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BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES

ADP-Glucose Pyrophosphorylase-Deficient Pea Embryos Reveal Specific Transcriptional and Metabolic Changes of Carbon-Nitrogen Metabolism and Stress Responses^1,[W]

Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, D–06466 Gatersleben, Germany (K.W., T.R., F.H., M.M., I.S., H.W.); Institute for Genome Research and Systems Biology, Center for Biotechnology, Bielefeld University, D–33615 Bielefeld, Germany (H.K.); Max-Planck-Institut für Molekulare Pflanzenphysiologie, D–14476 Potsdam-Golm, Germany (A.F., A.R.F.); Leibniz-Institut für Pflanzenbiochemie, D–06120 Halle (Saale), Germany (O.M., C.W.); Biology Department, Trent University, Peterborough, Ontario, Canada K9J 7B8 (R.J.N.E.); and Christian Albrechts University of Kiel, Institute of Botany, D–24098 Kiel, Germany (C.D.)

We present a comprehensive analysis of ADP-glucose pyrophosphorylase (AGP)-repressed pea (Pisum sativum) seeds using transcript and metabolite profiling to monitor the effects that reduced carbon flow into starch has on carbon-nitrogen metabolism and related pathways. Changed patterns of transcripts and metabolites suggest that AGP repression causes sugar accumulation and stimulates carbohydrate oxidation via glycolysis, tricarboxylic acid cycle, and mitochondrial respiration. Enhanced provision of precursors such as acetyl-coenzyme A and organic acids apparently support other pathways and activate amino acid and storage protein biosynthesis as well as pathways fed by cytosolic acetyl-coenzyme A, such as cysteine biosynthesis and fatty acid elongation/metabolism. As a consequence, the resulting higher nitrogen (N) demand depletes transient N storage pools, specifically asparagine and arginine, and leads to N limitation. Moreover, increased sugar accumulation appears to stimulate cytokinin-mediated cell proliferation pathways. In addition, the deregulation of starch biosynthesis resulted in indirect changes, such as increased mitochondrial metabolism and osmotic stress. The combined effect of these changes is an enhanced generation of reactive oxygen species coupled with an up-regulation of energy-dissipating, reactive oxygen species protection, and defense genes. Transcriptional activation of mitogen-activated protein kinase pathways and oxylipin synthesis indicates an additional activation of stress signaling pathways. AGP-repressed embryos contain higher levels of jasmonate derivatives; however, this increase is preferentially in nonactive forms. The results suggest that, although metabolic/osmotic alterations in iAGP pea seeds result in multiple stress responses, pea seeds have effective mechanisms to circumvent stress signaling under conditions in which excessive stress responses and/or cellular damage could prematurely initiate senescence or apoptosis.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hans Weber (weber{at}ipk-gatersleben.de).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.129940

^* Corresponding author; e-mail weber{at}ipk-gatersleben.de.

Received September 16, 2008; accepted November 4, 2008; published November 5, 2008.

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