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Published on June 12, 2003; 10.1104/pp.102.017376


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Received November 7, 2002
Returned for revision December 19, 2002
Accepted February 25, 2003

Energy Status and Its Control on Embryogenesis of Legumes. Embryo Photosynthesis Contributes to Oxygen Supply and Is Coupled to Biosynthetic Fluxes

Hardy Rolletschek , Hans Weber *, and Ljudmilla Borisjuk

Institut für Pflanzengenetik und Kulturpflanzenforschung, D-06466 Gatersleben, Germany

* Corresponding author; email: weber{at}ipk-gatersleben.de.

Legume seeds are heterotrophic and dependent on mitochondrial respiration. Due to the limited diffusional gas exchange, embryos grow in an environment of low oxygen. O2 levels within embryo tissues were measured using microsensors and are lowest in early stages and during night, up to 0.4% of atmospheric O2 concentration (1.1 µM). Embryo respiration was more strongly inhibited by low O2 during earlier than later stages. ATP content and adenylate energy charge were lowest in young embryos, whereas ethanol emission and alcohol dehydrogenase activity were high, indicating restricted ATP synthesis and fermentative metabolism. In vitro and in vivo experiments further revealed that embryo metabolism is O2 limited. During maturation, ATP levels increased and fermentative metabolism disappeared. This indicates that embryos become adapted to the low O2 and can adjust its energy state on a higher level. Embryos become green and photosynthetically active during differentiation. Photosynthetic O2 production elevated the internal level up to approximately 50% of atmospheric O2 concentration (135 µM). Upon light conditions, embryos partitioned approximately 3-fold more [14C]sucrose into starch. The light-dependent increase of starch synthesis was developmentally regulated. However, steady-state levels of nucleotides, free amino acids, sugars, and glycolytic intermediates did not change upon light or dark conditions. Maturing embryos responded to low O2 supply by adjusting metabolic fluxes rather than the steady-state levels of metabolites. We conclude that embryogenic photosynthesis increases biosynthetic fluxes probably by providing O2 and energy that is readily used for biosynthesis and respiration.




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