Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling

The formation of 5-aminolevulinic acid (ALA) in tetrapyrrole biosynthesis is widely controlled by environmental and metabolic feedback cues that determine the influx into the entire metabolic path. Because of its central role as the rate-limiting step, we hypothesised a potential role of ALA biosynt...

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Main Authors: Olaf eCzarnecki, Christine eGläßer, Jin-Gui eChen, Klaus F. X. Mayer, Bernhard eGrimm
Format: Article
Language:English
Published: Frontiers Media S.A. 2012-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00236/full
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spelling doaj-6edec5cf04664358b49d8be013a897802020-11-25T00:36:57ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2012-10-01310.3389/fpls.2012.0023634201Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus SignallingOlaf eCzarnecki0Olaf eCzarnecki1Christine eGläßer2Jin-Gui eChen3Klaus F. X. Mayer4Bernhard eGrimm5Humboldt University BerlinOak Ridge National LaboratoryHelmholtz Zentrum MünchenOak Ridge National LaboratoryHelmholtz Zentrum MünchenHumboldt University BerlinThe formation of 5-aminolevulinic acid (ALA) in tetrapyrrole biosynthesis is widely controlled by environmental and metabolic feedback cues that determine the influx into the entire metabolic path. Because of its central role as the rate-limiting step, we hypothesised a potential role of ALA biosynthesis in tetrapyrrole-mediated retrograde signalling and exploited the direct impact of ALA biosynthesis on nuclear gene expression (NGE) by using two different approaches. Firstly, the Arabidopsis gun1, hy1 (gun2), hy2 (gun3), gun4 mutants showing uncoupled NGE from the physiological state of chloroplasts were thoroughly examined for regulatory modifications of ALA synthesis and transcriptional control in the nucleus. We found that reduced ALA-synthesising capacity is common to analysed gun mutants. Inhibition of ALA synthesis by gabaculine (GAB) that inactivates glutamate-1-semialdhyde aminotransferase and ALA feeding of wild-type and mutant seedlings corroborate the expression data of gun mutants. Transcript level of photosynthetic marker genes were enhanced in norflurazon (NF)-treated seedlings upon additional GAB treatment, while enhanced ALA amounts diminish these RNA levels in NF-treated wild-type in comparison to the solely NF-treated seedlings. Secondly, the impact of posttranslationally down-regulated ALA synthesis on NGE was investigated by global transcriptome analysis of GAB-treated Arabidopsis seedlings and the gun4-1 mutant, which is also characterized by reduced ALA formation. A common set of significantly modulated genes was identified indicating ALA synthesis as a potential signal emitter. The overrepresented gene ontology categories of genes with decreased or increased transcript abundance highlight a few biological processes and cellular functions, which are remarkably affected in response to plastid-localised ALA biosynthesis. These results support the hypothesis that ALA biosynthesis correlates with retrograde signalling-mediated control of NGE.http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00236/fullMicroarray Analysisretrograde signallingALA synthesisgabaculinegun mutants
collection DOAJ
language English
format Article
sources DOAJ
author Olaf eCzarnecki
Olaf eCzarnecki
Christine eGläßer
Jin-Gui eChen
Klaus F. X. Mayer
Bernhard eGrimm
spellingShingle Olaf eCzarnecki
Olaf eCzarnecki
Christine eGläßer
Jin-Gui eChen
Klaus F. X. Mayer
Bernhard eGrimm
Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
Frontiers in Plant Science
Microarray Analysis
retrograde signalling
ALA synthesis
gabaculine
gun mutants
author_facet Olaf eCzarnecki
Olaf eCzarnecki
Christine eGläßer
Jin-Gui eChen
Klaus F. X. Mayer
Bernhard eGrimm
author_sort Olaf eCzarnecki
title Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
title_short Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
title_full Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
title_fullStr Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
title_full_unstemmed Evidence for a Contribution of ALA Synthesis to Plastid-To-Nucleus Signalling
title_sort evidence for a contribution of ala synthesis to plastid-to-nucleus signalling
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2012-10-01
description The formation of 5-aminolevulinic acid (ALA) in tetrapyrrole biosynthesis is widely controlled by environmental and metabolic feedback cues that determine the influx into the entire metabolic path. Because of its central role as the rate-limiting step, we hypothesised a potential role of ALA biosynthesis in tetrapyrrole-mediated retrograde signalling and exploited the direct impact of ALA biosynthesis on nuclear gene expression (NGE) by using two different approaches. Firstly, the Arabidopsis gun1, hy1 (gun2), hy2 (gun3), gun4 mutants showing uncoupled NGE from the physiological state of chloroplasts were thoroughly examined for regulatory modifications of ALA synthesis and transcriptional control in the nucleus. We found that reduced ALA-synthesising capacity is common to analysed gun mutants. Inhibition of ALA synthesis by gabaculine (GAB) that inactivates glutamate-1-semialdhyde aminotransferase and ALA feeding of wild-type and mutant seedlings corroborate the expression data of gun mutants. Transcript level of photosynthetic marker genes were enhanced in norflurazon (NF)-treated seedlings upon additional GAB treatment, while enhanced ALA amounts diminish these RNA levels in NF-treated wild-type in comparison to the solely NF-treated seedlings. Secondly, the impact of posttranslationally down-regulated ALA synthesis on NGE was investigated by global transcriptome analysis of GAB-treated Arabidopsis seedlings and the gun4-1 mutant, which is also characterized by reduced ALA formation. A common set of significantly modulated genes was identified indicating ALA synthesis as a potential signal emitter. The overrepresented gene ontology categories of genes with decreased or increased transcript abundance highlight a few biological processes and cellular functions, which are remarkably affected in response to plastid-localised ALA biosynthesis. These results support the hypothesis that ALA biosynthesis correlates with retrograde signalling-mediated control of NGE.
topic Microarray Analysis
retrograde signalling
ALA synthesis
gabaculine
gun mutants
url http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00236/full
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