title: 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.
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom. i.finkemeier@lmu.de
authors.forename: Iris
authors.initials: I
authors.lastname: Finkemeier
authors.forename: Ann-Christine
authors.initials: AC
authors.lastname: König
authors.forename: William
authors.initials: W
authors.lastname: Heard
authors.forename: Adriano
authors.initials: A
authors.lastname: Nunes-Nesi
authors.forename: Phuong Anh
authors.initials: PA
authors.lastname: Pham
authors.forename: Dario
authors.initials: D
authors.lastname: Leister
authors.forename: Alisdair R
authors.initials: AR
authors.lastname: Fernie
authors.forename: Lee J
authors.initials: LJ
authors.lastname: Sweetlove
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000502:physiology; D029681:Arabidopsis Proteins / Q000235:genetics; D002264:Carboxylic Acids / Q000378:metabolism*; D002473:Cell Wall / Q000378:metabolism; D019343:Citric Acid / Q000378:metabolism / Q000494:pharmacology; D003517:Cyclopentanes / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D005875:Gibberellins / Q000378:metabolism; D008293:Malates / Q000378:metabolism / Q000494:pharmacology; D020411:Oligonucleotide Array Sequence Analysis; D054883:Oxylipins / Q000378:metabolism; D010788:Photosynthesis; D010937:Plant Growth Regulators / Q000378:metabolism*; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics; D018749:RNA, Plant / Q000235:genetics; D015398:Signal Transduction; D013312:Stress, Physiological; D013997:Time Factors; D059467:Transcriptome
chemical_list: D029681:Arabidopsis Proteins; D002264:Carboxylic Acids; D003517:Cyclopentanes; D005875:Gibberellins; D008293:Malates; D054883:Oxylipins; D010937:Plant Growth Regulators; D012333:RNA, Messenger; D018749:RNA, Plant; D019343:Citric Acid; C011006:jasmonic acid; C030298:malic acid