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

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

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'.

Chloroplasts, Intracellular communication, Metabolites, Mitochondria, Plastids, Signalling
0962-8436
Pfannschmidt, Thomas
0ed646f6-14f3-424a-b315-0e0290d87dfe
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Van Aken, Olivier
f8df5f99-4082-4708-9b92-71a6b1be014b
Quiros, Pedro M.
69c77d36-5ead-4739-beaa-5fb5e245a982
Pfannschmidt, Thomas
0ed646f6-14f3-424a-b315-0e0290d87dfe
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Van Aken, Olivier
f8df5f99-4082-4708-9b92-71a6b1be014b
Quiros, Pedro M.
69c77d36-5ead-4739-beaa-5fb5e245a982

Pfannschmidt, Thomas, Terry, Matthew J., Van Aken, Olivier and Quiros, Pedro M. (2020) Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells. Philosophical Transactions of the Royal Society B: Biological Sciences, 375 (1801), [20190396]. (doi:10.1098/rstb.2019.0396).

Record type: Article

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'.

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Retrograde signals from endosymbiotic organelles - a common control principle in eukaryotic cells - accepted version - Accepted Manuscript
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Accepted/In Press date: 6 April 2020
e-pub ahead of print date: 4 May 2020
Published date: 22 June 2020
Keywords: Chloroplasts, Intracellular communication, Metabolites, Mitochondria, Plastids, Signalling

Identifiers

Local EPrints ID: 441221
URI: http://eprints.soton.ac.uk/id/eprint/441221
ISSN: 0962-8436
PURE UUID: 2fa3f55f-15f7-48ab-8f96-a949c3da3272
ORCID for Matthew J. Terry: ORCID iD orcid.org/0000-0001-5002-2708

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Date deposited: 05 Jun 2020 16:31
Last modified: 26 Nov 2021 02:38

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Contributors

Author: Thomas Pfannschmidt
Author: Olivier Van Aken
Author: Pedro M. Quiros

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