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.
Highlights
The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status
To establish whether carboxylic acids have a general role in the regulation of transcript abundances, the influence of exogenously supplied malate and citrate on the Arabidopsis transcriptome was analyzed in leaf slices
Reverse transcriptase PCR analysis revealed that the AOX1a (At3g22370) transcript of Arabidopsis was increased to a peak level after an 8-h treatment with 1 mM citrate and malate (Fig. 1A)
Summary
The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Sheen and coworkers demonstrated that, in addition to its enzymatic role, hexokinase functions as a key enzyme in sugar signaling, acting as a direct metabolite sensor in plants that senses hexose concentrations in order to control sugar-regulated gene expression (Jang et al, 1997; Moore et al, 2003). Intracellular kinases, such as the evolutionarily conserved SUCROSE NONFERMENTING1-related kinases, regulate transcription under energy or nutrient deficiency to restore metabolic homeostasis. Iron citrate was shown to competitively inhibit the activities of protein Tyr phosphatases and thereby to enhance mitogen-activated protein kinase (MAPK) signaling (Gomez et al, 2010)
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