Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 11 (5), 338-49

Indispensable Roles of Plastids in Arabidopsis Thaliana Embryogenesis

Affiliations

Indispensable Roles of Plastids in Arabidopsis Thaliana Embryogenesis

Shih-Chi Hsu et al. Curr Genomics.

Abstract

The plastid is an organelle vital to all photosynthetic and some non-photosynthetic eukaryotes. In the model plant Arabidopsis thaliana, a number of nuclear genes encoding plastid proteins have been found to be necessary for embryo development. However, the exact roles of plastids in this process remain largely unknown. Here we use publicly available datasets to obtain insights into the relevance of plastid activities to A. thaliana embryogenesis. By searching the SeedGenes database (http://www.seedgenes.org) and recent literature, we found that, of the 339 non-redundant genes required for proper embryo formation, 108 genes likely encode plastid-targeted proteins. Nineteen of these genes are necessary for development of preglobular embryos and/or their conversion to globular embryos, of which 13 genes encode proteins involved in non-photosynthetic metabolism. By contrast, among 38 genes which are dispensable for globular embryo formation but necessary for further development, only one codes for a protein involved in metabolism. Products of 21 of the 38 genes play roles in plastid gene expression and maintenance. Examination of RNA profiles of embryos at distinct growth stages obtained in laser-capture microdissection coupled with DNA microarray experiments revealed that most of the identified genes are expressed throughout embryo morphogenesis and maturation. These findings suggest that metabolic activities are required at preglobular and throughout all stages of embryo development, whereas plastid gene expression becomes necessary during and/or after the globular stage to sustain various activities of the organelle including photosynthetic electron transport.

Keywords: Arabidopsis thaliana; SeedGenes.; embryogenesis; globular embryo; microarray; plastid; preglobular embryo.

Figures

Fig. (1). Overview of terminal phenotype classification of SeedGenes and microarray analyses on embryo development.
Fig. (1). Overview of terminal phenotype classification of SeedGenes and microarray analyses on embryo development.
A series of embryo development stages are listed in different boxes in the arrow (from left to right: early to late stages) and corresponding embryos (approximately to scale) are shown above the arrow. The stages at which embyos were taken for laser capture microdissection and microarray analyses (http://seedgenenetwork.net) are listed below the arrow and indicated by brown lines. Gene Expression Omnibus Accession numbers of the data are: GSE11262, 12403, 12404, 15160, and 15165. The terminal phenotypes of embryo-defective mutants were defined by SeedGenes (http://www.seedgenes.org). *According to SeedGenes database, mutant embryos were removed from seeds prior to desiccation and examined under a dissecting microscope. Seeds classified as I [preglobular] often contain an early globular embryo too small to be seen upon seed dissection. These early globular embryos can be seen using Nomarski optics. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this paper).
Fig. (2). Flow chart indicating the identification of <i>Arabidopsis thaliana</i> genes encode plastid proteins indispensable for embryogenesis.
Fig. (2). Flow chart indicating the identification of Arabidopsis thaliana genes encode plastid proteins indispensable for embryogenesis.
The SeedGenesdatabase (http://www.seedgenes.org; last updated December, 2007) contains 358 A. thaliana genes that give a seed phenotype when disrupted by mutation. Among these genes, 323 of them are necessary for embryogenesis and their disruption results in arrests in development. To determine the localization of encoded proteins, three approaches were used: literature search, Plant Proteome Database (PPDB) search, and compurter algorithm prediction (TargetP). Literature search also revealed that 16 additional genes are necessary for embryogenesis and 7 of them encode plastid proteins, resulting in a total of 108 non-redudant genes necessary for embryogenesis.
Fig. (3). Functional grouping of genes encoding plastid proteins essential for <i>A. thaliana</i> embryogenesis.
Fig. (3). Functional grouping of genes encoding plastid proteins essential for A. thaliana embryogenesis.
TGenes essential for A. thaliana embryogenesis and encoding plastidic proteins are grouped by their mutant phenotypes and predicted functions. Predicted functions are based on sequence comparison and/or experimental data, and divided into six categories: metabolism (orange blocks), plastid gene maintence and expession (yellow blocks), protein homeostasis (green blocks), protein trafficking (blue blocks), transport (purple blocks), and unknown (gray blocks). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this paper).
Fig. (4). Expression pattern of gene encoding plastid proteins necessary for <i>A. thaliana</i> embryogenesis.
Fig. (4). Expression pattern of gene encoding plastid proteins necessary for A. thaliana embryogenesis.
Heat map showing the variation in levels (Z-score) of the indicated mRNAs encoding plastid proteins in embryos at different stages of development (columns: pg, preglobular; g, globular; h, heart; lc, linear cotyledon; mg, matrue green). Predicted functions of gene products are indicated in parentheses (M, metabolism; PGME, plastid gene maintenance and expression; PH, protein homeostasis; PT, protein trafficking; T, transport; U, unknown). Genes with an expression under the detection limit at all five stages were not included in the analysis.

Similar articles

See all similar articles

Cited by 22 PubMed Central articles

See all "Cited by" articles

References

    1. Keeling P . The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2010;365:729–748. - PMC - PubMed
    1. Corriveau J L, Coleman A W. Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am. J. Bot. 1988;75:1443–1458.
    1. Zhang Q, Liu Y. Sodmergen. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cyto-plasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 2003;44:941–951. - PubMed
    1. Waters M, Pyke K. Plastid development and differentiation. In: Møller S G, editor. Annual Plant Reviews, Plastids. Vol. 13. Oxford: Blackwell; 2005. pp. 30–59.
    1. Seo M, Koshiba T. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 2002;7:41–48. - PubMed

LinkOut - more resources

Feedback