title: GUN4-Protoporphyrin IX Is a Singlet Oxygen Generator with Consequences for Plastid Retrograde Signaling.
abstract: The genomes uncoupled 4 (GUN4) protein is a nuclear-encoded, chloroplast-localized, porphyrin-binding protein implicated in retrograde signaling between the chloroplast and nucleus, although its exact role in this process is still unclear. Functionally, it enhances Mg-chelatase activity in the chlorophyll biosynthesis pathway. Because GUN4 is present only in organisms that carry out oxygenic photosynthesis and because it binds protoporphyrin IX (PPIX) and Mg-PPIX, it has been suggested that it prevents production of light- and PPIX- or Mg-PPIX-dependent reactive oxygen species. A chld-1/GUN4 mutant with elevated PPIX has a light-dependent up-regulation of GUN4, implicating this protein in light-dependent sensing of PPIX, with the suggestion that GUN4 reduces PPIX-generated singlet oxygen, O2(a(1)Δg), and subsequent oxidative damage (Brzezowski, P., Schlicke, H., Richter, A., Dent, R. M., Niyogi, K. K., and Grimm, B. (2014) Plant J. 79, 285-298). In direct contrast, our results show that purified GUN4 and oxidatively damaged ChlH increase the rate of PPIX-generated singlet oxygen production in the light, by a factor of 5 and 10, respectively, when compared with PPIX alone. Additionally, the functional GUN4-PPIX-ChlH complex and ChlH-PPIX complexes generate O2(a(1)Δg) at a reduced rate when compared with GUN4-PPIX. As O2(a(1)Δg) is a potential plastid-to-nucleus signal, possibly through second messengers, light-dependent O2(a(1)Δg) generation by GUN4-PPIX is proposed to be part of a signal transduction pathway from the chloroplast to the nucleus. GUN4 thus senses the availability and flux of PPIX through the chlorophyll biosynthetic pathway and also modulates Mg-chelatase activity. The light-dependent O2(a(1)Δg) generation from GUN4-PPIX is thus proposed as the first step in retrograde signaling from the chloroplast to the nucleus.
authors.affiliation: From the Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, New South Wales 2109, Australia.
authors.forename: Shabnam
authors.initials: S
authors.lastname: Tarahi Tabrizi
authors.affiliation: the Department of Biophysics, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland, and.
authors.forename: Artur
authors.initials: A
authors.lastname: Sawicki
authors.affiliation: the National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Shuaixiang
authors.initials: S
authors.lastname: Zhou
authors.affiliation: the National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China.
authors.forename: Meizhong
authors.initials: M
authors.lastname: Luo
authors.affiliation: From the Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, New South Wales 2109, Australia, robert.willows@mq.edu.au.
authors.forename: Robert D
authors.initials: RD
authors.lastname: Willows
mesh_terms: D016825:Chlamydomonas reinhardtii / Q000235:genetics / Q000378:metabolism*; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism*; D047908:Intracellular Signaling Peptides and Proteins / Q000235:genetics / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D011524:Protoporphyrins / Q000378:metabolism*; D017382:Reactive Oxygen Species / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology*
chemical_list: D047908:Intracellular Signaling Peptides and Proteins; D010940:Plant Proteins; D011524:Protoporphyrins; D017382:Reactive Oxygen Species; C028025:protoporphyrin IX
keywords: chlorophyll; chloroplast; genomes uncoupled 4; magnesium; magnesium chelatase; photosynthesis; reactive oxygen species (ROS); singlet oxygen