Developmental Stages Ontology Principles

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Plant Structure Development Stages Ontology

Contents

Objectives

The main objective of the Plant Structure Developmental Stage Ontology is to describe developmental stages of organs and organ systems of a 'generic' plant. Series of developmental stages are defined based on temporal landmarks delineated by morphological and anatomical changes, as described in published literature. Instead of providing detailed species-specific staging in a form of a 'parallel bins' for each structure, we opted to integrate existing species-specific temporal ontologies (developed by TAIR and Gramene), creating standardized, 'generic' staging system for each plant organ and organ system.

This ontology is the first multi-species representation of developmental stages in plants - it is applicable to all plants.

There is a very specific purpose for creating such ontology - primarily to facilitate cross database queries and to foster its consistent use for annotations of developmental stage specific gene expressions, for meaningful description of phenotypes and for standardized description of biological samples in plant databases and in the plant research community. Its comprehensiveness is therefore restricted by its main purpose - cross-species comparison and cross-database queries.

This ontology is part of our web-accessible database and it can be searched using the ontology browser at the Planteome web site (planteome.org). It is structured as a simple hierarchical tree with six top nodes, representing main organ systems. A hierarchical structure of the ontology has an obvious advantage of having ontological terms that are computable; thus, this generic plant ontology has potential for both, cross-species comparison and cross-database queries.

Organizing principles and rationales

While creating this ontology, the POC agreed to avoid conceptual overlaps with the Gene Ontology (GO), which already has plant development terms as a part of the Biological process ontology. Therefore, to make distinction between GO Biological process terms, we arbitrarily restricted 'domain knowledge' of this developmental stages ontology and focused on a temporal aspect, in which chronological developmental stages are described by the main morphological and anatomical changes observed for each plant structure. To display correct progression of described stages, alphabetical or numerical prefixes were added to the term names in most plant structure nodes (for example, see children terms of 'leaf development stages' or 'root development stages').

Species-specific terms as synonyms

Similar to the other two aspects of the Plant Ontology, synonymy was utilized to link the species-specific stages from existing temporal ontologies at Gramene and TAIR to the 'generic' developmental stages in the PO. A user can find species-specific terms from the respective databases on a term detail page (in the synonym field) in the ontology browser. On the same term detail page, in the External References filed, the URL links to the mapped keyword(s) in Gramene and TAIR are provided.

When describing generic developmental stages of a flowering plant, it was not possible to have 'all inclusive' stages that would be pertinent to all monocots and eudicots. An example is 'embryo development stages', with several children terms, each describing a specific stage of embryo development in either well-studied model dicots (Arabidopsis and Capsella), or in monocots, namely grasses. Since embryo development in Arabidopsis and in grasses follows very different developmental patterns, there are only few terms (stages) common for both, such as 'proembryo stage' or 'transition stage'. Species-specific stages of Arabidopsis embryo development from TAIR ontology were added as synonyms to the corresonding stages in PO, while stages describing embryo development in rice in the existing Gramene ontology will be soon added as synonyms to the pertinent stages in the PO. Therefore, synonymy, as applied in PO, facilitates cross-species comparison, although, in this particular case, such comparison is only possible at higher level, i.e., 'embryo development stages'. At the same time, synonymy allows for a retrieval of species-specific information. For example, by choosing species-specific filter options in the ontology browser, it is possible to search for terms/stages pertinent for Arabidopsis embryo development and also to retrieve genes expressed during embryo development only in Arabidopsis or in rice.

Relationship types

The exclusive term-to-term relationship type used in this ontology is "is_a" (an instance of). It indicates the relationship between a term and its parent term in the ontological structure, meaning that the term is a subclass of its parent. For example, 'B leaf expansion' is_a (a subclass) of the parent term, 'leaf developmental stages', which in turn is a subclass of the 'plant structure developmental stages'.

Top nodes in the Plant Structure Developmental Stages Ontology

There are currently 118 terms that describe development stages of main organs and organ systems of a flowering plant. Terms are organized as a simple hierarchy or 'structured list', and arranged in six main nodes:

Two top nodes, 'fruit development stage' and 'inflorescence development stage' don't have any generic stages, due to the complex nature of their development and vast differences in formation of these organs among flowering plants. In both cases, it was impossible to create generic stages of fruit and inflorescence development that would be pertinent for eudicots and monocots. At later times, if required, a limited number of higher level species-specific terms may be added to facilitate gene annotations and phenotype description.

Flower developmental stages

The goal was to include common stages for a generic flower, and for all floral organs, starting with primordial stage ('primordium visible') for each respective floral organ. The following floral organs are included:

Ovule and megagametophyte development stages encompass monosporic, bisporic and tetrasporic types of embryo sac development (Reiser and Fisher, 1993). To accommodate this, seven generic stages are created, from 'A megaspore mother cell enlarges' to the last 'G eight nucleate megagametophyte stage'.

Anther and pollen development stages are based on the descriptions for:

Terms in the anther node describes morphological changes specifically in the anther tissues, while pollen node includes stages of two- and three-celled pollen development.

Leaf developmental stages

The main four stages of leaf development were based on description by Poethig (1997), and on description of leaf development stages in rice (Itoh et al, 2005). The following instances of 'leaf development stages' are pertinent for simple leaf and compound leaf, encompassing eudicots and monocots:

vascular leaf initiation stage, PO:0001050

vascular leaf initiation stage, PO:0001051
vascular leaf expansion stage, PO:0001052
vascular leaf post-expansion stage, PO:0001053
vascular leaf senescent stage, PO:0001054

Root development stages

Instead of creating separate developmental stages for primary, lateral and crown root, we defined several 'generic' stages of root development, common for all three root types. Based on descriptions for cereal root development (Hochholdinger et al, 2004), and for Arabidopsis lateral root development (Casimiro et al, 2003), there are five generic stages of root development:

Seed development stages

Similar to the flower development stages node, general progression of seed development is described, as well as developmental stages of seed parts (endosperm and embryo), which are included as children nodes. The exception is the development of the seed coat (not represented in this ontology) - due to the complex and variable nature of its development. It was difficult to define the common stages for species with single integument vs. those with inner and outer integument, and also stages that would be common for monocot (for instance, grasses) and eudicots.

Embryo development stages

Stages of embryo development are based on classic studies of model plant species (Arabidopsis and Capsella), reviewed by West and Harada (1993)

  • cereal crops, maize (Abbe and Stein, 1954, Sheridan and Clark, 1987)
  • rice (Itoh et al, 2005) in particular.

Endosperm development stages are based on descriptions of free-nuclear endosperm development in Arabidopsis and cereals (Olsen, 2004), also taking into consideration endosperm patterning in both persistent and transient endosperms (Costa et al, 2004).

References

  • Abbe, EC, Stein, OL. (1954) The growth of the shoot apex in maize: embryogeny. American J Bot, 41: 285?293.
  • Bedinger P and Russell SD (1994) Gametogenesis in maize. In The Maize Handbook, M. Freeling and V. Walbot, eds (New York: Springer-Verlag), pp. 48-60.
  • Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ. (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci, 8:165-171. [pdf]
  • Costa LM, Gutierrez-Marcos JF, Dickinson HG. (2004) More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci, 9: 507-514. [pdf]
  • Goldberg, RB, de Paiva, G. and Yadegari, R. (1994) Plant embryogenesis: zygote to seed. Science 266: 605-614.
  • Hochholdinger F, Park WJ, Sauer M, Woll K. (2004) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci., 9: 42-48.[pdf]
  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y. (2005) Rice Plant Development: from Zygote to Spikelet. Plant Cell Physiol, 46:23-47. [pdf]
  • Laux T, Wurschum T, Breuninger H. (2004) Genetic regulation of embryonic pattern formation. Plant Cell, 16: S190-202.[pdf]
  • Malamy JE, Benfey PN. (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 124:33-44. [pdf]
  • Olsen OA, Linnestad C, Nichols SE. (1999) Developmental biology of the cereal endosperm. Trends Plant Sci, 4: 253-257. [pdf]
  • Olsen OA. (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell, 16: S214-227. [pdf]
  • Poethig S. (1997) Leaf morphogenesis. Plant Cell, 9: 1077-1087. [pdf]
  • Regan, SM, Moffatt BA. (1990) Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. Plant Cell 2: 877-889. [pdf]
  • Reiser L, Fischer RL. (1993) The Ovule and the Embryo Sac. Plant Cell, 5:1291-1301. [pdf]
  • Robinson-Beers, K, Pruitt, RE, and Gasser CS. (1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4, 1237-1249. [pdf]
  • Sanders, PM, Bui, AQ. , Weterings, K, McIntire, KN, Hsu, Y-C, Lee, PY, Truong, MT, Beals, TP, and Goldberg RB. (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant. Reprod.11, 1-27. [pdf]
  • Sheridan WF, Clark JK. (1987) Maize embryogeny: a promising experimental system. Trends Genet, 3: 3-6.
  • Smyth, DR, Bowman, JL, and Meyerowitz, EM. (1990) Early flower development in Arabidopsis. Plant Cell 2, 755-767. [pdf]
  • West MAL, Harada JJ. (1993) Embryogenesis in Higher Plants: An Overview. Plant Cell, 5: 1361-1369. [pdf]
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IN DISCUSSION