Control of Retrograde Signaling by Rapid Turnover of GENOMES UNCOUPLED1

Wu, Guo-Zhang; Chalvin, Camille; Hoelscher, Matthijs P.; Meyer, Etienne H.; Wu, Xu; Bock, Ralph

doi:10.1104/pp.18.00009

Cited by 87 publications

(138 citation statements)

References 81 publications

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“…The GUN1 protein is a pentatricopeptide repeat (PPR) protein with a small MutS-related (SMR) domain 7 . The function of GUN1 is unknown, but it has been proposed to have a role in plastid protein homeostasis [13][14][15][16] , and can interact with proteins involved in both plastid protein synthesis and the tetrapyrrole pathway 13 To further explore the interaction of GUN1 with tetrapyrrole biosynthesis, we first tested whether GUN1 could alter the flow through the tetrapyrrole pathway 17 ( Supplementary Fig. 1).…”

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confidence: 99%

“…5). Since GUN1 accumulates detectable levels only at very young stages of leaf development 16 , proteins were extracted from 4-day-old seedlings and subjected to the hemin binding assay ( Fig. 3f).…”

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confidence: 99%

“…The mechanism for this restriction is unknown but may be related to the observation here that GUN1 can bind metal-porphyrins and/or that it can interact with the tetrapyrrole enzymes porphobilinogen deaminase and uroporphyrinogen III decarboxylase 2 that catalyze shared steps in the tetrapyrrole pathway 13 . GUN1 is not a very abundant protein 16 and it is unlikely that any restriction of the flow of tetrapyrroles is due to sequestration.…”

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confidence: 99%

“…Rather, we propose that the mode of action of GUN1 is regulatory. Moreover, the rapid degradation in the light 16 would permit an increased flow of tetrapyrroles at a time when the demand for photosynthetic tetrapyrroles, both heme and Chl, is at its greatest.…”

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GUN1 regulates tetrapyrrole biosynthesis

Shimizu

Mochizuki

Nagatani

et al. 2019

Preprint

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The biogenesis of the photosynthetic apparatus in developing chloroplasts requires the assembly of proteins encoded on both nuclear and chloroplast genomes 1 . To coordinate 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 2 . 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 3 . Of the six reported gun mutations, five are in tetrapyrrole biosynthesis proteins 4-6 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 6 . However, the molecular consequences of the strongest of the gun mutants, gun1 7 , 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-tonucleus retrograde signaling pathway.It has long been established that the expression of a large number of nuclear genes encoding chloroplast proteins is dependent on the presence of intact chloroplasts 8 and mutations affecting chloroplast function or treatments with inhibitors such as norflurazon (NF) or lincomycin (Lin) result in the strong downregulation of many photosynthesis-related genes 7,9,10 . Mutants that lack this ability to co-ordinate the nuclear and chloroplast genomes were identified by their ability to retain expression of

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GUN1 regulates tetrapyrrole biosynthesis

Shimizu

Mochizuki

Nagatani

et al. 2019

Preprint

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“…Here, we have investigated the role of GUN1 under conditions that trigger its accumulation to detectable levels, i.e. in Arabidopsis cotyledons during early stages of chloroplast biogenesis in the presence of either lincomycin (Lin; Wu et al, 2018) or of mutations that affect plastid protein homeostasis, by depleting levels of the FtsH protease complex ( ftsh ), reducing plastid ribosome activity ( prps21-1 , prpl11-1 and rh50-1 ) or disrupting plastid protein import and folding ( cphsp70-1 ). We show that GUN1 is important for NEP-dependent transcript accumulation, possibly being a key component of the NEP-dependent compensatory mechanism activated upon conditions that alter chloroplast protein homeostasis and PEP activity.…”

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GUN1 influences the accumulation of NEP-dependent transcripts and chloroplast protein import in Arabidopsis cotyledons upon perturbation of chloroplast protein homeostasis

Tadini

Peracchio

Trotta

et al. 2019

Preprint

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Correct chloroplast development and function require coordinated expression of chloroplast and nuclear genes. This is achieved through chloroplast signals that modulate nuclear gene expression in accordance with the chloroplast's needs. Genetic evidence indicates that GUN1, a chloroplast-localized pentatricopeptide-repeat (PPR) protein with a C-terminal Small MutS-Related (SMR) domain, is involved in integrating multiple developmental and stress-related signals in both young seedlings and adult leaves. Recently, GUN1 was found to interact physically with factors involved in chloroplast protein homeostasis, and with enzymes of tetrapyrrole biosynthesis in adult leaves that function in various retrograde signaling pathways. Here we show that, following perturbation of chloroplast protein homeostasis i) by growth in lincomycin-containing medium, or ii) in mutants defective in either the FtsH protease complex (ftsh), plastid ribosome activity (prps21-1 and prpl11-1) or plastid protein import and folding (cphsp70-1), GUN1 influences NEP-dependent transcript accumulation during cotyledon greening and also intervenes in chloroplast protein import. import Chloroplast biogenesis is achieved through a cascade of events that include cytosolic synthesis of chloroplasttargeted proteins, followed by their import, assembly and folding, while unfolded/misfolded proteins and damaged or malformed chloroplasts are degraded (Sakamoto et al., 2008; Jarvi and López-Jauez, 2013; Izumi and Nakamura, 2018; Otegui, 2018). Most chloroplast-targeted proteins enter the chloroplasts via the protein complexes TOC ('translocon at outer envelope of chloroplast') and TIC ('translocon at inner envelope of chloroplast'). On the cytosolic side, precursor proteins are directed to the Toc34 and Toc159 receptors through the interaction of their chloroplast-targeting peptides with the chaperone heat shock protein 90 (Hsp90) and the guidance complex formed by Hsp70 and a 14-3-3 protein. Active transport through the chloroplast envelope is then mediated by an ATP-dependent import motor, consisting of Hsp70, Hsp90 and the stromal Hsp93 (ClpC2) proteins (Kessler and Schnell, 2009; Sjuts et al., 2017).On the stromal side, transcription of the plastid-encoded genes in higher plants requires two different RNA polymerases: the nuclear-encoded RNA polymerase (NEP), also termed RpoTp (located specifically in the chloroplasts and encoded by the RPOT3 gene) or RpoTmp (located both in mitochondria and plastids and encoded by the RPOT2 gene) and the plastid-encoded RNA polymerase (PEP) (Yu et al., 2014; Börner et al., 2015). NEP is a monomeric T3-T7 bacteriophage-type RNA polymerase that is mainly responsible for transcribing housekeeping genes, whereas PEP is a bacterial-type multisubunit enzyme largely tasked with transcribing photosynthesis-related genes. Chloroplast development is associated with a shift in the primary RNA polymerase from NEP to PEP. Furthermore, compensatory responses can be observed between the two RNA polymerases, as depletion of PEP activ...

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The Enigmatic Roles of PPR‐SMR Proteins in Plants

Zhang

2019

Advanced Science

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The pentatricopeptide repeat (PPR) protein family, with more than 400 members, is one of the largest and most diverse protein families in land plants. A small subset of PPR proteins contain a C‐terminal small MutS‐related (SMR) domain. Although there are relatively few PPR‐SMR proteins, they play essential roles in embryo development, chloroplast biogenesis and gene expression, and plastid‐to‐nucleus retrograde signaling. Here, recent advances in understanding the roles of PPR‐SMR proteins and the SMR domain based on a combination of genetic, biochemical, and physiological analyses are described. In addition, the potential of the PPR‐SMR protein SOT1 to serve as a tool for RNA manipulation is highlighted.

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Control of Retrograde Signaling by Rapid Turnover of GENOMES UNCOUPLED1

Cited by 87 publications

References 81 publications

GUN1 regulates tetrapyrrole biosynthesis

GUN1 regulates tetrapyrrole biosynthesis

GUN1 influences the accumulation of NEP-dependent transcripts and chloroplast protein import in Arabidopsis cotyledons upon perturbation of chloroplast protein homeostasis

The Enigmatic Roles of PPR‐SMR Proteins in Plants

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