Organ-specific analysis of the anaerobic primary metabolism in rice and wheat seedlings. I: Dark ethanol production is dominated by the shoots

Abstract

During anaerobiosis in darkness the main route for ATP production in plants is through glycolysis in combination with fermentation. We compared the organ-specific anaerobic fermentation of flooding-tolerant rice (Oryza sativa) and sensitive wheat (Triticum aestivum) seedlings. A sensitive laser-based photoacoustic trace gas detection system was used to monitor emission of ethanol and acetaldehyde by roots and shoots of intact seedlings. Dark-incubated rice seedlings released 3 times more acetaldehyde and 14 times more ethanol than wheat seedlings during anaerobiosis. Ninety percent of acetaldehyde originated from shoots of both species. In comparison to wheat shoots, the high ethanol production of rice shoots correlated with larger amounts of soluble carbohydrates, and higher activities of fermentative enzymes. After 24 h of anaerobiosis in darkness rice shoots still contained 30% of aerated ATP level, which enabled seedlings to survive this period. In contrast, ATP content declined almost to zero in wheat shoots and roots, which were irreversibly damaged after a 24-h anaerobic period. When plants were anaerobically and dark incubated for 4 h and subsequently transferred back to aeration, shoots showed a transient peak of acetaldehyde release indicating prompt re-oxidation of ethanol. Post-anoxic acetaldehyde production was lower in rice seedlings than in wheat. This observation accounts for a more effective acetaldehyde detoxification system in rice. Compared to wheat the greater tolerance of rice seedlings to transient anaerobic periods is explained by a faster fermentation rate of their shoots allowing a sufficient ATP production and an efficient suppression of toxic acetaldehyde formation in the early re-aeration period.

Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes

“…ADH and PDC activity increased considerably at 72 h of hypoxia up to 24 h post-hypoxia, followed by its respective metabolite, ethanol. Therefore, change in lactate fermentation to alcoholic fermentation represents an important indicator of the ability of a plant to survive hypoxia without extensive cell damage (Mustroph et al, 2006(Mustroph et al, , 2010.…”

A Shoot-Specific Hypoxic Response of Arabidopsis Sheds Light on the Role of the Phosphate-Responsive Transcription Factor PHOSPHATE STARVATION RESPONSE1

“…Plant material was ground in liquid nitrogen, and metabolites were extracted with perchloric acid as previously described (Mustroph et al, 2006a). The contents of Glc, Fru, Suc, starch, and adenylates were determined as in Mustroph et al (2006a) and phosphorylated metabolites as in Burrell et al, (1994).…”

“…The contents of Glc, Fru, Suc, starch, and adenylates were determined as in Mustroph et al (2006a) and phosphorylated metabolites as in Burrell et al, (1994). The content of Pi was determined as described by Itaya and Ui (1966).…”

“…First, ATP is a key metabolite, and its content can be compromised upon exposure to the two stresses. During oxygen deficiency, ATP becomes limiting due to a deficit in mitochondrial respiration (Mustroph et al, 2005(Mustroph et al, , 2006a(Mustroph et al, , 2006bBranco-Price et al, 2008). A lack of phosphate also limits ATP synthesis (Dancer et al, 1990;Rao and Terry, 1995;Morcuende et al, 2007).…”

Differential Anoxic Expression of Sugar-Regulated Genes Reveals Diverse Interactions between Sugar and Anaerobic Signaling Systems in Rice

“…Instead, fermentation-mediated sugar metabolism provides cellular energy, albeit with very low efficiency. The resultant change in basic energy metabolism causes cellular ATP levels drop to at least 30% of those under aerobic conditions (Greenway and Gibbs, 2003;Mustroph et al, 2006;Raymond et al, 1985). Rice is one of only a few plant species that survive the energetically unfavorable consequences of submergence.…”