The chloroplast envelope triose-phosphate/phosphate translocator (TPT) is responsible for carbohydrate export during photosynthesis. Using measurements of carbohydrates, partitioning of assimilated 14 CO 2 , photosynthetic gas exchange, and chlorophyll fluorescence, we show that a mutant of Arabidopsis lacking the TPT increases synthesis of starch compared to the wild type, thereby compensating for a deficiency in its ability to export triose-phosphate from the chloroplast. However, during growth under high light, the capacity for starch synthesis becomes limiting so that the chloroplastic phosphate pool is depleted, resulting in a restriction on electron transport, a reduction in the rate of photosynthesis, and slowed plant growth. Under the same conditions but not under low light, we observe release of 14 C label from starch, indicating that its synthesis and degradation occur simultaneously in the light. The induction of starch turnover in the mutant specifically under high light conditions leads us to conclude that it is regulated by one or more metabolic signals, which arise as a result of phosphate limitation of photosynthesis.During photosynthesis, the triose-phosphate/phosphate translocator (TPT) of the chloroplast inner envelope membrane mediates the counterexchange of stromal triose-phosphates (triose-P) derived from CO 2 fixation with cytosolic orthophosphate (P i ), thus providing the cytosol with the precursors for Suc synthesis. Optimum rates of photosynthesis require the regulated exchange of metabolites through TPT. If triose-P is withdrawn from the chloroplast too quickly, the Calvin cycle is depleted of intermediates. Alternatively, if transport through TPT is too slow, phosphorylated intermediates accumulate in the chloroplast, resulting in a depletion of stromal P i , which in turn has the potential to restrict ATP synthesis, again restricting CO 2 fixation (Edwards and Walker, 1983). Under normal circumstances, the potential inhibition of photosynthesis due to P i limitation is ameliorated by activation of ADP-Glc pyrophosphorylase (AGPase; Sowokinos, 1981;Sowokinos and Preiss, 1982), leading to an increase in the rate of starch synthesis and a resulting release of P i .Studies on transgenic potato (Solanum tuberosum) and tobacco (Nicotiana tabacum) plants possessing altered amounts of TPT have established the central role of this translocator in the integration of assimilate partitioning during photosynthesis (Barnes et al., 1994;Heineke et al., 1994; HĂ€usler et al., 1998 HĂ€usler et al., , 2000a HĂ€usler et al., , 2000b. The patterns of carbohydrate synthesis in such plants suggest that they compensate metabolically for the reduced levels of TPT by diverting assimilate into starch, releasing the P i required for continued photosynthesis. Remarkably, despite the changes in carbohydrate metabolism, plants with as little as 20% of wild-type TPT activity show little or no reduction in the maximum rate of CO 2 assimilation under ambient atmospheric conditions, and no change in growth rate (Ries...