Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • Thomas Pfannschmidt
  • Matthew J Terry
  • Olivier Van Aken
  • Pedro M Quiros

Organisationseinheiten

Externe Organisationen

  • University of Southampton
  • Lund University Centre for Sustainability Studies (LUCSUS)
  • Wellcome Trust Sanger Institute
Forschungs-netzwerk anzeigen

Details

OriginalspracheEnglisch
Aufsatznummer20190396
FachzeitschriftPhilosophical Transactions of the Royal Society B: Biological Sciences
Jahrgang375
Ausgabenummer1801
Frühes Online-Datum4 Mai 2020
PublikationsstatusVeröffentlicht - 22 Juni 2020

Abstract

Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

Zitieren

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells. / Pfannschmidt, Thomas; Terry, Matthew J; Van Aken, Olivier et al.
in: Philosophical Transactions of the Royal Society B: Biological Sciences, Jahrgang 375, Nr. 1801, 20190396, 22.06.2020.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Pfannschmidt T, Terry MJ, Van Aken O, Quiros PM. Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells. Philosophical Transactions of the Royal Society B: Biological Sciences. 2020 Jun 22;375(1801):20190396. Epub 2020 Mai 4. doi: 10.1098/rstb.2019.0396
Download
@article{457ea15dc638431ba24dfcc16b1834c9,
title = "Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells",
abstract = "Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.",
keywords = "Eukaryotic Cells/metabolism, Organelles/metabolism, Signal Transduction, Symbiosis/physiology, Mitochondria, Chloroplasts, Metabolites, Intracellular communication, Signalling, Plastids",
author = "Thomas Pfannschmidt and Terry, {Matthew J} and {Van Aken}, Olivier and Quiros, {Pedro M}",
year = "2020",
month = jun,
day = "22",
doi = "10.1098/rstb.2019.0396",
language = "English",
volume = "375",
journal = "Philosophical Transactions of the Royal Society B: Biological Sciences",
issn = "0080-4622",
publisher = "The Royal Society",
number = "1801",

}

Download

TY - JOUR

T1 - Retrograde signals from endosymbiotic organelles

T2 - a common control principle in eukaryotic cells

AU - Pfannschmidt, Thomas

AU - Terry, Matthew J

AU - Van Aken, Olivier

AU - Quiros, Pedro M

PY - 2020/6/22

Y1 - 2020/6/22

N2 - Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

AB - Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

KW - Eukaryotic Cells/metabolism

KW - Organelles/metabolism

KW - Signal Transduction

KW - Symbiosis/physiology

KW - Mitochondria

KW - Chloroplasts

KW - Metabolites

KW - Intracellular communication

KW - Signalling

KW - Plastids

UR - http://www.scopus.com/inward/record.url?scp=85085078399&partnerID=8YFLogxK

U2 - 10.1098/rstb.2019.0396

DO - 10.1098/rstb.2019.0396

M3 - Article

C2 - 32362267

VL - 375

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0080-4622

IS - 1801

M1 - 20190396

ER -