Open Access

IMGD: an integrated platform supporting comparative genomics and phylogenetics of insect mitochondrial genomes

  • Wonhoon Lee1, 2, 3,
  • Jongsun Park3, 4, 5, 6,
  • Jaeyoung Choi3, 4, 6,
  • Kyongyong Jung3, 4,
  • Bongsoo Park7,
  • Donghan Kim3, 4, 6,
  • Jaeyoung Lee1,
  • Kyohun Ahn4,
  • Wonho Song4,
  • Seogchan Kang7,
  • Yong-Hwan Lee3, 4, 5, 6, 8Email author and
  • Seunghwan Lee1, 2, 3Email author
Contributed equally
BMC Genomics200910:148

https://doi.org/10.1186/1471-2164-10-148

Received: 23 October 2008

Accepted: 07 April 2009

Published: 07 April 2009

Abstract

Background

Sequences and organization of the mitochondrial genome have been used as markers to investigate evolutionary history and relationships in many taxonomic groups. The rapidly increasing mitochondrial genome sequences from diverse insects provide ample opportunities to explore various global evolutionary questions in the superclass Hexapoda. To adequately support such questions, it is imperative to establish an informatics platform that facilitates the retrieval and utilization of available mitochondrial genome sequence data.

Results

The Insect Mitochondrial Genome Database (IMGD) is a new integrated platform that archives the mitochondrial genome sequences from 25,747 hexapod species, including 112 completely sequenced and 20 nearly completed genomes and 113,985 partially sequenced mitochondrial genomes. The Species-driven User Interface (SUI) of IMGD supports data retrieval and diverse analyses at multi-taxon levels. The Phyloviewer implemented in IMGD provides three methods for drawing phylogenetic trees and displays the resulting trees on the web. The SNP database incorporated to IMGD presents the distribution of SNPs and INDELs in the mitochondrial genomes of multiple isolates within eight species. A newly developed comparative SNU Genome Browser supports the graphical presentation and interactive interface for the identified SNPs/INDELs.

Conclusion

The IMGD provides a solid foundation for the comparative mitochondrial genomics and phylogenetics of insects. All data and functions described here are available at the web site http://www.imgd.org/.

Background

The mitochondrial genomes of members of the superclass Hexapoda (generally referred to as the 'insects') are typically approximately 15 kilobases (kb) in length and encode 37 genes, including 13 protein coding genes (PCGs), 2 ribosomal RNA genes (rRNAs), and 22 transfer RNA genes (tRNAs). Owing to its small size, high copy number, and relatively infrequent gene rearrangements, the mitochondrial genome has been extensively used for phylogenetic analyses [14]. Phylogenetic analysis based on the mitochondrial gene sequences is often limited to closely related species, due to the high rate of nucleotide substitutions. However, variations in the mitochondrial gene content and order have been utilized to elucidate evolutionary relationships among distantly-related species, on the basis of shared derived characteristics that denote the common ancestry of a given group [5].

Recent years, the number of sequenced mitochondrial genomes has been increasing fast due to rapidly growing sequencing capacity [6]. For example, more than 1,200 metazoan mitochondrial genomes have already been sequenced completely [7, 8]. The abundance of available mitochondrial genomes has led to the development of the following web-based relational databases that are specialized for archiving the resulting data: GObase [9], AMiGA [10], Mitome [8], MamMibase [11], OGRe [7], and NCBI Organelle Genome Resources [12]. Some of these resources also provide tools for data analysis and/or viewing: MamMibase provides a web-based phylogenetic analysis tool for studying evolutionary relationships on the basis of the archived mitochondrial genomes [11] and Mitome provides a graphical mitochondrial genome browser [8]. In order to more effectively support uses of the rapidly accumulating mitochondrial genome sequences, an integrated platform that provides a diverse array of analysis tools is necessary.

Single nucleotide polymorphisms (SNPs) in the insect mitochondrial genome sequences can support fine-scale phylogenetic analyses, as illustrated in the following examples. Twenty-four biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae), which could not be distinguished by morphological characteristics, were resolved [13]. SNPs in the cytochrome c oxidase subunits I (COI) locus of Aedes aegypti (Diptera: Cuclicidae) were used to differentiate four strains [14]. Based on the fully sequenced mitochondrial genomes in the genus Flustrellidra (Ctenostomata: Flustrellidridae), a SNP analysis was conducted to identify a suitable gene maker for distinguishing morphologically similar species [15].

Partially sequenced mitochondrial genes from a very large number of species also provide valuable markers for phylogenetic analysis. For example, the COI gene has been used extensively for species identification in the 'DNA barcoding' projects [16, 17]. In particular, in Hexapoda, DNA barcoding projects covering multiple orders have been conducted [1821], resulting in at least 50,000 partial sequences of COI loci in the NCBI. Because the cytochrome c oxidase subunits II (COII) locus is relatively small (approximately 600 bp) and can be amplified well by PCR from diverse species [22, 23], many researchers have sequenced this locus, yielding more than 15,000 sequences from Hexapoda. Due to the large number of characterized insect species, sequences of these loci are an excellent resource for comprehensive phylogenetic analyses of insects; however, such data have not yet been archived in the currently available mitochondrial genome databases.

A new integrated platform named the Insect Mitochondrial Genome Database (IMGD; http://www.imgd.org/) was developed to better integrate available mitochondrial gene and genome sequences and to provide bioinformatics tools for efficient data retrieval and utilization. The IMGD archives the sequences of 112 completely sequenced and 20 nearly completed mitochondrial genome sequences, as well as partial sequences of 113,985 mitochondrial genomes (Tables 1, 2, 3) from 25,747 insect species using the standardized framework of the Comparative Fungal Genomics Platform (CFGP; http://cfgp.snu.ac.kr/) [24]. SNPs in the mitochondrial genomes of multiple isolates within eight species were identified via the SNP Analysis Platform (SAP; http://sap.snu.ac.kr/; J. Park et al., unpublished) and presented through the SNU Genome Browser (http://genomebrowser.snu.ac.kr/) [25]. BLAST [26], tRNAScan-SE [27], and mFold [28] were also incorporated into IMGD. Additionally, three phylogenetic analysis tools, including ClustalW, PHYML, and PHYLIP [2931], were integrated into IMGD to facilitate analyses across multiple species: these tools are available through the web interface supported by Phyloviewer (http://www.phyloviewer.org/; B. Park et al., unpublished). To assist the comparison of these sequences and phylogenetic analysis within selected taxa, a new user interface, termed the Species-driven User Interface (SUI), was designed and implemented. The IMGD provides a highly integrated environment for conducting evolutionary studies of insects using their mitochondrial gene/genome sequences.
Table 1

List of the number of mitochondrial sequences in Hexapoda archived in the IMGD

Order

Species

CGa

NGb

PGc

Archaeognatha

10

4

0

15

Blattaria

274

1

0

991

Coleoptera

6,594

8

4

25,783

Collembola

133

6

2

947

Dermaptera

35

0

0

63

Diplura

10

3

0

24

Diptera

3,846

24

2

26,982

Embioptera

14

0

0

26

Ephemeroptera

288

1

0

742

Grylloblattodea

17

0

1

113

Hemiptera

1,851

20

5

7,299

Hymenoptera

4,144

3

2

14,737

Isoptera

647

7

0

2,842

Lepidoptera

4,556

7

2

19,380

Mantodea

188

1

0

717

Mantophasmatodea

17

1

0

194

Mecoptera

61

0

0

141

Megaloptera

7

2

0

409

Neuroptera

143

2

0

437

Odonata

525

0

1

1,734

Orthoptera

919

14

0

4,744

Phasmatodea

64

0

1

482

Phthiraptera

527

3

0

2,155

Plecoptera

184

1

0

529

Protura

2

0

0

6

Psocoptera

121

1

0

338

Raphidioptera

4

0

0

5

Siphonaptera

35

0

0

134

Strepsiptera

6

0

0

7

Thysanoptera

154

1

0

857

Trichoptera

343

0

0

1,100

Zoraptera

1

0

0

2

Zygentoma

27

2

0

50

Total

25,747

112

20

113,985

aCompletely sequenced mitochondrial genome, bNearly completely sequenced mitochondrial genome, and cPartially sequenced mitochondrial gene sequences

Table 2

List of 56 whole mitochondrial genomes of hexapod species (Part I. 52 holometabolous species) archived in IMGD

Order

Species

Size (bp)

GC (%)

PCGs

tRNAs

rRNAs

Coleoptera

Chaetosoma scaritides*

15,511

20.96

13

22

2

Coleoptera

Crioceris duodecimpunctata

15,880

23.11

13

22

2

Coleoptera

Cyphon sp. BT0012

15,919

24.83

13

22

2

Coleoptera

Priasilpha obscura*

16,603

23.49

13

22

2

Coleoptera

Pyrocoelia rufa

17,739

22.59

13

22

2

Coleoptera

Pyrophorus divergens

16,120

30.56

13

22

2

Coleoptera

Rhagophthalmus lufengensis

15,982

20.37

13

22

2

Coleoptera

Rhagophthalmus ohbai

15,704

20.85

13

19

2

Coleoptera

Sphaerius sp. BT0074*

15,121

19.28

13

22

2

Coleoptera

Tetraphalerus bruchi

15,689

33.01

13

22

2

Coleoptera

Trachypachus holmbergi*

15,722

20.54

13

22

2

Coleoptera

Tribolium castaneum

15,881

28.32

13

22

2

Diptera

Anopheles funestus*

15,354

21.84

7

22

2

Diptera

Anopheles gambiae

15,363

22.44

13

22

2

Diptera

Anopheles quadrimaculatus A Orlando

15,455

22.64

13

22

2

Diptera

Bactrocera oleae Italy

15,815

27.41

13

22

2

Diptera

Bactrocera oleae Portugal

15,815

27.37

13

22

2

Diptera

Ceratitis capitata

15,980

22.52

13

22

2

Diptera

Chrysomya putoria

15,837

23.30

13

23

2

Diptera

Cochliomyia hominivorax

16,022

23.10

13

22

2

Diptera

Cydistomyia duplonotata

16,247

22.07

13

23

2

Diptera

Drosophila ananassae

14,920

22.59

13

22

2

Diptera

Drosophila erecta

14,952

22.77

13

22

2

Diptera

Drosophila grimshawi

14,874

23.24

13

22

2

Diptera

Drosophila mauritiana G52

14,964

22.29

13

22

2

Diptera

Drosophila melanogaster

19,517

17.84

13

22

2

Diptera

Drosophila mojavensis

14,904

23.54

13

22

2

Diptera

Drosophila simulans KY007

14,946

22.33

13

22

2

Diptera

Drosophila simulans KY045

14,946

22.36

13

22

2

Diptera

Drosophila simulans KY201

14,946

22.32

13

22

2

Diptera

Drosophila simulans KY215

14,946

22.33

13

22

2

Diptera

Drosophila persimilis

14,930

22.70

13

22

2

Diptera

Drosophila virilis

14,949

23.25

13

22

2

Diptera

Drosophila willistoni

14,915

22.76

13

22

2

Diptera

Drosophila yakuba

16,019

21.41

13

22

2

Diptera

Simosyrphus grandicornis

16,141

19.16

13

22

2

Diptera

Stomoxys calcitrans*

16,790

21.07

12

23

2

Diptera

Trichophthalma punctata

16,396

26.04

13

21

2

Hymenoptera

Abispa ephippium

16,953

19.39

13

26

2

Hymenoptera

Apis mellifera

16,343

15.14

13

22

2

Hymenoptera

Bombus ignites

16,434

13.22

13

22

2

Hymenoptera

Vanhornia eucnemidarum*

16,574

19.86

13

18

2

Hymenoptera

Xenos vesparum*

14,519

20.68

13

23

1

Lepidoptera

Adoxophyes honmai

15,680

19.61

13

22

2

Lepidoptera

Bombyx mandarina

15,928

18.32

13

22

2

Lepidoptera

Bombyx mori C-108

15,656

18.64

13

22

2

Lepidoptera

Coreana raphaelis

15,314

17.34

13

23

2

Lepidoptera

Manduca sexta

15,516

18.21

13

23

2

Lepidoptera

Ochrogaster lunifer

15,593

22.16

13

22

2

Lepidoptera

Ostrinia furnacalis*

14,536

19.62

13

22

2

Lepidoptera

Ostrinia nubilalis*

14,535

19.84

13

22

2

Lepidoptera

Saturnia boisduvalii

15,360

19.38

13

22

2

Megaloptera

Corydalus cornutus

15,687

25.10

13

22

2

Megaloptera

Protohermes concolorus

15,851

24.17

13

22

2

Neuroptera

Ascaloptynx appendiculatus

15,877

24.43

13

22

2

Neuroptera

Polystoechotes punctatus

16,036

21.04

12

22

2

*Nearly completely sequenced mitochondrial genome.

Table 3

List of 76 whole mitochondrial genomes of hexapod species (Part II. 73 species excluding holometabolous orders) archived in IMGD

Order

Species

Size (bp)

GC (%)

PCGs

tRNAs

rRNAs

Archaeognatha

Nesomachilis australica

15,474

31.17

13

21

2

Archaeognatha

Pedetontus silvestrii

15,879

25.66

13

22

2

Archaeognatha

Petrobius brevistylis

15,698

32.12

13

22

2

Archaeognatha

Trigoniophthalmus alternatus

16,197

28.59

13

22

2

Zygentoma

Thermobia domestica

15,152

33.01

13

22

2

Zygentoma

Tricholepidion gertschi

15,267

31.40

13

22

2

Collembola

Cryptopygus antarcticus

15,297

29.10

13

23

2

Collembola

Gomphiocephalus hodgsoni

15,075

25.92

13

22

2

Collembola

Friesea grisea

15,425

27.73

13

22

2

Collembola

Onychiurus orientalis*

12,984

30.89

13

20

1

Collembola

Orchesella villosa

14,924

27.82

13

22

2

Collembola

Podura aquatica*

13,809

34.21

13

20

1

Collembola

Sminthurus viridis

14,817

30.56

13

22

2

Collembola

Tetrodontophora bielanensis

15,455

27.32

13

22

2

Diplura

Campodea fragilis

14,965

27.44

13

22

2

Diplura

Campodea lubbocki

14,974

25.19

13

22

2

Diplura

Japyx solifugus

15,785

35.18

13

22

2

Ephemeroptera

Parafronurus youi

15,481

33.62

13

23

2

Odonata

Orthetrum triangulare melania*

14,033

26.09

13

19

2

Grylloblattodea

Grylloblatta sculleni*

15,595

29.71

12

19

2

Blattaria

Periplaneta fuliginosa

14,996

24.85

13

22

2

Isoptera

Reticulitermes flavipes IS13

16,565

33.82

13

22

2

Isoptera

Reticulitermes flavipes IS57

16,569

33.76

13

22

2

Isoptera

Reticulitermes flavipes IS58

16,567

33.78

13

22

2

Isoptera

Reticulitermes hageni

16,590

34.45

13

22

2

Isoptera

Reticulitermes santonensis IS54

16,567

33.91

13

22

2

Isoptera

Reticulitermes virginicus IS59

16,513

34.12

13

22

2

Isoptera

Reticulitermes virginicus IS60

15,966

34.37

13

22

2

Mantodea

Tamolanica tamolana

16,055

24.73

13

22

2

Mantophasmatodea

Sclerophasma paresisense

15,500

24.94

13

22

2

Orthoptera

Acrida willemsei

15,601

23.78

13

22

2

Orthoptera

Anabrus simplex

15,766

30.56

13

22

2

Orthoptera

Calliptamus italicus

15,675

26.74

13

22

2

Orthoptera

Chorthippus chinensis

15,599

24.89

13

22

2

Orthoptera

Deracantha onos

15,650

30.76

13

22

2

Orthoptera

Gryllotalpa orientalis

15,521

29.51

13

22

2

Orthoptera

Gryllotalpa pluvialis

15,525

27.80

13

22

2

Orthoptera

Locusta migratoria

15,722

24.67

13

22

2

Orthoptera

Myrmecophilus manni

15,323

29.82

13

22

2

Orthoptera

Oxya chinensis

15,443

24.11

13

22

2

Orthoptera

Ruspolia dubia

14,971

29.14

13

22

2

Orthoptera

Gastrimargus marmoratus

15,924

24.82

13

22

2

Orthoptera

Gampsocleis gratiosa

15,929

34.69

13

22

2

Orthoptera

Troglophilus neglectus

15,810

26.63

13

23

2

Phasmatodea

Timema californicum*

14,387

27.86

13

19

1

Plecoptera

Pteronarcys princeps

16,004

28.54

13

22

2

Hemiptera

Aeschyntelus notatus*

14,532

24.29

13

22

2

Hemiptera

Aleurochiton aceris

15,388

22.10

13

21

2

Hemiptera

Aleurodicus dugesii

15,723

13.67

13

20

2

Hemiptera

Bemisia tabaci

15,322

24.32

13

22

2

Hemiptera

Coptosoma bifaria

16,179

28.67

13

22

2

Hemiptera

Dysdercus cingulatus

16,249

22.31

13

22

2

Hemiptera

Geocoris pallidipennis*

14,592

24.14

13

22

2

Hemiptera

Hydaropsis longirostris

16,521

24.54

13

22

2

Hemiptera

Macroscytus subaeneus*

14,620

26.21

13

22

2

Hemiptera

Malcus inconspicuus

15,575

22.20

13

22

2

Hemiptera

Neomaskellia andropogonis

14,496

18.73

13

18

2

Hemiptera

Neuroctenus parus

15,354

31.14

13

22

2

Hemiptera

Nezara viridula

16,889

23.12

13

22

2

Hemiptera

Orius niger*

14,494

23.47

13

22

2

Hemiptera

Pachypsylla venusta

14,711

25.00

13

22

2

Hemiptera

Phaenacantha marcida*

14,540

26.54

13

22

2

Hemiptera

Philaenus spumarius

16,324

23.01

13

22

2

Hemiptera

Physopelta gutta

14,935

25.49

13

22

2

Hemiptera

Riptortus pedestris

17,191

23.41

13

22

2

Hemiptera

Saldula arsenjevi

15,324

25.39

13

22

2

Hemiptera

Schizaphis graminum

15,721

16.06

13

22

2

Hemiptera

Tetraleurodes acacia

15,080

28.02

13

19

2

Hemiptera

Trialeurodes vaporariorum

18,414

27.70

13

22

2

Hemiptera

Triatoma dimidiate

17,019

30.43

13

22

2

Hemiptera

Yemmalysus parallelus

15,747

22.82

13

22

2

Phthiraptera

Bothriometopus macrocnemis

15,564

29.20

13

25

2

Phthiraptera

Campanulotes bidentatus

14,804

29.88

13

22

2

Phthiraptera

Heterodoxus macropus

14,670

20.72

13

22

2

Psocoptera

Lepidopsocid sp. RS2001

16,924

20.98

13

22

2

Thysanoptera

Thrips imaginis

15,407

23.43

13

23

2

*Nearly completely sequenced mitochondrial genome.

Construction and content

System architecture and design

The IMGD consists of three integrated layers: i) a standardized data warehouse that is supported by CFGP [24], ii) the middleware platform for the integration of various bioinformatics programs via standardized input and output interfaces, and iii) the web-based user interface, including the Species-driven User Interface (Figure 1A). In order to support the efficient archiving and analysis of a very large number of heterogeneous mitochondrial gene sequences (Table 2 and Table 3), a standardized structure for sequence data was required: this requirement was solved using CFGP [24], which has demonstrated its reliability and expandability via several published databases [3237].
Figure 1

The system architecture and pipeline of IMGD. (A) Each rectangular box shows three layers. In the standardized data warehouse, diverse databases are placed. The middleware platform manages not only BLAST, tRNAScan-SE, and mFold but also six phylogenetic tools managed by Phyloviewer (http://www.phyloviewer.org/). The web-based user interface supports browsing all information deposited in IMGD. (B) The pipeline for archiving hexapod mitochondrial sequences and calculating their properties was presented as a flowchart diagram.

To support phylogenetic studies using the archived hexapod mitochondrial sequences, ClustalW (Version 1.83), PHYLIP (Version 3.68), and PHYML (Version 3.0) [2931], which support the Neighbour Joining (NJ), Maximum Parsimony (MP), and Maximum Likelihood (ML) methods, respectively, were incorporated. The visualization and management of the resulting phylogenetic data are supported by the Phyloviewer (http://www.phyloviewer.org/), which has been successfully employed in other platforms [24, 34, 35]. BLAST [26] was integrated with datasets containing mitochondrial gene sequences and hexapod taxonomy information, and tRNAscan-SE (Version 1.23) [27] and mFold (Version 3.2) [28] were embedded to allow for the display and comparison of secondary structures of tRNAs and anticodon sequences.

The user interface of IMGD provides the Mitochondrial Genome Browser, which is founded on the SNU Genome Browser (http://genomebrowser.snu.ac.kr/) [25], to support the browsing and comparison of mitochondrial genome sequences in both the text and graphical forms via an interactive interface, and the Partial Sequence Browser to allow for the browsing of partially sequenced mitochondrial sequences. The IMGD also provides the Object Browser, which can collect and move selected sequences in IMGD into the Favorite, a personalized virtual storage space, for further data analyses using the analysis tools in both IMGD and CFGP [24]. The IMGD archives sequences and taxonomical information from more than 25,000 hexapod species. To facilitate the organization and presentation of data according to the taxonomic position/grouping of the species of origin, a new interface named the Species-driven User Interface (SUI) was designed and implemented in IMGD.

Pipeline for updating the IMGD data warehouse

To support periodic updating of the IMGD data warehouse, the following automatic analysis pipeline was developed (Figure 1B). In the first step, completely and partially sequenced mitochondrial genome sequences are downloaded from NCBI using proper keywords after filtering out unpublished sequences. The downloaded sequences are subsequently filtered using several stop words in order to remove non-mitochondrial sequences. Secondly, the mitochondrial genome parsers, which were written in PERL, parse and store the filtered data into the data warehouse. Thirdly, adjoined stop codons at the 3'-end of the PCGs that overlap with neighboring PCGs or tRNAs in the mitochondrial genome [38], are manually checked to determine whether they are correct or not. Lastly, certain properties of the genome, including the CG content, AT skew, and codon usage, are calculated for graphical representations via SNU Genome Browser, and various cache tables are updated. In the final step, BLAST datasets, tRNA annotation information via both tRNAScan-SE [27] and mFold [28], and SNP databases are updated.

Taxonomic origins of the sequences data archived in IMGD

The IMGD archives 132 hexapod mitochondrial genomes and 113,985 GenBank accessions of partially sequenced mitochondrial genes, consisting of 102,430 PCGs, 19,452 rRNAs, and 17,944 tRNAs, from 25,747 species belonging to 33 orders (Table 1). More than 10,000 mitochondrial gene sequences were derived from >1,000 species in the orders Coleoptera, Lepidoptera, Hymenoptera, and Diptera. In particular, members of Diptera and Coleoptera account for 26 (20.00%) and 12 (9.23%) mitochondrial genomes, respectively, reflecting active researches on these orders [39, 40]. In contrast, the following 13 orders (39.39%) are represented only by less than 50 species in total: Dermaptera, Siphonaptera, Zygentoma, Grylloblattodea, Mantophasmatodea, Embioptera, Diplura, Archaeognatha, Strepsiptera, Megaloptera, Raphidioptera, Protura, and Zoraptera (Table 1). The underrepresentation of mitochondrial gene sequences from many orders suggests that to adequately support the analysis of evolutionary relationships within the Hexapoda, these underrepresented orders require more attention.

Notable features in hexapod mitochondrial genomes

The genome size, GC content, and the number of PCGs, tRNAs, and rRNAs of the 132 mitochondrial genomes archived in IMGD (Table 2 and Table 3) were assessed (Figure 2). The GC content ranges from 13.22% to 35.18% with an average of 25.09%, showing the association at the order level (Figure 2A). The genome sizes vary from 12,984 bp to 19,517 bp, with an average of 15,617 bp with no clear correlation at any taxon levels (Figure 2B). Analyses of gene order in the 112 completely sequenced mitochondrial genomes revealed several interesting features. In 42 genomes (37.50%), which represent 12 orders, at least 222 gene insertions, deletions, inversions, and translocations were identified relative to the gene arrangement of the ancestral insect Drosophila yakuba [3, 41] (Lee et al., in preparation). Gene translocations and inversions were detected in the following 12 orders: Collembola, Archaeognatha, Zygentoma, Hemiptera, Thysanoptera, Psocoptera, Phthiraptera, Neuroptera, Hymenoptera, Orthoptera, Lepidoptera, and Diptera. Gene insertions and deletions were detected in Collembola, Ephemeroptera, Orthoptera, Hemiptera, Phthiraptera, Diptera, and Lepidoptera.
Figure 2

Estimates of the GC content and genome size of the 132 hexapod mitochondrial genomes. (A) The ranges of the GC content in the nearly completely and the completely sequenced mitochondrial genomes are shown. The closed red circle indicates the average GC content, and the blue and red bars present the maximum and minimum GC contents, respectively. (B) The distribution of mitochondrial genome sizes in different hexapod orders is shown. The closed red circle indicates the average mitochondrial genome size and the blue and red bars present the largest and smallest genome sizes, respectively (see also Table 2 and Table 3).

Examples of phylogenetic analyses results using insectmitochondrial genomes

To demonstrate the utility of IMGD for phylogenetic analysis and also to test the system, many phylogenetic analyses using the data archived in IMGD have been conducted (e.g., Figure 3). Figure 3A shows an ML phylogenetic tree based on 19 completely sequenced and 5 nearly completed mitochondrial genomes in the order Hemiptera, which clearly shows two major suborder clades (Sternorrhyncha + Auchenorrhyncha and Heteroptera). The MP trees based on the COI gene sequences (Figure 3B and 3C) revealed more comprehensive phylogenetic relationships than those derived from previous studies in the orders Phthiraptera [4244] and Mantophasmatodea [45, 46].
Figure 3

Examples of phylogenetic analyses conducted using data and tools in IMGD. (A) ML tree of the 24 Hemipteran species (19 completely and 5 nearly completed mitochondrial genomes) with Thrips imaginis (Thysanoptera) as an outgroup was constructed using DNAML. S, Sternorrhyncha; A, Auchenorrhyncha; H, Heteroptera. (B) MP tree built based on 88 COI sequences from 70 Phthirapteran species using DNAPARS, is shown. Ptycta johnsoni (Psocoptera) was used as an outgroup. The blue square indicates the sequences originated from Johnson and Whiting (2002) [42]; green square, Johnson et al. (2003) [43]; blue triangle, Price and Johnson (2006) [44]; red, violet and yellow squares, and red triangle present unpublished mitochondrial gene sequences. (C) MP tree using 90 COI sequences from 14 Mantophasmatodean species, with Galloisiana yuasai (Grylloblattodea) as an outgroup, was drawn using DNAPARS. The red circle indicates the mitochondrial sequences reported by Damgaard et al. (2008) [46] and violet circle presents the sequences from the study of Klass et al. (2003) [45]. The numbers on individual nodes of the trees in A, B, and C indicate bootstrap values with 10, 100, and 100 repeats, respectively, and the names of the species used and NCBI accession numbers are shown at the end of individual branches.

Single Nucleotide Polymorphisms among 9 insect mitochondrial genomes

Single nucleotide polymorphisms (SNPs) in eight species with more than one mitochondrial genome having been sequenced (Table 4), were analyzed via the SNP Analysis Platform (http://sap.snu.ac.kr/), which is based on BLAST. A total of 856 SNPs and 30 insertion and deletions (INDELs) were identified (Table 4) from 187 kbp of aligned mitochondrial genome sequences (6 pair-wise comparisons of mitochondrial genomes). Among these, 621 SNPs (72.55%) were identified in 13 PCGs and designated as cSNPs. Figure 4 shows the average number of cSNPs in each species, order and PCG. Bactrocera oleae (BO), Drosophila simulans (DS), and Reticulitermes flavipes (RF) exhibited the highest frequency of cSNPs, similar to the results from previous genome sequence analyses [4749]. Among the 13 PCGs, the COI, NADH dehydrogenase subunit 4 (ND4), and/or NADH dehydrogenase subunit 5 (ND5) genes showed the highest frequency of SNPs in Diptera (COI and ND5) and Isoptera (cytochrome b, ND4, and ND5) (Figure 4). These regions can serve as potential molecular markers in population genetic studies of these three orders.
Table 4

List of mitochondrial genome comparisons for SNP analysis

Order

Source/Target Species

Size (bp)

Aligned (bp)

SNPs

INDELs

Diptera

Bactrocera oleae Italy vs

15,815

15,815

31

0

 

Bactrocera oleae portugal

15,815

15,815

  
 

Drosophila simulans KY007

14,946

14,946

25

2

 

Drosophila simulans KY045

14,946

14,946

  
 

Drosophila simulans KY007

14,946

14,946

17

2

 

Drosophila simulans KY201

14,946

14,946

  
 

Drosophila simulans KY007

14,946

14,946

6

0

 

Drosophila simulans KY215

14,946

14,946

  

Isoptera

Reticulitermes flavipes IS13 vs

16,565

16,561

393

14

 

Reticulitermes flavipes IS57

16,569

16,565

  
 

Reticulitermes flavipes IS13 vs

16,565

16,561

384

12

 

Reticulitermes flavipes IS58

16,567

16,563

  

Total

6 pair-wise comparisons

187,572

187,556

856

30

Figure 4

Distribution of SNPs in 13 PCGs in 9 mitochondrial genomes. The bar graph displays the distribution of SNPs in 13 PCGs of three insect species: BO, Bactrocera oleae; DS, Drosophila simulans; RF, Reticulitermes flavipes. ATP6 and 8 (ATP synthase subunit 6 and 8); COX1–3 (cytochrome c oxidase subunits I–III); CYTB (cytochrome b); ND1–6 (NADH dehydrogenase subunits 1–6); ND4L (NADH dehydrogenase subunit 4L) (see also Table 4).

Utilities and discussion

Species-driven User Interface (SUI)

The SUI of IMGD supports efficient data retrieval and analysis at multi-taxon levels. The SUI was developed using Ajax technology, which supports faster performance than other methods (e.g. JavaScript and Java applets). The SUI helps the users of IMGD search hexapod taxa using the 'Species search' and supports the addition and deletion of selected insect species via the 'Species cart' function, which is similar to the cart functions commonly used on online shopping sites (Figure 3). After placing the taxa of interest in the cart, they can be analyzed in the following ways: i) downloading nucleotide and protein sequences and/or storing them into the Favorite with various options, ii) comparing gene orders, GC content/AT skew, codon usage and position among mitochondrial genomes, iii) displaying tRNA secondary structures predicted by tRNAScan-SE [27] and mFold [28], iv) executing ClustalW for multiple sequence alignment and calculating phylogenetic trees based on three methods, including NJ, MP, and ML, with a bootstrapping option, v) executing a BLAST search against the selected taxa, and vi) saving species information into the Favorite for future analyses (Figure 5). Since SUI was designed using a standardized application programming interface (API), additional programs can be easily incorporated into SUI.
Figure 5

Species-driven User Interface (SUI) optimized for collecting data based on taxa. The Species-driven User Interface (SUI) consists of three parts: i) Species search, ii) Taxon browser, and iii) Species cart. The Species search function supports the search of species by species name. The Taxon browser provides the interface for browsing taxa in a hierarchical manner. The Species cart can store selected taxa, bridging the data from them to nine bioinformatics tools.

Gene order browser for graphical presentation of elements on the mitochondrial genome

Gene rearrangement events in the mitochondrial genomes can be used for tracing the evolutionary history of the mitochondrial genomes in Hexapoda (Lee et al., in preparation). The gene order browser implemented in IMGD was designed for efficient graphical presentation of PCGs, tRNAs, and rRNAs in the mitochondrial genome. To display different features on the genome graphically, the browser uses three different colors for PCGs, tRNAs, and rRNAs, and presents names of individual units (Figure 6). Moreover, the gene order browser displays the gene organizations using a specific gene as the start site for the linear genome diagrams regardless of the arbitrary start position given to individual mitochondrial genomes. Users can choose the number of mitochondrial genomes to be displayed by selecting them via SUI.
Figure 6

Gene order browser for graphical presentation of the mitochondrial gene order. The gene order browser consists of two parts: one is the option window and the other is the gene order diagram. In the option window, three options, including width, categories, and components, are displayed. After clicking 'Apply Options,' a gene order diagram based on the chosen option will be displayed. To indicate the nature of specific genetic elements on displayed mitochondrial genomes, the following abbreviations were used: A, tRNA-Ala;C, tRNA-Cys; D, tRNA-Asp; E, tRNA-Glu; F, tRNA-Phe; G, tRNA-Gly; H, tRNA-His; I, tRNA-Ile; K, tRNA-Lys; L, tRNA-Leu; M, tRNA-Met; N, tRNA-Asn; P, tRNA-Pro; Q, tRNA-Gln; R, tRNA-Arg; S, tRNA-Ser; T, tRNA-Thr; V, tRNA-Val; W, tRNA-Trp; Y, tRNA-Tyr; COX1–3, cytochrome c oxidase subunits I–III; CYTB, cytochrome b; ATP6 and ATP8, subunits 6 and 8 of the F0ATPase; ND1–6 and nad4L, NADH dehydrogenase subunits 1–6 and 4L; l-r and s-r, large and small subunit of ribosomal RNA genes; PCGs, protein coding genes; rRNAs, ribosomal RNA genes; tRNAs, transfer RNA genes.

Integrated platform for phylogenetic analyses supported by Phyloviewer

The Phyloviewer (http://www.phyloviewer.org/) provides four phylogenetic analysis programs (ClustalW, DNAPARS/PROTPARS, DNAML/PROML, and PHYML [2931]) via a common interface to support phylogenetic studies based on the mitochondrial gene/genome sequences archived in IMGD. Three different methods of drawing phylogenetic trees (NJ, MP, and ML) are currently available. In addition, the interactive capability of graphical presentation of sequence alignments and selecting and storing all sequences under a selected node in the resulting phylogenetic tree by clicking the node is also provided.

Comparative mitochondrial genomics via the SNU Genome Browser

To support intuitive visualization of sequences, SNPs, and INDELs between two mitochondrial genomes, the SNU Genome Browser (http://genomebrowser.snu.ac.kr/)[25] was implemented. This recently developed genome browser provides an interactive user interface that supports visualization of the alignment region between genomes with the capability of comparing multiple genomes simultaneously (Figure 7). It also supports the text browser function for displaying nucleotide sequences of a selected region, supporting the confirmation of SNPs and INDELs. The table browser provides a list of individual elements present in the selected region with their positional information in a tabular form.
Figure 7

Interactive graphical interface for visualizing aligned mitochondrial genomes via the SNU Genome Browser. The SNU Genome Browser displays SNPs/INDELs as well as PCGs, tRNAs, GC contents among the aligned genomes of Drosophila simulans KY007, KY045, and K201 strains.

Favorite, a personalized virtual space for storing data and conducting further analysis

Most of the data analysis and/or retrieval interfaces in IMGD provide the Object Browser, which allows users to save all or selected sequences and/or species shown into Favorite. This will help users manage their own datasets via IMGD. Through the interface of Favorite, BLAST, six different phylogenetics programs, and four data analysis tools are available for further analyses (Figure 8). The Favorite is linked to CFGP (http://cfgp.snu.ac.kr/), which provides not only diverse bioinformatic tools but also a data warehouse containing complete sequences of 19 insect nuclear genomes [24], so that further analyses with diverse resources can be conducted easily via this web interface.
Figure 8

Favorite, a personalized virtual space for data storage and further analyses. The browser in Favorite provides four options: 'Edit,' 'Function,' 'Analysis,' and 'Download.' Any sequences listed at the bottom part can be selected by users for analyzing the selected sequences using seven programs and four analysis tools via the web.

Conclusion

We developed IMGD to support versatile comparative analyses of hexapod mitochondrial gene/genome sequences. In IMGD, 132 completely or nearly-completely sequenced mitochondrial genomes and 113,985 mitochondrial gene sequences from 25,747 species were archived. The IMGD provides a variety of phylogenetic analysis tools via Phyloviewer, which supports the interactive graphical presentation of resultant phylogenetic trees. The IMGD, supported by the SNP analysis platform and the SNU Genome Browser, provides a graphical view of mitochondrial genome comparisons. In the near future, additional analysis tools, such as PAML [50] for the determination of positive/negative selection based on dS/dN values, will be integrated into IMGD. Moreover, based on the database of widely sequenced mitochondrial genes, an insect species identification system based on multiple loci can be developed. The IMGD is expected to significantly enhance evolutionary studies on the superclass Hexapoda using rapidly accumulating insect mitochondrial genome sequences.

Availability and requirements

All data described in this paper can be browsed and downloaded through the IMGD web site at http://www.imgd.org/.

Notes

Declarations

Acknowledgements

This research was supported by Korea Ministry of Environment as "The Eco-technopia 21 project", a grant from by Agricultural R&D Promotion Center, and a grant from Biogreen21 Project (20070301034032) to S.L. It was also supported by a grant from Crop Functional Genomics Center (CG1141), Korean Research Foundation Grant (KRF-2006-005-J04701), Biogreen21 Project (20080401034044) funded by Rural Development Administration and the Korea Science and Engineering Foundation (KOSEF) grant funded by the Korea government (MEST) (R11-2008-062-03001-0) to Y.H.L. J.P. acknowledges a graduate fellowship provided by the Ministry of Education through the Brain Korea 21 Project.

Authors’ Affiliations

(1)
Insect Biosystematics Laboratory, Seoul National University
(2)
Research Institute for Agricultural and Life Sciences, Seoul National University
(3)
Department of Agricultural Biotechnology, Seoul National University
(4)
Fungal Bioinformatics Laboratory, Seoul National University
(5)
Center for Fungal Pathogenesis, Seoul National University
(6)
Center for Fungal Genetic Resources, Seoul National University
(7)
Department of Plant Pathology, Penn State University
(8)
Center for Agricultural Biomaterials, Seoul National University

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This article is published under license to 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.