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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.


Evolution of the chloroplast retrograde signal for nuclear transcriptional regulation. After endosymbiosis, the chloroplast performed photosynthesis, generating photosynthetic metabolites as well as reactive oxygen species (ROS). The ability to sense and respond to these compounds in the cytoplasm should have been present even prior to the gene transfer event, and thus the nucleus was likely able to cope with them without any specific evolution (A). After the gene transfer event from the chloroplast to the nucleus, the location of the gene and its function differentiated. To modulate the function and amount of the gene product properly, the cell evolved a regulatory loop through a specific retrograde signaling pathway (B).
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Figure 2: Evolution of the chloroplast retrograde signal for nuclear transcriptional regulation. After endosymbiosis, the chloroplast performed photosynthesis, generating photosynthetic metabolites as well as reactive oxygen species (ROS). The ability to sense and respond to these compounds in the cytoplasm should have been present even prior to the gene transfer event, and thus the nucleus was likely able to cope with them without any specific evolution (A). After the gene transfer event from the chloroplast to the nucleus, the location of the gene and its function differentiated. To modulate the function and amount of the gene product properly, the cell evolved a regulatory loop through a specific retrograde signaling pathway (B).

Mentions: Before endosymbiosis, an ancient eukaryotic cell with a nucleus and mitochondria should have some, but not so highly complicated light-responsive regulation of gene expression because it was unnecessary to respond to the light environment as a non-photosynthetic organism. Conversely, cyanobacteria, which require oxygenic photosynthesis for their survival, should have a set of photosensory and photoregulatory mechanisms. Just after endosymbiosis, during the early stages of chloroplast evolution, light-responsive gene expression derived from cyanobacteria must have been completed inside the chloroplast (symbiont), and the regulation of nuclear gene expression should have been irrespective of the light conditions. However, mutual coordination of various cellular parameters, including metabolic fluxes, must have become crucial between the chloroplast and the host cell (Figure 2). In addition, gene transfer from the chloroplast to the nuclear genome has gradually occurred. Therefore, in a later phase of chloroplast evolution, light signals should have become transmitted into the nucleus to establish light-responsive coordinated gene expression as a photosynthetic eukaryote. During the subsequent evolution, plant-type photoreceptors and light signaling pathways were likely established.


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

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

Evolution of the chloroplast retrograde signal for nuclear transcriptional regulation. After endosymbiosis, the chloroplast performed photosynthesis, generating photosynthetic metabolites as well as reactive oxygen species (ROS). The ability to sense and respond to these compounds in the cytoplasm should have been present even prior to the gene transfer event, and thus the nucleus was likely able to cope with them without any specific evolution (A). After the gene transfer event from the chloroplast to the nucleus, the location of the gene and its function differentiated. To modulate the function and amount of the gene product properly, the cell evolved a regulatory loop through a specific retrograde signaling pathway (B).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Evolution of the chloroplast retrograde signal for nuclear transcriptional regulation. After endosymbiosis, the chloroplast performed photosynthesis, generating photosynthetic metabolites as well as reactive oxygen species (ROS). The ability to sense and respond to these compounds in the cytoplasm should have been present even prior to the gene transfer event, and thus the nucleus was likely able to cope with them without any specific evolution (A). After the gene transfer event from the chloroplast to the nucleus, the location of the gene and its function differentiated. To modulate the function and amount of the gene product properly, the cell evolved a regulatory loop through a specific retrograde signaling pathway (B).
Mentions: Before endosymbiosis, an ancient eukaryotic cell with a nucleus and mitochondria should have some, but not so highly complicated light-responsive regulation of gene expression because it was unnecessary to respond to the light environment as a non-photosynthetic organism. Conversely, cyanobacteria, which require oxygenic photosynthesis for their survival, should have a set of photosensory and photoregulatory mechanisms. Just after endosymbiosis, during the early stages of chloroplast evolution, light-responsive gene expression derived from cyanobacteria must have been completed inside the chloroplast (symbiont), and the regulation of nuclear gene expression should have been irrespective of the light conditions. However, mutual coordination of various cellular parameters, including metabolic fluxes, must have become crucial between the chloroplast and the host cell (Figure 2). In addition, gene transfer from the chloroplast to the nuclear genome has gradually occurred. Therefore, in a later phase of chloroplast evolution, light signals should have become transmitted into the nucleus to establish light-responsive coordinated gene expression as a photosynthetic eukaryote. During the subsequent evolution, plant-type photoreceptors and light signaling pathways were likely established.

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.