The Plant Structure Ontology, a Unified Vocabulary of Anatomy and Morphology of a Flowering Plant1,[W],[OA]
Elizabeth A. Kellogg2,
Peter F. Stevens2,
Leszek P. Vincent2,
Martin M. Sachs,
Noah T. Whitman,
Susan R. McCouch,
Mary L. Schaeffer,
Doreen H. Ware,
Lincoln D. Stein and
Seung Y. Rhee*
Department of Plant Biology, Carnegie Institution, Stanford, California
94305 (K.I., L.R., N.T.W., S.Y.R.); Department of Biology, University
of Missouri, St. Louis, Missouri 63121 (E.A.K.); Department of Plant
Breeding, Cornell University, Ithaca, New York 14853 (P.J., A.P.,
S.R.M.); Missouri Botanical Garden, St. Louis, Missouri 63121 (F.Z.,
P.F.S.); Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
11724 (S.A., D.H.W., L.D.S.); University of Missouri, Columbia,
Missouri 65211 (L.P.V., M.L.S.); Maize Genetics Cooperation, Stock
Center, and Department of Crop Sciences, University of Illinois,
Urbana, Illinois 61801 (M.M.S.); and United States Department of
Agriculture-Agricultural Research Service, Washington, DC 20250
(M.M.S., M.L.S., D.H.W.)
An Open Access article from Plant Physiology 143:587-599 (2007).
Formal description of plant phenotypes and standardized annotationof gene expression and protein localization data require uniformterminology that accurately describes plant anatomy and morphology.This facilitates cross species comparative studies and quantitativecomparison of phenotypes and expression patterns. A major drawbackis variable terminology that is used to describe plant anatomyand morphology in publications and genomic databases for differentspecies. The same terms are sometimes applied to different plantstructures in different taxonomic groups. Conversely, similarstructures are named by their species-specific terms. To addressthis problem, we created the Plant Structure Ontology (PSO),the first generic ontological representation of anatomy andmorphology of a flowering plant. The PSO is intended for a broadplant research community, including bench scientists, curatorsin genomic databases, and bioinformaticians. The initial releasesof the PSO integrated existing ontologies for Arabidopsis (Arabidopsisthaliana), maize (Zea mays), and rice (Oryza sativa); more recentversions of the ontology encompass terms relevant to Fabaceae,Solanaceae, additional cereal crops, and poplar (Populus spp.).Databases such as The Arabidopsis Information Resource, NottinghamArabidopsis Stock Centre, Gramene, MaizeGDB, and SOL GenomicsNetwork are using the PSO to describe expression patterns ofgenes and phenotypes of mutants and natural variants and areregularly contributing new annotations to the Plant Ontologydatabase. The PSO is also used in specialized public databases,such as BRENDA, GENEVESTIGATOR, NASCArrays, and others. Over10,000 gene annotations and phenotype descriptions from participatingdatabases can be queried and retrieved using the Plant Ontologybrowser. The PSO, as well as contributed gene associations,can be obtained at www.plantontology.org.
Angiosperms are one of the most diverse groups of plants thatvary greatly in morphology, size, habitat, and longevity. Agricultureis almost entirely dependent on angiosperms. Besides providingfood and fiber, angiosperms are important sources for pharmaceuticals,lumber, paper, and biofuel. Understanding the origins, mechanisms,and functions of morphological diversity in flowering plantsis one of the fundamental questions in plant biology. Modernapproaches to studying plant development integrate classicalknowledge in plant anatomy and development with molecular geneticsand genomics tools. Among powerful tools, analyses of mutantsthat affect developmental processes have shed new light on ourunderstanding of the complexity of plant development. More recently,high-throughput, genome-wide phenomic screens in Arabidopsis(Arabidopsis thaliana; for review, see Alonso and Ecker, 2006),and large-scale gene expression-profiling technologies (forreview, see Rensink and Buell, 2005) generated a huge amountof data in plant science. These tools and resources have thepotential to contribute to efforts to link genes with developmentalmorphology (i.e. genotype with phenotype) and make an impacton our understanding of functions of genes involved in plantdevelopment. However, an accurate interpretation of the functionof genes that control various aspects of plant development mustbe embedded in detailed knowledge of the anatomy and morphologyof a plant. Explicitly, the structural features of plant cells,tissues, and organs need to be correctly understood and uniformlydescribed. Accurate and standardized nomenclature for plantanatomy and morphology is also required for comparative purposes(i.e. for comparisons of genes involved in plant developmentamong related or evolutionarily distant taxa). Semantic perplexitypresents a major obstacle for conducting such comparative studiesin plants; similar plant structures are described by their species-specificterms. For example, in scientific publications, fruit is oftenreferred to as silique in Arabidopsis, grain or caryopsis inrice (Oryza sativa), and kernel in maize (Zea mays). Conversely,the inherent ambiguity of some plant anatomical terms led tothe same or similar terms being applied to different structures(e.g. cork cell in the epidermis of grasses and cork cell inthe periderm in all other angiosperms).
Standard vocabulary for describing anatomy and developmentalstages was developed for several plant species at major plantgenomic databases, such as Arabidopsis at The Arabidopsis InformationResource (TAIR; Berardini et al., 2004), rice and other cerealsat Gramene (Yamazaki and Jaiswal, 2005), and maize at MaizeGDB(Vincent et al., 2003). These vocabularies have been used todescribe gene expression data and mutant or natural variantphenotypes in several plant databases. However, they were developedindependently of each other and were based on different principlesand rules. In addition, variation in nomenclature used for differenttaxonomic groups in angiosperms presented obstacles for conductingqueries in more than one plant database and retrieving meaningfulresults. For the purpose of comparative genomics, diverse terminologyneeded to be organized into a standardized language that couldbe shared among individual databases and used for accurate descriptionof phenotypes and gene expression data.
To address these problems, the Plant Ontology Consortium (POC;Jaiswal et al., 2005) has developed a simple and extensiblecontrolled vocabulary that describes anatomy, morphology, andgrowth and developmental stages of a generic flowering plant.In addition, the POC has established a database through whichthe data curated using this vocabulary can be accessed in aone-stop manner. Here, we describe the first representationof anatomy and morphology of a generic flowering plant, thePlant Structure Ontology (PSO). This ontology represents themorphological-anatomical aspect of the Plant Ontology (PO);the temporal aspect and the Plant Growth and Developmental StagesOntology have been described elsewhere (Pujar et al., 2006).We also discuss the guiding principles and rationale for thedevelopment and maintenance of the PSO and its importance fordescribing phenotypes and large-scale gene expression data inreference plants and crop species.