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The making of a chloroplast.

Waters MT, Langdale JA - EMBO J. (2009)

Bottom Line: The exchange of genetic information from the chloroplast to the nucleus has resulted in considerable co-ordination in the activities of these two organelles during all stages of plant development.In addition, we discuss the mechanisms through which chloroplasts develop in different cell types, namely cotyledons and the dimorphic chloroplasts of the C(4) plant maize.Finally, we discuss recent data that suggest the specific regulation of the light-dependent phases of photosynthesis, providing a means to optimize photosynthesis to varying light regimes.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, UK.

ABSTRACT
Since its endosymbiotic beginning, the chloroplast has become fully integrated into the biology of the host eukaryotic cell. The exchange of genetic information from the chloroplast to the nucleus has resulted in considerable co-ordination in the activities of these two organelles during all stages of plant development. Here, we give an overview of the mechanisms of light perception and the subsequent regulation of nuclear gene expression in the model plant Arabidopsis thaliana, and we cover the main events that take place when proplastids differentiate into chloroplasts. We also consider recent findings regarding signalling networks between the chloroplast and the nucleus during seedling development, and how these signals are modulated by light. In addition, we discuss the mechanisms through which chloroplasts develop in different cell types, namely cotyledons and the dimorphic chloroplasts of the C(4) plant maize. Finally, we discuss recent data that suggest the specific regulation of the light-dependent phases of photosynthesis, providing a means to optimize photosynthesis to varying light regimes.

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A model for long-term photosynthetic regulation by GLK proteins. Under light-limiting conditions (left), the PET chain cannot supply sufficient ATP and reducing equivalents to the Calvin cycle, and, therefore, tends to be in an oxidized state. This prompts a chloroplast-derived signal to the nucleus (dashed arrow) that upregulates transcription of GLK genes. GLK proteins in turn bind to promoter sequences of genes that function in light harvesting, such as Lhcb and key chlorophyll biosynthetic genes. Transcript levels of these GLK target genes increase, leading to higher levels of the corresponding protein (Lhcb in this case), as depicted by the thicker arrow. Upregulation of chlorophyll biosynthesis and LHC assembly leads to higher specific chlorophyll levels, a lower Chl a/b ratio and more abundant grana (stacked discs of thylakoids), as observed in 35S:GLK transgenic plants. Increased grana abundance is associated with LHC trimers forming highly organized photosystem supercomplexes (Allen and Forsberg, 2001; Kovacs et al, 2006). When light is plentiful or even at inhibitory levels (right), the rate of CO2 fixation is insufficient to use all of the output of the light-harvesting reactions, resulting in an overly reduced PET. This triggers a negative signal (and/or absence of a positive signal) that leads to lower rates of GLK transcription. The accompanying decrease in Lhcb and chlorophyll-related gene transcripts eventually results in a fall in the light-harvesting components in the thylakoid membrane and lower chlorophyll levels. In turn, there are fewer, less stacked grana and a higher proportion of non-stacked, stromal lamellae, as observed in glk1 glk2 mutants. Together, these changes help to redress the imbalance between light absorption and CO2 fixation. Note that glk1 glk2 mutants are always paler than WT plants, suggesting that some degree of GLK activity is required under all conditions.
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f3: A model for long-term photosynthetic regulation by GLK proteins. Under light-limiting conditions (left), the PET chain cannot supply sufficient ATP and reducing equivalents to the Calvin cycle, and, therefore, tends to be in an oxidized state. This prompts a chloroplast-derived signal to the nucleus (dashed arrow) that upregulates transcription of GLK genes. GLK proteins in turn bind to promoter sequences of genes that function in light harvesting, such as Lhcb and key chlorophyll biosynthetic genes. Transcript levels of these GLK target genes increase, leading to higher levels of the corresponding protein (Lhcb in this case), as depicted by the thicker arrow. Upregulation of chlorophyll biosynthesis and LHC assembly leads to higher specific chlorophyll levels, a lower Chl a/b ratio and more abundant grana (stacked discs of thylakoids), as observed in 35S:GLK transgenic plants. Increased grana abundance is associated with LHC trimers forming highly organized photosystem supercomplexes (Allen and Forsberg, 2001; Kovacs et al, 2006). When light is plentiful or even at inhibitory levels (right), the rate of CO2 fixation is insufficient to use all of the output of the light-harvesting reactions, resulting in an overly reduced PET. This triggers a negative signal (and/or absence of a positive signal) that leads to lower rates of GLK transcription. The accompanying decrease in Lhcb and chlorophyll-related gene transcripts eventually results in a fall in the light-harvesting components in the thylakoid membrane and lower chlorophyll levels. In turn, there are fewer, less stacked grana and a higher proportion of non-stacked, stromal lamellae, as observed in glk1 glk2 mutants. Together, these changes help to redress the imbalance between light absorption and CO2 fixation. Note that glk1 glk2 mutants are always paler than WT plants, suggesting that some degree of GLK activity is required under all conditions.

Mentions: Arabidopsis glk1 glk2 double mutants are pale green and contain chloroplasts with non-stacked thylakoids and reduced levels of PET complexes (Fitter et al, 2002). Furthermore, they have an unusually high ratio of Chl a to Chl b: grown under identical conditions, the ratio in wild-type plants is ∼3.5 and in mutants ∼5.5 (Waters et al, 2009). This alteration is likely to result partly from reduced levels of LHC proteins, to which Chl b is exclusively bound (Green and Durnford, 1996). When GLK genes are overexpressed in a mutant background, the total chlorophyll content is greater than in comparable wild-type plants, and the Chl a/b ratio is reduced to wild-type levels or lower, suggesting that GLK proteins act to promote chlorophyll synthesis and LHC assembly (Waters et al, 2008, 2009). The GLK1 transcription factor acts directly on the promoters of genes encoding LHC proteins, especially those of LHCII, and key enzymes of the chlorophyll biosynthetic pathway (Waters et al, 2009). Accordingly, in GLK-overexpressing plants, transcript levels of these genes are significantly higher than in the wild type; crucially, however, genes encoding enzymes of the Calvin cycle are unaffected. Together, these findings imply that GLK proteins may be responsible for regulating the balance between the light-dependent stages of photosynthesis and carbon fixation. As GLK proteins regulate a large suite of genes involved in light-harvesting and thylakoid protein complexes, they represent a potent control point in the nucleus. Consistent with this notion, levels of GLK transcripts are sensitive to plastid-derived retrograde signals, at least one of which is GUN1 independent (Waters et al, 2009). In addition, GLK proteins act as cell autonomously, providing a means by which the specific photosynthetic requirements of each cell across the leaf can be regulated independently (Waters et al, 2008). Although it has yet to be established that whether redox-dependent retrograde signals affect GLK expression in mature plants, we propose a model in which GLK proteins act as key photosynthetic regulators as part of plant acclimation to variable environmental circumstances (Figure 3).


The making of a chloroplast.

Waters MT, Langdale JA - EMBO J. (2009)

A model for long-term photosynthetic regulation by GLK proteins. Under light-limiting conditions (left), the PET chain cannot supply sufficient ATP and reducing equivalents to the Calvin cycle, and, therefore, tends to be in an oxidized state. This prompts a chloroplast-derived signal to the nucleus (dashed arrow) that upregulates transcription of GLK genes. GLK proteins in turn bind to promoter sequences of genes that function in light harvesting, such as Lhcb and key chlorophyll biosynthetic genes. Transcript levels of these GLK target genes increase, leading to higher levels of the corresponding protein (Lhcb in this case), as depicted by the thicker arrow. Upregulation of chlorophyll biosynthesis and LHC assembly leads to higher specific chlorophyll levels, a lower Chl a/b ratio and more abundant grana (stacked discs of thylakoids), as observed in 35S:GLK transgenic plants. Increased grana abundance is associated with LHC trimers forming highly organized photosystem supercomplexes (Allen and Forsberg, 2001; Kovacs et al, 2006). When light is plentiful or even at inhibitory levels (right), the rate of CO2 fixation is insufficient to use all of the output of the light-harvesting reactions, resulting in an overly reduced PET. This triggers a negative signal (and/or absence of a positive signal) that leads to lower rates of GLK transcription. The accompanying decrease in Lhcb and chlorophyll-related gene transcripts eventually results in a fall in the light-harvesting components in the thylakoid membrane and lower chlorophyll levels. In turn, there are fewer, less stacked grana and a higher proportion of non-stacked, stromal lamellae, as observed in glk1 glk2 mutants. Together, these changes help to redress the imbalance between light absorption and CO2 fixation. Note that glk1 glk2 mutants are always paler than WT plants, suggesting that some degree of GLK activity is required under all conditions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2744177&req=5

f3: A model for long-term photosynthetic regulation by GLK proteins. Under light-limiting conditions (left), the PET chain cannot supply sufficient ATP and reducing equivalents to the Calvin cycle, and, therefore, tends to be in an oxidized state. This prompts a chloroplast-derived signal to the nucleus (dashed arrow) that upregulates transcription of GLK genes. GLK proteins in turn bind to promoter sequences of genes that function in light harvesting, such as Lhcb and key chlorophyll biosynthetic genes. Transcript levels of these GLK target genes increase, leading to higher levels of the corresponding protein (Lhcb in this case), as depicted by the thicker arrow. Upregulation of chlorophyll biosynthesis and LHC assembly leads to higher specific chlorophyll levels, a lower Chl a/b ratio and more abundant grana (stacked discs of thylakoids), as observed in 35S:GLK transgenic plants. Increased grana abundance is associated with LHC trimers forming highly organized photosystem supercomplexes (Allen and Forsberg, 2001; Kovacs et al, 2006). When light is plentiful or even at inhibitory levels (right), the rate of CO2 fixation is insufficient to use all of the output of the light-harvesting reactions, resulting in an overly reduced PET. This triggers a negative signal (and/or absence of a positive signal) that leads to lower rates of GLK transcription. The accompanying decrease in Lhcb and chlorophyll-related gene transcripts eventually results in a fall in the light-harvesting components in the thylakoid membrane and lower chlorophyll levels. In turn, there are fewer, less stacked grana and a higher proportion of non-stacked, stromal lamellae, as observed in glk1 glk2 mutants. Together, these changes help to redress the imbalance between light absorption and CO2 fixation. Note that glk1 glk2 mutants are always paler than WT plants, suggesting that some degree of GLK activity is required under all conditions.
Mentions: Arabidopsis glk1 glk2 double mutants are pale green and contain chloroplasts with non-stacked thylakoids and reduced levels of PET complexes (Fitter et al, 2002). Furthermore, they have an unusually high ratio of Chl a to Chl b: grown under identical conditions, the ratio in wild-type plants is ∼3.5 and in mutants ∼5.5 (Waters et al, 2009). This alteration is likely to result partly from reduced levels of LHC proteins, to which Chl b is exclusively bound (Green and Durnford, 1996). When GLK genes are overexpressed in a mutant background, the total chlorophyll content is greater than in comparable wild-type plants, and the Chl a/b ratio is reduced to wild-type levels or lower, suggesting that GLK proteins act to promote chlorophyll synthesis and LHC assembly (Waters et al, 2008, 2009). The GLK1 transcription factor acts directly on the promoters of genes encoding LHC proteins, especially those of LHCII, and key enzymes of the chlorophyll biosynthetic pathway (Waters et al, 2009). Accordingly, in GLK-overexpressing plants, transcript levels of these genes are significantly higher than in the wild type; crucially, however, genes encoding enzymes of the Calvin cycle are unaffected. Together, these findings imply that GLK proteins may be responsible for regulating the balance between the light-dependent stages of photosynthesis and carbon fixation. As GLK proteins regulate a large suite of genes involved in light-harvesting and thylakoid protein complexes, they represent a potent control point in the nucleus. Consistent with this notion, levels of GLK transcripts are sensitive to plastid-derived retrograde signals, at least one of which is GUN1 independent (Waters et al, 2009). In addition, GLK proteins act as cell autonomously, providing a means by which the specific photosynthetic requirements of each cell across the leaf can be regulated independently (Waters et al, 2008). Although it has yet to be established that whether redox-dependent retrograde signals affect GLK expression in mature plants, we propose a model in which GLK proteins act as key photosynthetic regulators as part of plant acclimation to variable environmental circumstances (Figure 3).

Bottom Line: The exchange of genetic information from the chloroplast to the nucleus has resulted in considerable co-ordination in the activities of these two organelles during all stages of plant development.In addition, we discuss the mechanisms through which chloroplasts develop in different cell types, namely cotyledons and the dimorphic chloroplasts of the C(4) plant maize.Finally, we discuss recent data that suggest the specific regulation of the light-dependent phases of photosynthesis, providing a means to optimize photosynthesis to varying light regimes.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, UK.

ABSTRACT
Since its endosymbiotic beginning, the chloroplast has become fully integrated into the biology of the host eukaryotic cell. The exchange of genetic information from the chloroplast to the nucleus has resulted in considerable co-ordination in the activities of these two organelles during all stages of plant development. Here, we give an overview of the mechanisms of light perception and the subsequent regulation of nuclear gene expression in the model plant Arabidopsis thaliana, and we cover the main events that take place when proplastids differentiate into chloroplasts. We also consider recent findings regarding signalling networks between the chloroplast and the nucleus during seedling development, and how these signals are modulated by light. In addition, we discuss the mechanisms through which chloroplasts develop in different cell types, namely cotyledons and the dimorphic chloroplasts of the C(4) plant maize. Finally, we discuss recent data that suggest the specific regulation of the light-dependent phases of photosynthesis, providing a means to optimize photosynthesis to varying light regimes.

Show MeSH
Related in: MedlinePlus