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Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype

Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype
Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype

Chloroplast development requires communication between the progenitor plastids and the nucleus, where most of the genes encoding chloroplast proteins reside. Retrograde signals from the chloroplast to the nucleus control the expression of many of these genes, but the signalling pathway is poorly understood. Tetrapyrroles have been strongly implicated as mediators of this signal with the current hypothesis being that haem produced by the activity of ferrochelatase 1 (FC1) is required to promote nuclear gene expression. We have tested this hypothesis by overexpressing FC1 and specifically targeting it to either chloroplasts or mitochondria, two possible locations for this enzyme. Our results show that targeting of FC1 to chloroplasts results in increased expression of the nuclear-encoded chloroplast genes GUN4, CA1, HEMA1, LHCB2.1, CHLH after treatment with Norflurazon (NF) and that this increase correlates to FC1 gene expression and haem production measured by feedback inhibition of protochlorophyllide synthesis. Targeting FC1 to mitochondria did not enhance the expression of nuclear-encoded chloroplast genes after NF treatment. The overexpression of FC1 also increased nuclear gene expression in the absence of NF treatment, demonstrating that this pathway is operational in the absence of a stress treatment. Our results therefore support the hypothesis that haem synthesis is a promotive chloroplast-to-nucleus retrograde signal. However, not all FC1 overexpression lines enhanced nuclear gene expression, suggesting there is still a lot we do not understand about the role of FC1 in this signalling pathway. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

Gun phenotype, Haem, Mitochondria, Plastid signalling, Tetrapyrroles
0962-8436
20190401
Page, Mike T.
c248f4b0-79ae-4ab3-a094-8713e947ec9d
Garcia-Becerra, Tania
3afa9c47-be57-4dc5-99ea-6b1e05d99d1f
Smith, Alison G.
2f820588-24d8-447e-add4-98d37b14c765
Terry, Matthew J
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Page, Mike T.
c248f4b0-79ae-4ab3-a094-8713e947ec9d
Garcia-Becerra, Tania
3afa9c47-be57-4dc5-99ea-6b1e05d99d1f
Smith, Alison G.
2f820588-24d8-447e-add4-98d37b14c765
Terry, Matthew J
a8c2cd6b-8d35-4053-8d77-3841c2427c3b

Page, Mike T., Garcia-Becerra, Tania, Smith, Alison G. and Terry, Matthew J (2020) Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 375 (1801), 20190401, [20190401]. (doi:10.1098/rstb.2019.0401).

Record type: Article

Abstract

Chloroplast development requires communication between the progenitor plastids and the nucleus, where most of the genes encoding chloroplast proteins reside. Retrograde signals from the chloroplast to the nucleus control the expression of many of these genes, but the signalling pathway is poorly understood. Tetrapyrroles have been strongly implicated as mediators of this signal with the current hypothesis being that haem produced by the activity of ferrochelatase 1 (FC1) is required to promote nuclear gene expression. We have tested this hypothesis by overexpressing FC1 and specifically targeting it to either chloroplasts or mitochondria, two possible locations for this enzyme. Our results show that targeting of FC1 to chloroplasts results in increased expression of the nuclear-encoded chloroplast genes GUN4, CA1, HEMA1, LHCB2.1, CHLH after treatment with Norflurazon (NF) and that this increase correlates to FC1 gene expression and haem production measured by feedback inhibition of protochlorophyllide synthesis. Targeting FC1 to mitochondria did not enhance the expression of nuclear-encoded chloroplast genes after NF treatment. The overexpression of FC1 also increased nuclear gene expression in the absence of NF treatment, demonstrating that this pathway is operational in the absence of a stress treatment. Our results therefore support the hypothesis that haem synthesis is a promotive chloroplast-to-nucleus retrograde signal. However, not all FC1 overexpression lines enhanced nuclear gene expression, suggesting there is still a lot we do not understand about the role of FC1 in this signalling pathway. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

Text
Page et al (2020) Phil Trans Roy Soc B - accepted version - Accepted Manuscript
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More information

Accepted/In Press date: 24 January 2020
e-pub ahead of print date: 4 May 2020
Published date: 22 June 2020
Keywords: Gun phenotype, Haem, Mitochondria, Plastid signalling, Tetrapyrroles

Identifiers

Local EPrints ID: 441025
URI: http://eprints.soton.ac.uk/id/eprint/441025
ISSN: 0962-8436
PURE UUID: 7d531639-6c8c-4b94-83e5-98557a33990a
ORCID for Matthew J Terry: ORCID iD orcid.org/0000-0001-5002-2708

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Date deposited: 27 May 2020 16:55
Last modified: 18 Feb 2021 16:46

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