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. 2021 Jan 13;185(4):1374–1380. doi: 10.1093/plphys/kiaa105

WARPP—web application for the research of parasitic plants

Lara M Kösters 1,2, Sarah Wiechers 3, Peter Lyko 1,2, Kai F Müller 3, Susann Wicke 1,2,✉,2
PMCID: PMC8133606  PMID: 33793906

Abstract

The lifestyle of parasitic plants is associated with peculiar morphological, genetic, and physiological adaptations that existing online plant-specific resources fail to adequately represent. Here, we introduce the Web Application for the Research of Parasitic Plants (WARPP) as an online resource dedicated to advancing research and development of parasitic plant biology. WARPP is a framework to facilitate international efforts by providing a central hub of curated evolutionary, ecological, and genetic data. The first version of WARPP provides a community hub for researchers to test this web application, for which curated data revolving around the economically important Broomrape family (Orobanchaceae) is readily accessible. The initial set of WARPP online tools includes a genome browser that centralizes genomic information for sequenced parasitic plant genomes, an orthogroup summary detailing the presence and absence of orthologous genes in parasites compared with nonparasitic plants, and an ancestral trait explorer showing the evolution of life-history preferences along phylogenies. WARPP represents a project under active development and relies on the scientific community to populate the web app’s database and further the development of new analysis tools. The first version of WARPP can be securely accessed at https://parasiticplants.app. The source code is licensed under GNU GPLv2 and is available at https://github.com/wickeLab/WARPP.

The WARPP online resource is a new, expandable, and interactive parasitic plant-specific data hub that provides online tools tailored to the peculiarities of parasitic angiosperms.

Introduction

Parasitic plants, which obtain water and nutrients from host organisms (Kujit, 1969), receive considerable attention in many areas of plant science and beyond. Peculiar morphological and physiological adaptations accompany the development of a heterotrophic mode of nutrient acquisition via parasitism. So-called haustorial parasites (i.e., parasitic plants in the narrower circumscription sensu Wicke and Naumann, 2018) use multifunctional feeding organs, haustoria, to attack roots or stems of nearby plants and directly tap into their vascular systems. Depending on the presence of photosynthetic activity or the lack thereof, plant biologists commonly distinguish between hemi- and holoparasites. The transition from hemi- to holoparasitism is gradual (e.g., Cuscuta spp.—Convolvulaceae, Revill et al., 2005). Some parasitic species may even change the mode of parasitism during their lifetime (e.g., Tozzia—Orobanchaceae, Weber, 1973), and in extreme cases, the entire vegetative growth of a parasite occurs inside the body of another plant (e.g., Viscum minimum—Viscaceae, Mauseth and Rezaei, 2013).

Research into parasitic plant biology has leaped forward in the past decade, generally benefitting from joint efforts to generate genomic resources and establish laboratory models for biochemical, genetic, and molecular studies (e.g., Tomilov et al., 2007; Pouvreau et al., 2013; Ishida et al., 2017; Waweru et al., 2019). Broad access to high-throughput methodologies such as parallel sequencing technologies has also allowed the gathering of comprehensive data from nonmodel parasites. Hence, associating genomic information with lifestyle preferences enabled unlocking mechanisms underlying major evolutionary transitions through comparative analysis (e.g., Wicke et al., 2013; Yang et al., 2015; Chen et al., 2020).

Data availability and sharing represent a fundament of science, and integrating various trait data or analysis tools is a promising way to generate robust research results. However, gathering phenotype information for parasitic plants remains a time-consuming challenge, thus hampering advances in linking phenotypic with genotypic traits. Besides a surprising lack of data on lifespan and lifestyle, information is often hidden in nondigitized print media or stored in various plant databases. However, general plant or biodiversity databases cannot adequately account for parasitic plants’ unique features, which include host preferences as well as the parasite’s feeding mode specialization—traits that are both absent from nonparasitic plants that make up 96% of land plant diversity. Thus, it remains challenging to retrieve parasitic plant-specific information, especially for species that, unlike some witchweed, broomrape, or dodder species, are of no economic importance or have raised public interest due to outstanding floristic values (e.g., Rafflesia, Indian paintbrush).

Curated resources specializing in parasitic plant biology remain scarce. Some websites like The Parasitic Plant Connection (Nickrent, 1997) or the Index of Orobanchaceae (Carlón et al., 2005) provide valuable information revolving around parasitic plant systematics and taxonomy, but database searchability is limited. Other resources focus on lineage-specific genomic data, but lack coverage of parasite diversity and offer only limited biological species information (e.g., PPGP website at ppgp.huck.psu.edu; Cuscuta campestris genome project: www.plabipd.de/project_cuscuta2/start.ep; Dodderbase: www.dodderbase.org).

Here, we introduce WARPP, a Web App for the Research of Parasitic Plants, as an effort to build a community hub for access and information sharing of parasitic plant-specific data. We developed WARPP as an expandable platform to store phenotype and ecological information of lifestyle and life-history preferences, gather data of biochemical peculiarities, and provide information on available genetic data. The first version of WARPP provides an initial framework for the research community, whose help will be essential to populate the resource with data for all parasitic plant families and to continue developing new online analysis tools optimized for parasitic plant biology.

Website content

The first online version of the parasitic plant web app, WARPP, is accessible for guests and registered users at https://parasiticplants.app. We built the database of WARPP (Figure 1) with version 10.12 of the PostgreSQL Database Management System. Server-side development employed Ruby 2.6.1 and Ruby on Rails 5.2.3. Ruby on Rails offers a mature framework for speedy and productive development that provides flexibility and versatility for the integration of additional tools and external modules. Currently, almost 20% of our code is made up of JavaScript or CoffeeScript, which enables frontend aspects of WARPP that depend on interactivity, reactivity, and speed.

Figure 1.

Figure 1

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Simplified database structure and modules of WARPP. The WARPP database consists of three central data tables (light and medium green), which store trait information of parasitic plants over various taxonomic levels, and supporting tables link externally fetched species-specific data (dark green) to the main table. Three database tables hold data for the Ancestral Trait Explorer and the Orthogroup module (purple). Trees can be linked to orthogroups, which themselves are linked to taxa while storing information on the respective genes and their functions. Additional tables store user information and data they provided to WARPP (blue). A polymorphic association links users to their submitted server jobs (yellow). Italicized terms indicate associations, whereas others specify attributes. Relationships between tables and their types are indicated by lines.

Among the most important Ruby gems used are Puma as the web server, Ancestry for representing hierarchical (tree-) data structures, Devise for user management, and Capistrano for deployment. Background jobs are enabled by use of Sidekiq in combination with Redis. Additionally, we use the Whenever-gem in collaboration with the job scheduler Cron to regularly update database entries. For example, recent data from PubMed and GenBank are fetched once a week. Taxonomy data originates from GBIF, fetched once, whereas its species occurrence data are fetched each time a particular species view is selected. Images of parasitic plant species are obtained from the iNaturalist network (https://www.inaturalist.org).

Client-side development was based on Bootstrap CSS and JavaScript, supplemented by various JavaScript libraries and software such as JBrowse (Buels et al., 2016) for the genome browser, Leaflet for map data visualization, and D3 (Bostock et al., 2011) for tree visualization. We use font awesome icons. App performance was tested in Firefox 72.0.1, 73.0.1, and 75.0 (64-bit), Safari 13.0.4 and 13.1, and Google Chrome 80.0.3987.116 (Official Build; 64-bit) on Windows, macOS, and Linux.

The database structure of WARPP is tailored to the specific requirements of parasitic organisms, which no existing database implements. For example, we outsourced species attributes like lifestyle (“parasitic specialization”) to separate models, which enables cross-links to corresponding references. Attributes use a single-table inheritance method, where they share one database table and are distinguished by type. The representation of parasite relationships employs a self-join model, which works similar to a follower/following relationship between users, and facilitates cross-linking to references.

We designed WARPP as a modular system (Figure 1), which offers flexibility for extensions and user interaction in future versions. It was our primary goal to develop a platform that handles parasite-specific data. Alongside these efforts, we developed a first set of online analysis tools to jointly analyze phenotype and genotype data, and we continue to improve the interconnection of these tools with one another and additional units, to be added in future versions.

Module 1—taxonomy viewer

Users can choose from 21 parasitic plant families. They are then redirected to the taxonomy view that provides users with a draggable and zoomable tree. The tree displays all taxa up to the genus level in a radial format that is complemented by an additional collapsible list to the right. Selecting either the genus in the tree or list by clicking expands another list view that displays all species belonging to the selected genus. Navigation with either the tree or the list view is straightforward, while also providing an overview of phylogenetic relationships. The list view can also be used to access a page with detailed information about databased species. We allow for filtering taxa based on phenotypic traits. To this end, we linked both the tree and list views with a collapsible filter form that includes multiple select options for lifestyle and lifespan. Whereas the list view will only show genera that include species matching the filter options, the tree will highlight all genera that match the filter criteria and tone down those that do not. A separate container provides additional information on the availability of detailed information, as well as the detailed information itself that is linked to the respective genus. Detailed information is provided for lifestyle, lifespan, and habit in the form of pie charts.

Module 2—species view

Species pages display information of ecological and phenotypic traits with references and hyperlinks to the data sources (Figure 2). WARPP focuses on providing information on parasitic plant lifestyle, lifespan, and habit, as well as chromosome number and genome size. These data are provided in a table format, complemented by a dropdown menu containing facts about host plants and epiparasites specific to the parasitic plant species. Links to NCBI databases give an overview of all available sequence data for each parasitic plant and highlight the ten most recent publications indexed in PubMed.

Figure 2.

Figure 2

Open in a new tab

Snapshots of WARPP. A, The Species View provides general trait data such as the parasitic specialization and host preferences, an overview of available nucleotide data, as well as images and information of the geographic distribution for every parasitic species. B, The Ancestral Trait Explorer displays the evolution of life-history traits along parasitic plant phylogenies. C, The Orthogroup View shows an overview of the presence and absence of genes for parasitic and nonparasitic angiosperms. D, The Genome Browser provides access to genome data of parasitic plants, allowing users to zoom into genomic scaffolds to browse gene features and access coding data.

Additionally, we implemented a world map with an overlay of species occurrence data fetched from GBIF using the JavaScript Leaflet library. A container holds images of the respective species, where available. Authorized users will be able to submit new information of trait data, which are subject to curation. As database curators, higher-rank users that are selected according to their demonstrated experience in the field will be permitted to directly edit species entries in a separate view.

Module 3—edit function

Editing species entries will only be available for higher-rank users. These users will be able to add and delete data for hosts and parasites, upload photos of a particular species, update the species name, and provide information on lifestyle, lifespan, and potential species traits added in the future. All such edits will need references to be submitted. Whereas submitted information will accept personal observations as reference, these may change the reliability score of the entry. Submissions other than images will be saved but have to be checked first before the corresponding species entry is updated.

Module 4—ancestral trait explorer

The ancestral trait view is the first of five tools that will be featured in the first version of WARPP. Like the taxonomy tree view, this module uses JavaScript’s D3 library. However, the displayed phylogenetic tree is a dichotomous dendrogram that displays only a subtree with up to four levels (Figure 2). Future versions will render tree depths according to the browser window size. To navigate the tree, a user can select, i.e., click on any node to move away from the root node, which will slide the small subtree forward toward internal nodes and leaves (species). Backward navigation towards the root will load the previously shown levels. Users can search for their species of interest, and the tree will map the respective node and its parent nodes.

The trait reconstruction view is based on Maximum Likelihood reconstructions of life-history traits over the phylogeny of a parasitic plant family. Likelihood values displaying the probabilities of a trait at each internode are displayed as pie charts on the subtree and will be magnified on the bar to the right upon selection. The reconstruction of phylogenetic relationships within families is based entirely on available genetic data that are fused by supertree methods. Hence, species for which no molecular phylogenetic data are available will be omitted in trait reconstructions. In WARPP, we have implemented the Ancestral Trait Explorer exemplarily for the Broomrape family (Orobanchaceae), with more families to follow soon. For Orobanchaceae, two separate topologies can be rendered, as nuclear and plastid data produced incongruent phylogenies. Ancestral trait reconstructions of parasitic plants will be implemented for other families in the same way as the WARPP database fills with the particular trait and phylogenetic data. The underlying methodology for phylogenetic and trait reconstruction is provided and will be regularly updated in the WARPP documentation.

Module 5—orthogroup viewer

The second readily accessible tool of WARPP provides users access to information of orthologous gene information, implemented in the Orthogroup Viewer module (Figure 2). Users get a full list of orthogroups, i.e., gene families, obtained from an Orthofinder analysis of 100 parasitic and nonparasitic angiosperm genomes. A search function allows users to look up functional assignments, NCBI protein IDs, and the CDS locus tags. The selection of an orthogroup leads to a separate, detailed view of this gene family, showing the orthogroup members’ relationships to one another as an expandable gene tree, as well as the list of species and proteins with functional annotations. Each orthogroup’s gene tree is a clickable, zoomable, and draggable object. Hovering over a leaf node will render more information in a separate container, including a link that leads to the respective location in the genome browser, if available. We provide users the option to download both the corresponding tree file in Newick format and a multifasta file with the orthogroup’s sequences. Future versions of the Orthogroup Viewer will feature orthogroup-specific updates regarding the nature of gene losses, if any, as well as alternative gene tree reconstructions.

Module 6—genome browser

A third tool featured in WARPP is a genome browser, which enables access to genomic data for all parasitic plant species’ published (annotated) genome data (Figure 2). In this first version, users can browse genome data for Striga asiatica, C. campestris, and C. australis, as well as for the nonparasitic model plant Arabidopsis thaliana. We use JBrowse to visualize genomic data. Our assembly hub was built with published assemblies and annotation files. The genome browser will be updated as soon as newer assemblies of the currently featured taxa become available, or when new parasitic plant genomes are released. Users who wish to share their parasitic plant genome data with the research community via WARPP are invited to so, for which the developer will set up the corresponding framework.

Module 7—BLAST tool

A parasitic plant-specific BLAST tool is the first type of job-based tool of WARPP. Users can submit fasta files of up to 10 MB (e.g., 3,000 sequences of ∼3 kb in length) as single or batch requests for a BLAST search against our custom parasitic plant database. Upon submission, users can set a number of parameters themselves, may request an e-mail notification when the job has finished, and can download the zipped result files. The initial database contains assembled genome and transcriptome data of many parasitic plant species (list available and regularly updated in WARPP), including C. australis (Sun et al., 2018), C. campestris (Vogel et al., 2018), several Orobanchaceae members (some species of Orobanche and Phelipanche—Wicke et al., 2016; Cusimano and Wicke, 2016; e.g., S. asiatica—Yoshida et al., 2019), as well as the legacy builds of the Parasitic Plant Genome Project (e.g., Wickett et al., 2011; Westwood et al., 2012; Honaas et al., 2013; Yang et al., 2016). The database is updated and expanded in biweekly intervals, whereby unassembled read data available from NCBI’s Short Read Archive will be added, following a standardized data cleaning and assembly pipeline (methodology to be published online as part of the WARPP documentation).

Module 8—PPG Scorer

We implemented PPGS (Plastid Pseudogene Scorer), an experimental tool that enables users to scan the plastid genomes of (parasitic) flowering plants for the presence of 78 typically conserved plastid genes and obtain a “functionality” measure for each of these genes based on reading frame and protein identity comparisons with reference plastome data; the underlying method will be presented elsewhere. Users can adjust PPGS to their specific needs by selecting from a list of parameters that modify gene search stringency. Users can request e-mail notification regarding the status of their jobs upon submission. The job itself will run in the background and can be accessed later through a server job table. Upon completion of a job, functionality scores will be displayed in a table; the full results can be downloaded. To provide users more context regarding their results, PPGS also provides the reference database and a median “functionality score” per query.

Module 7—user management

For full access to WARPP, users are asked to sign up, which will provide access to the full suite of tools, including existing and new tools as they become available. Nonregistered users can browse the website, including the Taxonomy Browser, Orthogroup viewer, and Trait Reconstruction Explorer. Registered users gain access to the PPGS and BLAST tool. Above that, higher-rank users may post submissions for taxon editing, submit trait data, upload images of their favorite parasites, and suggest additional tools. In doing so, users can actively contribute to populating the database. Submitted data will be curated before uploading it to the database. Users can become curators, for which they will need to demonstrate their expertise, e.g. through publications in the different subject areas.

Summary and outlook

Future development of the app will include converting the Ruby on Rails core to an API-only backend, and communicating with it via a more productive, more performant (desktop-like) Progressive Web App or even (semi-) native Apps using JavaScript Cross-Platform App Frameworks. The benefits of this conversion will include the possibility of much more complex user interactions for data analysis and data entry, including slicing and dicing large amounts of viewed data on the fly as needed, or simple local statistical analyses, even when offline. Beyond enabling more robust and snappier user interfaces in web browsers and web views inside (semi-)native clients, the envisioned service layer (RESTful JSON-API) would also facilitate the cross-talk with other databases and web services, as well as fully native clients (desktop or mobile) that may display and modify data from the app’s backend.

The data layer will see significant enhancements as well. An important future aspect will be to account adequately for taxonomic synonyms, which we envisage to do by setting up an active cross-talk with a taxonomic name server. Distribution data for taxa will be mirrored from public sources like GBIF not only for parasites but enabled for dynamic viewing in relation to (putative) host taxa. Future versions of WARPP will also feature more interactions between taxon attributes, trait reconstruction, and genetic data. In particular, we envisage enhancing the interoperability between WARPP tools. We also plan to implement a gene search and alignment interface, with which registered users can search genes and proteins of interest in a combined database of available parasitic plant genomes and transcriptomes. Moreover, genetic changes such as gene losses or ploidization events along the evolution of the various parasitic plant families will be set up in dedicated views, with background computation of phylogeny-aware analyses of phenotype-genotype association using database- and user-submitted data and reconstructions of evolutionary histories of parasitic plant families. In the long run, WARPP may become a hub to support concerted efforts into understanding the biology of parasitic plants.

Acknowledgments

We would like to thank the IT service teams of WWU Münster and HU Berlin for excellent support. The research and development of WARPP received funding from the Emmy Noether-program of the German Science Foundation (DFG, WI4507-3/1 to Su.Wi.) and intramural funding from WWU Münster (to Su.Wi.), all gratefully acknowledged.

Funding

This study was supported by German Science Foundation (DFG), Emmy Noether-grant WI4507/3-1.

 

Su.Wi. and K.F.M. conceived the overall app design and database structures, and supervised data collection, programming, and testing; Su.Wi. and L.M.K. conceived all data analysis modules and background pipelines; L.M.K. lead-programmed this application and all modules, with contribution from Sa.Wi., P.L., and Su.Wi.; L.M.K. conceived and completed frontend designs and data visualizations; P.L. and Su.Wi. curated batch-fetched data; Su.Wi. and L.M.K. wrote the article, with contributions of all the authors; Su.Wi. agrees to serve as the author responsible for contact and ensures communication.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plphys/pages/general-instructions) is: Susann Wicke (susann.wicke@hu-berlin.de).

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