Abstract
Large numbers of genes essential for embryogenesis in Arabidopsis encode enzymes of plastidial metabolism. Disruption of many of these genes results in embryo arrest at the globular stage of development. However, the cause of lethality is obscure. We examined the role of the plastidial oxidative pentose phosphate pathway (OPPP) in embryo development. In nonphotosynthetic plastids the OPPP produces reductant and metabolic intermediates for central biosynthetic processes. Embryos with defects in various steps in the oxidative part of the OPPP had cell division defects and arrested at the globular stage, revealing an absolute requirement for the production via these steps of ribulose-5-phosphate. In the nonoxidative part of the OPPP, ribulose-5-phosphate is converted to ribose-5-phosphate (R5P)-required for purine nucleotide and histidine synthesis-and subsequently to erythrose-4-phosphate, which is required for synthesis of aromatic amino acids. We show that embryo development through the globular stage specifically requires synthesis of R5P rather than erythrose-4-phosphate. Either a failure to convert ribulose-5-phosphate to R5P or a block in purine nucleotide biosynthesis beyond R5P perturbs normal patterning of the embryo, disrupts endosperm development, and causes early developmental arrest. We suggest that seed abortion in mutants unable to synthesize R5P via the oxidative part of the OPPP stems from a lack of substrate for synthesis of purine nucleotides, and hence nucleic acids. Our results show that the plastidial OPPP is essential for normal developmental progression as well as for growth in the embryo.
Highlights
Large numbers of genes essential for embryogenesis in Arabidopsis encode enzymes of plastidial metabolism
Beyond 4 DAF, embryos in phenotypically normal seeds of +/pgl3-3 progressed to maturity at the same rate as embryos from wild-type plants, whereas embryos in white seeds remained at the globular stage
To investigate whether the requirement for generation of R5P via the oxidative part of the plastidial oxidative pentose phosphate pathway (OPPP) stems from consumption of R5P or of E4P, we examined the effect on embryo development of mutations directly affecting enzymes on the pathways of either shikimate or nucleotide synthesis
Summary
Large numbers of genes essential for embryogenesis in Arabidopsis encode enzymes of plastidial metabolism. Mutants lacking plastidial isoforms of 6-phosphogluconolactonase (PGL3) and ribose-5-phosphate (R5P) isomerase (RPI3) are listed in the SeedGenes collection of embryolethal mutants (http://seedgenes.org/) [3, 4, 7, 8], and we showed that embryos arrest early in development in response to partial loss of the plastid envelope glucose-6-phosphate (Glc6P) transporter (GPT1) that provides the substrate for the OPPP [9] These observations imply that the first oxidative part of the plastidial OPPP (conversion of Glc6P to ribulose 5-phosphate [Ru5P]) (Fig. 1) has a specific, essential, but unknown role during embryogenesis.
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