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GUN1 regulates tetrapyrrole biosynthesis

GUN1 regulates tetrapyrrole biosynthesis
GUN1 regulates tetrapyrrole biosynthesis
The biogenesis of the photosynthetic apparatus in developing chloroplasts requires the assembly of proteins encoded on both nuclear and chloroplast genomes. To co-ordinate this process there needs to be communication between these organelles, and while we have a good understanding of how the nucleus controls chloroplast development, how the chloroplast communicates with the nucleus at this time is still essentially unknown. What we do know comes from pioneering work in which a series of genomes uncoupled (gun) mutants were identified that show elevated nuclear gene expression after chloroplast damage. Of the six reported gun mutations, five are in tetrapyrrole biosynthesis proteins and this has led to the development of a model for chloroplast-to-nucleus retrograde signaling in which ferrochelatase 1 (FC1)-dependent heme synthesis generates a positive signal promoting expression of photosynthesis-related genes. However, the molecular consequences of the strongest of the gun mutants, gun1, is unknown, preventing the development of a unifying hypothesis for chloroplast-to-nucleus signaling. Here, we show that GUN1 directly binds to heme and other metal-porphyrins, affects flux through the tetrapyrrole biosynthesis pathway and can increase the chelatase activity of FC1. These results raise the possibility that the signaling role of GUN1 may be manifested through changes in tetrapyrrole metabolism and supports a role for tetrapyrroles as mediators of a single biogenic chloroplast-to-nucleus retrograde signaling pathway.
Shimizu, Takayuki
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Mochizuki, Nobuyoshi
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Nagatani, Akira
2ede4c8b-5e99-4631-b03f-f618fdd87489
Watanabe, Satoru
ff628cc8-7225-417a-b373-f83b28196be9
Shimada, Tomohiro
17b7b894-6b87-4d5c-afa4-c1adf41c2c0d
Tanaka, Kan
36fed6e3-8f69-4381-80a0-762c937f9724
Hayashi, Yuuki
5d9a26cf-c52b-4266-8a82-f7fc767d3c54
Arai, Munehito
b70cc7c4-a542-4c2f-9c9c-2013b8a7afb0
Kacprzak, Sylwia M.
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Leister, Dario
824d999f-c42a-45a2-b7e2-9856b1e892fc
Okamoto, Haruko
cea35380-7618-44c8-a268-47b0198cc7f9
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Masuda, Tatsuru
56f9f097-1b54-4421-8afa-12eb0dff85cd
Shimizu, Takayuki
a1eeef3c-0d38-498d-8b2a-8759f71d81e4
Mochizuki, Nobuyoshi
aec0a19b-6399-485e-bc34-0979182c1084
Nagatani, Akira
2ede4c8b-5e99-4631-b03f-f618fdd87489
Watanabe, Satoru
ff628cc8-7225-417a-b373-f83b28196be9
Shimada, Tomohiro
17b7b894-6b87-4d5c-afa4-c1adf41c2c0d
Tanaka, Kan
36fed6e3-8f69-4381-80a0-762c937f9724
Hayashi, Yuuki
5d9a26cf-c52b-4266-8a82-f7fc767d3c54
Arai, Munehito
b70cc7c4-a542-4c2f-9c9c-2013b8a7afb0
Kacprzak, Sylwia M.
61c4bbb8-06e1-499d-89ee-290992e42a4e
Leister, Dario
824d999f-c42a-45a2-b7e2-9856b1e892fc
Okamoto, Haruko
cea35380-7618-44c8-a268-47b0198cc7f9
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Masuda, Tatsuru
56f9f097-1b54-4421-8afa-12eb0dff85cd

Shimizu, Takayuki, Mochizuki, Nobuyoshi, Nagatani, Akira, Watanabe, Satoru, Shimada, Tomohiro, Tanaka, Kan, Hayashi, Yuuki, Arai, Munehito, Kacprzak, Sylwia M., Leister, Dario, Okamoto, Haruko, Terry, Matthew J. and Masuda, Tatsuru (2019) GUN1 regulates tetrapyrrole biosynthesis. bioRxiv. (doi:10.1101/532036).

Record type: Article

Abstract

The biogenesis of the photosynthetic apparatus in developing chloroplasts requires the assembly of proteins encoded on both nuclear and chloroplast genomes. To co-ordinate this process there needs to be communication between these organelles, and while we have a good understanding of how the nucleus controls chloroplast development, how the chloroplast communicates with the nucleus at this time is still essentially unknown. What we do know comes from pioneering work in which a series of genomes uncoupled (gun) mutants were identified that show elevated nuclear gene expression after chloroplast damage. Of the six reported gun mutations, five are in tetrapyrrole biosynthesis proteins and this has led to the development of a model for chloroplast-to-nucleus retrograde signaling in which ferrochelatase 1 (FC1)-dependent heme synthesis generates a positive signal promoting expression of photosynthesis-related genes. However, the molecular consequences of the strongest of the gun mutants, gun1, is unknown, preventing the development of a unifying hypothesis for chloroplast-to-nucleus signaling. Here, we show that GUN1 directly binds to heme and other metal-porphyrins, affects flux through the tetrapyrrole biosynthesis pathway and can increase the chelatase activity of FC1. These results raise the possibility that the signaling role of GUN1 may be manifested through changes in tetrapyrrole metabolism and supports a role for tetrapyrroles as mediators of a single biogenic chloroplast-to-nucleus retrograde signaling pathway.

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More information

Published date: 28 January 2019

Identifiers

Local EPrints ID: 429336
URI: http://eprints.soton.ac.uk/id/eprint/429336
PURE UUID: d55d4ad5-7860-4f8b-90e2-888304208b89
ORCID for Matthew J. Terry: ORCID iD orcid.org/0000-0001-5002-2708

Catalogue record

Date deposited: 26 Mar 2019 17:30
Last modified: 10 Nov 2021 02:49

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Contributors

Author: Takayuki Shimizu
Author: Nobuyoshi Mochizuki
Author: Akira Nagatani
Author: Satoru Watanabe
Author: Tomohiro Shimada
Author: Kan Tanaka
Author: Yuuki Hayashi
Author: Munehito Arai
Author: Sylwia M. Kacprzak
Author: Dario Leister
Author: Haruko Okamoto
Author: Tatsuru Masuda

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