S, Ahn IP, Rho HS, Lee YH: MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol Microbiol 2005, 57:1224-1237.
  • [63]Coppin E, Silar P: Identification of PaPKS1, a polyketide synthase involved in melanin formation and its use as a genetic tool in Podospora anserina. Mycol Res 2007, 111:901-908.
  • [64]Thompson JE, Fahnestock S, Farrall L, Liao DI, Valent B, Jordan DB: The second naphthol reductase of fungal melanin biosynthesis in Magnaporthe grisea: tetrahydroxynaphthalene reductase. J Biol Chem 2000, 275:34867-34872.
  • [65]Keller NP, Hohn TM: Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 1997, 21:17-29.
  • [66]Fox EM, Gardiner DM, Keller NP, Howlett BJ: A Zn(II)2Cys6 DNA binding protein regulates the sirodesmin PL biosynthetic gene cluster in Leptosphaeria maculans. Fungal Genet Biol 2008, 45:671-682.
  • [67]Chen H, Lee MH, Daub ME, Chung KR: Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol 2007, 64:755-770.
  • [68]Schell MA: Control of Virulence and Pathogenicity Genes of Ralstonia Solanacearum by an Elaborate Sensory Network. Annu Rev Phytopathol 2000, 38:263-292.
  • [69]Bolker M: Ustilago maydis–a valuable model system for the study of fungal dimorphism and virulence. Microbiology 2001, 147:1395-1401.
  • [70]Stergiopoulos I, de Wit PJ: Fungal effector proteins. Annu Rev Phytopathol 2009, 47:233-263.
  • [71]Houterman PM, Cornelissen BJ, Rep M: Suppression of plant resistance gene-based immunity by a fungal effector. Plos Pathog 2008, 4:e1000061.
  • [72]Leonard G, Richards TA: Genome-scale comparative analysis of gene fusions, gene fissions, and the fungal tree of life. Proc Natl Acad Sci U S A 2012, 109:21402-21407.
  • [73]Feschotte C: Transposable elements and the evolution of regulatory networks. Nat Rev Genet 2008, 9:397-405.
  • [74]Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D'Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M: Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438:1105-1115.
  • [75]Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK: Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 2011, 12:R40.
  • [76]Clarkson JP, Staveley J, Phelps K, Young CS, Whipps JM: Ascospore release and survival in Sclerotinia sclerotiorum. Mycol Res 2003, 107:213-222.
  • [77]Schafer W: Molecular mechanisms of fungal pathogenicity to plants. Annu Rev Phytopathol 1994, 32:461-477.
  • [78]Gao JX, Liu T, Chen J: Insertional mutagenesis and cloning of the gene required for the biosynthesis of the non-host-specific toxin in Cochliobolus lunatus that causes maize leaf spot. Phytopathology 2014, 104:332-339.
  • [79]Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J: SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967.
  • [80]Stanke M, Tzvetkova A, Morgenstern B: AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol 2006, 7(Suppl 1):S11. 11–18
  • [81]Server R http://www.repeatmasker.org/ webcite
  • [82]Nielsen H, Engelbrecht J, Brunak S, von Heijne G: Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997, 10:1-6.
  • [83]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
  • [84]Chen Y, Yu P, Luo J, Jiang Y: Secreted protein prediction system combining CJ-SPHMM, TMHMM, and PSORT. Mamm Genome 2003, 14:859-865.
  • [85]Eisenhaber B, Bork P, Eisenhaber F: Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng 1998, 11:1155-1161.
  • [86]Graham MA, Silverstein KA, Cannon SB, VandenBosch KA: Computational identification and characterization of novel genes from legumes. Plant Physiol 2004, 135:1179-1197.
  • [87]Ostlund G, Schmitt T, Forslund K, Kostler T, Messina DN, Roopra S, Frings O, Sonnhammer EL: InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res 2010, 38:D196-D203.
  • [88]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
  • [89]Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9:299-306.
  • [90]Taylor JW, Berbee ML: Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 2006, 98:838-849.
  • [91]Lucking R, Huhndorf S, Pfister DH, Plata ER, Lumbsch HT: Fungi evolved right on track. Mycologia 2009, 101:810-822.
  • [92]Schomburg D, Schomburg I: Enzyme databases. Methods Mol Biol 2010, 609:113-128.
  • [93]Saier MH Jr, Tran CV, Barabote RD: TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 2006, 34:D181-D186.
  • [94]Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND: SMURF: Genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 2010, 47:736-741.
  • [95]Anand S, Prasad MV, Yadav G, Kumar N, Shehara J, Ansari MZ, Mohanty D: SBSPKS: structure based sequence analysis of polyketide synthases. Nucleic Acids Res 2010, 38:W487-W496.
  • [96]Scott-Craig JS, Panaccione DG, Pocard JA, Walton JD: The cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungus Cochliobolus carbonum is encoded by a 15.7-kilobase open reading frame. J Biol Chem 1992, 267:26044-26049.
  • [97]Haese A, Schubert M, Herrmann M, Zocher R: Molecular characterization of the enniatin synthetase gene encoding a multifunctional enzyme catalysing N-methyldepsipeptide formation in Fusarium scirpi. Mol Microbiol 1993, 7:905-914.
  • [98]Weber G, Schorgendorfer K, Schneider-Scherzer E, Leitner E: The peptide synthetase catalyzing cyclosporine production in Tolypocladium niveum is encoded by a giant 45.8-kilobase open reading frame. Curr Genet 1994, 26:120-125.
  • [99]Gardiner DM, Howlett BJ: Bioinformatic and expression analysis of the putative gliotoxin biosynthetic gene cluster of Aspergillus fumigatus. FEMS Microbiol Lett 2005, 248:241-248.
  • [100]Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K: Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 2000, 13:742-753.
  • [101]Benjamini Y, Yekutieli D: The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001, 29:1165-1188.
  文献评价指标  
  下载次数:34次 浏览次数:3次