Phloem Import and Storage Metabolism Are Highly Coordinated by the Low Oxygen Concentrations within Developing Wheat Seeds

Abstract

We studied the influence of the internal oxygen concentration in seeds of wheat (Triticum aestivum) on storage metabolism and its relation to phloem import of nutrients. Wheat seeds that were developing at ambient oxygen (21%) were found to be hypoxic (2.1%). Altering the oxygen supply by decreasing or increasing the external oxygen concentration induced parallel changes in the internal oxygen tension. However, the decrease in internal concentration was proportionally less than the reduction in external oxygen. This indicates that decreasing the oxygen supply induces short-term adaptive responses to reduce oxygen consumption of the seeds. When external oxygen was decreased to 8%, internal oxygen decreased to approximately 0.5% leading to a decrease in energy production via respiration. Conversely, increasing the external oxygen concentration above ambient levels increased the oxygen content as well as the energy status of the seeds, indicating that under normal conditions the oxygen supply is strongly limiting for energy metabolism in developing wheat seeds. The intermediate metabolites of seed storage metabolism were not substantially affected when oxygen was either increased or decreased. However, at subambient external oxygen concentrations (8%) the metabolic flux of carbon into starch and protein, measured by injecting 14 C-Suc into the seeds, was reduced by 17% and 32%, respectively, whereas no significant effect was observed at superambient (40%) oxygen. The observed decrease in biosynthetic fluxes to storage compounds is suggested to be part of an adaptive response to reduce energy consumption preventing excessive oxygen consumption when oxygen supply is limited. Phloem transport toward ears exposed to low (8%) oxygen was significantly reduced within 1 h, whereas exposing ears to elevated oxygen (40%) had no significant effect. This contrasts with the situation where the distribution of assimilates has been modified by removing the lower source leaves from the plant, resulting in less assimilates transported to the ear in favor of transport to the lower parts of the plant. Under these conditions, with two strongly competing sinks, elevated oxygen (40%) did lead to a strong increase in phloem transport to the ear. The results show that sink metabolism is affected by the prevailing low oxygen concentrations in developing wheat seeds, determining the import rate of assimilates via the phloem.

Prospects for increasing starch and sucrose yields for bioethanol production

“…Under ambient conditions, the oxygen concentration inside developing wheat endosperm was only 2%, and increasing the oxygen concentration around the ear from 21% to 40% resulted in a significant higher ATP:ADP ratio in the endosperm (van Dongen et al, 2004). However, in short-term experiments, this high concentration of oxygen did not result in higher rates of starch synthesis (van Dongen et al, 2004).…”

“…Under ambient conditions, the oxygen concentration inside developing wheat endosperm was only 2%, and increasing the oxygen concentration around the ear from 21% to 40% resulted in a significant higher ATP:ADP ratio in the endosperm (van Dongen et al, 2004). However, in short-term experiments, this high concentration of oxygen did not result in higher rates of starch synthesis (van Dongen et al, 2004). In developing barley seeds, there was a positive spatial correlation between ATP concentration and starch synthesis, and a negative correlation between ATP and oxygen concentrations (Rolletschek et al, 2004).…”

Nonsymbiotic Hemoglobin-2 Leads to an Elevated Energy State and to a Combined Increase in Polyunsaturated Fatty Acids and Total Oil Content When Overexpressed in Developing Seeds of Transgenic Arabidopsis Plants

“…1). Previous studies have shown that the energy status is colimiting for the rates of Suc import (Vigeolas et al, 2003;van Dongen et al, 2004) and lipid biosynthesis in developing seeds of different species (Vigeolas et al, 2003;Rolletschek et al, 2005Rolletschek et al, , 2007. Moreover, external conditions, such as light, can have a considerable impact on oil accumulation in seeds by affecting energy and redox parameters (Ruuska et al, 2004;Goffman et al, 2005;Li et al, 2006).…”

“…Seeds of various species have been found to develop in an internal environment with about 2% to 4% (v/v) oxygen, compared with 21% (v/v) oxygen outside (Porterfield et al, 1999;Gibon et al, 2002;Rolletschek et al, 2002Rolletschek et al, , 2005Rolletschek et al, , 2007Geigenberger, 2003;Vigeolas et al, 2003, van Dongen et al, 2004. The positive effect of AHb2 on the energy state of the seeds, therefore, may be attributable to a specific role of AHb2 related to the low internal oxygen concentrations within the seeds.…”

The K+ battery-regulating Arabidopsis K+ channel AKT2 is under the control of multiple post-translational steps

“…31 As a consequence, phloem transport is very susceptible to decreasing oxygen supply to the plant. 29,32 It is therefore comprehensible that the above mentioned support by the K + driving force for sucrose retrieval is especially relevant in the phloem. Indeed Gajdanowicz et al 25 showed that transgenic plants lacking the AKT2 K + channel were severely impaired in growth when exposed to mild hypoxia (10% v:v), whereas growth of wild-type plants was unaffected by this treatment.…”