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, 155 (4), 1678-89

Identification of Nuclear Genes Encoding Chloroplast-Localized Proteins Required for Embryo Development in Arabidopsis

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Identification of Nuclear Genes Encoding Chloroplast-Localized Proteins Required for Embryo Development in Arabidopsis

Nicole Bryant et al. Plant Physiol.

Abstract

We describe here the diversity of chloroplast proteins required for embryo development in Arabidopsis (Arabidopsis thaliana). Interfering with certain chloroplast functions has long been known to result in embryo lethality. What has not been reported before is a comprehensive screen for embryo-defective (emb) mutants altered in chloroplast proteins. From a collection of transposon and T-DNA insertion lines at the RIKEN chloroplast function database (http://rarge.psc.riken.jp/chloroplast/) that initially appeared to lack homozygotes and segregate for defective seeds, we identified 23 additional examples of EMB genes that likely encode chloroplast-localized proteins. Fourteen gene identities were confirmed with allelism tests involving duplicate mutant alleles. We then queried journal publications and the SeedGenes database (www.seedgenes.org) to establish a comprehensive dataset of 381 nuclear genes encoding chloroplast proteins of Arabidopsis associated with embryo-defective (119 genes), plant pigment (121 genes), gametophyte (three genes), and alternate (138 genes) phenotypes. Loci were ranked based on the level of certainty that the gene responsible for the phenotype had been identified and the protein product localized to chloroplasts. Embryo development is frequently arrested when amino acid, vitamin, or nucleotide biosynthesis is disrupted but proceeds when photosynthesis is compromised and when levels of chlorophyll, carotenoids, or terpenoids are reduced. Chloroplast translation is also required for embryo development, with genes encoding chloroplast ribosomal and pentatricopeptide repeat proteins well represented among EMB datasets. The chloroplast accD locus, which is necessary for fatty acid biosynthesis, is essential in Arabidopsis but not in Brassica napus or maize (Zea mays), where duplicated nuclear genes compensate for its absence or loss of function.

Figures

Figure 1.
Figure 1.
Distribution of protein functions in three datasets of Arabidopsis mutants defective in chloroplast-localized proteins. Genes were classified as having an embryo-defective, pigment-defective, or other loss-of-function mutant phenotype. A, Percentages of genes with assigned (colored) and unassigned (gray) protein functions. Gene totals are indicated in brackets. B, Examples of function subclasses that differ widely between the three datasets: (a) PPR and RNA-binding proteins; (b) ribosomal proteins; (c) photosynthesis; (d) biosynthesis of amino acids, vitamins, nucleotides, and fatty acids; (e) biosynthesis of chlorophyll, carotenoids, and terpenoids; (f) biosynthesis of lipids; modification of fatty acids and lipids; (g) biosynthesis and modification of complex carbohydrates. Gene totals for each dataset are indicated. See Supplemental Table S5 for additional details.

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