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The early days of plastid retrograde signaling with respect to replication and transcription.

Tanaka K, Hanaoka M - Front Plant Sci (2013)

Bottom Line: The plastid signal was originally defined as a pathway that informs the nucleus of the chloroplast status and results in the modulation of expression of nuclear-encoded plastid protein genes.We recently demonstrated in a primitive red alga that the plastid-derived Mg-protoporphyrin IX activates nuclear DNA replication (NDR) through the stabilization of a G1 cyclin, which coordinates the timing of organelle and NDR.In this short article, we discuss the origins, early days and evolution of the plastid retrograde signal(s).

View Article: PubMed Central - PubMed

Affiliation: Chemical Resources Laboratory, Tokyo Institute of Technology Yokohama, Japan.

ABSTRACT
The plastid signal was originally defined as a pathway that informs the nucleus of the chloroplast status and results in the modulation of expression of nuclear-encoded plastid protein genes. However, the transfer of chloroplast genes into the nuclear genome is a prerequisite in this scheme, although it should not have been established during the very early phase of chloroplast evolution. We recently demonstrated in a primitive red alga that the plastid-derived Mg-protoporphyrin IX activates nuclear DNA replication (NDR) through the stabilization of a G1 cyclin, which coordinates the timing of organelle and NDR. This mechanism apparently does not involve any transcriptional regulation in the nucleus, and could have been established prior to gene transfer events. However, a retrograde signal mediating light-responsive gene expression may have been established alongside gene transfer, because essential light sensing and regulatory systems were originally incorporated into plant cells by the photosynthetic endosymbiont. In this short article, we discuss the origins, early days and evolution of the plastid retrograde signal(s).

No MeSH data available.


Related in: MedlinePlus

Evolution of the coupling between ODR and NDR. (A) Prior to endosymbiosis, the ancestral cyanobacteria were living phototrophically and dependent on light, while the host eukaryotic cells were proliferating independent of light conditions. After the engulfment, the primitive chloroplast would have required light for proliferation, while the host did not. Therefore, the uniquely acquired chloroplast may have been lost if the host cell could proliferate in the dark. A newly evolved checkpoint system, “light checkpoint” in the figure, prevented host proliferation in the dark to maintain the endosymbiotic association. (B) Architecture of the light checkpoint. Under dark conditions, an F-box component of E3-ubiquitin ligase, Fbx3, recognizes Cyclin1, resulting in ubiquitination and prompt degradation. Cyclin1 is the cyclin that forms a complex with CDKA and activates NDR, and thus, degradation of Cyclin1 prevents NDR in the dark. Light illumination somehow activates ODR and results in the accumulation of Mg-ProtoIX in the cytosol. Interaction of Mg-ProtoIX with Fbx3 prevents the ubiquitination of Cyclin1 and induces the activation of CDKA and NDR.
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Figure 1: Evolution of the coupling between ODR and NDR. (A) Prior to endosymbiosis, the ancestral cyanobacteria were living phototrophically and dependent on light, while the host eukaryotic cells were proliferating independent of light conditions. After the engulfment, the primitive chloroplast would have required light for proliferation, while the host did not. Therefore, the uniquely acquired chloroplast may have been lost if the host cell could proliferate in the dark. A newly evolved checkpoint system, “light checkpoint” in the figure, prevented host proliferation in the dark to maintain the endosymbiotic association. (B) Architecture of the light checkpoint. Under dark conditions, an F-box component of E3-ubiquitin ligase, Fbx3, recognizes Cyclin1, resulting in ubiquitination and prompt degradation. Cyclin1 is the cyclin that forms a complex with CDKA and activates NDR, and thus, degradation of Cyclin1 prevents NDR in the dark. Light illumination somehow activates ODR and results in the accumulation of Mg-ProtoIX in the cytosol. Interaction of Mg-ProtoIX with Fbx3 prevents the ubiquitination of Cyclin1 and induces the activation of CDKA and NDR.

Mentions: Prior to endosymbiosis, the cell cycle of the host eukaryote was probably non-phototrophic and likely driven by the usual Cyclin/CDK system that is unrelated to the external light conditions for photosynthesis. However, the cyanobacterial endosymbiont must have required light for proliferation. Thus, the endosymbiont of the early photosynthetic eukaryote was likely to be lost under dark conditions, unless some mechanism to couple the host–symbiont proliferation cycles evolved (Figure 1). The mechanism for the ODR–NDR coupling described above requires basically only one specific protein, Fbx3, to be established as an additional cytoplasmic component. Providing that the evolution of Fbx3 adequately explains the chloroplast-to-nucleus DNA replication coupling, this mechanism could have been established at a very early phase of chloroplast evolution because of its extreme simplicity. In addition, it should be noted that this mechanism does not require any gene transfer events from the chloroplast to the nucleus. Since the well-known plastid retrograde signals are related to the transcriptional regulation of nuclear genes encoding chloroplast-targeted proteins, gene transfer events are prerequisite for their existence. The establishment of endosymbiosis would have been prior to such gene transfer events, and our recent findings may have supported the stabilization of the transition states. A similar coupling mechanism has also been suggested to be present in vascular plant cells (Kobayashi et al., 2009), again indicating its common and early origin during plant evolution.


The early days of plastid retrograde signaling with respect to replication and transcription.

Tanaka K, Hanaoka M - Front Plant Sci (2013)

Evolution of the coupling between ODR and NDR. (A) Prior to endosymbiosis, the ancestral cyanobacteria were living phototrophically and dependent on light, while the host eukaryotic cells were proliferating independent of light conditions. After the engulfment, the primitive chloroplast would have required light for proliferation, while the host did not. Therefore, the uniquely acquired chloroplast may have been lost if the host cell could proliferate in the dark. A newly evolved checkpoint system, “light checkpoint” in the figure, prevented host proliferation in the dark to maintain the endosymbiotic association. (B) Architecture of the light checkpoint. Under dark conditions, an F-box component of E3-ubiquitin ligase, Fbx3, recognizes Cyclin1, resulting in ubiquitination and prompt degradation. Cyclin1 is the cyclin that forms a complex with CDKA and activates NDR, and thus, degradation of Cyclin1 prevents NDR in the dark. Light illumination somehow activates ODR and results in the accumulation of Mg-ProtoIX in the cytosol. Interaction of Mg-ProtoIX with Fbx3 prevents the ubiquitination of Cyclin1 and induces the activation of CDKA and NDR.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539659&req=5

Figure 1: Evolution of the coupling between ODR and NDR. (A) Prior to endosymbiosis, the ancestral cyanobacteria were living phototrophically and dependent on light, while the host eukaryotic cells were proliferating independent of light conditions. After the engulfment, the primitive chloroplast would have required light for proliferation, while the host did not. Therefore, the uniquely acquired chloroplast may have been lost if the host cell could proliferate in the dark. A newly evolved checkpoint system, “light checkpoint” in the figure, prevented host proliferation in the dark to maintain the endosymbiotic association. (B) Architecture of the light checkpoint. Under dark conditions, an F-box component of E3-ubiquitin ligase, Fbx3, recognizes Cyclin1, resulting in ubiquitination and prompt degradation. Cyclin1 is the cyclin that forms a complex with CDKA and activates NDR, and thus, degradation of Cyclin1 prevents NDR in the dark. Light illumination somehow activates ODR and results in the accumulation of Mg-ProtoIX in the cytosol. Interaction of Mg-ProtoIX with Fbx3 prevents the ubiquitination of Cyclin1 and induces the activation of CDKA and NDR.
Mentions: Prior to endosymbiosis, the cell cycle of the host eukaryote was probably non-phototrophic and likely driven by the usual Cyclin/CDK system that is unrelated to the external light conditions for photosynthesis. However, the cyanobacterial endosymbiont must have required light for proliferation. Thus, the endosymbiont of the early photosynthetic eukaryote was likely to be lost under dark conditions, unless some mechanism to couple the host–symbiont proliferation cycles evolved (Figure 1). The mechanism for the ODR–NDR coupling described above requires basically only one specific protein, Fbx3, to be established as an additional cytoplasmic component. Providing that the evolution of Fbx3 adequately explains the chloroplast-to-nucleus DNA replication coupling, this mechanism could have been established at a very early phase of chloroplast evolution because of its extreme simplicity. In addition, it should be noted that this mechanism does not require any gene transfer events from the chloroplast to the nucleus. Since the well-known plastid retrograde signals are related to the transcriptional regulation of nuclear genes encoding chloroplast-targeted proteins, gene transfer events are prerequisite for their existence. The establishment of endosymbiosis would have been prior to such gene transfer events, and our recent findings may have supported the stabilization of the transition states. A similar coupling mechanism has also been suggested to be present in vascular plant cells (Kobayashi et al., 2009), again indicating its common and early origin during plant evolution.

Bottom Line: The plastid signal was originally defined as a pathway that informs the nucleus of the chloroplast status and results in the modulation of expression of nuclear-encoded plastid protein genes.We recently demonstrated in a primitive red alga that the plastid-derived Mg-protoporphyrin IX activates nuclear DNA replication (NDR) through the stabilization of a G1 cyclin, which coordinates the timing of organelle and NDR.In this short article, we discuss the origins, early days and evolution of the plastid retrograde signal(s).

View Article: PubMed Central - PubMed

Affiliation: Chemical Resources Laboratory, Tokyo Institute of Technology Yokohama, Japan.

ABSTRACT
The plastid signal was originally defined as a pathway that informs the nucleus of the chloroplast status and results in the modulation of expression of nuclear-encoded plastid protein genes. However, the transfer of chloroplast genes into the nuclear genome is a prerequisite in this scheme, although it should not have been established during the very early phase of chloroplast evolution. We recently demonstrated in a primitive red alga that the plastid-derived Mg-protoporphyrin IX activates nuclear DNA replication (NDR) through the stabilization of a G1 cyclin, which coordinates the timing of organelle and NDR. This mechanism apparently does not involve any transcriptional regulation in the nucleus, and could have been established prior to gene transfer events. However, a retrograde signal mediating light-responsive gene expression may have been established alongside gene transfer, because essential light sensing and regulatory systems were originally incorporated into plant cells by the photosynthetic endosymbiont. In this short article, we discuss the origins, early days and evolution of the plastid retrograde signal(s).

No MeSH data available.


Related in: MedlinePlus