Abstract
Investigation of the metabolome and the transcriptome of pollen of lily (Lilium longiflorum) gave a comprehensive overview of metabolic pathways active during pollen germination and tube growth. More than 100 different metabolites were determined simultaneously by gas chromatography coupled to mass spectrometry, and expressed genes of selected metabolic pathways were identified by next-generation sequencing of lily pollen transcripts. The time-dependent changes in metabolite abundances, as well as the changes after inhibition of the mitochondrial electron transport chain, revealed a fast and dynamic adaption of the metabolic pathways in the range of minutes. The metabolic state prior to pollen germination differed clearly from the metabolic state during pollen tube growth, as indicated by principal component analysis of all detected metabolites and by detailed observation of individual metabolites. For instance, the amount of sucrose increased during the first 60 minutes of pollen culture but decreased during tube growth, while glucose and fructose showed the opposite behavior. Glycolysis, tricarbonic acid cycle, glyoxylate cycle, starch, and fatty acid degradation were activated, providing energy during pollen germination and tube growth. Inhibition of the mitochondrial electron transport chain by antimycin A resulted in an immediate production of ethanol and a fast rearrangement of metabolic pathways, which correlated with changes in the amounts of the majority of identified metabolites, e.g. a rapid increase in γ-aminobutyric acid indicated the activation of a γ-aminobutyric acid shunt in the tricarbonic acid cycle, while ethanol fermentation compensated the reduced ATP production after inhibition of the oxidative phosphorylation.
Highlights
Investigation of the metabolome and the transcriptome of pollen of lily (Lilium longiflorum) gave a comprehensive overview of metabolic pathways active during pollen germination and tube growth
A significant decrease in the mean tube length was observed in the presence of 20 mM antimycin A, an inhibitor of complex III of the mitochondrial electron transport chain, whereas the germination frequency was not affected, confirming previous studies (Rounds et al, 2010)
The results of the principal component analysis (Fig. 9; Supplemental Fig. S8A) support the idea that pollen metabolism changes at the transition from germination to tube growth, which can be observed in the time dependence of metabolite abundances
Summary
Investigation of the metabolome and the transcriptome of pollen of lily (Lilium longiflorum) gave a comprehensive overview of metabolic pathways active during pollen germination and tube growth. Inhibition of the mitochondrial electron transport chain by antimycin A resulted in an immediate production of ethanol and a fast rearrangement of metabolic pathways, which correlated with changes in the amounts of the majority of identified metabolites, e.g. a rapid increase in g-aminobutyric acid indicated the activation of a g-aminobutyric acid shunt in the tricarbonic acid cycle, while ethanol fermentation compensated the reduced ATP production after inhibition of the oxidative phosphorylation. Kuhlemeier and coworkers identified the pyruvate dehydrogenase bypass by which pollen grains produce ethanol to support the tricarbonic acid (TCA) cycle and lipid biosynthesis (Tadege et al, 1999; Mellema et al, 2002; Gass et al, 2005) This aerobic fermentation can be induced by blocking aerobic respiration with inhibitors of the electron transport chain (antimycin A, potassium cyanide) or the mitochondrial F-type ATPase (Rounds et al, 2010). Detailed studies may reveal that at least parts of the pollen metabolism might be different due to its specific physiological role as suggested by Colaço et al (2012)
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