1471-2164-9-586 1471-2164 Database <p>SNUGB: a versatile genome browser supporting comparative and functional fungal genomics</p> Jung Kyongyong lulupon0@snu.ac.kr Park Jongsun starflr@snu.ac.kr Choi Jaeyoung amethyst1016@gmail.com Park Bongsoo pbsfree@gmail.com Kim Seungill ksi2204@gmail.com Ahn Kyohun dksrygns00@snu.ac.kr Choi Jaehyuk jaehyuk2@snu.ac.kr Choi Doil doil@snu.ac.kr Kang Seogchan sxk55@psu.edu Lee Yong-Hwan yonglee@snu.ac.kr

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

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

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

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

Department of Plant Science, Seoul National University, Seoul 151-921, Korea

Center for Fungal Pathogenesis, Seoul National University, Seoul 151-921, Korea

 BMC Genomics 1471-2164 2008 9 1 586 http://www.biomedcentral.com/1471-2164/9/586 19055845 10.1186/1471-2164-9-586 15 5 2008 04 12 2008 04 12 2008 2008 Jung 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

Since the full genome sequences of Saccharomyces cerevisiae were released in 1996, genome sequences of over 90 fungal species have become publicly available. The heterogeneous formats of genome sequences archived in different sequencing centers hampered the integration of the data for efficient and comprehensive comparative analyses. The Comparative Fungal Genomics Platform (CFGP) was developed to archive these data via a single standardized format that can support multifaceted and integrated analyses of the data. To facilitate efficient data visualization and utilization within and across species based on the architecture of CFGP and associated databases, a new genome browser was needed.

Results

The Seoul National University Genome Browser (SNUGB) integrates various types of genomic information derived from 98 fungal/oomycete (137 datasets) and 34 plant and animal (38 datasets) species, graphically presents germane features and properties of each genome, and supports comparison between genomes. The SNUGB provides three different forms of the data presentation interface, including diagram, table, and text, and six different display options to support visualization and utilization of the stored information. Information for individual species can be quickly accessed via a new tool named the taxonomy browser. In addition, SNUGB offers four useful data annotation/analysis functions, including 'BLAST annotation.' The modular design of SNUGB makes its adoption to support other comparative genomic platforms easy and facilitates continuous expansion.

Conclusion

The SNUGB serves as a powerful platform supporting comparative and functional genomics within the fungal kingdom and also across other kingdoms. All data and functions are available at the web site http://genomebrowser.snu.ac.kr/.

Background

As the number of sequenced genomes rapidly increases, search and comparison of sequence features within and between species has become an integral part of most biological inquires. To facilitate uses of the sequenced genomes, numerous bioinformatics tools have been developed; among these, genome browser plays an essential role by providing various means for viewing genome sequences and annotated features (e.g., chromosomal position and context of individual genes, protein/nucleotide sequences, structures of exon/intron, and promoters) via graphical and text interfaces. Widely utilized genome browsers include: (i) Ensembl http://www.ensembl.org/, which is specialized for mammalian genomics and comparative genomics 1, (ii) UCSC Genome Browser http://genome.ucsc.edu/, which archives genome sequences of 30 vertebrate and 24 non-vertebrate species 2, (iii) GBrowse http://gmod.org/wiki/Gbrowse, a widely-used component-based genome browser 3, and (iv) Map Viewer http://www.ncbi.nlm.nih.gov/projects/mapview at the National Center for Biotechnology Information (NCBI), which covers a large number of organisms 4. A new genome browser based on the Google map engine, called the X::Map Genome Browser http://xmap.picr.man.ac.uk/5, contains genomes of three mammalian species and is specialized for supporting microarray analyses based on the Affymetrix platform 6.

Since complete S. cerevisiae genome sequences were released in 1996, more than 90 fungal/oomycete species have been sequenced with many additional species being currently sequenced 7. A few sequencing centers, such as the Broad Institute http://www.broad.mit.edu/ and the JGI http://www.jgi.doe.gov/, have sequenced most of the fungal genomes and provide their own genome browsers to support data visualization and utilization. Although they use standardized formats, such as fasta and gff3, for data presentation and distribution, each center uses its own data formats for sequences, annotation data, and other chromosomal information. In addition, some of the sequenced fungal genomes lack certain data, such as exon positions. These problems have hampered the integration and visualization of all available genome sequences via a single genome browser. As a solution for this problem, a group at Duke University http://fungal.genome.duke.edu/ installed an open-source browser called the GBrowse 3 after reannotating genome sequences of 42 fungal species from multiple sequencing centers through the use of their own annotation pipeline consisting of several gene prediction programs; large scale evolutionary analyses were conducted based on the archived genomes, demonstrating the usefulness of unified and standardized data formats 8.

A large number of sequenced fungal genomes have provided opportunities to compare genome sequences and features at multiple taxon levels, revealing potential mechanisms underpinning fungal evolution and biology 89101112131415161718; however, due to the complexity and vast scale of the resulting data, presentation of these data in an easily accessible format is challenging. To overcome this limitation, both the database construction and the pipeline/tools for comparative analyses should be carefully designed. One good example is the e-Fungi project http://www.e-fungi.org.uk/19, which archives genome sequences of 34 fungal and 2 oomycete species and supports various queries via the web interface. Comparative fungal genomics studies have been conducted using e-Fungi 911. Yeast Gene Order Browser (YGOB; http://wolfe.gen.tcd.ie/ygob/) 20 archives genome sequences of the species belonging to the subphylum Saccharomycotina and provides a graphical gene order browser, which helps the dissection of evolutionary history of genome changes during yeast speciation 21. Although these platforms provide useful tools and data, only certain fungal genomes are covered, and the function of user-friendly access to sequence information and graphical presentation of data are limited.

The Comparative Fungal Genomics Platform (CFGP; http://cfgp.snu.ac.kr/) was established to archive all publicly available fungal and oomycete genome sequences using a unified data format and to support multifaceted analyses of the stored data via a newly developed user interface named as Data-driven User Interface 7. Currently, CFGP archives genome sequences of 92 fungal and 6 oomycete species (137 different datasets) and also carries genome sequences of 55 plant, animal and bacterial species (56 datasets). Taking advantage of the data warehouse and functionalities in CFGP, several databases specialized for certain gene families or functional groups have been constructed, one of which is the Fungal Transcription Factor Database (FTFD; http://ftfd.snu.ac.kr/) 22. This database identified and classified all fungal transcription factors and provides a phylogenomic platform supporting analyses of individual transcription factor families 23. In addition, Fungal Cytochrome P450 Database (FCPD; http://p450.riceblast.snu.ac.kr/) 24, Fungal Secretome Database (FSD; http://fsd.snu.ac.kr/; Choi et al., unpublished), Fungal Expression Database (FED; http://fed.snu.ac.kr/; Park et al., unpublished) have been constructed or are currently being constructed. The CFGP was also used to manage high-throughput experimental data and link them to corresponding genes 2526 and to maintain the Phytophthora database http://www.phytophthoradb.org/27.

To support comparative genomics analyses using CFGP and offer tools for versatile data visualization, we newly developed a genome browser named as the Seoul National University Genome Browser (SNUGB; http://genomebrowser.snu.ac.kr/). We chose to develop a new genome browser instead of adopting one of the existing browsers in part because the adoption required conversion of the data archived in CFGP into new formats, and the existing browsers do not support the integration of additional databases, such as the InterPro and customized homologous gene databases available through SNUGB. We also wanted to have a browser based on the architecture of CFGP and associated databases so that we would be able to quickly present updated contents in these resources and seamlessly integrate new tools for data processing, visualization, and/or utilization.

The SNUGB currently covers genome sequences and associated information for 92 fungal and 6 oomycete species (137 datasets), which is the largest among the available fungal genome browser services on the web. These 92 fungal species cover four phyla and one subphylum based on a recently revised fungal taxonomy framework 28 (Table 1, 2, and 3). It also houses genome sequences of 12 plant, 18 insect, and 3 nematode species and human genome sequences (38 datasets), to support comparison of fungal genomes with those in other kingdoms (Table 4). The taxonomy browser implemented in the SNUGB provides an easy means to access genome sequences of specific species via two ways. The SNUGB provides lists of putative orthologous genes of all fungal ORFs and a tool for comparison of genomic contexts of any orthologous genes among chosen species. In addition, SNUGB displays the InterPro terms assigned to each ORF as well as the genomic regions where expressed sequence tags (ESTs) are matched. With these functionalities, SNUGB will serve as a powerful platform supporting comprehensive fungal comparative genomics.

<p>Table 1</p>

List and characteristics of the fungal genomes belonging to the subphylum Pezizomycota archived in SNUGB.

Species a

Size (Mb)

# of ORFs

# of Exons

C b

I b

E b

Source

Refs

Fungi (Kingdom) e

Ascomycota (Phylum)

Pezizomycotina (Subphylum)

A: Botrytis cinerea T: Botryotinia fuckeliana

42.7

16,448

43,358

N

Y

N

BI

N

Sclerotinia sclerotiorum

38.3

14,522

40,623

N

Y

N

BI

N

Aspergillus clavatus

27.9

9,121

27,959

N

Y

N

BI

17 44

Aspergillus flavus

36.8

12,604

40,971

N

Y

N

BI

16

Aspergillus fumigatus AF293

29.4

9,887

28,164

8

Y

N

TIGR

45

Aspergillus fumigatus A1163

29.2

9,929

29,094

N

Y

N

TIGR

44

A:Aspergillus nidulans T:Emericella nidulans

30.1

10,701

35,525

8

Y

N

BI

14

Aspergillus niger ATCC1015

37.2

11,200

34,971

N

Y

N

JGI

N

Aspergillus niger CBS513.88

34.0

14,086

50,371

8

Y

N

NCBI

38

A: Aspergillus oryzae T: Eurotium oryzae

37.1

12,063

35,319

N

Y

N

DOGAN

46

Aspergillus terreus

29.3

10,406

33,116

N

Y

N

BI

17

A:Aspergillus fischerianus T: Neosartorya fischerid

32.6

10,403

N

N

N

N

BI

44

Penicillium chrysogenum

32.2

12,791

40,441

N

N

N

NCBI

47

Penicillium marneffei

28.5

10,638

34,306

N

N

N

TIGR

N

Coccidioides immitis RS

28.9

10,457

36,137

N

Y

N

BI

N

Coccidioides immitis H538.4

27.7

10,663

34,503

N

Y

N

BI

N

Coccidioides immitis RMSCC 2394

28.8

10,408

34,807

N

Y

N

BI

N

Coccidioides immitis RMSCC 3703

27.6

10,465

33,931

N

Y

N

BI

N

Coccidioides posadasii Silveria

27.5

10,125

33,520

N

Y

N

BI

N

Coccidioides posadasii C735

26.7

N

N

N

N

N

BI

N

Coccidioides posadasii CPA0001

28.7

N

N

N

N

N

BI

N

Coccidioides posadasii CPA0020

27.3

N

N

N

N

N

BI

N

Coccidioides posadasii CPA0066

27.7

N

N

N

N

N

BI

N

Coccidioides posadasii RMSCC 1037

26.7

N

N

N

N

N

BI

N

Coccidioides posadasii RMSCC 1038

26.2

N

N

N

N

N

BI

N

Coccidioides posadasii RMSCC 1040

26.5

N

N

N

N

N

BI

N

Coccidioides posadasii RMSCC 2133

27.9

N

N

N

N

N

BI

N

Coccidioides posadasii RMSCC 3488

28.1

9,964

33,484

N

Y

N

BI

N

Coccidioides posadasii RMSCC 3700

25.5

N

N

N

N

N

BI

N

Paracoccidioides brasiliensis Pb01

33.0

9,136

37,310

N

Y

N

BI

N

Paracoccidioides brasiliensis Pb03

29.1

9,264

31,468

N

Y

N

BI

N

Paracoccidioides brasiliensis Pb18

30.0

8,741

33,239

N

Y

N

BI

N

Blastomyces dermatitidis

61.8

N

N

N

N

N

WGSC

N

A: Histoplasma capsulatum G217B T: Ajellomyces capsulatus G217B

41.3

8,038

26,711f

N

Y

N

WGSC

N

A: Histoplasma capsulatum G186AR T: Ajellomyces capsulatus G186AR

29.9

7,454

24,562f

N

Y

N

WGSC

N

A: Histoplasma capsulatum NAm1 T: Ajellomyces capsulatus NAm1

33.0

9,349

32,844

N

Y

N

BI

N

A: Histoplasma capsulatum H143 T: Ajellomyces capsulatus H143

39.0

7,365

25,164f

N

Y

N

BI

N

A: Histoplasma capsulatum H88 T: Ajellomyces capsulatus H88

37.9

7,428

25,356f

N

Y

N

BI

N

A: Arthroderma gypseum T: Microsporum gypseum

23.3

8,876

28,624

N

Y

N

BI

N

Microsporum canis

23.3

N

N

N

N

N

BI

N

Trichophyton equinum

24.2

N

N

N

N

N

BI

N

Ascosphaera apis

21.6

N

N

N

N

N

BGM

48

Uncinocarpus reesii

22.3

7,798

24,094

N

Y

N

BI

N

Chaetomium globosum d

34.9

11,124

N

N

N

N

BI

N

Epichloe festucae

27.0

N

N

N

N

N

OU

N

A: Fusarium graminearum PH-1 T: Gibberella zeae PH-1

36.6

13,321

37,549

N

Y

N

BI

37

A: Fusarium graminearum GZ3639 T:Gibberella zeae GZ3639c

15.1

6,694

11,692f

N

Y

N

BI

37

Fusarium oxysporum f. sp. lycopersici 4286

61.4

17,608

47,051

15

Y

N

BI

N

A: Fusarium verticillioides 7600 T:Gibberella moniliformis 7600

41.9

14,199

39,058

N

Y

N

BI

N

A: Fusarium solani MPVI T:Nectria haematococca MPVI

51.3

15,707

48,387

N

Y

N

JGI

N

A: Pyricularia oryzae 70–15 T:Magnaporthe oryzae 70–15

41.6

12,841

34,189

7

Y

Y

BI

49

A: Pyricularia oryzae 70–15 chromosome 7 T:Magnaporthe oryzae 70–15 chromosome 7

4.0

1,122

3,289

1

Y

N

50

Cryphonectria parasitica

43.9

11,184

33,090

N

N

N

JGI

N

Neurospora crassa OR74A

39.2

9,842

27,188

8

Y

N

BI

51

Podospora anserina DSM980

35.7

10,596

24,437

9

Y

N

IGM

52

Trichoderma atroviride IMI206040

36.1

11,100

32,563

N

Y

N

JGI

N

A:Trichoderma reesei QM6a T: Hypocrea jecorina QM6a

33.5

9,129

27,891

N

Y

N

JGI

53

A:Trichoderma virens Gv29-8 T:Hypocrea virens Gv29-8

38.8

11,643

34,673

N

Y

N

JGI

N

Talaromyces stipitatus ATCC 10500

35.6

N

N

N

N

N

TIGR

N

Verticillium dahliae VaLs. 17

33.9

10,575

29,736

N

N

N

BI

N

Verticillium albo-atrum VaMs. 102

32.9

10,239

28,842

N

N

N

BI

N

Alternaria brassicicola

32.0

N

N

N

N

N

WGSC

N

A:Bipolaris maydis T:Cochliobolus heterostrophus C5

34.9

9,633

28,007

N

N

N

JGI

N

Pyrenophora tritici-repentis

38.0

12,169

32,717

N

Y

N

BI

N

A: Septoria tritici T: Mycosphaerella graminicola

41.9

11,395

30,629

N

Y

N

JGI

N

A:Paracercospora fijiensis T:Mycosphaerella fijiensis

73.4

10,327

25,289

N

Y

N

JGI

N

A: Stagonospora nodorum T: Phaeosphaeria nodorum

37.2

16,597

44,017

N

Y

N

BI

54

Total

2,844.0

637,006

1,755,655

8

43

1

aA indicates anamorph name and T presents teleomorph name of fungi.

bC means chromosomes, I indicates InterPro, and E presents EST.

cIncomplete coverage of genome information

dInsufficient exon/intron information

eTaxonomy based on 28

fORFs and exons were predicted by AUGUSTUS 2.0.3 with species-specific training datasets 55.

'Y' indicates the existence of information in each field, and 'N' indicates the lack of information.

 <p>Table 2</p>

List and characteristics of the fungal genomes belonging to the subphyla Saccharomycotina and Taphrinomycotina archived in SNUGB.

Species a

Size (Mb)

# of ORFs

# of Exons

C b

I b

E b

Source

Refs

Fungi (Kingdom) e

Ascomycota (Phylum)

Saccharomycotina (Subphylum)

Candida albicans SC5314

14.3

6,090

6,624

N

Y

N

SGTC

56 57

Candida albicans WO-1

14.4

6,160

6,395

N

Y

N

BI

N

Candida dubliniensis d

14.5

6,027

N

N

N

N

SI

N

Candida glabrata CBS138

12.3

5,165

5,249

N

Y

N

CBS

58

A: Candida guilliermondii T: Pichia guilliermondii

10.6

5,920

5,935

N

Y

N

BI

N

Candida lusitaniae

12.1

5,941

5,956

N

Y

N

BI

N

Candida parapsilosis

13.1

5,733

5,733

N

Y

N

BI

N

Candida tropicalis

14.7

6,258

6,292

N

Y

N

BI

N

Candida tropicalis f

2.1

N

N

N

N

N

GS

59

Ashbya gossypii

8.8

4,717

4,943

7

Y

N

NCBI

60

Debaryomyces hansenii

12.2

6,354

6,710

7

Y

N

CBS

58

Debaryomyces hansenii f

2.3

N

N

N

N

N

GS

61

A: Candida sphaerica T: Kluyveromyces lactis

10.7

5,327

5,457

N

Y

N

GS

58

A: Candida sphaerica T: Kluyveromyces lactisf

5.1

N

N

N

N

N

GS

62

A: Candida kefyr T:Kluyveromyces marxianusf

2.0

N

N

N

N

N

GS

63

Kluyveromyces polysporus DSM70294

14.7

5,367

5,524

N

Y

N

SIG

64

Kluyveromyces thermotolerans f

2.2

N

N

N

N

N

GS

65

Kluyveromyces waltii

10.9

4,935

5,395

N

Y

N

BI

66

Lodderomyces elongisporus

15.5

5,802

5,856

N

Y

N

BI

N

Saccharomyces bayanus MCYC 623

11.5

9,385

9,385

N

Y

N

BI

13

Saccharomyces bayanus 623-6C YM4911

11.9

4,966

4,966

N

Y

N

WGSC

12

Saccharomyces bayanus var. uvarumf

4.5

N

N

N

N

N

GS

67

Saccharomyces castellii

11.4

4,677

4,677

N

Y

N

WGSC

12

A: Candida robusta S288C T: Saccharomyces cerevisiae S288C

12.2

6,692

7,042

16

Y

N

SGD

68

A: Candida robusta RM11-1a T: Saccharomyces cerevisiae RM11-1a

11.7

5,696

5,988

N

Y

N

BI

N

A: Candida robusta YJM789 T: Saccharomyces cerevisiae YJM789

12.0

5,903

6,153

N

Y

N

SI

69

Saccharomyces exiguus f

2.0

N

N

N

N

N

GS

70

Saccharomyces kluyveri

11.0

2,968

2,968

N

Y

N

WGSC

12

Saccharomyces kluyveri f

2.2

N

N

N

N

N

GS

71

Saccharomyces kudriavzevii

11.2

3,768

3,768

N

Y

N

WGSC

12

Saccharomyces mikatae

11.5

9,016

9,016

N

Y

N

BI

13

Saccharomyces mikatae

10.8

3,100

3,100

N

Y

N

WGSC

12

Saccharomyces paradoxus

11.9

8,939

8,939

N

Y

N

BI

13

Saccharomyces servazzii f

2.0

N

N

N

N

N

GS

72

Pichia angusta f

4.5

N

N

N

N

N

GS

73

Pichia stipitis

15.4

5,839

8,428

N

Y

N

JGI

74

Pichia sorbitophila f

3.8

N

N

N

N

N

GS

75

A: Candida lipolytica T: Yarrowia lipolytica

20.5

6,524

7,264

6

Y

N

CBS

58

A: Candida lipolytica T: Yarrowia lipolyticaf

4.6

N

N

N

N

N

GS

76

Zygosaccharomyces rouxii f

4.1

N

N

N

N

N

GS

77

Taphrinomycotina (Subphylum)

Pneumocystis carinii c, d

6.3

4,020

N

N

N

N

SI

N

Schizosaccharomyces japonicus

11.3

5,172

10,321

N

Y

N

BI

N

Schizosaccharomyces pombe

12.6

5,058

9,869

3

Y

N

GDB

78

Schizosaccharomyces octosporus

11.2

4,925

10,168

N

N

N

BI

N

Total

424.6

176,444

188,121

5

28

0

aA indicates anamorph name and T presents teleomorph name of fungi.

bC means chromosomes, I indicates InterPro, and E presents EST.

cIncomplete coverage of genome information

dInsufficient exon/intron information

eTaxonomy based on 28

fSequences from Random Sequence Tag (RST)

'Y' indicates the existence of information in each field, and 'N' indicates the lack of information.

 <p>Table 3</p>

List and characteristics of the genomes belonging to the phyla Basidiomycota, Chytridiomycota, and Microsporidia, the subphylum Mucoromycotina, and the phylum Peronosporomycota (oomycetes) archived in SNUGB.

Species a

Size (Mb)

# of ORFs

# of Exons

C b

I b

E b

Source

Refs

Fungi (Kingdom) e

Basidiomycota (Phylum)

Agricomycotina (Subphylum)

Postia placenta

90.9

17,173

116,596

N

Y

N

JGI

N

T: Phanerochaete chrysosporium A: Sporotrichum pruinosum

35.1

10,048

58,746

N

Y

N

JGI

79

Coprinus cinereus

36.3

13,544

72,887

N

Y

N

BI

N

Laccaria bicolor

64.9

20,614

111,290

N

Y

N

JGI

80

A: Cryptococcus neoformans Serotype A T: Filobasidiella neoformans Serotype A

19.5

7,302

43,325

20

Y

N

BI

N

A: Cryptococcus neoformans Serotype B T: Filobasidiella neoformans Serotype B

19.0

6,870

40,589

N

Y

N

NCBI

N

A: Cryptococcus neoformans Serotype D B-3501A T: Filobasidiella neoformans Serotype D B-3501A

18.5

6,431

40,942

N

Y

N

SGTC

41

A: Cryptococcus neoformans Serotype D JEC21 T: Filobasidiella neoformans Serotype D JEC21

19.1

6,475

40,811

N

Y

N

SGTC

41

Pucciniomycotina (Subphylum)

Sporobolomyces roseus

21.2

5,536

39,911

N

Y

N

JGI

N

Puccinia graminis

88.7

20,567

95,838

N

Y

N

BI

N

Ustilaginomycotina (Subphylum)

Malassezia globosa CBS7966

9.0

4,286

4,286

N

N

N

PGC

15

Malassezia restricta CBS7877c

4.6

N

N

N

N

N

PGC

15

Ustilago maydis 521

19.7

6,689

11,589

N

Y

N

BI

81

Ustilago maydis FB1

19.3

6,950

10,310f

N

Y

N

BI

81

Chytridiomycota (Phylum)

Batrachochytrium dendrobatidis JEL423

23.9

8,818

38,551

N

Y

N

BI

N

Batrachochytrium dendrobatidis JAM81

24.3

8,732

37,423

N

Y

N

JGI

N

Mucoromycotina (Subphylum incertae sedis)

Rhizopus oryzae

46.1

17,467

57,981

N

Y

N

BI

N

Phycomyces blakesleeanus

55.9

14,792

71,502

N

Y

N

JGI

N

Microsporidia (Phylum)

Encephalitozoon cuniculi

2.5

1,996

2,002

N

Y

N

GS

82

Antonospora locustae d

6.1

2,606

N

N

N

N

JBPC

N

Stramenopila (Kingdom) e

Peronosporomycota (Phylum)

Phytophthora capsici

107.8

17,414

45,661

N

N

N

JGI

N

Phytophthora infestans d

228.5

22,658

N

N

N

N

BI

N

Phytophthora ramorum

66.7

15,743

40,639

N

Y

N

JGI

83

Phytophthora sojae

86.0

19,027

53,552

N

Y

N

JGI

83

Hyaloperonospora parasitica

83.6

14,789

24,907

N

Y

N

VBI

N

Pythium ultimum

44.3

N

N

N

N

N

N

Total

1,241.5

276,527

1,058,878

1

20

0

aA indicates anamorph name and T presents teleomorph name of fungi

bC means chromosomes, I indicates InterPro, and E presents EST.

cIncomplete coverage of genome information

dInsufficient exon/intron information

eTaxonomy based on 28

fORFs and exons were predicted by AUGUSTUS 2.0.3 with species-specific training datasets 55.

'Y' indicates the existence of information in each field, and 'N' indicates the lack of information.

 <p>Table 4</p>

List and characteristics of the non-fungal genomes archived in SNUGB.

Species a

Size (Mb)

# of ORFs

# of Exons

C b

I b

E b

Source

Refs

Chloroplastida (Kingdom) e

Streptophyta (Phylum)

Arabidopsis thaliana

119.2

28,581

150,369

5

Y

N

TAIR

33

Carica papaya

271.7

N

N

N

N

N

PGSC

84

Glycine max

996.9

62,199

281,102

N

N

N

JGI

N

Lycopersicon esculentum c

39.9

8,725

29,707

N

Y

N

SOL

N

Medicago truncatula

278.7

38,334

122,889

8

Y

N

MTGSP

85 86 87

Oryza sativa var. Indicad

426.3

49,710

N

N

N

N

BGI

88 89

Oryza sativa var. Japonica

372.1

66,710

319,140

12

Y

N

IRGSP

89 90

Populus trichocarpa

485.5

45,555

193,687

N

Y

N

JGI

91

Ricinus communis d

362.5

38,613

N

N

N

N

TIGR

N

Selaginella moellendorffii

212.8

22,285

124,645

N

Y

N

JGI

N

Sorghum bicolor

738.5

36,338

165,149

11

Y

N

JGI

N

Vitis vinifera

497.5

30,434

149,351

19

Y

N

GS

92

Zea mays d

2,314.7

420,732

N

N

N

N

MGSP

N

Metazoa (Kingdom)

Arthropoda (Phylum)

Apis mellifera

235.2

11,062

71,496

N

N

N

HBGP

93

Acyrthosiphon pisum

446.6

N

N

N

N

N

BCM

N

Bombyx mori

397.7

21,302

82,381

N

N

N

BGI

94

Drosophila ananassae

231.0

15,276

56,595

N

N

N

FB

95

Drosophila erecta

152.7

15,324

56,924

N

N

N

FB

95

Drosophila grimshawi

200.5

15,270

56,647

N

N

N

FB

95

Drosophila melanogaster

168.7

20,923

96,745

N

N

N

FB

96

Drosophila mojavensis

193.8

14,849

55,013

N

N

N

FB

95

Drosophila persimilis

188.4

17,235

59,116

N

N

N

FB

95

Drosophila pseudoobscura

152.7

16,363

57,864

N

N

N

FB

97

Drosophila sechellia

166.6

16,884

58,584

N

N

N

FB

95

Drosophila simulans

137.8

15,983

54,294

N

N

N

FB

95

Drosophila virilise

206.0

14,680

55,005

N

N

N

FB

95

Drosophila willistoni

235.5

15,816

56,641

N

N

N

FB

95

Drosophila yakuba

165.7

15,423

59,098

N

N

N

FB

95

Glossina morsitans

205.7

N

N

N

N

N

TIGR

N

Nasonia vitripennis

239.6

27,957

98,570f

N

N

N

BCM

N

Tribolium castaneum

152.1

14,274

58,381f

N

N

N

BCM

N

Nematoda (Phylum)

Caenorhabditis elegans

100.3

26,902

175,232

7

N

N

WB

34

Caenorhabditis briggsae d

108.5

20,669

N

N

N

N

WB

98

Caenorhabditis remanei

145.4

N

N

N

N

N

WB

N

Vertebrata (Phylum)

Homo sapiens Celera assembly

2,828.4

28,057

273,999

N

N

N

NCBI

99

Homo sapiens HuRef assembly

2,843.9

27,937

273,135

N

N

N

NCBI

100

Homo sapiens NCBI Reference

2,870.8

29,319

284,553

N

N

N

NCBI

100

Homo sapiens

3,665.5

43,570

452,099

29

N

N

EM

100

Total

21,241.0

1,294,281

4,142,169

7

8

0

aA indicates anamorph name and T presents teleomorph name of fungi

bC means chromosomes, I indicates InterPro, and E presents EST.

cIncomplete coverage of genome information

dInsufficient exon/intron information

eTaxonomy based on 101

fORFs and exons were predicted by AUGUSTUS 2.0.3 with species-specific training datasets 55.

'Y' indicates the existence of information in each field, and 'N' indicates the lack of information.

Construction, content, and applications

Data processing via an automated pipeline and the function of Positional Database

Positional information of functional/structural units that are present on individual contigs/chromosomes, such as the start and stop sites of ORFs and exons/introns, was collected from the data warehouse of CFGP and stored in the Position Database of SNUGB. New types of data, such as Simple Sequence Repeats (SSRs) on the genome, can be easily added to the Positional Database for visualization via SNUGB. Along with the positional information, for each data, data type (e.g., ORFs), primary key, and any additional information were saved into the partitioned tables, which were designed for enhancing the speed of data retrieval. Through the primary key, SNUGB can display detailed information of each datum (e.g., sequences) stored at external sources. Considering the large number of available fungal genome sequences and those that are currently being sequenced, in addition to this data standardization scheme, a standardized pipeline for data extraction and management is needed to organize the data and to ensure orderly expansion of SNUGB.

The pipeline developed for SNUGB processes each genome data set via the following steps. Firstly, once whole genome sequences are deposited in the data warehouse of CFGP, the integrity of genome information, such as the position information of functional/structural units, is inspected. Several properties of the whole genome, such as the length and the GC content, are calculated. Secondly, the GC content, AT-skew, and CG-skew are calculated via 50-bp sliding windows with 20 bp steps. Thirdly, for each gene, three types of sequence information, including coding sequences (sequences from the start to stop codon without introns), gene sequences (sequences from the start to stop codon with introns), and transcript sequences (sequences from the transcription start site to end site without intron sequence), if transcript information is available, are generated based on the genome annotation information. Fourthly, all data generated in the previous steps are transferred into the Position Database to support graphical representation of these features. Fifthly, if the genome has chromosomal map information, including genetic map and optical map, this information is converted into a standardized format and stored in SNUGB for graphical representation via Chromosome Viewer. Lastly, after subjecting all ORFs in the genome through the InterPro Scan 29, the genomic position of each domain predicted by the InterPro Scan is calculated and stored into the Position Database.

Modular design of SNUGB facilitates its application

To facilitate the efficient implementation of SNUGB in diverse genomics platforms, a modular design was used for its application programming interface (API). Through API, a diagram showing genome features in a selected region can be created using only their chromosomal positions and display options. Four recent publications illustrate the utility of this design: T-DNA Analysis Platform (TAP; http://tdna.snu.ac.kr/) provides the GC content and AT skew around T-DNA insertion sites on the chromosomes of Magnaporthe oryzae via a mini genome browser supported by SNUGB 25. The chromosomal distribution pattern of T-DNA insertion sites in M. oryzae http://atmt.snu.ac.kr/ was also displayed using SNUGB 26. Fungal Cytochrome P450 Database (FCPD; http://p450.riceblast.snu.ac.kr/) 24 employs SNUGB to present the chromosomal distribution pattern and contexts of cytochrome P450 genes in fungal genomes. Two databases, FED http://fed.snu.ac.kr/ and FSD http://fsd.snu.ac.kr/, utilize SNUGB for presenting the genomic context of the region matched to EST and secreted proteins, respectively. Moreover, Systematical Platform for Identifying Mutated Proteins (SysPIMP; http://pimp.starflr.info/) 30 and Insect Mitochondrial Genome Database (IMGD; http://www.imgd.org; Lee et al., under revision) also adopted SNUGB for data presentation. These examples illustrate the utility of SNUGB.

Properties of the fungal/oomycete genomes archived in SNUGB

Among the 98 fungal/oomyvete species (137 genome datasets) covered by SNUGB, 77 species (111 genome datasets; 81%) belong to the phylum Ascomycota (Table 1 and 2), and 10 species (14 genome datasets; 10%) belong to the phylum Basidiomycota (Table 3). In contrast, the phyla Chytridiomycota and Micosporidia are represented only by one (2 datasets) and two species (both belong to the subphylum Mucoromycotina), respectively (Table 3). Six oomycete genomes, derived from Phytophthora, Hyaloperonospora, and Pythium species, are available for comparison with fungal genomes (Table 3). Although oomycetes belong to the kingdom Stramenophla and show closer phylogenetic relationships to algae and diatoms than fungi 31, due to their morphological similarities to fungi, they have been traditionally grouped with fungi.

The datasets that cover the whole genome (121 out of the 137 datasets) were analyzed to investigate genome properties. The average size of the genomes, measured by adding lengths of all scaffolds together, is 31.42 Mb which is one-seventeenth of plant genomes (547.41 Mb in the phylum Streptophyta) and one-seventh of insect genomes (215.36 Mb in the phylum Arthropoda) (Figure 1A). The fungal/oomycete genome sizes ranged from 2.5 Mb (Encephalitozoon cuniculi) to 228.5 Mb (Phytophthora infestans); the genome of E. cuniculi is shorter than that of Escherichia coli (4.6 Mb) 32, while the genome of P. infestans is much larger than the genomes of Arabidopsis thaliana (119.2 Mb) 33 and Caenorhabditis elegans (100.5 Mb) 34, indicating no clear relationship between the genome size and the organismal complexity 35. With regard to the average genome sizes in different taxon groups, the phylum Microsporidia, known as ancestral fungi, shows the smallest average size (4.28 Mb), while oomycetes show the largest at 102.83 Mb (Figure 1A). In the phylum Basidiomycota, which is large and very diverse, the degree of difference in average genome sizes within each of the represented subphyla is highest in the fungal kingdom: the ratios of standard deviation to the average length in three subphyla Agricomycotina, Pucciniomycotina, and Ustilaginomycotina are 71.95%, 86.93%, and 57.46%, respectively (Figure 1B). The subphylum Pucciniomycotina displays the largest size with large variation (Figure 1A and 1B), while two subphyla Saccharomycotina and Taphrinomycotina belonging to the phylum Ascomycota exhibit the relatively low degree of variations (Figure 1B), probably because only closely related species have been sequenced. Although the average genome sizes varied from group to group, ANOVA and TukeyHSD tests (P < 0.05) showed only the difference between fungi and oomycetes was significant (Figure 1A). The GC content of fungal genomes ranges from 32.523% (Pneumocystis carinii in subphylum Taphrinomycotina) to 56.968% (Phanerochaete chrysosporium in the subphylum Agricomycotina), while the GC content of plant and insect genomes ranges from 29.638% to 46.850% (Figure 1C). Although the coding regions exhibit higher GC contents than the rest of the genome, there is no relationship between the proportion of ORFs on the genome and the GC content of the whole genomes (linear regression; R2 = 0.04; Figure 1C and 1D).

<p>Figure 1</p>

Characteristics of the 137 fungal and oomycetes genomes archived in SNUGB

Characteristics of the 137 fungal and oomycetes genomes archived in SNUGB. In all graphs, the first six groups correspond to subphyla and the rests indicate phyla. Error bars indicate variation of data within each taxonomic group. The last two phyla were used as outgroup. In graphs A, E, F, and G, each color of bar indicates distinct group supported by Turkey HSD test. (A) Average genome size. (B) the ratio of variation of genome size to the average genome size. (C) Average GC ratio of each subphylum/phylum. (D) The percentage of coding regions to the genome length. (E) Average number of total ORFs. (F) The total number of ORFs per Mb (= ORF density). (G) The average exon number of each ORFs.

The number of total proteins encoded by each organism was once considered to reflect organism's characteristics 36. Based on the size of total proteomes, all sequenced fungal and oomycete species were divided into three groups: The medium group contains the subphylum Pezizomycotina in Ascomycota and the subphyla Agricomycota and Puccinomycotina in Basidiomycota, the small group includes three subphyla Saccharomycotina, Taphrinomycotina, and Ustilagomycotina and the phylum Microsporidia, and the large group has the subphylum Mucoromycotina and the phylum Oomycota (ANOVA and TukeyHSD; P < 0.05; Figure 1E). This grouping shows that the number of total ORFs does not correlate with taxonomic positions at the phylum level, however, at the subphylum level, the correlation was high. For example, subphyla Saccharomycotina and Taphrinomycotina can be distinguishable from Pezizomycotina based on this character. The ORF density classified the sequenced species into three distinct groups, Oomycetes, Microsporidia and the rest, through ANOVA and TukeyHSD test (P < 0.05; Figure 1F). Taken together, these three indicators can be used to divide fungal subphyla/phyla. For example, the subphylum Pezizomycotina shows the medium-level of ORF number and ORF density, while the subphylum Saccharomycotina displays the low-level of ORF number but its ORF density is comparable to that of the subphylum Pezizomycotia. Both the number of ORFs and the ORF density are high for oomycetes, exhibiting a pattern different from fungi.

The number of exons per ORF was investigated, resulting in four groups (ANOVA and TukeyHSD test; P < 0.05; Figure 1G). With the exception of the subphylum Ustilagomycotina, the phylum Basidiomycota exhibits the highest number (~6). The subphyla Saccharomycotina and Mycoromycotina show the lowest value (nearly 1), indicating that almost all their genes do not have introns.

Comparison of genome sequences of multiple isolates within species

For 14 fungal species, two or more strains have been sequenced (Table 5). For some species, such as Fusarium graminearum, additional isolate(s) were sequenced only at a low coverage (e.g., 0.4× coverage for the second strain of F. graminearum); however, even such low-coverage provided some insights into the evolution of pathogenicity in this important cereal pathogen 37. Except Aspergillus niger, Histoplasma capsulatum, and Paracoccidioides brasiliensis, all strains within same species showed less than 1 Mb variation in genome sizes (Table 5). It is possible that the 3.2 Mb difference between two A. niger strains is in part due to different sequencing coverage: the coverage of ATCC1015 was 8.9× while CBS513.88 was 7× http://genome.jgi-psf.org/Aspni1/Aspni1.info.html38. The differences among three P. brasiliensis genomes, ranging from 29.1 Mb to 33.0 Mb, may reflect their distinct phylogenetic positions 39. The differences among five H. capsulatum genomes may be due to a combination of different levels of sequencing coverage http://www.broad.mit.edu/annotation/genome/histoplasma_capsulatum/Info.html and different geological origins 40. Three isolates of H. capsulatum and P. brasiliensis showed approximately 1% difference in the GC content, whereas the degree of GC content variation among 11 strains of Coccidioides posadasii was only 0.5%. Four Cryptococcus neoformans strains, representing three different serotypes (A, B and D), showed around 0.3% variation in the GC content, and within a serotype (two serotype D strains) the difference was only 0.043% 41. Isolates of Candida albicans, Saccharomyces bayanus, and Batrachochytrium dendrobatidis showed only 0.01% variation in the GC content. These intraspecific variations of genome properties can be compared in detail via SNUGB.

<p>Table 5</p>

Basic properties of different strains of fungal genomes deposited in SNUGB.

Species

# of Strains

Genome size (Mb)

GC content (%)

Fungi (Kingdom)

Ascomycota (Phylum)

Pezizomycotina (Subphylum)

Aspergillus fumigatus

2

29.3 ± 0.1

49.672 ± 0.178

Aspergillus niger

2

35.6 ± 2.3

50.365 ± 0.012

Coccidioides immitis

4

28.3 ± 0.7

46.529 ± 0.514

Coccidioides posadasii

11

27.2 ± 0.9

46.839 ± 0.537

Histoplasma capsulatum

5

36.2 ± 4.7

43.400 ± 1.859

Paracoccidioides brasiliensis

3

30.7 ± 2.0

43.868 ± 0.930

Fusarium graminearum a

2

36.6

48.283

Saccharomycotina (Subphylum)

Candida albicans

2

14.4 ± 0.1

33.462 ± 0.010

Saccharomyces cerevisiae

3

11.9 ± 0.3

38.252 ± 0.090

Saccharomyces bayanus

2

11.7 ± 0.3

40.196 ± 0.011

Saccharomyces mikatae b

2

11.1 ± 0.5

37.920 ± 0.315

Basidiomycota (Phylum)

Agricomycotina (Subphylum)

Cryptococcus neoformans

4

19.2 ± 0.2

48.251 ± 0.316

Ustilaginomycotina (Subphylum)

Ustilago maydis

2

19.7 ± 0.0

53.995 ± 0.045

Chytridiomycota (Phylum)

Batrachochytrium dendrobatidis

2

24.1 ± 0.3

39.261 ± 0.011

Chloroplastida (Kingdom)

Charophyta (Phylum)

Oryza sativa

2

399.2 ± 38.4

43.530 ± 0.046

Vertebrata (Phylum)

Vertebrata (Phylum)

Homo sapiens

4

3,052.2 ± 409.3

40.878 ± 0.042

aOne of strains are incomplete whole genome sequences, so that standard deviation of genome length and GC content are not calculated.

bSame strain but different version of assembly

Update of SNUGB

The number of on-going fungal genome sequencing projects is approximately 40 http://fungalgenomes.org/wiki/Fungal_Genome_Links. 37 strains of S. cerevisiae and 25 strains of S. paradoxus were already sequenced and released by the Sanger institute http://www.sanger.ac.uk/Teams/Team118/sgrp/, indicating that more than 100 additional fungal genomes will be available soon. Next generation high throughput sequencing technologies, such as GS Flx, Solexa, and SOLiD 4243, will further accelerate the rate of fungal genome sequencing, emphasizing the importance of frequently updating SNUGB. With the aid of the developed pipeline, SNUGB will be updated whenever new fungal genome sequences have been publicly released with annotation information. A notice for updated genomes will be posted on the SNUGB web site.

Functions and tools

Taxonomy browser

To support selection of species of interests based on their taxonomic positions, a web-based tool, named as the taxonomy browser, was developed. Considering an anticipated increase in comparing genome sequences and features across multiple species to investigate evolutionary questions at the genome scale, such a tool is necessary to provide an overview of the taxonomic positions of the sequenced species and their evolutionary relationships with other fungi to users of SNUGB and to assist them in selecting appropriate species for comparative analyses. The taxonomy browser provides two methods for accessing the data archived in SNUGB, one of which is text-search using species name (Figure 2A). When a user begins typing a species name in the text box, the full name will be completed automatically to assist a quick search of species. The other method is using the taxonomical hierarchy (i.e., tree of life). When a user clicks a specific taxon (e.g., phylum), taxonomy browser will present all subgroups within the chosen taxon for further selection (Figure 2B).

<p>Figure 2</p>

Taxonomy browser

Taxonomy browser. A screenshot of data generated using Taxonomy browser is shown. (A) Search interface by species name shows a list of species along with inserted string. (B) Taxonomical tree shows a lineage of the chosen species and its genome datasets deposited in SNUGB.

Chromosome viewer and Contig/ORF browser

Three different methods can be used to access genomic information. For those with chromosomal map data (21 species), their chromosomal maps can be displayed via Chromosome viewer (Figure 3A). The following color scheme was used to denote the level of completeness: i) chromosome constructed using genetic or optical map data (with gaps) as blue (Chromosomes 1 to 7 of M. oryzae; Figure 3A), ii) chromosome map based on a combination of sequences and genetic/optical map data as pink (e.g., chromosomes of A. niger), and iii) unassigned contigs (labeled as Chromosome Ex of M. oryzae; Figure 3A) as light blue. For the species without chromosomal map information, SNUGB provides the contig and ORF browsers, which display the name of contig and ORFs, respectively, and allow users to search them using their names (Figures 3B and 3C).

<p>Figure 3</p>

Chromosome viewer, Contig Viewer, and ORF Viewer

Chromosome viewer, Contig Viewer, and ORF Viewer. (A) The chromosome viewer displays seven chromosomes of M. oryzae with a size indicator at the right side. At the bottom, the interface allows for jumping directly to a specific region by selecting chromosome/contigs and its position. (B) The contig viewer provides a list of contigs with its length. Through this interface, contigs can be searched by name. (C) The ORF viewer presents the names and lengths of ORFs with search function.

Graphical Browser with six different display formats

Gene annotation information in a selected area of chromosome or contig, such as transcripts, ORFs, and exon/intron structure, and InterPro domains 29, can be displayed through three formats: i) the 'single' format shows these features as bars; ii) the 'squish' format displays them via color-coded diagrams without description; and iii) the 'pack' format presents them as small color-coded icons with description (Figure 4A). These graphical formats were also used by UCSC Genome Browser 2. In addition, the GC content and AT/CG skew information for individual chromosomes can be displayed via three formats: i) color-coded bar graph, ii) line, and iii) dotted lines along with a description of data (Figure 4B). For species with EST data (Table 1), the genomic region corresponding to each EST sequence can be displayed along with ORF and InterPro domains to help users identify predicted gene structure and expressed regions (see Figure 4A). Presentation of these data is supported by Fungal Expression Database http://fed.snu.ac.kr/.

<p>Figure 4</p>

Six different display methods of the genome content and properties via Graphical browser

Six different display methods of the genome content and properties via Graphical browser. (A) The graphical browser in SNUGB shows the genome context via three different formats: bar, squash, and pack. At the bottom, ORFs, ESTs, and InterPro domains on chromosome 1 of M. oryzae are displayed. (B) Three graphic representations, including graph, line, and Single line (S. line), of the AT-skew, GC-skew, and GC content are shown.

Table browser and Text browser

Although graphical presentation of genomic features helps users view global patterns, the graphical browser does not provide sequences or a list of elements present in a chosen area. To provide such information, we developed two additional tools named as the table browser and the text browser. The table browser provides a list of the names and chromosomal/contig positions of all elements present in a selected region in the csv format, which can be opened using the Excel program (Figure 5A). The text browser provides sequences in a selected region. If ORFs exist in the region, exons and introns are presented using different colors and cases; this function is useful for designing primers and transferring selected sequences to a different data analysis environment (Figure 5B). Additionally, all InterPro domains present on each ORF are displayed as special characters under corresponding sequences so that putative functional domains can be easily recognized at the sequence level. The table and text browser can display sequences up to 50 kb.

<p>Figure 5</p>

Table and Text browsers

Table and Text browsers. (A) The table browser shows all ORFs, ESTs, and InterPro domains in a selected region as a list. (B) The text browser displays sequences showing exon/intron region as different colors and EST and InterPro domains.

Kingdom-wide identification of the putative orthologues of individual fungal proteins via BLAST and comparison of the genomic contexts and properties of homologous proteins among species via the Session History function

To identify putative orthologues of individual fungal proteins, BLAST searches with each of the 924,343 fungal proteins against all proteins were performed using the e-value of 1e-5 as the cut-off line. The 'BLAST annotation' tab shows a list of putative orthologues of a chosen gene product in other species with their BLAST e-values (see Figure 6A). To compare the genomic contexts around the orthologous genes between species or among multiple species, users can store the genomic contexts of the genes using the Session History function, in which the stored genomic contexts can be displayed in one screen (Figure 6B). In each session, other information, such as the GC content and InterPro terms, can also be presented to further support the comparison.

<p>Figure 6</p>

BLAST annotation to catalog homologous proteins

BLAST annotation to catalog homologous proteins. (A) A result of 'BLAST annotation' is shown with the corresponding gene names, species names, and e-values of putative homologs. 'Genome Browser' button after gene name can display the genome context of the selected gene, and 'Mini GB' button will show genome contexts of the selected gene as a smaller size to provide a quick overview, supported by MiniGB. The session can be stored by clicking the save link inside the small SNUGB image. (B) Two independent sessions showing homologs of two genes, MGG_01378.5 and FGSG_01632.3, are shown. Clicking the red button X at the bottom will hide the session.

Additional functionalities of SNUGB

The 'flexible-range-select' function allows users to select a chromosomal segment by clicking a mouse at the start site and moving it over the desired segment; the selected area will be displayed as shaded box, and the subsequent click displays an enlarged view of the selected segment (Figure 3A). Through the 'high-resolution-diagram' function, users can obtain a high-resolution image (more than 3,000 pixels in width) showing various features on a whole chromosome, such as ORFs, InterPro terms, and GC content. This image can be downloaded as image file via both the graphical genome browser and the session-storage function.

Conclusion

The SNUGB supports efficient and versatile visualization and utilization of rapidly increasing fungal genome sequence data, as well as those from selected organisms in other kingdoms, to address various types of questions at the genome scale. Properties and features of the archived fungal genomes are available for viewing and comparison in SNUGB. The taxonomy browser helps users easily access the genomes of individual species and provides taxonomic positions of chosen species, and the chromosome map function shows the whole genome of selected species. The graphical browser, table browser, and text browser present a global view of genomic contexts in a selected chromosomal region and support analyses of sequences in the region. The 'BLAST annotation' provides lists of putatively orthologous proteins in the fungal kingdom and facilitates comparison of the genomic contexts of their genes across multiple species. The SNUGB also allows users to manage their own work histories via the SNUGB web site.

Availability and requirements

All data and functionalities in this paper can be freely accessed through the SNUGB web site at http://genomebrowser.snu.ac.kr/. The source code, a set of programs, and database structure of SNUGB will be publicly released in the future after finalizing packaging of SNUGB to be opened.

Abbreviations

PZ: the subphylum Pezizomycotina; SC: the subphylum Saccharomycotina; TP: the subphylum Taphrinophycotina; AG: the subphylum Agricomycotina; PC: the subphylum Pucciniomycotina; US: the subphylum Ustilagomycotina; CH: the phylum Chytridiomycota; MU: the subphylum Mucoromycotina; MS: the phylum Microsporidia; OO: oomycete (the phylum Peronosporomycota); AT: the phylum Arthropoda; ST: the phylum Streptophyta; BCM: Baylor College of Medicine; BGI: Beijing Genome Institute; BGM: Baylor College of Medicine; BI: Broad Institute; CBS: Center For Biological Sequences; DOGAN: Database Of the Genomes Analyzed at Nite; EM: Ensembl; FB: Flybase; GDB: GeneDB; GS: Genoscope; HBGP: Honey Bee Genome Project; IGM: Instituté de Génétique et Microbiologie; IRGSP: International Rice Genome Sequencing Project; JBPC: Josephine Bay Paul Center for Comparative Molecular Biology and Evolution; JGI: DOE Joint Genomic Institute; MGSP: Maize Genome Sequencing Project; MTGSP: Medicago Truncatula Genome Sequencing Project; OU: Oklahoma University; PGC: Procter & Gamble Co; PGSC: Papaya Genome Sequencing Consortium; SGTC: Stanford Genome Technology Center; SI: Sanger Institute; SIG: Trinity College Dublin: Smurfit Institute of Genetics; TAIR: The Arabidopsis Information Resource; VGI: Virginia Bioinformatics Institute; WB: Wormbase; WGSC: Washington University Genome Sequencing Center.

Authors' contributions

JP and YHL planed and managed this project, KJ designed the web site, KJ, JP, BP, KA, JYC, and JHC implemented various functions to SNUGB, JP, JYC, SIK, and DC processed genome sequences, and JP, SK and YHL wrote the manuscript.

Acknowledgements

We thank Donghan Kim and Wonho Song for collecting genome sequences from various web sites. 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 YHL. A USDA-NRI grant to SK (2008-55605-18773) also supported this work. KJ and JP thank graduate fellowships provided by the Ministry of Education through the Brain Korea 21 Project.

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