Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity

Abstract

SummaryTo analyse the energy status of Vicia faba embryos in relation to differentiation processes, we measured ATP concentrations directly in cryosections using a quantitative bioluminescence-based imaging technique. This method provides a quantitative picture of the ATP distribution close to the in vivo situation. ATP concentrations were always highest within the axis. In pre-storage cotyledons, the level was low, but it increased strongly in the course of further development, starting from the abaxial region of cotyledons and moving towards the interior. Greening pattern, chlorophyll distribution and photosynthetic O 2 production within embryos temporally and spatially corresponded to the ATP distribution, implicating that the overall increase of the energy state is associated to the greening process. ATP patterns were associated to the photosynthetic capacity of the embryo. The general distribution pattern as well as the steady state levels of ATP were developmentally regulated and did not change upon dark/light conditions. The major storage protein legumin started to accumulate in abaxial regions with high ATP, whereas starch localized in regions with relatively lower ATP levels. This suggests a role of the energy state in the partitioning of assimilates into the different storage-product classes. Highest biosynthetic rates occurred when cotyledons became fully green and contained high ATP levels, implicating that a photoheterotrophic state was required to ensure high¯uxes. Based on these data, we propose a model for the role of embryonic photosynthesis to improve the energy status of the embryo.

Snowy cotyledon 2: the identification of a zinc finger domain protein essential for chloroplast development in cotyledons but not in true leaves

“…The plastids of green embryos are referred to as being photoheterotrophic. They fix only very little CO 2 and their main photosynthetic function seems to be the production of ATP and oxygen (Borisjuk et al 2003). Photosynthesis in embryos that is required for the deposition of storage material within the maturing seed seems not to be essential for seed maturation since chlorophyll-deficient embryos of albino and xantha mutants accumulate significant storage material that allows them to germinate (Runge et al 1995;Sundberg et al 1997).…”

Transcriptional Programs of Early Reproductive Stages in Arabidopsis

“…This included, for instance, enzymes from the nonmevalonate isoprenoid pathway, cystathione gamma synthetase, which is involved in S-adenosylmethionine generation and Asp aminotransferase, which serves to recycle generated ammonium. Oxygen and ATP are limiting in developing embryos, and photosynthesis in embryos is important for oxygen supply (Eastmond et al, 1996;Ruuska et al, 2002;Borisjuk et al, 2003;Rolletschek et al, 2003). Although expression of genes for chlorophyll biosynthesis was increased, no significant changes were found for photosynthesis genes (data not shown).…”

Extracellular ATP Induces the Accumulation of Superoxide via NADPH Oxidases in Arabidopsis

“…The most obvious mechanism for ATP release into the plant extracellular matrix (ECM) would be wounding. Cytoplasmic ATP concentrations in plant cells typically range between 0.5 and 1 mM, depending on their metabolic state (Gout et al, 1992;Borisjuk et al, 2003). Phloem sap may also have near millimolar ATP (Geigenberger et al, 1993).…”