- Data Note
- Open Access
BrassicaTED - a public database for utilization of miniature transposable elements in Brassica species
- Jayakodi Murukarthick†1,
- Perumal Sampath†1,
- Sang Choon Lee1,
- Beom-Soon Choi2,
- Natesan Senthil3,
- Shengyi Liu4 and
- Tae-Jin Yang1Email author
https://doi.org/10.1186/1756-0500-7-379
© Murukarthick et al.; licensee BioMed Central Ltd. 2014
- Received: 7 May 2014
- Accepted: 13 June 2014
- Published: 20 June 2014
Abstract
Background
MITE, TRIM and SINEs are miniature form transposable elements (mTEs) that are ubiquitous and dispersed throughout entire plant genomes. Tens of thousands of members cause insertion polymorphism at both the inter- and intra- species level. Therefore, mTEs are valuable targets and resources for development of markers that can be utilized for breeding, genetic diversity and genome evolution studies. Taking advantage of the completely sequenced genomes of Brassica rapa and B. oleracea, characterization of mTEs and building a curated database are prerequisite to extending their utilization for genomics and applied fields in Brassica crops.
Findings
We have developed BrassicaTED as a unique web portal containing detailed characterization information for mTEs of Brassica species. At present, BrassicaTED has datasets for 41 mTE families, including 5894 and 6026 members from 20 MITE families, 1393 and 1639 members from 5 TRIM families, 1270 and 2364 members from 16 SINE families in B. rapa and B. oleracea, respectively. BrassicaTED offers different sections to browse structural and positional characteristics for every mTE family. In addition, we have added data on 289 MITE insertion polymorphisms from a survey of seven Brassica relatives. Genes with internal mTE insertions are shown with detailed gene annotation and microarray-based comparative gene expression data in comparison with their paralogs in the triplicated B. rapa genome. This database also includes a novel tool, K BLAST (Karyotype BLAST), for clear visualization of the locations for each member in the B. rapa and B. oleracea pseudo-genome sequences.
Conclusions
BrassicaTED is a newly developed database of information regarding the characteristics and potential utility of mTEs including MITE, TRIM and SINEs in B. rapa and B. oleracea. The database will promote the development of desirable mTE-based markers, which can be utilized for genomics and breeding in Brassica species. BrassicaTED will be a valuable repository for scientists and breeders, promoting efficient research on Brassica species. BrassicaTED can be accessed at http://im-crop.snu.ac.kr/BrassicaTED/index.php.
Keywords
- Brassica
- Miniature inverted-repeat transposable element (MITE)
- Terminal-repeat retrotransposon in miniature (TRIM)
- Miniature form transposable elements (mTEs)
- Short interspersed elements (SINEs)
- TE Database
Findings
Background
Transposable elements (TEs) are ubiquitous and compose a large fraction of most of eukaryotic genomes. For example, more than 80% of the maize genome[1] and 40% of the B. rapa genome are occupied by transposons[2]. TEs can be mobilized and accumulated in the genome through cut and paste mechanism or a replicative transposition mechanism. Transposition of TEs can cause gene knock-out or rearrangement, altered regulation of expression, acquisition of novel function, and/or gene structure modification[3–5]. Although plant genomes have large numbers of TEs, most of them remain as non-autonomous TEs, which cannot transpose without the assistance of a “partner” element providing transposition enzymes, because of accumulation of mutations, incomplete transposition processes or genetic and epigenetic control[4, 6]. Miniature form transposable elements (mTEs) are especially small (<800 bp) TEs that are present in high copy numbers. They lack functional coding genes and rely on trans-activation by long and complete counterpart autonomous TEs[3, 7–9]. The mTEs include the terminal repeat retrotransposon in miniature (TRIM), short interspersed element (SINE) and miniature inverted-repeat transposable element (MITE)[4, 8–10] families.
TRIMs are derivatives of retrotransposons from which the coding domain for transposition has been lost. TRIMs have terminal direct repeats (TDRs) (100–250 bp) flanked by 5-bp target site duplications (TSDs) and contain an internal sequence that begins with the signature region of the primer binding site (PBS) of tRNA-methionine and ends with a polypurine tract (PPT) motif[8, 11, 12]. Studies have suggested that amplification and mobilization of TRIM elements are controlled by autonomous partner elements like LTR retrotransposons. TRIMs have been identified in various plant species and are present at moderately high levels, with 2000 copies, in the Brassica genome[8, 11, 13]. TRIM element-based markers have been effective for high quality mapping in Brassica[11].
Short interspersed elements (SINEs) are non-autonomous, non-LTR retrotransposons that are transcribed by RNA polymerase III and widely distributed in eukaryotic organisms[10, 14]. SINEs have unique structural features, with so-called head, body and tail sequences, and have been found in higher copy numbers in animals than in plants[15–17]. For instance, the Alu SINE family is present in > 1,500,000 copies in the human genome and covers > 11% of the total genome[14, 18, 19]. Propagation, maintenance and movement of SINEs are controlled by long-interspersed nucleotide elements (LINEs). To date, 210 SINE families from various plant and animal genomes including 16 SINE families related to Brassicaceae have been reported in SINEBase[20].
MITEs are small, non-autonomous class II DNA transposons that are AT-rich and have DNA structures characteristic of TEs, like terminal inverted repeats (TIRs) and TSD of variable lengths. Based on their TSD, most MITEs have been classified into several superfamilies. Stowaway superfamily members recognize 2-bp (TA) nucleotides and duplicate these at their terminal region via insertion. Similarly, Tourist superfamily members produce unique TAA duplications, hAT superfamily members produce 5-, 6-, or 8-bp TSD, Mutator superfamily members produce 9- or 10-bp TSD, and En/Spm superfamily members produce 3-bp non-unique TSD[4]. Available evidence suggests that MITEs originate through either internal deletion or cross mobilization from autonomous transposable elements[3]. MITEs can amplify into high copy numbers, although the MITEs are thought be mobilized through cut-and-paste mechanisms. Analysis of complete information for MITEs on a genome-wide scale will be important for a better understanding of how MITE transposition can produce high copy numbers, as well as of their influence on genome evolution[21].
mTEs are stably maintained and highly dispersed throughout the genome, often in association with genic regions, where they can alter gene structure and function[22, 23]. Insertion of MITEs has been reported to cause changes in pigmentation and flowering time in potato and rice, respectively[24, 25]. However, most mTE insertions may not cause phenotypic changes but can alter gene expression and epigenetic patterns[8, 26–28]. Their high copy number and close association with gene-rich regions make mTEs a potential source of molecular markers, mTE-based marker systems have been successfully developed in various species for genetic mapping as well as analysis of genetic diversity, genome-wide association and evolution[8, 29–34].
The genus Brassica (family Brassicaceae) is composed of more than 3700 species including important vegetable and oil-seed crops such as kimchi-cabbage, cabbage, and oilseed rape (B. rapa, B. oleracea and B. napus)[35]. B. rapa was the first Brassica vegetable to be sequenced and annotated, revealing recent genome triplication at 13–17 MYA, after divergence from Arabidopsis thaliana 20 MYA[2]. While only 6% of the A. thaliana genome is occupied by TEs[36, 37], around 38-40% of the B. rapa and B. oleracea genome is derived from TEs[2]. Genome analysis has suggested that TEs are important players not only in terms of genome size increases but also for gene and genome evolution, especially in the recently triplicated Brassica genome[2]. Recently, a plant MITE database was created for 41 sequenced plant genomes, and 174 MITE families from B. rapa were identified using in silico MITE identification tools[38]. However, experimental validation of identified mTE families and genome-scale characterization of their members with biological utility for Brassica species have not been developed or included in any databases. Furthermore, there is no resource with information regarding the distribution of TRIM, SINE and MITE families in various genomic regions for the Brassica species. Therefore, we aimed to establish a unique web portal containing detailed characterization of TEs in Brassica species. As a starting point, we have investigated the MITE, TRIM and SINE families of B. rapa and B. oleracea at the whole-genome scale and developed a database, BrassicaTED (Brassica Transposable Elements Database), for effective utilization of MITE, TRIM and SINEs in the Brassica genome.
Construction and content
Three-tier architecture of BrassicaTED. The client tier receives input from users and sends the request to an Apache server. The middle tier receives the request, processes it and passes it to the database tier through PHP and MySQL. The user request is extracted from MySQL as a table and displayed on a browser in the html page.
Browse
Display of the Browse and Search panels of BrassicaTED. [1-I] The Browse page for the MITE family listing characterized MITEs. [1-O] Output display of the selected MITE family. [2-I] Query page to retrieve MITE family members on each chromosome. [2-O] Result display of MITE member page. [3-O] Display of all MITE families and MITE insertion polymorphism. [4-I] Query box for Paralogs & Expression tab. [4-O] Paralog partners and ortholog gene display for selected genes.
Search
The Search section was developed to allow exploration of annotation and analysis for each mTE family in detail. In this section, there are five sub-categories: MITE Members, TRIM Members, SINE Members, IP Survey, and Gene & Expression (Figure 2).
MITE members
B. rapa pseudo-chromosome sequences with unanchored scaffolds (283 Mb) and gene annotation information (version 1.2) were obtained from the publically available database[42]. We included 20 MITE families that were identified from our studies and others in Brassica[8, 30, 43–45]. Consensus representative sequences of the 20 MITE families were used to identify their members from 283 Mb B. rapa pseudo-chromosome sequences. The physical position of each MITE on the B. rapa pseudo-chromosome was described using a custom Perl script. A total of 5894 MITEs (Br-members) were recently identified in the B. rapa genome[45]. Among them, 98% could be classified based on the type of genomic sequence in which they were located, such as intergenic region, 5’- or 3’-UTR, exon or coding sequence (CDS), and intron, whereas the remaining 2% were located on unannotated scaffolds of the B. rapa genome.
The recent availability of 385 Mb of B. oleracea pseudo-chromosome sequences (version 1.0)[46, 47] allowed that analysis to expand to the B. oleracea genome. Similar to B. rapa, a total of 6026 members (Bo-Members) were annotated based on physical position and gene annotation information for B. oleracea[42]. This work revealed that compared with Br-members, very few Bo-members (three) are present in the CDS of B. oleracea[45].
TRIM members
Characteristics of five TRIM families in the B . rapa and B . oleracea genomes
TRIM family | No. of TRIM members in B. rapa (283 Mb) genome | No. of TRIM members in B. oleracea (385 Mb) genome | Copies in A. thaliana (119 Mb) | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Total | Intergenic spacea | Near geneb | Elements in genic regions | Un mappedd | Total | Intergenic spacea | Near geneb | Elements in genic regions | ||||||||
5’ UTRc | CDS | Intron | 3’ UTRc | 5’ UTRc | CDS | Intron | 3’ UTRc | |||||||||
TB-1 | 206 | 71 | 54 | 12 | 1 | 39 | 17 | 12 | 273 | 164 | 61 | 17 | 0 | 19 | 12 | 65 |
TB-2 | 319 | 147 | 92 | 15 | 2 | 35 | 18 | 10 | 321 | 162 | 110 | 11 | 0 | 29 | 9 | 16 |
TB-3 | 52 | 22 | 7 | 4 | 3 | 8 | 4 | 4 | 51 | 25 | 15 | 3 | 1 | 3 | 4 | 0 |
TB-4 | 351 | 157 | 78 | 14 | 7 | 37 | 14 | 44 | 392 | 235 | 106 | 19 | 2 | 16 | 14 | 0 |
TB-5 | 465 | 233 | 96 | 8 | 1 | 40 | 13 | 74 | 602 | 397 | 150 | 21 | 0 | 13 | 21 | 96 |
Total | 1393 | 630 | 327 | 53 | 14 | 159 | 66 | 144 | 1639 | 983 | 442 | 71 | 3 | 80 | 60 | 177 |
SINE members
Characteristics of 16 SINE families in the B . rapa and B . oleracea genomes
SINE family | No. of SINE members in B. rapa (283 Mb) genome | No. of SINE members in B. oleracea (385 Mb) genome | Copies in A. thaliana (119 Mb) | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Total | Intergenic spacea | Near geneb | Elements in genic regions | Un mappedd | Total | Intergenic spacea | Near geneb | Elements in genic regions | ||||||||
5’ UTRc | CDS | Intron | 3’ UTRc | 5’ UTRc | CDS | Intron | 3’ UTRc | |||||||||
SB-1 | 3 | 3 | 0 | 0 | 0 | 0 | 0 | 0 | 98 | 49 | 32 | 7 | 0 | 4 | 6 | 0 |
SB-2 | 43 | 2 | 0 | 2 | 0 | 38 | 1 | 0 | 59 | 8 | 4 | 0 | 0 | 45 | 2 | 132 |
SB-3 | 134 | 70 | 36 | 6 | 0 | 12 | 6 | 4 | 278 | 156 | 80 | 20 | 0 | 9 | 13 | 4 |
SB-4 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 38 |
SB-5 | 155 | 72 | 54 | 6 | 0 | 11 | 7 | 5 | 375 | 205 | 99 | 23 | 0 | 18 | 30 | 3 |
SB-6 | 248 | 134 | 71 | 12 | 0 | 7 | 14 | 10 | 394 | 213 | 132 | 21 | 0 | 7 | 21 | 28 |
SB-7 | 372 | 202 | 106 | 17 | 0 | 11 | 20 | 16 | 355 | 197 | 119 | 16 | 0 | 2 | 21 | 3 |
SB-8 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 80 | 28 | 26 | 14 | 0 | 2 | 10 | 0 |
SB-9 | 141 | 62 | 49 | 7 | 0 | 6 | 12 | 5 | 201 | 102 | 69 | 11 | 0 | 7 | 12 | 0 |
SB-10 | 16 | 5 | 10 | 0 | 0 | 0 | 0 | 1 | 134 | 67 | 48 | 7 | 0 | 6 | 6 | 0 |
SB-11 | 4 | 4 | 0 | 0 | 0 | 0 | 0 | 0 | 56 | 22 | 25 | 3 | 0 | 2 | 4 | 0 |
SB-12 | 10 | 5 | 3 | 0 | 0 | 2 | 0 | 0 | 101 | 46 | 37 | 7 | 0 | 5 | 6 | 0 |
SB-13 | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 95 | 43 | 30 | 7 | 0 | 7 | 8 | 0 |
SB-14 | 142 | 69 | 43 | 9 | 0 | 12 | 8 | 1 | 137 | 74 | 37 | 10 | 0 | 6 | 10 | 0 |
SB-15 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | 0 |
SB-16 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 4 |
Total | 1270 | 629 | 373 | 59 | 0 | 99 | 68 | 42 | 2364 | 1210 | 738 | 146 | 1 | 120 | 149 | 212 |
Insertion polymorphism (IP) survey
MITE insertion polymorphism analysis shows intra- and inter- species polymorphism between B. rapa and B. oleracea. Representative analysis of intra (A)- and inter (B)- species polymorphism between B. rapa and B. oleracea. The original gels are shown in A and B, whereas (A’) and (B’) show the corresponding images generated based on the gel scores. The accessions used for the MIP survey are the same as those in[30].
Gene and expression analysis
BrassicaTED includes information regarding paralogous genes in B. rapa and their orthologs from A. thaliana, obtained from the B. rapa genome database[42]. Single, duplicate, and triplicate paralogs and their orthologs in A. thaliana are listed according to the gene order in A. thaliana. The expression level of B. rapa genes with internal MITE insertion was surveyed against the B. rapa 24 k microarray database, which was generated from four different stress treatments: cold (4°C), salt (250 mM NaCl), drought (air-dry) and ABA (100 μM)[49].
Tools
Display of tools panel. Display of K BLAST [A] and NCBI BLAST [B] and Sequence Extractor [C].
K BLAST
We developed a new tool, which we call K BLAST (Karyotype BLAST), to map the unique query sequence (s) onto homologous chromosomal regions and visualize the resulting distribution pattern. Users can visualize the locations of many different query sequences on each chromosome in different colors using K BLAST. It is a straightforward approach to inspect the distribution or dispersion of any DNA sequences (e.g. genes or repeats) on the chromosomes of B. rapa and B. oleracea. We have also included A. thaliana genome sequence for use in K BLAST.
BLAST
The tool panel offers the standard NCBI BLAST program for sequence similarity searches against the genome sequences. Users can match nucleotide or protein sequence (s) against database sequences such as whole-genome sequences of B. rapa, B. oleracea, and A. thaliana.
Sequence extract
We incorporated a sequence extractor tool using Python script. This can be utilized by entering single or multiple start and end positions in column tab-delimited format in the input query box for specific regions on the selected chromosome of B. rapa and B. oleracea. This tool also provides an optional input box to add flanking region length for input start and end positions.
Utility and discussion
TEs are important factors affecting genome size and genome evolution. Among those, miniature form TEs (mTEs) are valuable targets for genomics and phylogenetic studies. Comprehensive analysis and tools are desirable for effective utilization of mTEs for molecular studies, and were lacking. We developed BrassicaTED web as an interface for extensive characterization of MITEs, TRIM and SINEs in the Brassica genome. We will keep adding newly identified mTE elements to our database.BrassicaTED provides three sections (Browse, Search, and Tools) with user-friendly navigation. First, there are three parts of the Browse section: one each for MITEs, TRIMs and SINEs. Users can choose any MITE family in the list box and click ‘submit’ to enter the area pertaining to that family (Figure 2 [1-I]). This tab retrieves a summary of all MITE families included, such as MITE element classification, sequence information, structure, total members of a particular family with navigation to view the members and their closely related members, etc. (Figure 2 [1-O]). Similarly, TRIM and SINE family members can also be queried to obtain the family characterization by choosing any element from that family section. The Browse panel thus allows users to find summaries of complete information about families of MITEs, TRIMs and SINEs.In the Search panel, users can type the name of any family in the search box to find its members. Using the position drop-down option, users can filter the members returned by choosing the required genomic location (intergenic, CDS, intron, UTR) and clicking ‘Search’ for retrieval (Figure 2 [2-I]). This retrieves members of the selected family in each chromosome, their start and end positions on the chromosome, the length of the query alignment and e-value threshold, obtained from annotation (Figure 2 [2-O]). When ‘intergenic’ is chosen, the names of the two genes flanking the element are returned. When other options like CDS, intron, 5′UTR and 3′UTR are chosen, the member located in the corresponding genic regions is given with the gene name.
Brassica genomes contain triplicated homologous counterparts relative to the genome of A. thaliana[2, 50]. Recent investigation of BraSto-2 suggested that MITEs may have important roles in triplicated Brassica genome evolution[30]. BrassicaTED also provides navigation tools to determine paralogous partners and microarray-based gene expression profiles of individual mTE-inserted genes (Figure 2 [2-I]). Transposition of MITEs, TRIM and SINEs in various genomic locations can alter the gene structure and also gene expression patterns[8, 30, 44]. mTEs associated with genes may cause gene silencing, sub-functionalization or neo-functionalization. The information regarding mTE position and annotation of genes harboring mTE insertion will be helpful for association studies and candidate gene approaches by comparison of their functional diversity among a range of accessions.
The Search panel also includes IP survey, which is a valuable source for genomics, genetic diversity studies, and evolutionary analysis[31, 51, 52]. Currently, there are about 18349 IP targets from 41 mTEs known in the Brassica genome and >50-85% of them are related to genic regions. The accumulated IP marker information from 289 MITE targets (Figure 2 [3-O]) will be effectively used for Brassica genomics studies. We surveyed 289 MIP targets that provided good genetic diversity based on presence or absence of a MITE in the target region among different accessions. MIP survey profiles in seven different Brassica derivatives were scored as 1, 2 and 3 for insertion as a full site, non-insertion as an empty site and both insertion and non-insertion as corresponding full and empty sites, respectively. The gel analysis has also been included as a link and users can view the gel profile with graphical images and accession information by clicking the link (Figure 3). This information will help researchers choose MIP primers for diversity studies using their own population. We will continue to update our database with more IP analysis of mTE targets. We also welcome other researchers to submit their data regarding mTEs of Brassica species.
The next sub-section of the Search panel is ‘Gene & Expression’. As a mesopolyploid species, the B. rapa genome has been estimated to contain 41,174 protein coding genes in triplicated form compared to the genome of A. thaliana[2]. Our study on BraMi-1 MITE insertion suggests that MITEs may modify the structure of one copy among such triplicated genes and eventually its expression pattern[8, 30]. The ‘Gene & Expression’ analysis provides information regarding paralogous genes and 24 k microarray expression profiles for any gene of B. rapa. Under this sub-section, users can find differential expression patterns of mTE-inserted genes via comparison with expression of their paralogs. Users can obtain the available paralogous partner and gene sequences in FASTA format for any B. rapa gene by entering the gene ID (Figure 2 [4-I]). Clicking the ‘Expression’ link navigates to another page where the user can select expression profiles derived from four stress treatments: cold, salt, drought and ABA (Figure 2 [4-O]). The expression level of the selected genes will be shown with output as a graph or a table. This feature will be updated with more microarray datasets and can be used to analyze expression differences for any gene of interest.
Output display of the K BLAST tool using three mTE families.
In sum, we have characterized members of 41 mTE families using the whole-genome pseudo-chromosome sequences of B. rapa and B. oleracea, which allowed us to develop a database to promote effective utilization of TEs. Previously developed databases for B. rapa such as BRAD mostly handle distribution and mining of whole-genome data[42]. Similarly, the B. oleracea genome database (Bolbase)[46] was designed to provide genomic data, which mainly includes whole genome sequence, annotation and synteny comparison with B. rapa and A. thaliana. Though recently reported database for plant MITEs, P-MITE, has data for MITE families from 41 plant species, it does not provide specific information regarding MITE insertion positions in the B. rapa and B. oleracea genomes. By contrast, BrassicaTED is built to establish an interactive web platform for all types of mTEs and includes in-depth analysis of 41 mTE families in B. rapa and B. oleracea, as well as in A. thaliana. In addition, BrassicaTED provides tools to extract gene sequences and compare the expression of paralogous genes using the 24 k microarray datasets.
Conclusion
BrassicaTED is a new database exclusively made with mTEs of Brassica species, especially from B. rapa and B. oleracea. This will be an important repository to promote the utilization of mTEs and the elucidation of the effects of mTEs on genome evolution in Brassica species. Unlike other publically available Brassica databases, BrassicaTED has a unique user-friendly visualization tool (K-BLAST) and a microarray expression data comparison tool for B. rapa. BrassicaTED will be a valuable storehouse for scientists and breeders who work on Brassica species and will be continuously updated as more data is uncovered.
Availability and requirements
Datasets in BrassicaTED are freely accessible for research purposes for non-profit and academic organizations at http://im-crop.snu.ac.kr/BrassicaTED/index.php. The database is optimized for Internet Explorer, Mozilla Firefox, Google Chrome and Safari.
Notes
Declarations
Acknowledgments
This work was supported by Golden Seed Project (Center for Horticultural Seed Development, No. 309008-05-1-cg000), Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), Rural Development Administration (RDA) and Korea Forest Service (KFS), and a grant from the Next-Generation BioGreen 21 Program (No. PJ009076), Rural Development Administration, Republic of Korea. Perumal Sampath was supported by a Korean Government Scholarship (KGSP) 2008–2013 from the National Institute for International Education (NIIED), Ministry of Education, Science, and Technology, Republic of Korea.
Authors’ Affiliations
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