The Plastid Isoform of Triose Phosphate Isomerase Is Required for the Postgerminative Transition from Heterotrophic to Autotrophic Growth in Arabidopsis

Abstract

Abstract During postgerminative seedling establishment, reserves stored during seed filling are mobilized to provide energy and carbon for the growing seedling until autotrophic growth is possible. A plastid isoform of triose phosphate isomerase (pdTPI) plays a crucial role in this transition from heterotrophic to autotrophic growth. A T-DNA insertion in Arabidopsis thaliana pdTPI resulted in a fivefold reduction in transcript, reduced TPI activity, and a severely stunted and chlorotic seedling that accumulated dihydroxyacetone phosphate (DHAP), glycerol, and glycerol-3-phosphate. Methylglyoxal (MG), a by-product of DHAP, also accumulated in the pdtpi mutant. Wild-type seed sown in the presence of any of these four metabolites resulted in a phenocopy of this pdtpi mutant, although MG and DHAP were the most effective based upon dosage. These metabolites (except MG) are by-products of triacylglycerol mobilization and precursors for glycerolipid synthesis, suggesting that lipid metabolism may also be affected. Lipid profiling revealed lower monogalactosyl but higher digalactosyl lipids. It is unclear whether the change in lipid composition is a direct or indirect consequence of the pdtpi mutation, as ribulose-1,5-bis-phosphate carboxylase/oxygenase expression, chloroplast morphology, and starch synthesis are also defective in this mutant. We propose that DHAP and MG accumulation in developing plastids delays the transition from heterotrophic to autotrophic growth, possibly due to MG toxicity.