Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle

Research output: Contribution to journalReview articleResearchpeer review

Authors

  • Thomas Pfannschmidt
  • Robert Blanvillain
  • Livia Merendino
  • Florence Courtois
  • Fabien Chevalier
  • Monique Liebers
  • Björn Grübler
  • Elisabeth Hommel
  • Silva Lerbs-Mache

External Research Organisations

  • University Grenoble-Alpes (UGA)
  • Centre national de la recherche scientifique (CNRS)
  • French Alternative Energies and Atomic Energy Commission (CEA)
  • Institut de recherche en technologies et sciences pour le vivant (iRTSV)
  • Laboratoire Physiologie Cellulaire & Végétale
  • Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE)
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Details

Original languageEnglish
Pages (from-to)6957-73
Number of pages17
JournalJournal of experimental botany
Volume66
Issue number22
Publication statusPublished - Dec 2015
Externally publishedYes

Abstract

Chloroplasts are the sunlight-collecting organelles of photosynthetic eukaryotes that energetically drive the biosphere of our planet. They are the base for all major food webs by providing essential photosynthates to all heterotrophic organisms including humans. Recent research has focused largely on an understanding of the function of these organelles, but knowledge about the biogenesis of chloroplasts is rather limited. It is known that chloroplasts develop from undifferentiated precursor plastids, the proplastids, in meristematic cells. This review focuses on the activation and action of plastid RNA polymerases, which play a key role in the development of new chloroplasts from proplastids. Evolutionarily, plastids emerged from the endosymbiosis of a cyanobacterium-like ancestor into a heterotrophic eukaryote. As an evolutionary remnant of this process, they possess their own genome, which is expressed by two types of plastid RNA polymerase, phage-type and prokaryotic-type RNA polymerase. The protein subunits of these polymerases are encoded in both the nuclear and plastid genomes. Their activation and action therefore require a highly sophisticated regulation that controls and coordinates the expression of the components encoded in the plastid and nucleus. Stoichiometric expression and correct assembly of RNA polymerase complexes is achieved by a combination of developmental and environmentally induced programmes. This review highlights the current knowledge about the functional coordination between the different types of plastid RNA polymerases and provides working models of their sequential expression and function for future investigations.

Keywords

    Biological Evolution, Chloroplasts/metabolism, DNA-Directed RNA Polymerases/metabolism, Enzyme Activation, Life Cycle Stages, Plants/metabolism, RNA, Plant/metabolism

Cite this

Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. / Pfannschmidt, Thomas; Blanvillain, Robert; Merendino, Livia et al.
In: Journal of experimental botany, Vol. 66, No. 22, 12.2015, p. 6957-73.

Research output: Contribution to journalReview articleResearchpeer review

Pfannschmidt, T, Blanvillain, R, Merendino, L, Courtois, F, Chevalier, F, Liebers, M, Grübler, B, Hommel, E & Lerbs-Mache, S 2015, 'Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle', Journal of experimental botany, vol. 66, no. 22, pp. 6957-73. https://doi.org/10.1093/jxb/erv415
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abstract = "Chloroplasts are the sunlight-collecting organelles of photosynthetic eukaryotes that energetically drive the biosphere of our planet. They are the base for all major food webs by providing essential photosynthates to all heterotrophic organisms including humans. Recent research has focused largely on an understanding of the function of these organelles, but knowledge about the biogenesis of chloroplasts is rather limited. It is known that chloroplasts develop from undifferentiated precursor plastids, the proplastids, in meristematic cells. This review focuses on the activation and action of plastid RNA polymerases, which play a key role in the development of new chloroplasts from proplastids. Evolutionarily, plastids emerged from the endosymbiosis of a cyanobacterium-like ancestor into a heterotrophic eukaryote. As an evolutionary remnant of this process, they possess their own genome, which is expressed by two types of plastid RNA polymerase, phage-type and prokaryotic-type RNA polymerase. The protein subunits of these polymerases are encoded in both the nuclear and plastid genomes. Their activation and action therefore require a highly sophisticated regulation that controls and coordinates the expression of the components encoded in the plastid and nucleus. Stoichiometric expression and correct assembly of RNA polymerase complexes is achieved by a combination of developmental and environmentally induced programmes. This review highlights the current knowledge about the functional coordination between the different types of plastid RNA polymerases and provides working models of their sequential expression and function for future investigations.",
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Download

TY - JOUR

T1 - Plastid RNA polymerases

T2 - orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle

AU - Pfannschmidt, Thomas

AU - Blanvillain, Robert

AU - Merendino, Livia

AU - Courtois, Florence

AU - Chevalier, Fabien

AU - Liebers, Monique

AU - Grübler, Björn

AU - Hommel, Elisabeth

AU - Lerbs-Mache, Silva

N1 - © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.

PY - 2015/12

Y1 - 2015/12

N2 - Chloroplasts are the sunlight-collecting organelles of photosynthetic eukaryotes that energetically drive the biosphere of our planet. They are the base for all major food webs by providing essential photosynthates to all heterotrophic organisms including humans. Recent research has focused largely on an understanding of the function of these organelles, but knowledge about the biogenesis of chloroplasts is rather limited. It is known that chloroplasts develop from undifferentiated precursor plastids, the proplastids, in meristematic cells. This review focuses on the activation and action of plastid RNA polymerases, which play a key role in the development of new chloroplasts from proplastids. Evolutionarily, plastids emerged from the endosymbiosis of a cyanobacterium-like ancestor into a heterotrophic eukaryote. As an evolutionary remnant of this process, they possess their own genome, which is expressed by two types of plastid RNA polymerase, phage-type and prokaryotic-type RNA polymerase. The protein subunits of these polymerases are encoded in both the nuclear and plastid genomes. Their activation and action therefore require a highly sophisticated regulation that controls and coordinates the expression of the components encoded in the plastid and nucleus. Stoichiometric expression and correct assembly of RNA polymerase complexes is achieved by a combination of developmental and environmentally induced programmes. This review highlights the current knowledge about the functional coordination between the different types of plastid RNA polymerases and provides working models of their sequential expression and function for future investigations.

AB - Chloroplasts are the sunlight-collecting organelles of photosynthetic eukaryotes that energetically drive the biosphere of our planet. They are the base for all major food webs by providing essential photosynthates to all heterotrophic organisms including humans. Recent research has focused largely on an understanding of the function of these organelles, but knowledge about the biogenesis of chloroplasts is rather limited. It is known that chloroplasts develop from undifferentiated precursor plastids, the proplastids, in meristematic cells. This review focuses on the activation and action of plastid RNA polymerases, which play a key role in the development of new chloroplasts from proplastids. Evolutionarily, plastids emerged from the endosymbiosis of a cyanobacterium-like ancestor into a heterotrophic eukaryote. As an evolutionary remnant of this process, they possess their own genome, which is expressed by two types of plastid RNA polymerase, phage-type and prokaryotic-type RNA polymerase. The protein subunits of these polymerases are encoded in both the nuclear and plastid genomes. Their activation and action therefore require a highly sophisticated regulation that controls and coordinates the expression of the components encoded in the plastid and nucleus. Stoichiometric expression and correct assembly of RNA polymerase complexes is achieved by a combination of developmental and environmentally induced programmes. This review highlights the current knowledge about the functional coordination between the different types of plastid RNA polymerases and provides working models of their sequential expression and function for future investigations.

KW - Biological Evolution

KW - Chloroplasts/metabolism

KW - DNA-Directed RNA Polymerases/metabolism

KW - Enzyme Activation

KW - Life Cycle Stages

KW - Plants/metabolism

KW - RNA, Plant/metabolism

U2 - 10.1093/jxb/erv415

DO - 10.1093/jxb/erv415

M3 - Review article

C2 - 26355147

VL - 66

SP - 6957

EP - 6973

JO - Journal of experimental botany

JF - Journal of experimental botany

SN - 0022-0957

IS - 22

ER -

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