Skip to main content

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home
  • Log in
  • My Cart

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
Research Article

The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis

Takayuki Shimizu, Sylwia M. Kacprzak, Nobuyoshi Mochizuki, Akira Nagatani, Satoru Watanabe, View ORCID ProfileTomohiro Shimada, Kan Tanaka, Yuuki Hayashi, View ORCID ProfileMunehito Arai, View ORCID ProfileDario Leister, Haruko Okamoto, View ORCID ProfileMatthew J. Terry, and View ORCID ProfileTatsuru Masuda
  1. aGraduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, 153-8902 Tokyo, Japan;
  2. bSchool of Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
  3. cGraduate School of Science, Kyoto University, Sakyo-ku, 606-8502 Kyoto, Japan;
  4. dDepartment of Bioscience, Tokyo University of Agriculture, Setagaya-ku, 156-8502 Tokyo, Japan;
  5. eLaboratory for Chemistry and Life Science, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8503, Japan;
  6. fSchool of Agriculture, Meiji University, Kawasaki-shi, 214-8571 Kanagawa, Japan;
  7. gPlant Molecular Biology, Faculty of Biology, Ludwig Maximilians Universität München, D-82152 Planegg-Martinsried, Germany;
  8. hInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom

See allHide authors and affiliations

PNAS December 3, 2019 116 (49) 24900-24906; first published November 15, 2019; https://doi.org/10.1073/pnas.1911251116
Takayuki Shimizu
aGraduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, 153-8902 Tokyo, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sylwia M. Kacprzak
bSchool of Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nobuyoshi Mochizuki
cGraduate School of Science, Kyoto University, Sakyo-ku, 606-8502 Kyoto, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Akira Nagatani
cGraduate School of Science, Kyoto University, Sakyo-ku, 606-8502 Kyoto, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Satoru Watanabe
dDepartment of Bioscience, Tokyo University of Agriculture, Setagaya-ku, 156-8502 Tokyo, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tomohiro Shimada
eLaboratory for Chemistry and Life Science, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8503, Japan;
fSchool of Agriculture, Meiji University, Kawasaki-shi, 214-8571 Kanagawa, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Tomohiro Shimada
Kan Tanaka
eLaboratory for Chemistry and Life Science, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8503, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yuuki Hayashi
aGraduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, 153-8902 Tokyo, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Munehito Arai
aGraduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, 153-8902 Tokyo, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Munehito Arai
Dario Leister
gPlant Molecular Biology, Faculty of Biology, Ludwig Maximilians Universität München, D-82152 Planegg-Martinsried, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Dario Leister
Haruko Okamoto
bSchool of Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
hInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Matthew J. Terry
bSchool of Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
hInstitute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Matthew J. Terry
Tatsuru Masuda
aGraduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro-ku, 153-8902 Tokyo, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Tatsuru Masuda
  • For correspondence: ctmasuda@fye.c.u-tokyo.ac.jp
  1. Edited by Krishna K. Niyogi, University of California, Berkeley, CA, and approved October 22, 2019 (received for review July 2, 2019)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Significance

The signaling pathway between chloroplasts and the nucleus (retrograde signaling) is important for the correct development of the photosynthetic apparatus of plant seedlings. The pathway is still not understood, but the majority of mutants with altered signaling (gun mutants) implicate the tetrapyrrole molecule heme in this process. In this article, we have demonstrated that the major retrograde signaling protein GUN1 can bind tetrapyrroles and regulate the flow through the tetrapyrrole biosynthesis pathway. The results support a role for tetrapyrroles in mediating retrograde signaling and open up the opportunity to develop a unifying hypothesis for this pathway that takes account of all identified gun mutants.

Abstract

The biogenesis of the photosynthetic apparatus in developing seedlings requires the assembly of proteins encoded on both nuclear and chloroplast genomes. To coordinate this process there needs to be communication between these organelles, but the retrograde signals by which the chloroplast communicates with the nucleus at this time are still essentially unknown. The Arabidopsis thaliana genomes uncoupled (gun) mutants, that show elevated nuclear gene expression after chloroplast damage, have formed the basis of our understanding of retrograde signaling. Of the 6 reported gun mutations, 5 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, are poorly understood, preventing the development of a unifying hypothesis for chloroplast-to-nucleus signaling. Here, we show that GUN1 directly binds to heme and other porphyrins, reduces flux through the tetrapyrrole biosynthesis pathway to limit heme and protochlorophyllide synthesis, 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, supporting a role for tetrapyrroles as mediators of a single biogenic chloroplast-to-nucleus retrograde signaling pathway.

  • retrograde signaling
  • chloroplast
  • heme
  • tetrapyrrole
  • gun mutants

Footnotes

  • ↵1Present address: School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom.

  • ↵2To whom correspondence may be addressed. Email: ctmasuda{at}fye.c.u-tokyo.ac.jp.
  • Author contributions: M.J.T. and T.M. designed research; T. Shimizu, S.M.K., N.M., T. Shimada, K.T., Y.H., M.A., and T.M. performed research; T. Shimizu, S.M.K., A.N., S.W., T. Shimada, K.T., Y.H., M.A., D.L., H.O., M.J.T., and T.M. analyzed data; and N.M., M.J.T., and T.M. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: All plasmid constructs are available from Addgene (accession IDs 136357–136363).

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1911251116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

View Full Text
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis
Takayuki Shimizu, Sylwia M. Kacprzak, Nobuyoshi Mochizuki, Akira Nagatani, Satoru Watanabe, Tomohiro Shimada, Kan Tanaka, Yuuki Hayashi, Munehito Arai, Dario Leister, Haruko Okamoto, Matthew J. Terry, Tatsuru Masuda
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24900-24906; DOI: 10.1073/pnas.1911251116

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis
Takayuki Shimizu, Sylwia M. Kacprzak, Nobuyoshi Mochizuki, Akira Nagatani, Satoru Watanabe, Tomohiro Shimada, Kan Tanaka, Yuuki Hayashi, Munehito Arai, Dario Leister, Haruko Okamoto, Matthew J. Terry, Tatsuru Masuda
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24900-24906; DOI: 10.1073/pnas.1911251116
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley

Article Classifications

  • Biological Sciences
  • Plant Biology
Proceedings of the National Academy of Sciences: 116 (49)
Table of Contents

Submit

Sign up for Article Alerts

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Smoke emanates from Japan’s Fukushima nuclear power plant a few days after tsunami damage
Core Concept: Muography offers a new way to see inside a multitude of objects
Muons penetrate much further than X-rays, they do essentially zero damage, and they are provided for free by the cosmos.
Image credit: Science Source/Digital Globe.
Water from a faucet fills a glass.
News Feature: How “forever chemicals” might impair the immune system
Researchers are exploring whether these ubiquitous fluorinated molecules might worsen infections or hamper vaccine effectiveness.
Image credit: Shutterstock/Dmitry Naumov.
Venus flytrap captures a fly.
Journal Club: Venus flytrap mechanism could shed light on how plants sense touch
One protein seems to play a key role in touch sensitivity for flytraps and other meat-eating plants.
Image credit: Shutterstock/Kuttelvaserova Stuchelova.
Illustration of groups of people chatting
Exploring the length of human conversations
Adam Mastroianni and Daniel Gilbert explore why conversations almost never end when people want them to.
Listen
Past PodcastsSubscribe
Panda bear hanging in a tree
How horse manure helps giant pandas tolerate cold
A study finds that giant pandas roll in horse manure to increase their cold tolerance.
Image credit: Fuwen Wei.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Subscribers
  • Librarians
  • Press
  • Cozzarelli Prize
  • Site Map
  • PNAS Updates
  • FAQs
  • Accessibility Statement
  • Rights & Permissions
  • About
  • Contact

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490