RoBuST: an integrated genomics resource for the root and bulb crop families Apiaceae and Alliaceae
- Ashwini Bhasi1,
- Doug Senalik2,
- Philipp W Simon2,
- Brajendra Kumar3,
- Vinu Manikandan†3,
- Philge Philip†3 and
- Periannan Senapathy1, 3Email author
© Bhasi et al; licensee BioMed Central Ltd. 2010
Received: 22 May 2010
Accepted: 6 August 2010
Published: 6 August 2010
Root and bulb vegetables (RBV) include carrots, celeriac (root celery), parsnips (Apiaceae), onions, garlic, and leek (Alliaceae)—food crops grown globally and consumed worldwide. Few data analysis platforms are currently available where data collection, annotation and integration initiatives are focused on RBV plant groups. Scientists working on RBV include breeders, geneticists, taxonomists, plant pathologists, and plant physiologists who use genomic data for a wide range of activities including the development of molecular genetic maps, delineation of taxonomic relationships, and investigation of molecular aspects of gene expression in biochemical pathways and disease responses. With genomic data coming from such diverse areas of plant science, availability of a community resource focused on these RBV data types would be of great interest to this scientific community.
The RoBuST database has been developed to initiate a platform for collecting and organizing genomic information useful for RBV researchers. The current release of RoBuST contains genomics data for 294 Alliaceae and 816 Apiaceae plant species and has the following features: (1) comprehensive sequence annotations of 3663 genes 5959 RNAs, 22,723 ESTs and 11,438 regulatory sequence elements from Apiaceae and Alliaceae plant families; (2) graphical tools for visualization and analysis of sequence data; (3) access to traits, biosynthetic pathways, genetic linkage maps and molecular taxonomy data associated with Alliaceae and Apiaceae plants; and (4) comprehensive plant splice signal repository of 659,369 splice signals collected from 6015 plant species for comparative analysis of plant splicing patterns.
RoBuST, available at http://robust.genome.com, provides an integrated platform for researchers to effortlessly explore and analyze genomic data associated with root and bulb vegetables.
In the present decade, rapid advancements in DNA sequencing and molecular genetics techniques have generated a wealth of plant genomics, genetics, and breeding data. Whole genome sequences of several plants (arabidopsis, rice, wheat, grapes, etc) are now available and the sequencing of a number of additional plants is ongoing (lotus, papaya, cassava, tomato, potato, etc). The rapid proliferation of plant genome annotations generated by these efforts has led to the development of several data analysis platforms focused on specific plant groups - Gramene for grass genomics , SOL Genomics Network (SGN) for solanaceae , Legume Information System for legume species , GrainGenes for Triticeae and Avena  and GDR genome database for Rosaceae  are some examples. These resources integrate genomic sequence data, genetic maps, and phenotypic data associated with specific plant groups into a single user friendly platform and encourage researchers to get involved in annotation efforts. Such integrated repositories of plant group-specific data with active community contributions can greatly aid researchers in gaining a deeper understanding of plant genetics, plant taxonomy, plant pathology and plant physiology, and are valuable tools for supporting research initiatives focused on addressing challenges confronted in agriculture.
Interestingly, most of the plant data analysis platforms available today are focused on plant groups with high economic value and are associated with data collection from genome sequencing projects. Very few data analysis tools are available for less-studied "minor" and "orphan" crops with no ongoing genome sequencing efforts. Integrated data collection and annotation platforms focused on specific orphan crop families would be invaluable for researchers working on these crops.
Root and bulb vegetables (RBV) represent one such group of orphan crops [6, 7]. These include carrots, celeriac (root celery), parsnips (Apiaceae), onions, garlic, and leek (Alliaceae, sometimes referred to as the Allioideae subtribe Amaryllidaceae) - food crops common to virtually all agricultural regions and consumers' plates around the world. Yet the community of plant scientists working on RBV crops is small, perhaps as small as 10 to 25 full-time equivalent scientists in academic and government programs worldwide devoted to each of these crops. Most of this effort comes from breeders, geneticists, taxonomists, plant pathologists, and plant physiologists. A similar level of effort also comes from seed companies worldwide [8, 9]. Yet even with a relatively small scientific community, genomic data is becoming increasingly more abundant, primarily from efforts to develop molecular genetic maps, delineate taxonomic relationships and investigate molecular aspects of gene expression in biochemical pathways and disease response. With genomic data coming from such diverse areas of plant science, availability of a database focused on these root and bulb vegetable crop data would be of great interest to this small scientific community.
Plants that form storage roots and bulbs are included in several web sites that have a taxonomical or regional focus. For example, turnip and rutabaga are included in the Eurpoean Brassica Database , yacon (Smallanthus sonchifolius), a member of the Asteraceae, and wild yam (Dioscorea villosa), a member of the Dioscoraceae, are included in the Tropical Plant Database . Databases of the latter type rarely include genomic information. Furthermore, databases such as the SOL Genomics Network  include tuber-bearing species and genomic data for this plant family but comparable databases that focus on storage root or bulb-forming plants have not been developed. While the Apiaceae and Alliaceae include many species that do not form storage roots or bulbs, many wild and domesticated species in these two plant families do.
The RoBuST database has been developed for initiating a platform to collect and organize genomic information useful for genetics, breeding, taxonomy, plant physiology and other data highly relevant to root and bulb vegetables. The current release of RoBuST provides a comprehensive collection of sequence annotations of genes, RNAs, proteins, splice signals, regulatory elements and ESTs belonging to two root and bulb orphan crop families—Alliaceae and Apiaceae. RoBuST also has a unique data collection of Alliaceae/Apiaceae-specific gene function and trait annotations, molecular taxonomy data, genetic linkage maps, markers and biosynthetic pathways as well as an exhaustive collection of plant splicing data. A variety of sequence analysis and visualization tools are available in the RoBuST web interface for the integrated analysis of these diverse data sets.
Construction and content
Database and web interface development
The RoBuST database was developed in MySQL 4.1.The RoBuST web interface was developed using the CGI.pm, DBI.pm and GD.pm modules of Perl (5.8.8), and runs on an Apache (2.0.53) web server. Graphical display of genes, RNAs, intron-exon structures, splice junctions, and alternative splicing patterns were implemented in RoBuST using Gene Plot, Splice Signal Plot and AS Plot modules from the EuSplice  project. Additional graphical modules to display regulatory elements and other sequence elements were developed specifically for RoBuST using GD.pm.
Extraction of sequence annotations
Sequence records of Alliaceae and Apiaceae plant families were downloaded from GenBank  by submitting batch queries to its Entrez web interface. Gene, mRNA and other sub-sequence annotations are presented in a pre-determined data structure under the Feature Table section of GenBank records with each sub-sequence elements described as Feature Keys . We carefully analyzed the Feature Table structure and developed Perl programs to parse the Feature key data format and efficiently extract sub-sequence datasets. The Perl programs extracted position co-ordinates, sequences and additional annotations associated with each of following sequence data types: (1) Gene, (2) RNA, (3) CDS (4) EST, (5) Promoter, (6) Regulatory elements (Signal Peptide, Replication Origin, 5'UTR, Enhancer, TATA Signal, CAAT Signal, -10 Signal, -35 Signal, PolyA Signal, PolyA Site, Protein Bind, 3'UTR), (7) Repeat elements (Repeat Region, Repeat Unit, Transposons) and (8) Miscellaneous elements (Misc Feature, Precursor RNA, Prim Transcript, Mature Peptide, Primer Bind, Misc Signal, Stem Loop, Variation, Misc RNA, Transit Peptide). The extracted sequence and annotation data were populated into the back-end MySQL database.
Extraction of plant splicing data
Plant-specific annotation data files ("gbpln*.seq.gz") were downloaded from GenBank and all GenBank gene records which belong to plant species from Kingdom Viridiplantae were extracted. Since we were interested in splice signal information, all single-exon gene records were removed from this data set. This left 348,081 GenBank records covering 6015 Viridiplantae plant species, each of which had multi-exon gene annotations. These were further parsed to extract position coordinates and sequences associated with gene, mRNA, exon and intron structure, and donor and acceptor splice signals.
We submitted seventeen new carrot and garlic trait terms to Trait Ontology (TO), which is part of the Plant Ontology Consortium . All seventeen were accepted into TO and were assigned TO IDs and parent-child relationships. We implemented a hierarchy-based display of TO term lineage for these traits in the RoBuST Trait Ontology viewer using GraphViz .
We successfully mapped Gene Ontology (GO)  function annotations to 119 RoBuST genes as follows: InterPro  IDs corresponding to RoBuST genes were extracted from the database cross references (db_xrefs) provided under the CDS feature key tag in their corresponding GenBank files. The GO annotation file "interpro2go" was downloaded from InterPro and InterPro IDs associated with each of the 119 genes were mapped to the gene ontology information available in this file.
Utility and Discussion
Distribution of sequence data types in RoBuST
Sequence Data Type
The results page also has several informational tabs which provide additional data on the gene or RNA of interest. The "Summary" tab provides general information on the sequence record such as gene/RNA name and description, organism name, GenBank Accession/ID and links to the original GenBank record. The "Sequences" tab, provides options to download sequences of gene, RNA, coding sequence (CDS), protein and other sequence annotations (promoters, ESTs, regulatory elements, repeat elements etc). If a gene has an exon-intron structure, then the splice signal sequences of each of its splice junctions can be viewed by clicking on the "Splice Sites" tab. Database cross-references to five independent external databases (UniProtKB , InterPro, GOA , HSSP , and PDB  related to the gene/RNA of interest can be accessed through the "Other Info" tab.
Sequence Analysis Tools
RoBuST supports the diverse sequence analysis requirements of Alliaceae/Apiaceae research community by integrating the following sequence analysis tools to its user-friendly web interface. (1) Customized access to plant family-specific and species-specific BLAST  searches; (2) Primer Design Tools: Primer3Plus  and ExonPrimer3—a customized version of Primer3 which we developed so that users can design specific primers for exons from any Alliaceae or Apiaceae gene; (3) Emboss  pair-wise sequence alignment tools: Water for local alignment and Needle for global alignment; (4) Emboss open reading frame detection tool: Getorf; (5) VecScreen  for detecting vector contamination; (6) Splign  and Spidey  for exon-intron structure detection and splicing analysis.
Plant Splice Repository (PSR)
PSR can be mined to retrieve splicing annotations associated with an entire plant family, a specific plant species or even a specific gene of interest (Figure 1B). For any given gene, users can view its exon-intron structure, analyze donor and acceptor splice signals, exon and intron sequences flanking splice junctions as well as access the distribution of putative splice signals surrounding annotated splice junctions. Users can also download these gene-specific PSR datasets for further analysis.
PSR also has two unique splicing analysis tools which support in-depth mining of the extensive splicing data content. SpliceBlast-PL (Figure 1C) identifies potential plant-specific exon-intron structures within a query sequence of interest by aligning the query sequence against the entire plant splice signal collection in PSR and SpliceMatch-PL (Figure 1D) can be used to identify the prevalence of a splice signal sequence of interest within various plant genomes. It accepts user-submitted splice signal sequences as a query and retrieves hits in different plant species which have this same splice signal. Each of these hits can be analyzed in detail using graphical splice signal plots.
Genetic Linkage Maps
Complete and partial genetic linkage maps in RoBuST
Mapping Population Size
Number of Linkage Groups
Brasilia 1252 × B6274 RAPD Linkage Map (Leonardo Boiteux; partial map for linkage group bearing Mj-1 only)
Brasilia 1252 × B6274 AFLP Linkage Map (Leonardo Boiteux; partial map for linkage group bearing Mj-1 only)
Brasilia 1252 × B6274 RAPD Linkage Map (Leonardo Boiteux)
B493 × QAL Linkage Map (Carlos Santos)
B493 × QAL Linkage Map with DcMaster markers (Dariusz Grzebelus)
B493 × QAL Linkage Map with carotenoid genes (Brian Just)
BSB × HCM Linkage Map (Carlos Santos)
9304X7262 Linkage Map (B.S. Vivek)
Garlic Linkage Map 1 (Meryem Ipek)
Garlic Linkage Map 2 (Meryem Ipek)
Garlic Linkage Map 3 (Y. Zewdie)
Brigham Yellow Globe 15-23 × Alisa Craig 43 (Michael J. Havey)
RoBuST provides detailed graphical displays of the carotenoid and anthocyanin biosynthetic pathways of Daucus carota and S-alk(en)yl cysteine sulfoxide and allium flavor chemistry pathways of Allium sativum (Figure 1F). Information on pathway steps, substrates, enzymes catalyzing the reaction, links to the RoBuST records of pathway genes, genetic linkage map details for these genes, and 2D molecular structure of the pathway elements is available in the pathway display page. We plan to incorporate additional pathways from Alliaceae/Apiaceae species and welcome submissions from the research community to enhance the current collection.
Plant Taxonomy and Systematics
Common molecular taxonomy sequence annotations in RoBuST
Number of Apiaceae species with this sequence
Total number of sequences for Apiaceae
Number of Alliaceae species with this sequences
Total number of sequences for Alliaceae
External Transcribed Spacer (ETS)
Internal Transcribed Spacer (ITS)
Non Transcribed Spacer (NTS)
Trait Ontology and Gene Ontology Browsers
We have implemented an ontology browser for exploring functional annotations and trait features of Alliaceae and Apiaceae plants. Gene Ontology (GO) functional annotations for 43 Alliaceae and 76 Apiaceae genes can be accessed and analyzed in the GO annotation browser in RoBuST (Figure 1G).
Trait ontology terms accepted by TO consortium
Trait Ontology Term
Alpha carotene content
Cyclic carotene content
Acyclic carotene content
Cercospora leaf spot resistance
Protist disease resistance
Meloidogyne incognita resistance
Meloidogyne javanica resistance
Total water soluble content
Trait and functional annotations can be queried through the ontology browser using general keyword searches or by specific searches using ontology terms or accession IDs. Users can view complete information for each ontology term as well as parent and child terms and their relationships (Figure 1G).
We plan to expand the current data coverage in RoBuST in the future, and develop it into a one-stop resource for the root and bulb research community by providing comprehensive coverage of genomic data for all available root and bulb plant species. Since comparative analysis of genomic data from tuber forming plants and root and bulb plants could prove useful for understanding common mechanisms of bulb and tuber formation, we plan to link genomic information on tuber-bearing species from SGN to RoBuST. We will also incorporate interactive tools that can be used by root and bulb researchers to annotate sequences, phenotypes and traits, and to submit linkage maps, markers, molecular phylogeny data, pathways and other relevant data types which are of interest to the user community. Additionally, several comparative genomics tools will be made available in the next release of RoBuST and these tools will allow user-friendly cross-species comparative analysis of sequence annotations not only within the root and bulb plant group, but also against well annotated genomes such as rice, wheat, arabidopsis, barley, grape, potato and tomato. Since inter-database comparative analysis would be very useful in plant genome analysis and knowledge discovery, we will implement link integration of RoBuST data to Gramene and Ensembl. We will also provide gateways to ExDom  a database resource that will enable the comparative functional analysis of proteins and domains from these genomes. Furthermore, we will enable the capability for analyzing mutations in genes, RNAs and regulatory sequences in RoBuST using the EuSplice resource  and comparative analysis of alternative splicing events using the AspAlt resource .
Since the current sequence data in RoBuST is from a single data source—GenBank, we did not have data heterogeneity issues in this version release. However, we will be faced with data heterogeneity when we expand the RoBuST content to include data from different databases like SGN, Gramene and Ensembl in the next version release of RoBuST. To address this, we will adapt DAS protocols  in RoBuST and set up a DAS server which will make the import and export of data easy. This will ensure that RoBuST's future development and updates are not complicated by diverse data formats and data heterogeneity from different data sources.
The plant research community in agriculture often has a commodity-specific focus. Consequently, the availability of detailed information from diverse scientific disciplines has long been of interest to crop scientists. As genomic data is the common language of all biological disciplines, a focused collection of genomic data for an individual plant species or family provides a valuable tool for researchers specializing in particular crops. This fact led to the development of GrainGenes, SolGenes, etc. To this end, RoBuST has been developed for plant scientists working on root and bulb vegetable crops. The array of genomic information on these relatively poorly studied plants is not extensive but even today over 47,000 GenBank sequence records have been generated for Apiaceae and Alliaceae alone. With the recent advancements in next generation sequencing technology, an increase in genomic data for root and bulb orphan crops in public databases is imminent. Furthermore, there is little doubt that the whole genome of one or more species in Apiaceae will be sequenced in the next few years, especially since many species in this family have genomes in the size range of rice and tomato. The extraordinarily large size of Alliaceae genomes will impede their whole genome sequencing projects, but that fact notwithstanding, much more sequence information of Alliaceae will certainly be generated. With the certainty that next-generation sequencing will become a common research tool, the management of these large sequence datasets is receiving much attention by genomicists. Discussion of next-generation plant genetics is already underway  and similar strategies are being planned for use in plant taxonomy and physiology. We anticipate that specialized databases like RoBuST will become even more valuable for crop specialists as the database grows. While RoBuST assembles tools useful for genomics of root and bulb vegetables, it also provides tools to tie genomic data to genetic linkage data, plant traits and biochemical pathways of interest to geneticists, taxonomists, and physiologists, and it creates links to other related databases. This collection of features provides a network for communication from the DNA sequence level to the trait and crop level with relative ease. The tools assembled in RoBuST are intended to be of wide immediate interest to researchers working on root and bulb crops, and to also serve as a model of assembling diverse comparable data useful for any crop.
Availability and requirements
RoBuST is freely available to all non-commercial users at http://robust.genome.com.
We thank Vipin T. Sreedharan and Bipin Balan for providing technical support and Anup Viswanathan for designing the RobuST logo for the web interface.
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