Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves    

Abstract

The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Although some carboxylic acids have been implicated in the regulation of gene expression for select transcripts, it is unclear whether all carboxylic acids have the same effect, how many transcripts are affected, and how carboxylic acid signaling is integrated with other metabolite signals. In this study, we demonstrate that perturbations in cellular concentrations of citrate, and to a lesser extent malate, have a major impact on nucleus-encoded transcript abundance. Functional categories of transcripts that were targeted by both organic acids included photosynthesis, cell wall, biotic stress, and protein synthesis. Specific functional categories that were only regulated by citrate included tricarboxylic acid cycle, nitrogen metabolism, sulfur metabolism, and DNA synthesis. Further quantitative real-time polymerase chain reaction analysis of specific citrate-responsive transcripts demonstrated that the transcript response to citrate is time and concentration dependent and distinct from other organic acids and sugars. Feeding of isocitrate as well as the nonmetabolizable citrate analog tricarballylate revealed that the abundance of selected marker transcripts is responsive to citrate and not downstream metabolites. Interestingly, the transcriptome response to citrate feeding was most similar to those observed after biotic stress treatments and the gibberellin biosynthesis inhibitor paclobutrazol. Feeding of citrate to mutants with defects in plant hormone signaling pathways did not completely abolish the transcript response but hinted at a link with jasmonic acid and gibberellin signaling pathways. Our results suggest that changes in carboxylic acid abundances can be perceived and signaled in Arabidopsis (Arabidopsis thaliana) by as yet unknown signaling pathways.

Phosphorylation of Phosphoenolpyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi

“…Instead, our data for daily sucrose oscillations and KfPRR7, KfPRR37, KfTOC1-1, and KfGI transcript regulation support the proposal that the pathway of metabolic regulation suggested to integrate photosynthetic sugar metabolism with the clock in Arabidopsis plays a role in the partial loss of rhythmicity observed in this K. fedtschenkoi rPPCK1-3 line (Haydon et al, 2013). Alternatively, malate changes in the rPPCK1-3 line may influence the clock, as malate has been demonstrated to function to influence gene regulation (Finkemeier et al, 2013).…”

Mitochondrial and Chloroplast Stress Responses Are Modulated in Distinct Touch and Chemical Inhibition Phases

“…A metabolite analysis revealed that DIC substrates such as succinate and citrate are significantly reduced within 10 min of spray treatment, indicating that such rapid transcriptional responses occur to address a physiological change. Citrate is also known to trigger specific transcriptional response, but the target genes appear not to overlap with our findings, and the timeframe of 8 h used in these experiments is different (Finkemeier et al, 2013).…”

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

“…Indeed, addition of citrate led to AOX induction in soybean and tobacco (Vanlerberghe and McLntosh, 1996;Djajanegara et al, 2002;Gray et al, 2004). In Arabidopsis, induction of AOX1a by citrate treatments could not be confirmed, and the changes observed were either modest or absent (Ho et al, 2008;Finkemeier et al, 2013). Overall, the transcriptomic effects of externally supplied citrate in Arabidopsis are mild compared to those observed in tobacco and soybean (Djajanegara et al, 2002;Gray et al, 2004).…”