First published online June 12, 2003; 10.1104/pp.102.017376
Plant Physiology 132:1196-1206 (2003)
© 2003 American Society of Plant Biologists
BIOENERGETICS AND PHOTOSYNTHESIS
Energy Status and Its Control on Embryogenesis of Legumes. Embryo Photosynthesis Contributes to Oxygen Supply and Is Coupled to Biosynthetic Fluxes1
Hardy Rolletschek,
Hans Weber* and
Ljudmilla Borisjuk
Institut für Pflanzengenetik und Kulturpflanzenforschung, D-06466
Gatersleben, Germany
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.
Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.102.017376.
1 This work was supported by the Deutsche Forschungsgemeinschaft.
*
Corresponding author; e-mail
weber{at}ipk-gatersleben.de;
fax 49 -39482-5138.
Received November 7, 2002;
returned for revision December 19, 2002;
accepted February 25, 2003.
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