Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Björn Grübler
  • Livia Merendino
  • Sven O Twardziok
  • Morgane Mininno
  • Guillaume Allorent
  • Fabien Chevalier
  • Monique Liebers
  • Robert Blanvillain
  • Klaus F X Mayer
  • Silva Lerbs-Mache
  • Stéphane Ravanel
  • Thomas Pfannschmidt

External Research Organisations

  • Interdisciplinary Research Institute of Grenoble (IRIG)
  • École supérieure de physique et de chimie industrielles de la ville de Paris (ESPCI)
  • BIOGER INRA Institute
  • University Grenoble-Alpes (UGA)
  • Helmholtz Zentrum München - German Research Center for Environmental Health
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Details

Original languageEnglish
Pages (from-to)1203-1219
Number of pages17
JournalPlant physiology
Volume175
Issue number3
Publication statusPublished - Nov 2017
Externally publishedYes

Abstract

Plants possessing dysfunctional plastids due to defects in pigment biosynthesis or translation are known to repress photosynthesis-associated nuclear genes via retrograde signals from the disturbed organelles toward the nucleus. These signals are thought to be essential for proper biogenesis and function of the plastid. Mutants lacking plastid-encoded RNA polymerase-associated proteins (PAPs) display a genetic arrest in eoplast-chloroplast transition leading to an albino phenotype in the light. Retrograde signaling in these mutants, therefore, could be expected to be similar as under conditions inducing plastid dysfunction. To answer this question, we performed plastome- and genomewide array analyses in the pap7-1 mutant of Arabidopsis (Arabidopsis thaliana). In parallel, we determined the potential overlap with light-regulated expression networks. To this end, we performed a comparative expression profiling approach using light- and dark-grown wild-type plants as relative control for the expression profiles obtained from light-grown pap7-1 mutants. Our data indicate a specific impact of retrograde signals on metabolism-related genes in pap7-1 mutants reflecting the starvation situation of the albino seedlings. In contrast, light regulation of PhANGs and other nuclear gene groups appears to be fully functional in this mutant, indicating that a block in chloroplast biogenesis per se does not repress expression of them as suggested by earlier studies. Only genes for light harvesting complex proteins displayed a significant repression indicating an exclusive retrograde impact on this gene family. Our results indicate that chloroplasts and arrested plastids each emit specific signals that control different target gene modules both in positive and negative manner.

Keywords

    Arabidopsis/genetics, Arabidopsis Proteins/genetics, Chloroplast Proteins/genetics, Cluster Analysis, Gene Expression Profiling, Gene Expression Regulation, Plant/radiation effects, Gene Ontology, Gene Regulatory Networks, Genes, Plant, Light, Methyltransferases/genetics, Models, Biological, Morphogenesis/radiation effects, Mutation/genetics, Photosynthesis/genetics, Plastids/metabolism, RNA, Messenger/genetics, Signal Transduction/radiation effects

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Genetics
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physiology
  • Agricultural and Biological Sciences(all)
  • Plant Science

Cite this

Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1. / Grübler, Björn; Merendino, Livia; Twardziok, Sven O et al.
In: Plant physiology, Vol. 175, No. 3, 11.2017, p. 1203-1219.

Research output: Contribution to journalArticleResearchpeer review

Grübler, B, Merendino, L, Twardziok, SO, Mininno, M, Allorent, G, Chevalier, F, Liebers, M, Blanvillain, R, Mayer, KFX, Lerbs-Mache, S, Ravanel, S & Pfannschmidt, T 2017, 'Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1', Plant physiology, vol. 175, no. 3, pp. 1203-1219. https://doi.org/10.1104/pp.17.00982
Grübler, B., Merendino, L., Twardziok, S. O., Mininno, M., Allorent, G., Chevalier, F., Liebers, M., Blanvillain, R., Mayer, K. F. X., Lerbs-Mache, S., Ravanel, S., & Pfannschmidt, T. (2017). Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1. Plant physiology, 175(3), 1203-1219. https://doi.org/10.1104/pp.17.00982
Grübler B, Merendino L, Twardziok SO, Mininno M, Allorent G, Chevalier F et al. Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1. Plant physiology. 2017 Nov;175(3):1203-1219. doi: 10.1104/pp.17.00982
Grübler, Björn ; Merendino, Livia ; Twardziok, Sven O et al. / Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1. In: Plant physiology. 2017 ; Vol. 175, No. 3. pp. 1203-1219.
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title = "Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1",
abstract = "Plants possessing dysfunctional plastids due to defects in pigment biosynthesis or translation are known to repress photosynthesis-associated nuclear genes via retrograde signals from the disturbed organelles toward the nucleus. These signals are thought to be essential for proper biogenesis and function of the plastid. Mutants lacking plastid-encoded RNA polymerase-associated proteins (PAPs) display a genetic arrest in eoplast-chloroplast transition leading to an albino phenotype in the light. Retrograde signaling in these mutants, therefore, could be expected to be similar as under conditions inducing plastid dysfunction. To answer this question, we performed plastome- and genomewide array analyses in the pap7-1 mutant of Arabidopsis (Arabidopsis thaliana). In parallel, we determined the potential overlap with light-regulated expression networks. To this end, we performed a comparative expression profiling approach using light- and dark-grown wild-type plants as relative control for the expression profiles obtained from light-grown pap7-1 mutants. Our data indicate a specific impact of retrograde signals on metabolism-related genes in pap7-1 mutants reflecting the starvation situation of the albino seedlings. In contrast, light regulation of PhANGs and other nuclear gene groups appears to be fully functional in this mutant, indicating that a block in chloroplast biogenesis per se does not repress expression of them as suggested by earlier studies. Only genes for light harvesting complex proteins displayed a significant repression indicating an exclusive retrograde impact on this gene family. Our results indicate that chloroplasts and arrested plastids each emit specific signals that control different target gene modules both in positive and negative manner.",
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TY - JOUR

T1 - Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1

AU - Grübler, Björn

AU - Merendino, Livia

AU - Twardziok, Sven O

AU - Mininno, Morgane

AU - Allorent, Guillaume

AU - Chevalier, Fabien

AU - Liebers, Monique

AU - Blanvillain, Robert

AU - Mayer, Klaus F X

AU - Lerbs-Mache, Silva

AU - Ravanel, Stéphane

AU - Pfannschmidt, Thomas

N1 - Funding information: 1This work was supported by grants from the Deutsche For-schungsgemeinschaft (DFG) to T.P. (PF323-5-2) and the Deutsche Forschungsgemeinschaft (DFG) research group FOR 804. The study also received institutional support from the French National Research Agency (ANR-10-LABEX-04 GRAL Labex, Grenoble Alliance for Integrated Structural Cell Biology).

PY - 2017/11

Y1 - 2017/11

N2 - Plants possessing dysfunctional plastids due to defects in pigment biosynthesis or translation are known to repress photosynthesis-associated nuclear genes via retrograde signals from the disturbed organelles toward the nucleus. These signals are thought to be essential for proper biogenesis and function of the plastid. Mutants lacking plastid-encoded RNA polymerase-associated proteins (PAPs) display a genetic arrest in eoplast-chloroplast transition leading to an albino phenotype in the light. Retrograde signaling in these mutants, therefore, could be expected to be similar as under conditions inducing plastid dysfunction. To answer this question, we performed plastome- and genomewide array analyses in the pap7-1 mutant of Arabidopsis (Arabidopsis thaliana). In parallel, we determined the potential overlap with light-regulated expression networks. To this end, we performed a comparative expression profiling approach using light- and dark-grown wild-type plants as relative control for the expression profiles obtained from light-grown pap7-1 mutants. Our data indicate a specific impact of retrograde signals on metabolism-related genes in pap7-1 mutants reflecting the starvation situation of the albino seedlings. In contrast, light regulation of PhANGs and other nuclear gene groups appears to be fully functional in this mutant, indicating that a block in chloroplast biogenesis per se does not repress expression of them as suggested by earlier studies. Only genes for light harvesting complex proteins displayed a significant repression indicating an exclusive retrograde impact on this gene family. Our results indicate that chloroplasts and arrested plastids each emit specific signals that control different target gene modules both in positive and negative manner.

AB - Plants possessing dysfunctional plastids due to defects in pigment biosynthesis or translation are known to repress photosynthesis-associated nuclear genes via retrograde signals from the disturbed organelles toward the nucleus. These signals are thought to be essential for proper biogenesis and function of the plastid. Mutants lacking plastid-encoded RNA polymerase-associated proteins (PAPs) display a genetic arrest in eoplast-chloroplast transition leading to an albino phenotype in the light. Retrograde signaling in these mutants, therefore, could be expected to be similar as under conditions inducing plastid dysfunction. To answer this question, we performed plastome- and genomewide array analyses in the pap7-1 mutant of Arabidopsis (Arabidopsis thaliana). In parallel, we determined the potential overlap with light-regulated expression networks. To this end, we performed a comparative expression profiling approach using light- and dark-grown wild-type plants as relative control for the expression profiles obtained from light-grown pap7-1 mutants. Our data indicate a specific impact of retrograde signals on metabolism-related genes in pap7-1 mutants reflecting the starvation situation of the albino seedlings. In contrast, light regulation of PhANGs and other nuclear gene groups appears to be fully functional in this mutant, indicating that a block in chloroplast biogenesis per se does not repress expression of them as suggested by earlier studies. Only genes for light harvesting complex proteins displayed a significant repression indicating an exclusive retrograde impact on this gene family. Our results indicate that chloroplasts and arrested plastids each emit specific signals that control different target gene modules both in positive and negative manner.

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KW - Gene Ontology

KW - Gene Regulatory Networks

KW - Genes, Plant

KW - Light

KW - Methyltransferases/genetics

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KW - Morphogenesis/radiation effects

KW - Mutation/genetics

KW - Photosynthesis/genetics

KW - Plastids/metabolism

KW - RNA, Messenger/genetics

KW - Signal Transduction/radiation effects

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