ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses

verfasst von: Kathleen Weigelt, Helge Küster, Twan Rutten, Aaron Fait, Alisdair R. Fernie, Otto Miersch, Claus Wasternack, R. J.Neil Emery, Christine Desel, Felicia Hosein, Martin Müller, Isolde Saalbach, Hans Weber
Abstract: 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.
Externe Organisation(en): Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK)
Universität Bielefeld
Max-Planck-Institut für molekulare Pflanzenphysiologie
Leibniz-Institut für Pflanzenbiochemie, Halle (IPB)
Trent University
Christian-Albrechts-Universität zu Kiel (CAU)
Typ: Artikel
Journal: Plant physiology
Band: 149
Seiten: 395-411
Anzahl der Seiten: 17
ISSN: 0032-0889
Publikationsdatum: 01.01.2009
Publikationsstatus: Veröffentlicht
Peer-reviewed: Ja
ASJC Scopus Sachgebiete: Physiologie, Genetik, Pflanzenkunde
Elektronische Version(en): https://doi.org/10.1104/pp.108.129940 (Zugang: Offen)

BibTeX

@article{9fef7587d9244d29815d29c90e3484ff,
title = "ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses",
abstract = "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.",
author = "Kathleen Weigelt and Helge K{\"u}ster and Twan Rutten and Aaron Fait and Fernie, {Alisdair R.} and Otto Miersch and Claus Wasternack and Emery, {R. J.Neil} and Christine Desel and Felicia Hosein and Martin M{\"u}ller and Isolde Saalbach and Hans Weber",
year = "2009",
month = jan,
day = "1",
doi = "10.1104/pp.108.129940",
language = "English",
volume = "149",
pages = "395--411",
journal = "Plant physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "1",
}