The Alternaria genomes database: a comprehensive resource for a fungal genus comprised of saprophytes, plant pathogens, and allergenic species
© Dang et al.; licensee BioMed Central. . 2015
Received: 20 January 2015
Accepted: 2 March 2015
Published: 25 March 2015
Alternaria is considered one of the most common saprophytic fungal genera on the planet. It is comprised of many species that exhibit a necrotrophic phytopathogenic lifestyle. Several species are clinically associated with allergic respiratory disorders although rarely found to cause invasive infections in humans. Finally, Alternaria spp. are among the most well known producers of diverse fungal secondary metabolites, especially toxins.
We have recently sequenced and annotated the genomes of 25 Alternaria spp. including but not limited to many necrotrophic plant pathogens such as A. brassicicola (a pathogen of Brassicaceous crops like cabbage and canola) and A. solani (a major pathogen of Solanaceous plants like potato and tomato), and several saprophytes that cause allergy in human such as A. alternata isolates. These genomes were annotated and compared. Multiple genetic differences were found in the context of plant and human pathogenicity, notably the pro-inflammatory potential of A. alternata. The Alternaria genomes database was built to provide a public platform to access the whole genome sequences, genome annotations, and comparative genomics data of these species. Genome annotation and comparison were performed using a pipeline that integrated multiple computational and comparative genomics tools. Alternaria genome sequences together with their annotation and comparison data were ported to Ensembl database schemas using a self-developed tool (EnsImport). Collectively, data are currently hosted using a customized installation of the Ensembl genome browser platform.
Recent efforts in fungal genome sequencing have facilitated the studies of the molecular basis of fungal pathogenicity as a whole system. The Alternaria genomes database provides a comprehensive resource of genomics and comparative data of an important saprophytic and plant/human pathogenic fungal genus. The database will be updated regularly with new genomes when they become available. The Alternaria genomes database is freely available for non-profit use at http://alternaria.vbi.vt.edu.
Alternaria species are a major cause of necrotrophic diseases of plants and some of the most common fungi encountered by humans. There are several noteworthy examples of Alternaria spp. as major plant pathogens including but not limited to, A. brassicicola and A. solani. A. brassicicola causes black spot disease (also called dark leaf spot) on virtually every important cultivated Brassica spp. [1-3]. Black spot disease is of worldwide economic importance. For example, black spot can be a devastating foliar and seed-borne disease resulting in severe yield reductions in crops such as cabbage, broccoli, canola and rapeseed [4-6]. A. solani is the causal agent of early blight disease of several major Solanaceous crops including potato and tomato. Early blight caused by A. solani is considered one of the most destructive diseases of potatoes and tomatoes in the world [7,8].
Alternaria spp. are among the most well known producers of diverse secondary metabolites, especially toxins . Over 70 small molecule compounds have been reported from Alternaria . Some of these metabolites are potent mycotoxins (e.g. alternariol, alternariol methyl ether, tenuazonic acid, etc.) with mutagenic and teratagenic properties, and have been linked to certain forms of cancer . The occurrence of potentially harmful Alternaria metabolites in food and food products is becoming an increasing environmental concern . Other toxins are host specific or non-host specific phytotoxins and are important virulence factors during plant pathogenesis. To date many of the genes responsible for the production of these specialized metabolites are unknown although recently the genes responsible for production of the HDAC inhibitor depudecin in A. brassicicola was elucidated as well as the toxin Alternariol and Alternariol methyl ether in A. alternata [12-14]. Annotated genome sequence information was critical for these discoveries.
In addition to harboring many important plant pathogenic species, Alternaria spores are one of the most common and potent indoor and outdoor sources of airborne allergens. Epidemiological studies from a variety of locations worldwide indicate that Alternaria sensitivity is closely linked with the development of atopic asthma and up to 70% of mold-allergic patients have skin test reactivity to Alternaria [15-17]. Alternaria sensitivity has been shown to not only be a risk factor for asthma, but can also directly lead to the development of severe and potentially fatal asthma often more than any other fungus [15-19]. Although some research has been performed on the physiological and molecular identification of Alternaria allergens only three major and several minor allergenic proteins have been described . The biological role of these allergens and other secreted fungal products in the development of allergy and asthma is very poorly understood. Thus there is clearly a need to elucidate the role of Alternaria immunoreactive proteins and other molecules such as secondary/specialized metabolites in the development of allergic diseases from both diagnostic and immunotherapeutic perspectives.
In this article, we introduce the Alternaria genomes database that provides tools to browse and visualize genome sequences, genome annotations, whole genome alignments, and homologous data of the fungal genus Alternaria.
Content and construction
Description of the sequenced Alternaria genomes
Genome sequence size (Mb)
Predicted genes (#)
ATCC 66891, EGS 34–016, BMP 0269
Allergic diseases of human, leaf spot, rots of plants
ATCC 11680, BMP 0238, IHEM 4706
Allergic diseases of human, leaf spot, rots of plants (possibly A. tenuissima)
ATCC 96836, EGS 42–002, BMP 1950
Blackspot of brassica
ATCC 66982, EGS 34–039, BMP 0270
Allergic disease of human, leaf spot, rots of plants
ATCC 204491, EGS 39–128, BMP 0308
Stem canker of tomato
EGS 46–140, BMP 2343, SH-MIL-8 s
Brown/black spot of citrus
ATCC 204363, EGS 46–069, BMP 0317
Infecting and suppressing dodder (weed)
BMP 3062, NAF-8
Black spot disease of strawberry
EGS 90–0512, BMP 2338
Black spot, ring spot disease of pear
EGS 45–080, BMP 2327, BC2-RLR-1 s
Leaf spot of citrus
EGS 30–033, BMP 0313
Black/brown leaf spot of tobacco
BMP 3064, IFO8984
Leaf ring spot of apple
BMP 3063, M-71
Leaf ring spot of apple
BMP 3436, SH-MIL-20s
Leaf spot of citrus
ATCC 96828, EGS 34–015, BMP 0304
Leaf spot of plants
EGS 44–159, BMP 2335
Leaf spot of citrus
BMP 1963, CBS 635.80
Leaf spot and blight of safflower
ATCC MYA-998, EGS 45–075, BMP 0180
Leaf spot of solanaceae (pepper)
BMP 0172, ACR1
Leaf spot of solanaceae
ATCC 36613, BMP 0167
Leaf blight of carrots
BMP 1949, CH3
Leaf spot of cotton
BMP 0178, Z6B
Purple blotch, leaf blight and bulb rot of Allium (onion)
Early blight of potatoes and tomatoes
EGS 44–044, BMP 0179
Leaf spot of marigold
BMP 2032, CBS 109156
Leaf spot of tomato
Genome sequencing and assembly
Alternaria genomes were sequenced using various sequencing technologies including whole genome shotgun method with Sanger sequencing, GS-FLX 454, and Illumina HiSeq (Table 1). Genomes were assembled from sequencing reads using PCAP  (for Sanger sequencing), Newbler  (for GS-FLX 454), and Velvet  (for Illumina HiSeq). The physical map of A. brassicicola was constructed by generating fingerprints from the CSU-K35 A. brassicicola BAC library that were then used to scaffold the genome (Dang et al., unpublished).
Various computational functional annotations were performed on the conceptual protein sequences. The proteins were first searched against Genbank  and SwissProt  using BLAST to identify known proteins with similar sequences. The name/description of the known proteins was then transferred to the predicted proteins following the standard operating procedure (SOP) developed for fungi by the Broad Institute . Protein domain and family annotation was performed using the Interpro database  and PFAM . Gene ontology annotation was performed using Blast2GO  and Interpro.
Various fungal-related and additional annotations were also carried out using the pipeline. Signal peptides were predicted using SignalP , WoLF-Psort , and Phobius . Transmembrane proteins were predicted using TMHMM . Pathogenicity-related gene candidates were identified via multiple annotation data including BLAST search against PHI-base . Carbohydrate Active Enzymes were identified according to the CAZY database  and dbCAN . Potential allergens were identified using BLAST based homology searches and Allerdictor . Proteases were annotated using the batched BLAST search tool from the MEROPS database . Secondary metabolites were identified using SMURF .
Multiple genome comparison tasks were performed that utilized the genome sequences as well as the predicted genes/proteins from multiple species. Whole genome pairwise alignment was performed using Mauve progressive alignment software [52,53]. Orthologs and paralogs were identified using bidirectional best BLAST hits and Markov clustering via OrthoMCL .
Porting data to Ensembl database schema
Annotation and comparison data of Alternaria genomes are presented via the popular Ensembl genome browser platform  that was customized and installed at the Virginia Bioinformatics Institute. Outputs from the genome annotation pipeline as well as outputs from comparative genomics analyses were processed and converted to Ensembl compatible MySQL databases (both core and compara databases) using EnsImport, a custom suite of scripts we developed in Perl. EnsImport supports multiple standard file formats such as FASTA, AGP, GFF3 and XMFA, and outputs from widely-used tools such as BLAST, Interpro, RepeatMasker, OrthoMCL and Blast2GO.
Utility and discussion
Using Ensembl genome browser platform, the Alternaria genomes database provides a rich set of user-friendly tools to browse and visualize sequences, annotation, and comparison data. Data export and search features are also available. Detailed instructions on how to use the Ensembl browser are available on the ‘Help & Documentation’ section of the database. Here we only describe the most relevant features in the context of the Alternaria genomes project.
Genome region view
Comparative genomics view
Ensembl built-in functionality allows for exporting multiple types of data to various formats. Raw sequence and annotation data can be easily exported in multiple formats such as FASTA and GFF via available tools in Ensembl. A button to access data export feature is located on the left pane in the interface of the database. It is also possible to export the graphical visualization of multiple types of annotation and comparison data to multiple image formats that are suitable for publication or further editing.
Over the past few years, efforts in sequencing fungal genomes have facilitated the studies of the molecular basis of fungal pathogenicity as a whole system [56-59]. The Alternaria genomes database provides a comprehensive resource of genomics and comparative genomics data of an important plant and human pathogenic fungal genus Alternaria. In addition, the database may prove useful for discovery of genes encoding industrial enzymes, antibiotics, and other molecules with utility in medicine and agriculture.
These genome annotation and comparison data have recently facilitated several large-scale functional genomics studies that resulted in the discovery of many new genes that contribute to virulence especially secondary metabolite genes, mitogen-activated protein (MAP) kinases, and transcription factors in A. brassicicola [13,14,60-68]. Alternaria genome annotation and comparison data have also enabled comprehensive comparative studies of Alternaria genomes in the context of plant and human pathogenicity  (several other manuscripts are under preparation).
The use of the familiar Ensembl browser platform makes browsing and visualizing Alternaria genome annotation and comparison data convenient. As we continue our efforts in Alternaria genome sequencing and analysis, we will update this database as new genomes and relevant annotation data become available.
Availability and requirements
The Alternaria genomes database is freely available for non-commercial use at http://alternaria.vbi.vt.edu.
The authors wish to acknowledge William Spooner for helpful discussions regarding Ensembl installation. This work was supported by the grants NSF DEB-0918298 and NIFA 2004-35600-15030 to CL. This article is dedicated to the late Dr. Dennis L. Knudson.
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