Title: Bilin-dependent regulation of chlorophyll biosynthesis by GUN4

Abstract

Biosyntheses of chlorophyll and heme in oxygenic phototrophs share a common trunk pathway that diverges with insertion of magnesium or iron into the last common intermediate, protoporphyrin IX. Since both tetrapyrroles are pro-oxidants, it is essential that their metabolism is tightly regulated. Here, we establish that heme-derived linear tetrapyrroles (bilins) function to stimulate the enzymatic activity of magnesium chelatase (MgCh) via their interaction with GENOMES UNCOUPLED 4 (GUN4) in the model green alga Chlamydomonas reinhardtii. A key tetrapyrrole-binding component of MgCh found in all oxygenic photosynthetic species, CrGUN4, also stabilizes the bilin-dependent accumulation of protoporphyrin IX-binding CrCHLH1 subunit of MgCh in light-grown C. reinhardtii cells by preventing its photooxidative inactivation. Exogenous application of biliverdin IXα reverses the loss of CrCHLH1 in the bilin-deficient heme oxygenase (hmox1) mutant, but not in the gun4 mutant. We propose that these dual regulatory roles of GUN4:bilin complexes are responsible for the retention of bilin biosynthesis in all photosynthetic eukaryotes, which sustains chlorophyll biosynthesis in an illuminated oxic environment.

Authors:

Zhang, Weiqing ^[1]; Willows, Robert D.  ^[2];

• Search DOE PAGES for author "Willows, Robert D."
• Search DOE PAGES for ORCID "0000-0002-0731-2950"

Deng, Rui ^[3]; Li, Zheng  ^[3];

• Search DOE PAGES for author "Li, Zheng"
• Search DOE PAGES for ORCID "0000-0003-2428-1209"

Li, Mengqi ^[3]; Wang, Yan ^[3]; Guo, Yunling ^[3]; Shi, Weida  ^[3];

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• Search DOE PAGES for ORCID "0000-0001-7530-0268"

Fan, Qiuling ^[4]; Martin, Shelley S. ^[5]; Rockwell, Nathan C.  ^[5];

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• Search DOE PAGES for ORCID "0000-0002-7748-7019"

Lagarias, J. Clark  ^[5];

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• Search DOE PAGES for ORCID "0000-0002-2093-0403"

Duanmu, Deqiang  ^[3]

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• Search DOE PAGES for ORCID "0000-0002-9365-362X"

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+ Show Author Affiliations

1. State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, 430070 Wuhan, China,, Department of Molecular Sciences, Macquarie University, Sydney, NSW 2109, Australia,
2. Department of Molecular Sciences, Macquarie University, Sydney, NSW 2109, Australia,
3. State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, 430070 Wuhan, China,
4. College of Life Science and Technology, Huazhong Agricultural University, 430070 Wuhan, China,
5. Department of Molecular and Cellular Biology, University of California, Davis, CA 95616

Publication Date:

Tue May 11 00:00:00 EDT 2021

Research Org.:

Univ. of California, Davis, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC)

OSTI Identifier:

1847981

Alternate Identifier(s):

OSTI ID: 1850819; OSTI ID: 1905444

Grant/Contract Number:  

DOE DE-FG02-09ER16117; SC0002395; FG02-09ER16117

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 118 Journal Issue: 20; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; science & technology; heme oxygenase; bilin reductase; reactive oxygen species; photosynthesis; phycocyanobilin; bilin reductase chlamydomonas chlorophyll biosynthesis heme oxygenase photosynthesis phycocyanobilin reactive oxygen species