Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis

Aspartate transcarbamoylase (<i>ATC</i>) catalyzes the first committed step in pyrimidine de novo synthesis. As shown before, mutants with 80% reduced transcript and protein levels exhibit reduced levels of pyrimidine metabolites and thus nucleotide limitation and imbalance. Consequently...

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Main Authors: Leo Bellin, Diana Laura Garza Amaya, Vanessa Scherer, Tobias Pruß, Annalisa John, Andreas Richter, Torsten Möhlmann
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Molecules
Subjects:
Online Access:https://www.mdpi.com/1420-3049/28/4/1585
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author Leo Bellin
Diana Laura Garza Amaya
Vanessa Scherer
Tobias Pruß
Annalisa John
Andreas Richter
Torsten Möhlmann
author_facet Leo Bellin
Diana Laura Garza Amaya
Vanessa Scherer
Tobias Pruß
Annalisa John
Andreas Richter
Torsten Möhlmann
author_sort Leo Bellin
collection DOAJ
description Aspartate transcarbamoylase (<i>ATC</i>) catalyzes the first committed step in pyrimidine de novo synthesis. As shown before, mutants with 80% reduced transcript and protein levels exhibit reduced levels of pyrimidine metabolites and thus nucleotide limitation and imbalance. Consequently, reduced photosynthetic capacity and growth, accompanied by massive transcriptional changes, were observed. Here, we show that nucleotide de novo synthesis was upregulated during cold acclimation of <i>Arabidopsis thaliana</i> (ecotype Columbia, Col-0) plants, but <i>ATC</i> knockdown mutants failed to acclimate to this condition as they did not accumulate neutral sugars and anthocyanins. A global transcriptome analysis revealed that most of the transcriptional changes observed in Col-0 plants upon cold exposure were also evident in <i>ATC</i> knockdown plants. However, several responses observed in cold-treated Col-0 plants could already be detected in knockdown plants when grown under standard conditions, suggesting that these mutants exhibited typical cold responses without prior cold stimulation. We believe that nucleotide signaling is involved in “cold-like priming” and “cold acclimation” in general. The observed transcript levels of genes involved in central carbon metabolism and respiration were an exception to these findings. These were upregulated in the cold but downregulated in warm-grown <i>ATC</i> mutants.
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spelling doaj.art-0c12a7f191674691a9a14a101bb0ac782023-11-16T22:20:30ZengMDPI AGMolecules1420-30492023-02-01284158510.3390/molecules28041585Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in ArabidopsisLeo Bellin0Diana Laura Garza Amaya1Vanessa Scherer2Tobias Pruß3Annalisa John4Andreas Richter5Torsten Möhlmann6Faculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyFaculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyFaculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyFaculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyFaculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyInstitute for Biosciences, Physiology of Plant Metabolism, University of Rostock, Albert-Einstein-Strasse 3, D-18059 Rostock, GermanyFaculty of Biology, Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Straße, D-67663 Kaiserslautern, GermanyAspartate transcarbamoylase (<i>ATC</i>) catalyzes the first committed step in pyrimidine de novo synthesis. As shown before, mutants with 80% reduced transcript and protein levels exhibit reduced levels of pyrimidine metabolites and thus nucleotide limitation and imbalance. Consequently, reduced photosynthetic capacity and growth, accompanied by massive transcriptional changes, were observed. Here, we show that nucleotide de novo synthesis was upregulated during cold acclimation of <i>Arabidopsis thaliana</i> (ecotype Columbia, Col-0) plants, but <i>ATC</i> knockdown mutants failed to acclimate to this condition as they did not accumulate neutral sugars and anthocyanins. A global transcriptome analysis revealed that most of the transcriptional changes observed in Col-0 plants upon cold exposure were also evident in <i>ATC</i> knockdown plants. However, several responses observed in cold-treated Col-0 plants could already be detected in knockdown plants when grown under standard conditions, suggesting that these mutants exhibited typical cold responses without prior cold stimulation. We believe that nucleotide signaling is involved in “cold-like priming” and “cold acclimation” in general. The observed transcript levels of genes involved in central carbon metabolism and respiration were an exception to these findings. These were upregulated in the cold but downregulated in warm-grown <i>ATC</i> mutants.https://www.mdpi.com/1420-3049/28/4/1585pyrimidine de novo synthesiscold acclimationtranscriptomics
spellingShingle Leo Bellin
Diana Laura Garza Amaya
Vanessa Scherer
Tobias Pruß
Annalisa John
Andreas Richter
Torsten Möhlmann
Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
Molecules
pyrimidine de novo synthesis
cold acclimation
transcriptomics
title Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
title_full Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
title_fullStr Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
title_full_unstemmed Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
title_short Nucleotide Imbalance, Provoked by Downregulation of Aspartate Transcarbamoylase Impairs Cold Acclimation in Arabidopsis
title_sort nucleotide imbalance provoked by downregulation of aspartate transcarbamoylase impairs cold acclimation in arabidopsis
topic pyrimidine de novo synthesis
cold acclimation
transcriptomics
url https://www.mdpi.com/1420-3049/28/4/1585
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