scholarly journals The Role of Tetrapyrrole- and GUN1-Dependent Signaling on Chloroplast Biogenesis

Plants ◽  
2021 ◽  
Vol 10 (2) ◽  
pp. 196
Author(s):  
Takayuki Shimizu ◽  
Tatsuru Masuda
Keyword(s):  
Protein Import ◽  
Nuclear Gene ◽  
Retrograde Signaling ◽  
Chloroplast Biogenesis ◽  
Plastid Development ◽  
Nuclear Gene Expression ◽  
Coordinated Expression ◽  
Plastid Protein ◽  
Working Hypotheses

Chloroplast biogenesis requires the coordinated expression of the chloroplast and nuclear genomes, which is achieved by communication between the developing chloroplasts and the nucleus. Signals emitted from the plastids, so-called retrograde signals, control nuclear gene expression depending on plastid development and functionality. Genetic analysis of this pathway identified a set of mutants defective in retrograde signaling and designated genomes uncoupled (gun) mutants. Subsequent research has pointed to a significant role of tetrapyrrole biosynthesis in retrograde signaling. Meanwhile, the molecular functions of GUN1, the proposed integrator of multiple retrograde signals, have not been identified yet. However, based on the interactions of GUN1, some working hypotheses have been proposed. Interestingly, GUN1 contributes to important biological processes, including plastid protein homeostasis, through transcription, translation, and protein import. Furthermore, the interactions of GUN1 with tetrapyrroles and their biosynthetic enzymes have been revealed. This review focuses on our current understanding of the function of tetrapyrrole retrograde signaling on chloroplast biogenesis.

scholarly journals Coordination of Plastid Protein Import and Nuclear Gene Expression by Plastid-to-Nucleus Retrograde Signaling

2009 ◽  
Vol 151 (3) ◽  
pp. 1339-1353 ◽  
Author(s):  
Tomohiro Kakizaki ◽  
Hideo Matsumura ◽  
Katsuhiro Nakayama ◽  
Fang-Sik Che ◽  
Ryohei Terauchi ◽  
...  
Keyword(s):  
Gene Expression ◽  
Protein Import ◽  
Nuclear Gene ◽  
Retrograde Signaling ◽  
Nuclear Gene Expression ◽  
Plastid Protein

scholarly journals Coordination of plastid and nuclear gene expression

2003 ◽  
Vol 358 (1429) ◽  
pp. 135-145 ◽  
Author(s):  
John C. Gray ◽  
James A. Sullivan ◽  
Jun-Hui Wang ◽  
Cheryl A. Jerome ◽  
Daniel MacLean
Keyword(s):  
Nuclear Gene ◽  
Nuclear Genes ◽  
Regulation Of Transcription ◽  
Nuclear Gene Expression ◽  
Plastid Genomes ◽  
Expression Of Genes ◽  
Genes Encoding ◽  
Coordinated Expression ◽  
Plastid Protein ◽  
Related Proteins

The coordinated expression of genes distributed between the nuclear and plastid genomes is essential for the assembly of functional chloroplasts. Although the nucleus has a pre–eminent role in controlling chloroplast biogenesis, there is considerable evidence that the expression of nuclear genes encoding photosynthesis–related proteins is regulated by signals from plastids. Perturbation of several plastid–located processes, by inhibitors or in mutants, leads to decreased transcription of a set of nuclear photosynthesis–related genes. Characterization of arabidopsis gun ( genomes uncoupled ) mutants, which express nuclear genes in the presence of norflurazon or lincomycin, has provided evidence for two separate signalling pathways, one involving tetrapyrrole biosynthesis intermediates and the other requiring plastid protein synthesis. In addition, perturbation of photosynthetic electron transfer produces at least two different redox signals, as part of the acclimation to altered light conditions. The recognition of multiple plastid signals requires a reconsideration of the mechanisms of regulation of transcription of nuclear genes encoding photosynthesis–related proteins.

scholarly journals GUN1 regulates tetrapyrrole biosynthesis

2019 ◽  
Author(s):  
Takayuki Shimizu ◽  
Nobuyoshi Mochizuki ◽  
Akira Nagatani ◽  
Satoru Watanabe ◽  
Tomohiro Shimada ◽  
...  
Keyword(s):  
Chloroplast Development ◽  
Photosynthetic Apparatus ◽  
Nuclear Gene ◽  
Retrograde Signaling ◽  
Tetrapyrrole Biosynthesis ◽  
Metal Porphyrins ◽  
Nuclear Gene Expression ◽  
Chloroplast Genomes ◽  
Tetrapyrrole Metabolism

The biogenesis of the photosynthetic apparatus in developing chloroplasts requires the assembly of proteins encoded on both nuclear and chloroplast genomes1. 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 unknown2. 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 damage3. Of the six reported gun mutations, five are in tetrapyrrole biosynthesis proteins4-6 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 genes6. However, the molecular consequences of the strongest of the gun mutants, gun17, 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.

scholarly journals The retrograde signaling protein GUN1 regulates tetrapyrrole biosynthesis

2019 ◽  
Vol 116 (49) ◽  
pp. 24900-24906 ◽  
Author(s):  
Takayuki Shimizu ◽  
Sylwia M. Kacprzak ◽  
Nobuyoshi Mochizuki ◽  
Akira Nagatani ◽  
Satoru Watanabe ◽  
...  
Keyword(s):  
Photosynthetic Apparatus ◽  
Nuclear Gene ◽  
Retrograde Signaling ◽  
Biosynthesis Pathway ◽  
Tetrapyrrole Biosynthesis ◽  
Positive Signal ◽  
Nuclear Gene Expression ◽  
Chloroplast Genomes ◽  
Tetrapyrrole Metabolism

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.

scholarly journals Role of Temperature Stress on Chloroplast Biogenesis and Protein Import in Pea

2009 ◽  
Vol 150 (2) ◽  
pp. 1050-1061 ◽  
Author(s):  
Siddhartha Dutta ◽  
Sasmita Mohanty ◽  
Baishnab C. Tripathy
Keyword(s):  
Temperature Stress ◽  
Protein Import ◽  
Chloroplast Biogenesis

scholarly journals Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype

2020 ◽  
Vol 375 (1801) ◽  
pp. 20190401 ◽  
Author(s):  
Mike T. Page ◽  
Tania Garcia-Becerra ◽  
Alison G. Smith ◽  
Matthew J. Terry
Keyword(s):  
Gene Expression ◽  
Feedback Inhibition ◽  
Nuclear Gene ◽  
Signalling Pathway ◽  
Chloroplast Genes ◽  
Nuclear Gene Expression ◽  
Retrograde Signalling ◽  
Genes Encoding ◽  
Retrograde Signal

Chloroplast development requires communication between the progenitor plastids and the nucleus, where most of the genes encoding chloroplast proteins reside. Retrograde signals from the chloroplast to the nucleus control the expression of many of these genes, but the signalling pathway is poorly understood. Tetrapyrroles have been strongly implicated as mediators of this signal with the current hypothesis being that haem produced by the activity of ferrochelatase 1 (FC1) is required to promote nuclear gene expression. We have tested this hypothesis by overexpressing FC1 and specifically targeting it to either chloroplasts or mitochondria, two possible locations for this enzyme. Our results show that targeting of FC1 to chloroplasts results in increased expression of the nuclear-encoded chloroplast genes GUN4 , CA1 , HEMA1 , LHCB2.1, CHLH after treatment with Norflurazon (NF) and that this increase correlates to FC1 gene expression and haem production measured by feedback inhibition of protochlorophyllide synthesis. Targeting FC1 to mitochondria did not enhance the expression of nuclear-encoded chloroplast genes after NF treatment. The overexpression of FC1 also increased nuclear gene expression in the absence of NF treatment, demonstrating that this pathway is operational in the absence of a stress treatment. Our results therefore support the hypothesis that haem synthesis is a promotive chloroplast-to-nucleus retrograde signal. However, not all FC1 overexpression lines enhanced nuclear gene expression, suggesting there is still a lot we do not understand about the role of FC1 in this signalling pathway. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

scholarly journals Retrograde signalling in a virescent mutant triggers an anterograde delay of chloroplast biogenesis that requires GUN1 and is essential for survival

2020 ◽  
Vol 375 (1801) ◽  
pp. 20190400 ◽  
Author(s):  
Naresh Loudya ◽  
Tolulope Okunola ◽  
Jia He ◽  
Paul Jarvis ◽  
Enrique López-Juez
Keyword(s):  
Protein Import ◽  
Early Stage ◽  
Plastid Development ◽  
Plastid Genomes ◽  
Expression Of Genes ◽  
Fitness Value ◽  
Retrograde Signalling ◽  
Value Loss ◽  
Elevated Expression ◽  
Plastid Protein

Defects in chloroplast development are ‘retrograde-signalled’ to the nucleus, reducing synthesis of photosynthetic or related proteins. The Arabidopsis cue8 mutant manifests virescence, a slow-greening phenotype, and is defective at an early stage in plastid development. Greening cotyledons or early leaf cells of cue8 exhibit immature chloroplasts which fail to fill the available cellular space. Such chloroplasts show reduced expression of genes of photosynthetic function, dependent on the plastid-encoded polymerase (PEP), while the expression of genes of housekeeping function driven by the nucleus-encoded polymerase (NEP) is elevated, a phenotype shared with mutants in plastid genetic functions. We attribute this phenotype to reduced expression of specific PEP-controlling sigma factors, elevated expression of RPOT (NEP) genes and maintained replication of plastid genomes (resulting in densely coalesced nucleoids in the mutant), i.e. it is due to an anterograde nucleus-to-chloroplast correction, analogous to retention of a juvenile plastid state. Mutants in plastid protein import components, particularly those involved in housekeeping protein import, also show this ‘retro-anterograde’ correction. Loss of CUE8 also causes changes in mRNA editing. The overall response has strong fitness value: loss of GUN1, an integrator of retrograde signalling, abolishes elements of it (albeit not others, including editing changes), causing bleaching and eventual seedling lethality upon cue8 gun1 . This highlights the adaptive significance of virescence and retrograde signalling. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

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

2019 ◽  
Author(s):  
Luca Tadini ◽  
Carlotta Peracchio ◽  
Andrea Trotta ◽  
Monica Colombo ◽  
Ilaria Mancini ◽  
...  
Keyword(s):  
Protein Import ◽  
Nuclear Gene ◽  
Protein Homeostasis ◽  
Pentatricopeptide Repeat ◽  
Transcript Accumulation ◽  
Chloroplast Protein Import ◽  
Chloroplast Protein ◽  
Ppr Protein ◽  
Coordinated Expression ◽  
And Function

AbstractCorrect 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.

scholarly journals HnRNPA2 is a novel histone acetyltransferase that mediates mitochondrial stress-induced nuclear gene expression

2016 ◽  
Vol 2 (1) ◽  
Author(s):  
Manti Guha ◽  
Satish Srinivasan ◽  
Kip Guja ◽  
Edison Mejia ◽  
Miguel Garcia-Diaz ◽  
...  
Keyword(s):  
Gene Expression ◽  
Mitochondrial Dna ◽  
Transcriptional Activation ◽  
Nuclear Gene ◽  
C2c12 Cells ◽  
Retrograde Signaling ◽  
Epigenetic Mechanism ◽  
Mitochondrial Stress ◽  
Nuclear Gene Expression ◽  
Mitochondrial Dna Copy Number

Abstract Reduced mitochondrial DNA copy number, mitochondrial DNA mutations or disruption of electron transfer chain complexes induce mitochondria-to-nucleus retrograde signaling, which induces global change in nuclear gene expression ultimately contributing to various human pathologies including cancer. Recent studies suggest that these mitochondrial changes cause transcriptional reprogramming of nuclear genes although the mechanism of this cross talk remains unclear. Here, we provide evidence that mitochondria-to-nucleus retrograde signaling regulates chromatin acetylation and alters nuclear gene expression through the heterogeneous ribonucleoprotein A2 (hnRNAP2). These processes are reversed when mitochondrial DNA content is restored to near normal cell levels. We show that the mitochondrial stress-induced transcription coactivator hnRNAP2 acetylates Lys 8 of H4 through an intrinsic histone lysine acetyltransferase (KAT) activity with Arg 48 and Arg 50 of hnRNAP2 being essential for acetyl-CoA binding and acetyltransferase activity. H4K8 acetylation at the mitochondrial stress-responsive promoters by hnRNAP2 is essential for transcriptional activation. We found that the previously described mitochondria-to-nucleus retrograde signaling-mediated transformation of C2C12 cells caused an increased expression of genes involved in various oncogenic processes, which is retarded in hnRNAP2 silenced or hnRNAP2 KAT mutant cells. Taken together, these data show that altered gene expression by mitochondria-to-nucleus retrograde signaling involves a novel hnRNAP2-dependent epigenetic mechanism that may have a role in cancer and other pathologies.

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