Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed

Abstract

The conversion of photosynthate to seed storage reserves is crucial to plant fitness and agricultural production, yet quantitative information about the efficiency of this process is lacking. To measure metabolic efficiency in developing seeds, rapeseed (Brassica napus) embryos were cultured in media in which all carbon sources were [U-14 C]-labeled and their conversion into CO 2 , oil, protein, and other biomass was determined. The conversion efficiency of the supplied carbon into seed storage reserves was very high. When provided with 0, 50, or 150 mmol m 22 s 21 light, the proportion of carbon taken up by embryos that was recovered in biomass was 60% to 64%, 77% to 86%, and 85% to 95%, respectively. Light not only improved the efficiency of carbon storage, but also increased the growth rate, the proportion of 14 C recovered in oil relative to protein, and the fixation of external 14 CO 2 into biomass. Embryos grown at 50 mmol m 22 s 21 in the presence of 5 mM 1,1-dimethyl-3-(3,4-dichlorophenyl) urea (an inhibitor of photosystem II) were reduced in total biomass and oil synthesis by 3.2-fold and 2.8-fold, respectively, to the levels observed in the dark. To explore if the reduced growth and carbon conversion efficiency in dark were related to oxygen supplied by photosystem II, embryos and siliques were cultured with increased oxygen. The carbon conversion efficiency of embryos remained unchanged when oxygen levels were increased 3-fold. Increasing the O 2 levels surrounding siliques from 21% to 60% did not increase oil synthesis rates either at 1,000 mmol m 22 s 21 or in the dark. We conclude that light increases the growth, efficiency of carbon storage, and oil synthesis in developing rapeseed embryos primarily by providing reductant and/or ATP.In seed crops, yield is primarily a function of the production of assimilates by the leaves and other green parts of the plant and the utilization of these assimilates to synthesize reserve materials in the seeds. In addition to its importance to agricultural productivity, efficient storage of assimilates by seeds is essential to provide metabolic precursors and chemical energy to power the young seedling until it can capture its own energy from the sun. Within a species, seedling growth is positively correlated with seed size (Howe and Richter, 1982;Stanton, 1984;Vaughton and Ramsey, 1998;Sousa et al., 2003) and seedlings grown from large seeds have higher rates of establishment than those from small seeds (Black, 1958;Grime and Jeffery, 1965;Armstrong and Westoby, 1993;Burke and Grime, 1996). Thus, the amount of reserves stored in the seed will in large part determine the success of the young seedling.Seeds are not simply passive receptacles for the assimilates and minerals provided by the mother plant. They synthesize complex molecules from simple raw materials in relatively precise amounts and proportions (Egli, 1998). Green seeds are photosynthetically active and are able to fix carbon (Watson and Duffus, 1991;Eastmond et al., 1996). As a consequence, the light re...

Quantitative Multilevel Analysis of Central Metabolism in Developing Oilseeds of Oilseed Rape during in Vitro Culture

“…One further possible limitation of the in vitro system is related to the role of potential oxygen limitation during seed development. While there are no indications that in vitro-grown embryos of oilseed rape lack oxygen (Goffman et al, 2005), contrasting data have been reported for in planta developing embryos (Vigeolas et al, 2003). Under relatively low ambient light levels, reduced oxygen tension can have a strong impact on the energy state in developing oilseed rape seeds, change metabolic fluxes, and impact oil content.…”

“…Yet, we deem the choice of our experimental system to be useful for several reasons. In multiple 13 C-based MFA studies, our in vitro embryo culture system has proven to allow well-resolved measurements of flux distribution in central metabolism (Schwender and Ohlrogge, 2002;Schwender et al, 2003Schwender et al, , 2004Schwender et al, , 2006Goffman et al, 2005;Junker et al, 2007), which is currently not achievable with a similar experimental system in planta. One further possible limitation of the in vitro system is related to the role of potential oxygen limitation during seed development.…”

“…In particular, while many studies infer metabolism in oilseeds on a molecular genetic level, the aim here was to explore the significance of metabolic control. For such integrative analysis, the measurement of metabolic flux ( 13 C-based MFA) is of central importance (Fernie et al, 2005); therefore, we chose in vitro embryo culture as an experimental system that has been used successfully before in multiple biochemical and 13 C-based MFA studies (Schwender and Ohlrogge, 2002;Schwender et al, 2003Schwender et al, , 2004Schwender et al, , 2006Goffman et al, 2005;Junker et al, 2007). Given the practical limitations associated with extending a high-intensity systems biology approach to several hundred accessions, an initial screen was conducted to identify a diverse panel of materials that contrasted with respect to their embryo composition.…”

A Heteromeric Plastidic Pyruvate Kinase Complex Involved in Seed Oil Biosynthesis inArabidopsis

“…stimulation of fatty acid synthesis in green seeds (Goffman et al, 2005). Distinct differences between the two isoforms in Arabidopsis were also discovered.…”

Compartmentation of Triacylglycerol Accumulation in Plants

“…A strict light dependence of FA synthesis in leaf chloroplasts has been known for years (16), but the relevance to TAG accumulation in oilseeds was revealed only recently at the metabolic level. Even low levels of light penetrating to developing embryos provide sufficient reductant and ATP to power FA biosynthesis (17). Moreover, the activity of ribulose-bisphosphate carboxylase/oxygenase (Rubisco) in developing seeds functions not for net photosynthetic carbon fixation but rather to recycle CO 2 released by PDH and other decarboxylation reactions.…”