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Fungal cytochrome P450 database

Jongsun Park123, Seungmin Lee1, Jaeyoung Choi12, Kyohun Ahn1, Bongsoo Park4, Jaejin Park12, Seogchan Kang4* and Yong-Hwan Lee1235*

Author Affiliations

1 Fungal Bioinformatics Laboratory, Seoul National University, Seoul 151-921, Korea

2 Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Korea

3 Center for Fungal Genetic Resource, Seoul National University, Seoul 151-921, Korea

4 Department of Plant Pathology, The Pennsylvania State University, University Park, PA 16802, USA

5 Center for Agricultural Biomaterials, Seoul National University, Seoul 151-921, Korea

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BMC Genomics 2008, 9:402  doi:10.1186/1471-2164-9-402

The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2164/9/402


Received:3 April 2008
Accepted:28 August 2008
Published:28 August 2008

© 2008 Park et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

Cytochrome P450 enzymes play critical roles in fungal biology and ecology. To support studies on the roles and evolution of cytochrome P450 enzymes in fungi based on rapidly accumulating genome sequences from diverse fungal species, an efficient bioinformatics platform specialized for this super family of proteins is highly desirable.

Results

The Fungal Cytochrome P450 Database (FCPD) archives genes encoding P450s in the genomes of 66 fungal and 4 oomycete species (4,538 in total) and supports analyses of their sequences, chromosomal distribution pattern, and evolutionary histories and relationships. The archived P450s were classified into 16 classes based on InterPro terms and clustered into 141 groups using tribe-MCL. The proportion of P450s in the total proteome and class distribution in individual species exhibited certain taxon-specific characteristics.

Conclusion

The FCPD will facilitate systematic identification and multifaceted analyses of P450s at multiple taxon levels via the web. All data and functions are available at the web site http://p450.riceblast.snu.ac.kr/ webcite.

Background

Cytochrome P450 is the collective name for a super family of heme-containing monooxygenases. P450 enzymes not only participate in the production of diverse metabolites but also play critical roles in organism's adaptation to specific ecological and/or nutritional niches by modifying potentially harmful environmental chemicals. In fungi, P450 enzymes have contributed to exploration of and adaptation to diverse ecological niches [1,2].

Rapidly accumulating genome sequences from diverse fungal species, including more than 80 species with more currently being sequenced [3], offer opportunities to study the genetic and evolutionary mechanisms underpinning different fungal life styles at the genome level [4-7]. To support such studies with the focus on cytochrome P450s, we constructed a new platform named as the Fungal Cytochrome P450 Database (FCPD), which archives P450s in most sequenced fungal and oomycetes species and allows comparison of the archived data with previously published datasets, such as the Cytochrome P450 Engineering Database [8], a manually curated P450 database at http://drnelson.utmem.edu/CytochromeP450.html webcite (referred as the Nelson's P450 database herein), and P450 datasets derived from extensive phylogenetic analyses of selected fungal taxon groups [9,10]. The FCPD also supports multifaceted analyses of P450s using various web-based bioinformatics tools supported by the Comparative Fungal Genomics Platform (CFGP; http://cfgp.snu.ac.kr/ webcite) [3]. The FCPD, in combination with high-throughput experimental approaches, will advance our understanding of the roles and evolution of P450s.

Construction and content

Pipeline for identifying and classifying fungal P450s

To identify P450 proteins from genome sequences, standardized genome databases managed by CFGP (http://cfgp.snu.ac.kr/ webcite) [3] and annotated information of each ORF by InterPro scan [11] were used. The pipeline for the identification and archiving of P450s consists of four steps (Figure 1). In the first step, all proteins carrying one or more of 16 InterPro terms associated with cytochrome P450 were identified and classified according to associated InterPro terms. Domain information of P450 proteins was also retrieved from the InterPro scan results. To filter out potential false positives (i.e., those carrying a very short domain), the minimum length for IPR001128 (Cytochrome P450) was set at 25 amino acid (aa). Since some of these potential false positives might indeed belong to novel P450s, rather than discarding them, they were labelled as "questionable P450" in FCPD. Secondly, using the collection of putative P450 sequences, cache tables, especially for results from several statistical analyses, were created to speed up data retrieval. BLAST datasets were also generated to support BLAST searches of P450s via the FCPD web site and cluster analysis. Thirdly, class-specific and cluster-specific neighbour joining phylogenetic trees that show relationships among P450s within individual phylogenetic groups (e.g., Figure 2) were constructed (bootstrapped with 2,000 or 10,000 repeats), which are displayed by Phyloviewer (http://www.phyloviewer.org/ webcite; Park et al., unpublished) on the FCPD web site. Using the BLAST dataset, fungal P450s were clustered using tribe-MCL [12], and compared with the data in three publicly available databases: the Cytochrome P450 Engineering database [8], the Nelson's P450 database, and a set of phylogenetically analyzed P450s in multiple fungal species [9,10]. Results from this comparison were stored in the FCPD for viewing via the FCPD web site. For species with multiple versions of genome annotation, data generated using different versions were linked to provide the history of annotation.

thumbnailFigure 1. Data retrieval pipeline in FCPD. Four-steps involved in identifying and classifying fungal P450s in FCPD are presented as a flowchart.

thumbnailFigure 2. Phylogenetic analysis of E-class P450, group IV. A bootstrapped phylogenetic tree was constructed using Phyloviewer http://www.phyloviewer.org/ webcite. Four different clades in the tree are indicated as blue lines.

As the fourth step, using BLAST all P450s archived in FCPD were matched to the corresponding families in the Nelson's P450s database, which contains manually curated data based on the P450 International Nomenclature [13,14]. For each P450, the assigned family name was considered highly confident ('> = 44% identity' in the site), when the degree of aa sequence identity was 44% or higher. When no match at that level could be found in the Nelson's P450 database, the best hit in BLAST search was chosen to assign the family name and labelled as low confidence ('< 44% identity' in the site). Considering that P450s are very diverse and that the Nelson's P450 database covers less fungal species than FCPD, it is highly likely that some of the P450s with low confidence represent novel families that have yet to be registered in the Nelson's P450 database (Figure 3). This annotation result was stored in FCPD and can be viewed through the FCPD web site.

thumbnailFigure 3. Confidence levels in the family assignment of individual P450s in different fungal phyla. Five fungal phyla and oomycetes are shown below the X-axis. The Y-axis indicates the proportion of P450s classified with high confidence or low confidence. The numbers on the top of each bar indicate the number of P450 in each class.

In the genomes of 66 fungal and 4 oomycete species, 4,538 putative P450 genes were identified. Although oomycete species belong to the kingdom Stramenophila and show closer phylogenetic relationships to brown algae and diatoms [15], they have been traditionally studied by mycologists due to their morphological similarities with true fungi, and their P450s were included in FCPD.

Evaluation of the accuracy of annotation via the automated pipeline in FCPD by comparing with data archived in the manually curated Nelson's P450s database

The automated annotation process of P450 in FCPD may result in some false-positives and negatives. To evaluate its accuracy, all 886 P450s identified using the pipeline in 12 fungal species were compared with manually curated data in the Nelson's P450 database. The positive predictive value (PPV; the proportion of the predicted P450s in FCPD to P450s that have been archived in the Nelson's P450 database) was 0.894 (792 out of 886 P450s in FCPD were matched to P450s in Nelson's P450 database). Some putative false positives in FCPD appeared to be pseudo genes. Another factor that contributed to the discrepancy between the two sources is that some data in the Nelson's P450 database were based on a version earlier than what was used for FCPD (e.g., version 4 of Magnaporthe oryzae genome having been used for the former, while FCPD being based on version 5). Gene prediction models employed to analyze different versions might have had different predictions. In contrast, 1,032 out of 1,034 fungal P450s curated in the Nelson's P450 database were identified as P450 by the FCPD pipeline (99.8% sensitivity), supporting the reliability of the FCPD pipeline. The two P450s not identified as P450 by FCPD came from Phytophthora sojae and P. ramorum, respectively and corresponded to truncated sequences (34 and 89 aa, respectively, and were labelled as fragment of P450 in the Nelson's P450 database). Detailed analyses of the underlying reasons for the inconsistency between the two sources will help us improve the automated annotation pipeline of FCPD.

Notable features in fungal P450s in the taxonomic context

The numbers of P450s in individual species exhibited certain taxon-specific features (Table 1). Within the phylum Ascomycota, members of the subphylum Pezizomycotina typically carry around 100 P450s with the exception of four species (Coccidioides immitis, Histoplasma capsulatum, Uncinocarpus reessi and Neurospora crassa) that only carry 22 to 46 P450s. The proportion of P450s in the total proteome in the subphylum Pezizomycotina (0.63% in average) is twice as large as that of vertebrates (0.33%) but is less than that of plant species (0.82%). In contrast to the Pezizomycotina, species in the subphyla Saccharomycotina and Taphrinomycotina have a very few P450s (e.g., only 3 P450s in Saccharomyces cerevisiae and 2 P450s in Schizosaccharomyces pombe). Within the phylum Basidiomycota, Postia placenta carries 353 P450s (2.06% of the total proteome), while strains of Cryptococcus neoformans have 5 to 6 P450s (0.08% ~ 0.09% of the total proteome). Interestingly, Encephalitozoon cuniculi and Antonospora locustae, species in the phylum Mycosporodia, do not appear to have any P450s, probably reflecting their obligate, intracellular parasitic life style. Four oomycete species, including Phytophthora infestans, P. sojae, P. ramorum and Hyaloperonospora parasitica, also carry relatively low numbers of P450s (9 to 35 and 0.06 to 0.2% of the total proteome).

Table 1. P450s in the fungal kingdom

Three P450 classes defined by InterPro terms, including group I in E-class P450, group IV in E-class P450 and Cytochrome P450, contain 3,866 out of 4,538 (85.2%) fungal/oomycete P450s. Only 8 out of 16 classes have fungal/oomycete P450s. Among other classes, P450s belonging to the pisatin demethylase (PDA)-like class are present only in the subphylum Pezizomycotina (phylum Ascomycota) and in the phylum Basidiomycota, suggesting the possibility that PDA-related P450s might have emerged twice independently during fungal evolution.

Distribution patterns of fungal P450s among clusters and clans

When fungal/oomycetes P450s were combined with 5,447 P450s extracted from 40 other eukaryotic and prokaryotic species and clustered using tribe-MCL (with inflation factor of 5.0; the most strict condition for clustering based on sequence similarity), 141 clusters were identified. Among these, 74 clusters contain only fungal P450s, suggesting that many fungal P450s have a configuration unique to fungi. The taxonomic origins of fungal P450s in the 26 clusters that contain more than 10 fungal P450s were analyzed (Figure 4). P450s in the phylum Ascomycota are dominant because of abundant genome sequences from members of this group. Cluster 19.1 is dominated by P450s encoded members of the subphylum Agricomycotina (phylum Basidiomycota) and Clusters 3.1 and 4.1 are Zygomycota-specific. Cluster 8.1 contains 101 out of 106 oomycetes P450s (95.3%). Nine P450s encoded by Batrachochytrium dendrobatidis, the only sequenced species in the phylum Chitridiomycota, are scattered to 8 clusters, suggesting that they likely have distinct functions and evolutionary origins. Sequences of additional genomes are needed to further investigate the evolution of P450s in this phylum.

thumbnailFigure 4. Distribution pattern of 25 major P450 clusters. Cluster names are shown below the X-axis, and the names of fungal phyla are shown at the y-axis. Non-fungi indicate P450s in plants and animals. The Z-axis indicates numbers of P450s in individual groups.

To compare the relationship between P450 clusters and clans, 115 clans identified in four species (including 375 P450s in total), including M. oryzae, Fusarium graminearum, N. crassa and Aspergillus nidulans [9], were collected and analyzed. Interestingly, only 4 out of 115 clans (6.1%) are scattered to more than one P450 clusters. For example, P450s included in clan FF59 were distributed to four P450 clusters (Clusters 4.1, 8.1, 31.1 and 73.1). However, each of the remaining clans belongs to one specific cluster, supporting a good correlation between two classification systems.

Assignment of P450s archived in FCPD to individual P450 families based on the international nomenclature scheme

The Nelson's P450 database classified 1,016 (98.26%) out of 1,034 fungal/oomycete P450s into 276 P450 families. Most P450s in FCPD (4,446 out of 4,538; 97.97%) were matched to corresponding families in the Nelson's P450 database (see above). 2,978 P450s (66.98%) were tagged to specific families with high confidence, while 1,468 P450s (33.02%) were assigned to families with low confidence (Figure 3). In the phylum Ascomycota, the assignment of 1,007 P450s (29.24%) was supported with low confidence. In the phylum Basidiomycota, the proportion was 44.56% (352 out of 790 P450s). More than 90% P450s (104 out of 110) in the phylum Zygomycota and 100% P450s in the phylum Chytridiomycota did not closely match with any families in the Nelson's P450 database. These results strongly suggest that new fungal families need to be defined.

Update of FCPD

Considering the rapid increase in fungal genome sequencing [3], timely update of FCPD is critical to present the latest information to users. The BLAST dataset, bootstrapped phylogenetic trees specific for individual classes and clusters, results from clustering analysis and annotation of P450s based on the international P450 nomenclature will be updated automatically once new P450s have been identified via the identification pipeline. Since the identification of P450s depends on the accuracy of a gene model employed to annotate the genome, as a new version of previously released genome sequences becomes available, FCPD will be updated with the data based on earlier versions being tagged as an "Old putative P450 sequences." Links between new and old versions will be provided.

Utilities and discussion

Accessing lists and sequences of fungal P450s based on species of origin and taxonomic position

To support efficient search and retrieval of sequences of P450s, data archived in FCPD can be browsed and searched through multiple methods. Upon selecting a species of interest, general information about the species and a list of its P450s can be viewed. From this list, any P450 sequences can be stored in a personal data repository called the Favorite, in which six useful bioinformatic tools can be utilized to analyze the stored data. The Favorite is a virtual space for storing sequences archived in CFGP [3]. A list of P450s belonging to each class defined by InterPro terms or cluster can also be displayed. Taxonomical distribution of P450s, resulted from comparison with data in the Cytochrome P450 Engineering Database (CYP450ED) [8] and two previous studies on fungal P450s [9,10], can be browsed. P450 sequences in FCPD can also be searched by gene name.

BLAST search of all or subsets of P450s

In FCPD, five different databases of P450s, including all P450s (including those from plants and animals), all fungal/oomycete P450s and three fungal phylum-specific databases of P450s, can be searched using BLAST. Additionally, fungal P450 sequences in the Nelson's P450 database can also be searched. From BLAST search results, sequences of individual P450s can be saved in the Favorite for subsequent analyses.

Analyses of P450s using tools in the Comparative Fungal Genomics Platform

Many on-line databases that archive gene families allow downloading of all or part of data to user's computer but often do not provide data analysis tools via the database site. Consequently, to conduct desired analyses, users may have to visit multiple websites to access desired data analysis tools and/or install programs in personal computer. In FCPD, sequences of one or more fungal P450s can be selected by clicking check boxes next to each P450 and stored them into the Favorite. The Object Browser in FCPD supports the transfer of chosen sequences from the Favorite to CFGP in which the data can be analyzed using six useful bioinformatics tools [3]. These tools include BLAST, ClustalW, InterPro Scan, PSort, SignalP 3.0 and BLASTMatrix. The BLASTMatrix is a novel tool for surveying the presence of genes homologous to a query in multiple species simultaneously. Once any new analysis tool has been added to CFGP, users of FCPD will be able to use the tool immediately.

Visualization of chromosomal distribution patterns of P450s via SNUGB

To aid for the visualization of chromosomal distribution pattern of P450s for species with available physical chromosome map information, FCPD provides a diagram illustrating position of P450s on individual chromosomes (Figure 5), which are drawn by a newly developed genome browser called SNUGB (http://genomebrowser.snu.ac.kr/ webcite; Jung et al., submitted). Currently, chromosomal maps of 13 fungal species are available.

thumbnailFigure 5. Chromosomal distribution of P450s on the genome of Aspergillus fumigatus. On eight chromosomes of A. fumigatus, P450s identified in FCPD were displayed as red bars with their names. When mouse cursor moves on each name, a yellowish label will appear, which provides link to information page of chosen P450. This display is supported by SNUGB http://genomebrowser.snu.ac.kr/ webcite.

Conclusion

To our knowledge, FCPD is the most comprehensive database that archives and classifies P450s in publicly available fungal and oomycete genomes (65 fungal and 4 oomycete species) through a systematic identification pipeline. The reliability of the pipeline in retrieving fungal P450 sequences was evaluated by comparing resulting data with other established datasets, and the data from these sources were archived in FCPD for comparison and search. The pipeline also links annotated information from different versions of fungal genome sequences. Numbers of P450s in individual fungal species vary widely, and fungal specific P450 clusters were found via clustering analysis. In combination with other bioinformatic platforms, such as CFGP http://cfgp.snu.ac.kr/ webcite[3], Phyloviewer (http://www.phyloviewer.org/ webcite; Park et al., unpublished), and SNUGB (http://genomebrowser.snu.ac.kr/ webcite; Jung et al., submitted), FCPD provides a highly integrated platform supporting systematic studies on fungal P450s.

Availability and requirements

All data described in this paper can be freely browsed and downloaded through the FCPD web site at http://p450.riceblast.snu.ac.kr/ webcite.

Authors' contributions

JSP, SK and Y–HL designed FCPD and wrote the manuscript. SL, KA, JC and BP developed the web site of FCPD. JSP, JC and BP developed the functionalities of FCPD supported by CFGP, Phyloviewer and SNUGB. JJP designed the FCPD web site.

Acknowledgements

This research was partially supported by grants from Crop Functional Genomics Center (CG1141) and a grant from Biogreen21 Project (20080401034044) funded by the Rural Development Administration to Y.H.L. A USDA-NRI grant to S.K. (2008-55605-18773) also supported this work. J.P. thanks to graduate fellowship provided by the Ministry of Education through the Brain Korea 21 Project.

References

  1. Maloney AP, VanEtten HD: A gene from the fungal plant pathogen Nectria haematococca that encodes the phytoalexin-detoxifying enzyme pisatin demethylase defines a new cytochrome P450 family.

    Mol Gen Genet 1994, 243(5):506-514. PubMed Abstract | Publisher Full Text OpenURL

  2. Brink HM, van Gorcom RFM, Hondel CAMJJ, Punt PJ: Cytochrome P450 Enzyme Systems in Fungi.

    Fungal Genet Biol 1998, 23(1):1-17. PubMed Abstract | Publisher Full Text OpenURL

  3. Park J, Park B, Jung K, Jang S, Yu K, Choi J, Kong S, Park J, Kim S, Kim H, Kim S, Kim JF, Blair JE, Lee K, Kang S, Lee YH: CFGP: a web-based, comparative fungal genomics platform.

    Nucleic Acids Res 2008, 36:D562-571. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  4. Park J, Kim H, Kim S, Kong S, Park J, Kim S, Han H, Park B, Jung K, Lee Y-H-: A comparative genome-wide analysis of GATA transcription factors in fungi.

    Genomics & Informatics 2006, 4(4):147-160. Publisher Full Text OpenURL

  5. Park J, Park J, Jang S, Kim S, Kong S, Choi J, Ahn K, Kim J, Lee S, Kim S, Park B, Jung K, Kim S, Kang S, Lee YH: FTFD: An Informatics Pipeline Supporting Phylogenomic Analysis of Fungal Transcription Factors.

    Bioinformatics 2008, 24(7):1024-1025. PubMed Abstract | Publisher Full Text OpenURL

  6. Cornell MJ, Alam I, Soanes DM, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Talbot NJ, Oliver SG: Comparative genome analysis across a kingdom of eukaryotic organisms: specialization and diversification in the fungi.

    Genome Res 2007, 17(12):1809-1822. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  7. Fitzpatrick DA, Logue ME, Stajich JE, Butler G: A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis.

    BMC Evol Biol 2006, 6:99. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  8. Fischer M, Knoll M, Sirim D, Wagner F, Funke S, Pleiss J: The Cytochrome P450 Engineering Database: a navigation and prediction tool for the cytochrome P450 protein family.

    Bioinformatics 2007, 23(15):2015-2017. PubMed Abstract | Publisher Full Text OpenURL

  9. Deng J, Carbone I, Dean R: The evolutionary history of Cytochrome P450 genes in four filamentous Ascomycetes.

    BMC Evol Biol 2007, 7(1):30. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  10. Doddapaneni H, Chakraborty R, Yadav JS: Genome-wide structural and evolutionary analysis of the P450 monooxygenase genes (P450ome) in the white rot fungus Phanerochaete chrysosporium: evidence for gene duplications and extensive gene clustering.

    BMC Genomics 2005, 6:92. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  11. Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bradley P, Bork P, Bucher P, Cerutti L, Copley R, Courcelle E, Das U, Durbin R, Fleischmann W, Gough J, Haft D, Harte N, Hulo N, Kahn D, Kanapin A, Krestyaninova M, Lonsdale D, Lopez R, Letunic I, Madera M, Maslen J, McDowall J, Mitchell A, Nikolskaya AN: InterPro, progress and status in 2005.

    Nucleic Acids Res 2005, 33:D201-205. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  12. Enright AJ, Van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families.

    Nucleic Acids Res 2002, 30(7):1575-1584. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  13. Nelson DR: Cytochrome P450 and the individuality of species.

    Arch Biochem Biophys 1999, 369(1):1-10. PubMed Abstract | Publisher Full Text OpenURL

  14. Nelson DR, Koymans L, Kamataki T, Stegeman JJ, Feyereisen R, Waxman DJ, Waterman MR, Gotoh O, Coon MJ, Estabrook RW, Gunsalus IC, Nebert DW: P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature.

    Pharmacogenetics 1996, 6(1):1-42. PubMed Abstract | Publisher Full Text OpenURL

  15. Wortman JR, Fedorova N, Crabtree J, Joardar V, Maiti R, Haas BJ, Amedeo P, Lee E, Angiuoli SV, Jiang B, Anderson MJ, Denning DW, White OR, Nierman WC: Whole genome comparison of the A. fumigatus family.

    Med Mycol 2006, 44(6):3-7. Publisher Full Text OpenURL

  16. 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: Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus.

    PLoS Genet 2008, 4(4):e1000046. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  17. Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, Dean RA, Bhatnagar D, Cleveland TE, Machida M, Yu J: Whole genome comparison of A. flavus and A. oryzae.

    Med Mycol 2006, 44(6):9-11. Publisher Full Text OpenURL

  18. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, Garcia JL, Garcia MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S: Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus.

    Nature 2005, 438(7071):1151-1156. PubMed Abstract | Publisher Full Text OpenURL

  19. 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(7071):1105-1115. PubMed Abstract | Publisher Full Text OpenURL

  20. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d'Enfert C, Geysens S, Goosen C, Groot GS: Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88.

    Nat Biotechnol 2007, 25(2):221-231. PubMed Abstract | Publisher Full Text OpenURL

  21. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R: Genome sequencing and analysis of Aspergillus oryzae.

    Nature 2005, 438(7071):1157-1161. PubMed Abstract | Publisher Full Text OpenURL

  22. 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: The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization.

    Science 2007, 317(5843):1400-1402. PubMed Abstract | Publisher Full Text OpenURL

  23. 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(7036):980-986. PubMed Abstract | Publisher Full Text OpenURL

  24. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ: Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism.

    Microbiol Mol Biol Rev 2004, 68(1):1-108.

    table of contents

    PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  25. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Segurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Dequard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarre B: The genome sequence of the model ascomycete fungus Podospora anserina.

    Genome Biol 2008, 9(5):R77. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  26. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A: Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina).

    Nat Biotechnol 2008, 26(5):553-560. PubMed Abstract | Publisher Full Text OpenURL

  27. Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SF, McDonald BA, Oliver RP: Dothideomycete Plant Interactions Illuminated by Genome Sequencing and EST Analysis of the Wheat Pathogen Stagonospora nodorum.

    Plant Cell 2007, 19(11):3347-3368. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  28. Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, Magee BB, Newport G, Thorstenson YR, Agabian N, Magee PT, Davis RW, Scherer S: The diploid genome sequence of Candida albicans.

    Proc Natl Acad Sci USA 2004, 101(19):7329-7334. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  29. van het Hoog M, Rast TJ, Martchenko M, Grindle S, Dignard D, Hogues H, Cuomo C, Berriman M, Scherer S, Magee BB, Whiteway M, Chibana H, Nantel A, Magee PT: Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes.

    Genome Biol 2007, 8(4):R52. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  30. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuveglise C, Talla E, Goffard N, Frangeul L, Aigle M, Anthouard V, Babour A, Barbe V, Barnay S, Blanchin S, Beckerich JM, Beyne E, Bleykasten C, Boisrame A, Boyer J, Cattolico L, Confanioleri F, De Daruvar A, Despons L, Fabre E, Fairhead C, Ferry-Dumazet H: Genome evolution in yeasts.

    Nature 2004, 430(6995):35-44. PubMed Abstract | Publisher Full Text OpenURL

  31. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pohlmann R, Luedi P, Choi S, Wing RA, Flavier A, Gaffney TD, Philippsen P: The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome.

    Science 2004, 304(5668):304-307. PubMed Abstract | Publisher Full Text OpenURL

  32. Scannell DR, Frank AC, Conant GC, Byrne KP, Woolfit M, Wolfe KH: Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication.

    Proc Natl Acad Sci USA 2007, 104(20):8397-8402. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  33. Kellis M, Birren BW, Lander ES: Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae.

    Nature 2004, 428(6983):617-624. PubMed Abstract | Publisher Full Text OpenURL

  34. Jeffries TW, Grigoriev IV, Grimwood J, Laplaza JM, Aerts A, Salamov A, Schmutz J, Lindquist E, Dehal P, Shapiro H, Jin YS, Passoth V, Richardson PM: Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis.

    Nat Biotechnol 2007, 25(3):319-326. PubMed Abstract | Publisher Full Text OpenURL

  35. Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, Majors J, Waterston R, Cohen BA, Johnston M: Finding functional features in Saccharomyces genomes by phylogenetic footprinting.

    Science 2003, 301(5629):71-76. PubMed Abstract | Publisher Full Text OpenURL

  36. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG: Life with 6000 genes.

    Science 1996, 274(5287):546-567. PubMed Abstract | Publisher Full Text OpenURL

  37. Gu Z, David L, Petrov D, Jones T, Davis RW, Steinmetz LM: Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae.

    Proc Natl Acad Sci USA 2005, 102(4):1092-1097. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  38. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S, Basham D, Bowman S, Brooks K, Brown D, Brown S, Chillingworth T, Churcher C, Collins M, Connor R, Cronin A, Davis P, Feltwell T, Fraser A, Gentles S, Goble A, Hamlin N, Harris D, Hidalgo J, Hodgson G, Holroyd S: The genome sequence of Schizosaccharomyces pombe.

    Nature 2002, 415(6874):871-880. PubMed Abstract | Publisher Full Text OpenURL

  39. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D: Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78.

    Nat Biotechnol 2004, 22(6):695-700. PubMed Abstract | Publisher Full Text OpenURL

  40. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buee M, Brokstein P, Canback B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I: The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis.

    Nature 2008, 452(7183):88-92. PubMed Abstract | Publisher Full Text OpenURL

  41. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA, Allen JE, Bosdet IE, Brent MR, Chiu R, Doering TL, Donlin MJ, D'Souza CA, Fox DS, Grinberg V, Fu J, Fukushima M, Haas BJ, Huang JC, Janbon G, Jones SJ, Koo HL, Krzywinski MI, Kwon-Chung JK, Lengeler KB, Maiti R: The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans.

    Science 2005, 307(5713):1321-1324. PubMed Abstract | Publisher Full Text OpenURL

  42. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, Deangelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL Jr: Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens.

    Proc Natl Acad Sci USA 2007, 104(47):18730-18735. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  43. Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L: Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis.

    Nature 2006, 444(7115):97-101. PubMed Abstract | Publisher Full Text OpenURL

  44. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP: Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.

    Nature 2001, 414(6862):450-453. PubMed Abstract | Publisher Full Text OpenURL

  45. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CM, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee MK, McDonald WH, Medina M: Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis.

    Science 2006, 313(5791):1261-1266. PubMed Abstract | Publisher Full Text OpenURL

  46. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM: A higher-level phylogenetic classification of the Fungi.

    Mycol Res 2007, 111(Pt 5):509-547. PubMed Abstract | Publisher Full Text OpenURL