=Paper= {{Paper |id=None |storemode=property |title=A plant disease extension of the Infectious Disease Ontology |pdfUrl=https://ceur-ws.org/Vol-897/session1-paper01.pdf |volume=Vol-897 |dblpUrl=https://dblp.org/rec/conf/icbo/WallsSEGSJ12 }} ==A plant disease extension of the Infectious Disease Ontology== https://ceur-ws.org/Vol-897/session1-paper01.pdf
           A plant disease extension of the Infectious Disease Ontology
                                             Ramona Walls1, Barry Smith2, Justin Elser3, Albert Goldfain4
                                                                          Dennis W. Stevenson1, Pankaj Jaiswal3
                                                                1.	
  New	
  York	
  Botanical	
  Garden,	
  Bronx,	
  NY,	
  USA,	
  	
  
                                                 2.	
  Department	
  of	
  Philosophy,	
  University	
  at	
  Buffalo,	
  Buffalo,	
  NY,	
  USA,	
  	
  
                                   3.	
  Department	
  of	
  Botany	
  and	
  Plant	
  Pathology,	
  Oregon	
  State	
  University,	
  Corvallis,	
  OR,	
  USA,	
  	
  
                                               4.	
  Computer	
  Science	
  Department,	
  Blue	
  Highway,	
  Inc.,	
  Syracuse,	
  NY,	
  USA	
  

ABSTRACT                                                                                                                   Tester, 2011). Complete genome sequences already exist for
Plants	
  from	
  a	
  handful	
  of	
  species	
  provide	
  the	
  primary	
  source	
  of	
  food	
  for	
              25 green plant species, of which 17 are agriculturally im-
all	
   people,	
   yet	
   this	
   source	
   is	
   vulnerable	
   to	
   multiple	
   stressors,	
   such	
   as	
  
disease,	
   drought,	
   and	
   nutrient	
   deficiency.	
   With	
   rapid	
   population	
  
                                                                                                                           portant (Anon, 2012), along with expression sequence tags
growth	
   and	
   climate	
   uncertainty,	
   the	
   need	
   to	
   produce	
   crops	
   that	
   can	
               (EST), unigene, mutant phenotype, and other data sets for
tolerate	
  or	
  resist	
  plant	
  stressors	
  is	
  more	
  crucial	
  than	
  ever.	
  Traditional	
                  hundreds of plant species. Additionally, a vast quantity of
plant	
   breeding	
   methods	
   may	
   not	
   be	
   sufficient	
   to	
   overcome	
   this	
   chal-­‐              information on plant diseases is available in resources like
lenge,	
  and	
  methods	
  such	
  as	
  high-­‐throughput	
  sequencing	
  and	
  automat-­‐
                                                                                                                           manuals, textbooks, extension program highlights, and crop
ed	
  scoring	
  of	
  phenotypes	
  can	
  provide	
  significant	
  new	
  insights.	
  Ontolo-­‐
gies	
  are	
  essential	
  tools	
  for	
  accessing	
  and	
  analysing	
  the	
  large	
  quantities	
                  management databases, but almost always in natural lan-
of	
  data	
  that	
  come	
  with	
  these	
  newer	
  methods.	
  As	
  part	
  of	
  a	
  larger	
  project	
           guage form. Access to and analysis of the growing quanti-
to	
  develop	
  ontologies	
  that	
  describe	
  plant	
  phenotypes	
  and	
  stresses,	
  we	
                         ties of genomic, phenomic, and free-text data can be greatly
are	
  developing	
  a	
  plant	
  disease	
  extension	
  of	
  the	
  Infectious	
  Disease	
  On-­‐                     facilitated when data are annotated using ontologies. The
tology	
  (IDOPlant).	
  The	
  IDOPlant	
  is	
  envisioned	
  as	
  a	
  reference	
  ontology	
  
designed	
   to	
   cover	
   any	
   plant	
   infectious	
   disease.	
   In	
   addition	
   to	
   novel	
  
                                                                                                                           development of ontologies can also foster consistency in the
terms	
   for	
   infectious	
   diseases,	
   IDOPlant	
   includes	
   terms	
   imported	
   from	
                     description of plant diseases, including aspects such as envi-
other	
  ontologies	
  that	
  describe	
  plants,	
  pathogens,	
  and	
  vectors,	
  the	
  geo-­‐                       ronmental factors, areas of endemism, phenotypes associat-
graphic	
  location	
  and	
  ecology	
  of	
  diseases	
  and	
  hosts,	
  and	
  molecular	
  func-­‐                    ed with diseases, and development stages of both plants and
tions	
  and	
  interactions	
  of	
  hosts	
  and	
  pathogens.	
  To	
  encompass	
  this	
  range	
  
of	
   data,	
   we	
   are	
   suggesting	
   in-­‐house	
   ontology	
   development	
   comple-­‐
                                                                                                                           pathogens. Finally, the standardization and reasoning power
mented	
   with	
   reuse	
   of	
   terms	
   from	
   orthogonal	
   ontologies	
   developed	
   as	
                   provided by using ontologies enhances data sharing among
part	
   of	
   the	
   Open	
   Biomedical	
   Ontologies	
   (OBO)	
   Foundry.	
   The	
   study	
   of	
               biomedical researchers, allowing the results of research in
plant	
   diseases	
   provides	
   an	
   example	
   of	
   how	
   an	
   ontological	
   framework	
                   plant pathology to be translated into applications for human
can	
   be	
   used	
   to	
   model	
   complex	
   biological	
   phenomena	
   such	
   as	
   plant	
                  or other animal diseases, and vice versa.
disease,	
  and	
  how	
  plant	
  infectious	
  diseases	
  differ	
  from,	
  and	
  are	
  similar	
  
to,	
  infectious	
  diseases	
  in	
  other	
  organism.	
                                                                      A plant disease is traditionally defined as a deviation
                                                                                                                           from normal physiological functioning that is harmful to a
1         INTRODUCTION                                                                                                     plant (Manners, 1993). Biotic factors or stressors such as
                                                                                                                           pests or pathogens and abiotic factors such as low tempera-
Plants are the primary food source on which almost every
                                                                                                                           ture, air pollution, or nutrient deficiency, may cause plant
other organism on earth depends, either directly or indirect-                                                              diseases. Infectious plant diseases are caused by pathogens,
ly, and six plant species – wheat, rice, corn, potato, sweet                                                               such as fungi, bacteria, and viruses. As part of a larger pro-
potato, and cassava – provide 80% of calories consumed by                                                                  ject to develop ontologies that describe both biotic and abi-
humans worldwide (FAO, 2012; Goudie & Cuff, 2001). It is                                                                   otic plant stresses, we are developing a plant disease exten-
imperative to develop higher-yielding crop varieties to sup-                                                               sion (IDOPlant) of the Infectious Disease Ontology (IDO)
port the growing human population. This can be done in two
                                                                                                                           (Cowell & Smith, 2010) as a reference ontology for plant
primary ways, (1) by increasing, e.g., the number or size of
                                                                                                                           disease. The goals are to provide plant scientists with the
grains on a cereal plant or tubers on a potato plant, and (2)
                                                                                                                           means to identify genomic and genetic signatures of host-
by reducing losses due to diseases and pests. Pre-harvest                                                                  pathogen interactions, resistance, or susceptibility, and to
disease and pest damage in the eight most important food                                                                   help agronomists and farmers by developing tools to identi-
and cash crops in the world account for ~42% of attainable                                                                 fy disease phenotypes and gather epidemiological statistics.
production, and infectious plant diseases also threaten plant
                                                                                                                                 IDOPlant will integrate and interoperate with member
conservation and human health (Anderson et al., 2004).
                                                                                                                           and candidate ontologies of the Open Biomedical Ontolo-
      Many challenges in plant pathology (the study of plant
                                                                                                                           gies (OBO) Foundry (Table 1), such as: the Plant Ontology
diseases) can potentially be met through advances in meth-
ods such as high-throughput sequencing and automated                                                                       (PO; describes the plant structures and the development
scoring of phenotypes (Studholme et al., 2011; Furbank &                                                                   stages at which infections happen or signs of disease are
                                                                                                                           observed), the Plant Trait Ontology (TO; describes pheno-
                                                                                                                           types or entities that are evaluated in plants, such as leaf
* To whom correspondence should be addressed:                                                                              color or grain yield), and the Gene Ontology (GO; describes
jaiswalp@science.oregonstate.edu



                                                                                                                                                                                       1
Walls et al.


ID           Ontology Name              Domain
                                                                                2     METHODS
PO           Plant Ontology1            plant structures and development
                                           stages                                 Throughout this paper, words in italics are ontology terms,
 GO          Gene Ontology2             biological processes, sub-cellular        e.g., pathogen. If the source ontology is not evident from
                                           components, molecular function         the context, then we prefix with the ontology ID, as in:
 TO          Trait Ontology3            plant traits                              IDO:pathogen. The IDOPlant and the Plant Phenotype and
 PATO        Phenotypic Quality On-     phenotypic qualities
                tology4
                                                                                  Stress Ontology are being constructed in web ontology
 OBI         Ontology for Biomedical protocols, instrumentation, materials, language (OWL), using the Protégé 4.1 software
                Investigations5                data, types of analysis            (http://protege.stanford.edu) The annotation standard for-
 ENVO        Environment Ontology6           environmental features and habitats  mat will follow the GO and PO model with the GAF2.0
 ChEBI       Chemical Entities of            chemical entities                    format (Gene Ontology, 2012).
                Biological Interest7
 GAZ         Gazetteer8                      geographical information
                                                                                         We began by reviewing whether the terms in the IDO
                                                                                  were adequately structured for describing plant infectious
 NCBItaxon NCBI Taxonomy Classi- taxonomic classification of living
                fication9                      organisms
                                                                                  diseases, including discussion with the developers of IDO
  Table 1. Some of the external ontologies needed to describe plant diseas-       and the Ontology for General Medical Science (OGMS;
  es. References: 1. Ilic et al., 2007, 2. Gene Ontology Consortium, 2010, 3.     http://code.google.com/p/ogms/). Next, following the strat-
  Jaiswal, 2011, 4. Mungall et al., 2010, 5. http://obi-ontology.org/             egy used in other IDO extensions, we created terms for the
  page/Main_Page, 6. http://http://www.environmentontolo gy.org/, 7.
  Degtyarenko et al. 2007, 8. http://bioportal.bioontolgy.org/ontologies          IDOPlant, such as plant infectious disease, specific to the
  /1397, 9 http://www.obofoundry.org/wiki/index.php/NCBI Taxon:                   needs of plant pathology. More specific terms, such as rice
  Main_Page.                                                                      bacterial blight disease were added as an example of how
the molecular functions of interacting genes from host and                        to model a specific disease and to provide terms to be used
pathogen as well as biological processes involving either                        in   annotating existing gene expression data available
host, pathogen, or both). The multi-organism process branch                      through    Gramene (http://www.gramene.org). Textual defini-
of the GO, developed as part of the PAMGO project (Giglio                        tions   and   relationships among terms are drawn from plant
et al., 2009), is especially relevant to the IDOPlant. To en-                    pathology      textbooks or journal articles, and are reviewed by
sure compatibility with research on non–plant diseases, the                      plant   disease   experts.
IDOPlant is created by downward population from the up-                                  Logical   definitions for IDOPlant terms are being con-
per-level terms of the IDO. The IDOPlant differs from exist-                     structed   in   OWL.    Many of the terms needed for logical def-
ing IDO extensions, because the latter focus on specific dis-                    initions   already    exist   in other ontologies. To access these
eases or pathogens, like Malaria or Brucellosis, that affect                     terms,    we  could   import    entire ontologies into the IDOPlant,
human or other animal health (Lin et al., 2011; Topalis et                       but   this  would    result   in many unnecessary terms and may
al., 2010). IDOPlant, in contrast, is designed to encompass                      cause    problems    if the resultant   ontology is too large. Import-
any plant infectious disease. Furthermore, the IDOPlant is                       ing   a  selected   subset   of  terms   creates problems as well. If
being developed as part of the larger Plant Phenotype and                        we   import     individual    terms   from  external ontologies, then
Stress Ontology Project, which is not limited to infectious                      we   lose  the   ontology   structure    they  are associated with and
diseases but encompasses any plant stress. Our approach                          the  reasoning     power   that   comes   with  it. If we import select-
calls for a multi-pronged strategy that includes creating new                    ed   terms     through    the    MIREOT      process    (Courtot et al.,
terms, as well as importing terms from, and building links                       2009),    which   imports    the  minimum     information   to reference
to, other ontologies.                                                            an   external     ontology,     we   have   to   update   the  IDOPlant
       The study of plant diseases provides an excellent ex-                     whenever      there  is a change    to the source   ontology.
ample of how the framework of the OBO Foundry (Smith et                                  To cope with these issues, we use a multi-pronged
al. 2007) allows us to describe complex biological phenom-                       strategy    that includes directly importing some terms and
ena using terms from multiple ontologies. By constructing                        building    bridge   files to link to external ontologies.
the IDOPlant within the OBO framework, we eliminate re-                          •  Terms     specific   to plant diseases are added to the
dundant efforts, have a head start in ontology term devel-                          IDOPlant      and   assigned    unique IDOPlant IDs, e.g.,
opment, and yield outcomes compatible with databases that                           IDOPlant:#######.
already annotate their data using OBO Foundry ontologies,                        • Terms falling near the bottom of the IDOPlant hierarchy
such as the Arabidopsis Information Resource (TAIR)                                 that are drawn from ontologies from which only a few
(Swarbreck et al., 2008), Gramene (Youens-Clark et al.,                             terms are needed are imported as single terms, using the
2011; Jaiswal, 2011) and Uniprot (The UniProt Consortium,                           original ontology ID. When appropriate, the MIREOT
2010). In this paper, we describe our plans for the overall                         method is used.	
  
structure of the IDOPlant, provide an example of how to                          • Content treated in ontologies from which many terms are
model plant disease data, and discuss the types of data that                        needed are accessed by simultaneously loading multiple
can be annotated with the IDOPlant.                                                 ontologies and creating relations among them using



2
                                                                                A plant disease extension of the Infectious Disease Ontology



  bridge files (Mungall et al., 2010). This applies specifi-                              The IDO consists primarily of terms specific to infec-
  cally to the three main ontologies (PO, TO, and PATO)                           tious disease, together with relevant terms imported from
  whose terms are needed to describe plant stresses. Users                        other ontologies, such as organism from OBI; disease, dis-
  will be required to open the entire suite of these ontolo-                      order, and disease course from OGMS; habitat from
  gies when annotating data with the IDOPlant.                                    ENVO; macromolecular complex, reproduction, and entry
• Taxonomic entities require special treatment, because we                        into host from GO; bacterium and virus from NCBItaxon;
  will ultimately need to import many terms for plant spe-                        and molecular entity from ChEBI. The IDO has created
  cies, disease organisms, and vector species. However, the                       many new terms, such as resistance to drug, infectious
  NCBItaxon ontology is very large and can be impractical                         agent, and infectious disease epidemic. The bulk of the
  to work with when loaded. Therefore, we will manually                           unique IDO terms can be used for the IDOPlant without
  import the necessary taxa into the IDOPlant from either                         modification. For example IDO:infectious disease is defined
  NCBItaxon or uBio (http://ubio.org).                                            as “A disease whose physical basis is an infectious disor-
• In the event that a term imported into the IDOPlant is                          der”. This in turn is based on the OGMS definition of dis-
  made obsolete in the source ontology, we will replace the                       ease: “A disposition (i) to undergo pathological processes
  term either with the term suggested by the source ontolo-                       that (ii) exists in an organism because of one or more disor-
  gy or with a new term created for the IDOPlant.
                                                                                  ders in that organism” (Scheuermann et al., 2009). Although
                                                                                  the wording of definitions such as this may be unfamiliar to
3 RESULTS AND DISCUSSION                                                          plant pathologists, the meaning is consistent with traditional
Researchers should contact the curators before using the                          treatments of plant disease (e.g., Manners, 1993).
IDOPlant, because it is under active development. A draft is                               IDO terms such as transition to clinical abnormality
available at http://purl.obolibrary.org/obo/idoplant.owl.                         or subclinical infection required careful consideration, be-
3.1 Using IDO for plant infectious diseases                                       cause the word “clinical” is not commonly used for plants.
                                                                                  We decided that the meaning of their definitions was appro-
Our review of the IDO suggests that it is generally appropri-                     priate for plants, despite the names. For example, a feature
ate as a foundation for the description of plant diseases. The                    of an organism is clinically abnormal when it: “(1) is not
IDO is rooted in the Basic Formal Ontology (BFO) (Arp &                           part of the life plan for an organism of the relevant type …
Smith, 2008) and in the OGMS, which increases compatibil-                         (2) is causally linked to an elevated risk either of pain or
ity with other OBO Foundry ontologies and helps to ensure                         other feelings of illness, or of death or dysfunction, and (3)
logically consistent use of type-subtype relations. For ex-                       is such that the elevated risk exceeds a certain threshold
ample, IDO:pathogen cannot be classified as a subtype of                          level” (Scheuermann et al., 2009). All three conditions can
IDO:process of establishing an infection, because they be-                        be met in plants. Although we cannot know if plants experi-
long to disjoint super-classes (BFO:continuant and                                ence pain or feelings of illness, we can assess death or dys-
BFO:occurrent, respectively).                                                     function in plants.
                                                                                                                    Another potential limitation
                                                                                                              of the IDO for use in plant science
                                                                                                              is the meaning of terms from the
                                                                                                              OGMS that were defined within
                                                                                                              the scope of clinical encounters
                                                                                                              involving humans. In particular,
                                                                                                              the definition of symptom from
                                                                                                              OGMS requires a host of a type
                                                                                                              that can report its experiences, and
                                                                                                              so is restricted to sentient hosts. In
                                                                                                              plant pathology, “symptom” is
                                                                                                              commonly used to describe the
                                                                                                              phenotypes that are associated
                                                                                                              with a plant disease. The pheno-
                                                                                                              types are independent of the dis-
                                                                                                              ease and the same phenotype or
                                                                                                              “symptom” may be associated
                                                                                                              with many different diseases. Fur-
 Fig. 1. 	
  Selected terms from the upper-level type-subtype hierarchy of the IDOPlant, with top-level terms thermore, diagnosis generally de-
 imported form the IDO (including terms imported to the IDO from BFO and other ontologies) and lower-         pends on a collection of pheno-
 level terms that were added as part of the IDOPlant (in bold). All arrows represent is_a relations. Dashed   types, and not every instance of a
arrows indicate several skipped intermediate steps in the ontology hierarchy.


                                                                                                                                                  3
Walls et al.



disease will display every phenotype that is typical of the              the material basis of an infectious disease, e.g., rice
disease. Rather than use the OGMS definition of symptom,                 bacterial leaf blight disease has_infectious_agent Xan-
we developed a new term for the IDOPlant:                                thamonas oryzae.
      plant disease symptom =def. A feature of a plant that is      In addition we are developing the following for IDOPlant:
      of the type that can be hypothesized to be involved in        has_plant_disease_symptom: This relation is used to indi-
      the realization of a plant disease.                                cate a phenotype, process, or independent continuant
      Comment: Features include phenotypes such pale yel-                that is evaluated to diagnose a disease. For example,
      low leaf color, processes such as sudden wilting, and              “rice bacterial leaf blight disease has_plant_disease_
      independent continuants such as leaf lesion.                       symptom leaf color pale yellow” means that pale yel-
The terms plant disease symptoms already exist in other                  low leaf color is a plant disease symptom (see above)
ontologies (primarily the TO), and will be linked to plant               of rice bacterial leaf blight disease, but it does not
diseases using the relation has_plant_disease_symptom (see               mean that every instance of rice bacterial leaf blight
section 3.3).                                                            disease has pale yellow leaves.
3.2 Terms from external ontologies                                  3.4 Modeling disease in the IDOPlant
      The study of plant diseases encompasses many do-              Much of the information available on plant diseases is in a
mains. In addition to IDO terms common to all infectious            natural language or free text form, such as: “Bacterial leaf
diseases, like pathogen or resistance, the IDOPlant needs           blight disease of rice is caused by Xanthomonas oryzae. It
terms to describe the taxonomy of host plants, pathogens,           produces pale yellow leaves in mature plants. In one report
and vectors, genomic and genetic data, the geographic loca-         the pathogen and the disease were reported in the Northern
tion and ecology of diseases and hosts, plant and fungal            Territory of Australia.” Using ontologies to process such
anatomy, plant and pathogen development, biological pro-            descriptions in a standardized form makes them comprehen-
cesses, and molecular functions. To encompass this range,           sible to computers and reasoners. For example, the descrip-
the IDOPlant is not only creating new ontology terms spe-           tion above could be converted (using natural language pro-
cific to its domain, but also integrating and linking to exist-     cessors or other mechanisms) to:
ing terms from multiple sources (Table 1). Whenever possi-                 disease: rice bacterial leaf blight dis-
ble, existing ontology terms are being used to create logical              ease | host species: Oryza sativa (rice)
                                                                           | caused by: Xanthomonas oryzae | has
definitions for IDOPlant terms. For example, rice bacterial                symptom: pale yellow leaves | reported
leaf blight is defined as “A bacterial blight disease (in                  in: Northern Territory
IDOPlant), that has as infectious agent Xanthomonas oryzae          This standardized text could then be made even more pow-
(from NCBItaxon)” (fig. 3). Terms from external ontologies          erful using ontology terms and relations (Fig. 3).
will also be used for relations such as rice bacterial leaf
blight disease has_plant_disease_symptom pale yellow leaf           3.5 Integrating data into the IDOPlant
color (from TO). Logical definitions allow us to use auto-          The current situation in the plant disease research communi-
mated reasoners to ensure that the ontology hierarchy is            ty is similar to that in the animal community when the GO,
sound and to infer sub-types and relations implied by the           MeSH (Savage, 2000), and CARO (Haendel et al., 2007)
definitions. These can then be added to the ontology
if correct or eliminated if incorrect or redundant
(Meehan et al., 2011).
3.3 IDOPlant relations
The IDO imports the Relation Ontology (RO)
(Smith et al., 2005), which includes basic relations
such as SubClassOf (is_a), part_of, participates_in,
inheres_in, bearer_of, has_disposition, has_role,
and has_function. In addition, we plan to incorpo-
rate several new relations:
has_material_basis: This relation is under devel-
      opment by the OGMS and will be added to the
      BFO. It is used to indicate the material basis of
      a disease. For infectious diseases, we use the
      has_infectious_agent relation.                      Fig. 3. 	
  Some of the terms and relations needed to model rice bacterial blight disease
                                                          in the IDOPlant. Following the IDO, a disease is treated as a disposition of an infected
has_infectious_agent: This relation, which is under       organism, which has a particular infectious agent. The IDOPlant can also be used to
      consideration by the IDO, is used to indicate       define terms in the TO, such as rice bacterial blight disease resistance, which is a
                                                          resistance to infectious disease that inheres in Oryza sativa.


4
                                                                     A plant disease extension of the Infectious Disease Ontology



projects were being initiated: A number of organism-              REFERENCES
specific databases are faced with large amounts of molecu-        Anderson, P.K. et al., 2004. Emerging infectious diseases of plants: patho-
lar, germplasm (stock), genotype, and phenotype data asso-               gen pollution, climate change and agrotechnology drivers. Trends in
ciated with function, phenotype, or environment. The shar-               Ecology & Evolution, 19(10), pp.535–544.
                                                                  Anon, 2012. Phytozome v7.0. Available at: http://www.phytozome.net/.
ing of the task of building a set of controlled vocabularies
                                                                  Arp, R. & Smith, B., 2008. Function, role, and disposition in Basic Formal
such as GO and PO has helped enormously to address the                   Ontology. Nature Precedings. Available at: http://hdl.handle.net
needs of multiple individual databases. The IDOPlant con-                /10101/ npre.2008.1941.1.
trolled vocabulary for plant infectious diseases will allow       Courtot, M. et al., 2009. MIREOT: the Minimum Information to Reference
                                                                         an External Ontology Term. Nature Precedings, (713). Available at:
database curators to store and retrieve the results of experi-
                                                                         http://precedings.nature.com/documents/3574/version/1.
ments related to diseases, including quantitative trait loci,     Cowell, L. & Smith, B., 2010. Infectious Disease Ontology. In Infectious
pathogen and host germplasm descriptions, microarray ex-                 Disease Informatics. New York, NY: Springer, pp. 373–395.
pression studies, gene knockouts, reporter gene expression        Degtyarenko et al. 2007. ChEBI: a database and ontology for chemical
patterns, and gene-gene interactions from host and patho-                entities of biological interest. Nuc Acids Research 36, pp.D344-D350.
                                                                  FAO, 2012. FAOSTAT, Food and Agricultural Organization of the United
gen. The Plant Phenotype and Stress Ontology Project aims                Nations. FAOSTAT. Available at: http://faostat.fao.org/default.aspx .
to overcome the obstacles in annotating data for complex          Furbank, R.T. & Tester, M., 2011. Phenomics – technologies to relieve the
biological concepts that span multiple ontologies by devel-              phenotyping bottleneck. Trends in Plant Science, 16(12), pp.635–644.
                                                                  The Gene Ontology Consortium, 2010. The Gene Ontology in 2010: exten-
oping both the ontology terms and the software tools needed
                                                                         sions and refinements. Nuc Acids Research 38, pp.D331-D335.
to annotate data from all aspects of plant diseases.              Gene Ontology, 2012. GO Annotation File Format Guide. Available at:
      To annotate plant infectious disease description data,             http://www.geneontology.org/GO.format.annotation.shtml.
the IDOPlant is reaching out to resources such as the Food        Giglio, M.G. et al., 2009. Applying the Gene Ontology in microbial annota-
and        Agriculture      Administration’s      AGROVOC                tion. Trends in Microbiology, 17(7), pp.262–268.
                                                                  Goudie, A. & Cuff, D.J., 2001. Encyclopedia of global change: environ-
(http://aims.fao.org/website/AGROVOC-Thesaurus/sub)                      mental change and human society, Oxford University Press.
and      the    International   Rice     Research     Institute   Haendel, M. et al., 2007. CARO - The Common Anatomy Reference On-
(http://www.knowledgebank.irri.org/rice.htm). These re-                  tology. In Anatomy Ontologies for Bioinformatics: Principles and
sources will enrich the IDOPlant by providing a wealth of                Practice. Computational Biology Series. Springer.
                                                                  Ilic, K., et al. 2007. The Plant Structure Ontology, a Unified Vocabulary of
information that can be incorporated into the ontology and               Anatomy and Morphology of a Flowering Plant. Plant Physiology:
by identifying gaps and errors. The IDOPlant can benefit                 143(2), pp.587-599
these organizations by making their content more easily           Jaiswal, P., 2011. Gramene Database: A Hub for Comparative Plant Ge-
accessible to semantic applications.                                     nomics. In A. Pereira, ed. Plant Reverse Genetics. Totowa, NJ: Hu-
                                                                         mana Press, pp. 247–275.
                                                                  Lin, Y., Xiang, Z. & He, Y., 2011. Brucellosis Ontology (IDOBRU) as an
4    CONCLUSIONS                                                         extension of the Infectious Disease Ontology. Journal of Biomedical
                                                                         Semantics, 2(1), p.9.
As the growing human population and climate change place          Manners, J.G., 1993. Principles of Plant Pathology, Cambridge, U.K.:
even more uncertainty on food supply, the need to under-                 Cambridge University Press.
stand the linkages between plant disease, environment, and        Meehan, T. et al., 2011. Logical development of the Cell Ontology. BMC
                                                                         Bioinformatics, 12(1), p.6.
yield is greater than ever. The IDOPlant and the Plant Phe-       Mungall, C. et al., 2010. Integrating phenotype ontologies across multiple
notype and Stress Ontology Project can contribute to this                species. Genome Biology, 11(1), p.R2.
challenge by making data on plant diseases more accessible.       Savage, A., 2000. Changes in MeSH Data Structure, NLM Technical Bul-
We are taking advantage of the interoperability of OBO                   letin. Available at:
                                                                         http://www.nlm.nih.gov/pubs/techbull/ma00/ma00_mesh.html.
Foundry ontologies to leverage existing terms to enhance          Scheuermann, R.H., Ceusters, W. & Smith, B., 2009. Toward an Ontologi-
the new IDOPlant extension, simultaneously enriching all                 cal Treatment of Disease and Diagnosis. Summit on Translational Bi-
ontologies involved by filling in terms needed for logical               oinformatics, 2009, p.116.
                                                                  Smith, B. et al., 2005. Relations in biomedical ontologies. Genome Biology,
definitions. By expanding the core terms of the IDO to                   6(5), p.R46.
plants, we can learn how plant diseases differ from, and are      Smith, B. et al., 2007. The OBO Foundry: coordinated evolution of ontolo-
similar to, infectious diseases in general.                              gies to support biomedical data integration. Nat Biotech, 25(11),
                                                                         pp.1251–1255.
                                                                  Studholme, D.J., Glover, R.H. & Boonham, N., 2011. Application of High-
ACKNOWLEDGEMENTS                                                         Throughput DNA Sequencing in Phytopathology. Ann Rev of Phyto-
                                                                         pathology, 49(1), pp.87–105.
RW, JE, DWS, and PJ are supported by NSF-IOS: 0822201             Swarbreck, D. et al., 2008. The Arabidopsis Information Resource (TAIR):
to the Plant Ontology Project. BS is supported by NIH:U54                gene structure and function annotation. Nuc Acids Research, 36(suppl
HG004028 (National Center for Biomedical Ontology) and                   1), p.D1009 –D1014.
                                                                  Topalis, P. et al., 2010. IDOMAL: an ontology for malaria. Malaria Jour-
NIH / NIAID R01 AI 77706-01 (Immune System Biological
                                                                         nal, 9(1), p.230.
Networks). Thanks to Lindsay Cowell, Laurel Cooper, Rob-          The UniProt Consortium, 2010. Ongoing and future developments at the
ert Hoehndorf, and three anonymous reviewers for com-                    Universal Protein Resource. Nuc Acids Research, 39(Database),
ments on earlier versions of this manuscript.                            p.D214–D219.
                                                                  Youens-Clark, K. et al., 2011. Gramene database in 2010: updates and
                                                                         extensions. Nuc Acids Research, 39(suppl 1), p.D1085 –D1094.



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