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Gerald E Edwards - One of the best experts on this subject based on the ideXlab platform.
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the unique structural and biochemical development of single cell c4 photosynthesis along longitudinal leaf gradients in bienertia sinuspersici and suaeda aralocaspica chenopodiaceae
Journal of Experimental Botany, 2016Co-Authors: Nuria K Koteyeva, Elena V. Voznesenskaya, James O Berry, Asaph B Cousins, Gerald E EdwardsAbstract:Temporal and spatial patterns of photosynthetic enzyme expression and structural maturation of Chlorenchyma cells along longitudinal developmental gradients were characterized in young leaves of two single cell C4 species, Bienertia sinuspersici and Suaeda aralocaspica Both species partition photosynthetic functions between distinct intracellular domains. In the C4-C domain, C4 acids are formed in the C4 cycle during capture of atmospheric CO2 by phosphoenolpyruvate carboxylase. In the C4-D domain, CO2 released in the C4 cycle via mitochondrial NAD-malic enzyme is refixed by Rubisco. Despite striking differences in origin and intracellular positioning of domains, these species show strong convergence in C4 developmental patterns. Both progress through a gradual developmental transition towards full C4 photosynthesis, with an associated increase in levels of photosynthetic enzymes. Analysis of longitudinal sections showed undeveloped domains at the leaf base, with Rubisco rbcL mRNA and protein contained within all chloroplasts. The two domains were first distinguishable in Chlorenchyma cells at the leaf mid-regions, but still contained structurally similar chloroplasts with equivalent amounts of rbcL mRNA and protein; while mitochondria had become confined to just one domain (proto-C4-D). The C4 state was fully formed towards the leaf tips, Rubisco transcripts and protein were compartmentalized specifically to structurally distinct chloroplasts in the C4-D domains indicating selective regulation of Rubisco expression may occur by control of transcription or stability of rbcL mRNA. Determination of CO2 compensation points showed young leaves were not functionally C4, consistent with cytological observations of the developmental progression from C3 default to intermediate to C4 photosynthesis.
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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C 4 Photosynthesis in Chenopodiaceae Species W
2013Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:shown to possess novel C 4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm
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structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single cell c 4 photosynthesis in bienertia sinuspersici
Planta, 2009Co-Authors: Joonho Park, Michael Knoblauch, Thomas W Okita, Gerald E EdwardsAbstract:Bienertia sinuspersici Akhani has an unusual mechanism of C4 photosynthesis which occurs within individual Chlorenchyma cells. To perform C4, the mature cells have two cytoplasmic compartments consisting of a central (CCC) and a peripheral (PCC) domain containing dimorphic chloroplasts which are interconnected by cytoplasmic channels. Based on leaf development studies, young Chlorenchyma cells have not developed the two cytoplasmic compartments and dimorphic chloroplasts. Fluorescent dyes which are targeted to membranes or to specific organelles were used to follow changes in cell structure and organelle distribution during formation of C4-type Chlorenchyma. Chlorenchyma cell development was divided into four stages: 1-the nucleus and chloroplasts occupy much of the cytoplasmic space and only small vacuoles are formed; 2-development of larger vacuoles, formation of a pre-CCC with some scattered chloroplasts; 3-the vacuole expands, cells have directional growth; 4-mature stage, cells have become elongated, with a distinctive CCC and PCC joined by interconnecting cytoplasmic channels. By staining vacuoles with a fluorescent dye and constructing 3D images of chloroplasts, and by microinjecting a fluorescence dye into the vacuole of living cells, it was demonstrated that the mature cell has only one vacuole, which is traversed by cytoplasmic channels connecting the CCC with the PCC. Immunofluorescent studies on isolated Chlorenchyma cells treated with cytoskeleton disrupting drugs suspended in different levels of osmoticum showed that both microtubules and actin filaments are important in maintaining the cytoplasmic domains. With prolonged exposure of plants to dim light, the cytoskeleton undergoes changes and there is a dramatic shift of the CCC from the center toward the distal end of the cell.
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the cytoskeleton maintains organelle partitioning required for single cell c4 photosynthesis in chenopodiaceae species
The Plant Cell, 2006Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm.
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differentiation of cellular and biochemical features of the single cell c4 syndrome during leaf development in bienertia cycloptera chenopodiaceae
American Journal of Botany, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Hossein Akhani, Vincent R. FranceschiAbstract:The terrestrial plant Bienertia cycloptera has been shown to accomplish C4 photosynthesis within individual Chlorenchyma cells by spatially separating the phases of carbon assimilation into distinct peripheral and central compartments. In this study, anatomical, physiological, and biochemical techniques were used to determine how this unique compartmentation develops. Western blots show ribulose-1,5-bisphosphate carboxylase (Rubisco) (chloroplastic) is present in the youngest leaves and increases during development, while levels of C4 enzymes—pyruvate,Pi dikinase (chloroplastic), phosphoenolpyruvate carboxylase (PEPC) (cytosol), and NAD-malic enzyme (mitochondrial)—increase later in development. Immunolocalization confirmed this for Rubisco and PEPC. The youngest Chlorenchyma cells have a central nucleus surrounded by monomorphic granal chloroplasts containing Rubisco. Later stages show progressive development of a central cytoplasmic compartment enriched with chloroplasts and mitochondria and of a peripheral cytoplasm with chloroplasts. A complex reticulum of connections between the compartments also developed and was characterized. d13C isotope analyses show mature leaves have distinct C4-type isotope composition, while the composition in younger leaves is ‘‘C 4like.’’ Based on the results, this form of single-cell C 4 photosynthesis develops from a common pool of organelles through partitioning to separate compartments, and the development of biochemically and ultrastructurally dimorphic chloroplasts.
Vincent R. Franceschi - One of the best experts on this subject based on the ideXlab platform.
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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C 4 Photosynthesis in Chenopodiaceae Species W
2013Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:shown to possess novel C 4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm
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the cytoskeleton maintains organelle partitioning required for single cell c4 photosynthesis in chenopodiaceae species
The Plant Cell, 2006Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm.
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differentiation of cellular and biochemical features of the single cell c4 syndrome during leaf development in bienertia cycloptera chenopodiaceae
American Journal of Botany, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Hossein Akhani, Vincent R. FranceschiAbstract:The terrestrial plant Bienertia cycloptera has been shown to accomplish C4 photosynthesis within individual Chlorenchyma cells by spatially separating the phases of carbon assimilation into distinct peripheral and central compartments. In this study, anatomical, physiological, and biochemical techniques were used to determine how this unique compartmentation develops. Western blots show ribulose-1,5-bisphosphate carboxylase (Rubisco) (chloroplastic) is present in the youngest leaves and increases during development, while levels of C4 enzymes—pyruvate,Pi dikinase (chloroplastic), phosphoenolpyruvate carboxylase (PEPC) (cytosol), and NAD-malic enzyme (mitochondrial)—increase later in development. Immunolocalization confirmed this for Rubisco and PEPC. The youngest Chlorenchyma cells have a central nucleus surrounded by monomorphic granal chloroplasts containing Rubisco. Later stages show progressive development of a central cytoplasmic compartment enriched with chloroplasts and mitochondria and of a peripheral cytoplasm with chloroplasts. A complex reticulum of connections between the compartments also developed and was characterized. d13C isotope analyses show mature leaves have distinct C4-type isotope composition, while the composition in younger leaves is ‘‘C 4like.’’ Based on the results, this form of single-cell C 4 photosynthesis develops from a common pool of organelles through partitioning to separate compartments, and the development of biochemically and ultrastructurally dimorphic chloroplasts.
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bienertia sinuspersici chenopodiaceae a new species from southwest asia and discovery of a third terrestrial c4 plant without kranz anatomy
Systematic Botany, 2005Co-Authors: Hossein Akhani, Elena V. Voznesenskaya, Gerald E Edwards, Vincent R. Franceschi, Joao Barroca, Nuria Koteeva, Seyed Mahmood Ghaffari, Hubert ZieglerAbstract:Our studies on the enigmatic genus Bienertia (Chenopodiaceae), with its C4 photosynthesis and lack of Kranz anatomy, led us to the discovery of a second species of this previously-supposed monotypic genus. The new species is named Bienertia sinuspersici after its main range around the Persian Gulf countries and the northern side of the Gulf of Oman. Bienertia sinuspersici occurs in hot climates and is a vicariant of Bienertia cycloptera, which is found at higher latitudes and elevations in temperate and cold deserts of the region. Like Bienertia cycloptera, the new species has unique Chlorenchyma cells with dimorphic chloroplasts and single cell C 4 photosynthesis. However, it differs anatomically by having mostly one to two layers of Chlorenchyma cells, versus two to three layers in Bienertia cycloptera. Furthermore, the new species has longer cotyledon leaves, larger seeds, larger flowers, and larger chromosomes, and differs in a set of micro-morphological features. All of this supports our conclusion that this widely distributed, novel plant is an overlooked new species. Bienertia sinuspersici grows well in very hot climates, under conditions which most species can barely tolerate. Its wide distribution indicates that its novel C 4 photosynthesis may confer advantages for CO2 fixation in these habitats not found in C4 species having con- ventional Kranz anatomy.
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functional compartmentation of c4 photosynthesis in the triple layered Chlorenchyma of aristida poaceae
Functional Plant Biology, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Vincent R. FranceschiAbstract:The genus Aristida (Poaceae), is composed of species that have Kranz anatomy and C4 photosynthesis. Kranz anatomy typically consists of two photosynthetic cell types: a layer of mesophyll cells where atmospheric CO2 is fixed into C4 acids, and an internal, Chlorenchymatous vascular bundle sheath to which C4 acids are transferred and then decarboxylated to donate CO2 to the C3 cycle. The anatomy of Aristida species is unusual as it has three distinct layers of Chlorenchyma cells surrounding the vascular tissue: an inner bundle sheath, an outer bundle sheath and the mesophyll cells. In this study of Aristida purpurea Nutt. var. longiseta, the functions of the three layers of Chlorenchyma cells relative to the C4 photosynthetic mechanism were determined using ultrastructural analysis, western blots, immunolocalisation of photosynthetic enzymes and starch histochemistry. The results indicate that mesophyll cells contain high levels of phosphoenolpyruvate carboxylase (PEPC) and pyruvate Pi dikinase (PPDK), and function to capture CO2 in the C4 cycle. The inner bundle sheath, which is high in Rubisco and contains NADP-malic enzyme and glycine decarboxylase, functions to transfer CO2 to the C3 cycle through decarboxylation of C4 acids and by decarboxylation of glycine in the glycolate pathway. The outer Chlorenchymatous sheath is where ADPG pyrophosphorylase is mainly located, and this cell layer functions as the primary site of starch storage. The outer sheath, which has low levels of Rubisco and PEPC, may also have a role in refixation of any CO2 that leaks from the inner bundle sheath cells.
Elena V. Voznesenskaya - One of the best experts on this subject based on the ideXlab platform.
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the unique structural and biochemical development of single cell c4 photosynthesis along longitudinal leaf gradients in bienertia sinuspersici and suaeda aralocaspica chenopodiaceae
Journal of Experimental Botany, 2016Co-Authors: Nuria K Koteyeva, Elena V. Voznesenskaya, James O Berry, Asaph B Cousins, Gerald E EdwardsAbstract:Temporal and spatial patterns of photosynthetic enzyme expression and structural maturation of Chlorenchyma cells along longitudinal developmental gradients were characterized in young leaves of two single cell C4 species, Bienertia sinuspersici and Suaeda aralocaspica Both species partition photosynthetic functions between distinct intracellular domains. In the C4-C domain, C4 acids are formed in the C4 cycle during capture of atmospheric CO2 by phosphoenolpyruvate carboxylase. In the C4-D domain, CO2 released in the C4 cycle via mitochondrial NAD-malic enzyme is refixed by Rubisco. Despite striking differences in origin and intracellular positioning of domains, these species show strong convergence in C4 developmental patterns. Both progress through a gradual developmental transition towards full C4 photosynthesis, with an associated increase in levels of photosynthetic enzymes. Analysis of longitudinal sections showed undeveloped domains at the leaf base, with Rubisco rbcL mRNA and protein contained within all chloroplasts. The two domains were first distinguishable in Chlorenchyma cells at the leaf mid-regions, but still contained structurally similar chloroplasts with equivalent amounts of rbcL mRNA and protein; while mitochondria had become confined to just one domain (proto-C4-D). The C4 state was fully formed towards the leaf tips, Rubisco transcripts and protein were compartmentalized specifically to structurally distinct chloroplasts in the C4-D domains indicating selective regulation of Rubisco expression may occur by control of transcription or stability of rbcL mRNA. Determination of CO2 compensation points showed young leaves were not functionally C4, consistent with cytological observations of the developmental progression from C3 default to intermediate to C4 photosynthesis.
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differentiation of cellular and biochemical features of the single cell c4 syndrome during leaf development in bienertia cycloptera chenopodiaceae
American Journal of Botany, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Hossein Akhani, Vincent R. FranceschiAbstract:The terrestrial plant Bienertia cycloptera has been shown to accomplish C4 photosynthesis within individual Chlorenchyma cells by spatially separating the phases of carbon assimilation into distinct peripheral and central compartments. In this study, anatomical, physiological, and biochemical techniques were used to determine how this unique compartmentation develops. Western blots show ribulose-1,5-bisphosphate carboxylase (Rubisco) (chloroplastic) is present in the youngest leaves and increases during development, while levels of C4 enzymes—pyruvate,Pi dikinase (chloroplastic), phosphoenolpyruvate carboxylase (PEPC) (cytosol), and NAD-malic enzyme (mitochondrial)—increase later in development. Immunolocalization confirmed this for Rubisco and PEPC. The youngest Chlorenchyma cells have a central nucleus surrounded by monomorphic granal chloroplasts containing Rubisco. Later stages show progressive development of a central cytoplasmic compartment enriched with chloroplasts and mitochondria and of a peripheral cytoplasm with chloroplasts. A complex reticulum of connections between the compartments also developed and was characterized. d13C isotope analyses show mature leaves have distinct C4-type isotope composition, while the composition in younger leaves is ‘‘C 4like.’’ Based on the results, this form of single-cell C 4 photosynthesis develops from a common pool of organelles through partitioning to separate compartments, and the development of biochemically and ultrastructurally dimorphic chloroplasts.
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bienertia sinuspersici chenopodiaceae a new species from southwest asia and discovery of a third terrestrial c4 plant without kranz anatomy
Systematic Botany, 2005Co-Authors: Hossein Akhani, Elena V. Voznesenskaya, Gerald E Edwards, Vincent R. Franceschi, Joao Barroca, Nuria Koteeva, Seyed Mahmood Ghaffari, Hubert ZieglerAbstract:Our studies on the enigmatic genus Bienertia (Chenopodiaceae), with its C4 photosynthesis and lack of Kranz anatomy, led us to the discovery of a second species of this previously-supposed monotypic genus. The new species is named Bienertia sinuspersici after its main range around the Persian Gulf countries and the northern side of the Gulf of Oman. Bienertia sinuspersici occurs in hot climates and is a vicariant of Bienertia cycloptera, which is found at higher latitudes and elevations in temperate and cold deserts of the region. Like Bienertia cycloptera, the new species has unique Chlorenchyma cells with dimorphic chloroplasts and single cell C 4 photosynthesis. However, it differs anatomically by having mostly one to two layers of Chlorenchyma cells, versus two to three layers in Bienertia cycloptera. Furthermore, the new species has longer cotyledon leaves, larger seeds, larger flowers, and larger chromosomes, and differs in a set of micro-morphological features. All of this supports our conclusion that this widely distributed, novel plant is an overlooked new species. Bienertia sinuspersici grows well in very hot climates, under conditions which most species can barely tolerate. Its wide distribution indicates that its novel C 4 photosynthesis may confer advantages for CO2 fixation in these habitats not found in C4 species having con- ventional Kranz anatomy.
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functional compartmentation of c4 photosynthesis in the triple layered Chlorenchyma of aristida poaceae
Functional Plant Biology, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Vincent R. FranceschiAbstract:The genus Aristida (Poaceae), is composed of species that have Kranz anatomy and C4 photosynthesis. Kranz anatomy typically consists of two photosynthetic cell types: a layer of mesophyll cells where atmospheric CO2 is fixed into C4 acids, and an internal, Chlorenchymatous vascular bundle sheath to which C4 acids are transferred and then decarboxylated to donate CO2 to the C3 cycle. The anatomy of Aristida species is unusual as it has three distinct layers of Chlorenchyma cells surrounding the vascular tissue: an inner bundle sheath, an outer bundle sheath and the mesophyll cells. In this study of Aristida purpurea Nutt. var. longiseta, the functions of the three layers of Chlorenchyma cells relative to the C4 photosynthetic mechanism were determined using ultrastructural analysis, western blots, immunolocalisation of photosynthetic enzymes and starch histochemistry. The results indicate that mesophyll cells contain high levels of phosphoenolpyruvate carboxylase (PEPC) and pyruvate Pi dikinase (PPDK), and function to capture CO2 in the C4 cycle. The inner bundle sheath, which is high in Rubisco and contains NADP-malic enzyme and glycine decarboxylase, functions to transfer CO2 to the C3 cycle through decarboxylation of C4 acids and by decarboxylation of glycine in the glycolate pathway. The outer Chlorenchymatous sheath is where ADPG pyrophosphorylase is mainly located, and this cell layer functions as the primary site of starch storage. The outer sheath, which has low levels of Rubisco and PEPC, may also have a role in refixation of any CO2 that leaks from the inner bundle sheath cells.
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proof of c4 photosynthesis without kranz anatomy in bienertia cycloptera chenopodiaceae
Plant Journal, 2002Co-Authors: Elena V. Voznesenskaya, Vincent R. Franceschi, Helmut Freitag, Olavi Kiirats, Elena G Artyusheva, Gerald E EdwardsAbstract:Summary Kranz anatomy, with its separation of elements of the C 4 pathway between two cells, has been an accepted criterion for function of C4 photosynthesis in terrestrial plants. However, Bienertia cycloptera (Chenopodiaceae), which grows in salty depressions of Central Asian semi-deserts, has unusual Chlorenchyma, lacks Kranz anatomy, but has photosynthetic features of C 4 plants. Its photosynthetic response to varying CO2 and O2 is typical of C4 plants having Kranz anatomy. Lack of night-time CO2 fixation indicates it is not acquiring carbon by Crassulacean acid metabolism. This species exhibits an independent, novel solution to function of the C4 mechanism through spatial compartmentation of dimorphic chloroplasts, other organelles and photosynthetic enzymes in distinct positions within a single Chlorenchyma cell. The Chlorenchyma cells have a large, spherical central cytoplasmic compartment interconnected by cytoplasmic channels through the vacuole to the peripheral cytoplasm. This compartment is filled with mitochondria and granal chloroplasts, while the peripheral cytoplasm apparently lacks mitochondria and has grana-deficient chloroplasts. Immunolocalization studies show enzymes compartmentalized selectively in the CC compartment, including Rubisco in chloroplasts, and NAD-malic enzyme and glycine decarboxylase in mitochondria, whereas pyruvate, Pi dikinase of the C 4 cycle is localized selectively in peripheral chloroplasts. Phosphoenolpyruvate carboxylase, a cytosolic C4 cycle enzyme, is enriched in the peripheral cytoplasm. Our results show Bienertia utilizes strict compartmentation of organelles and enzymes within a single cell to effectively mimic the spatial separation of Kranz anatomy, allowing it to function as a C 4 plant having suppressed photorespiration; this raises interesting questions about evolution of C 4 mechanisms.
Simon D X Chuong - One of the best experts on this subject based on the ideXlab platform.
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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C 4 Photosynthesis in Chenopodiaceae Species W
2013Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:shown to possess novel C 4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm
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protoplast isolation and transient gene expression in the single cell c4 species bienertia sinuspersici
Plant Cell Reports, 2011Co-Authors: Shiu-cheung Lung, Makoto Yanagisawa, Simon D X ChuongAbstract:Although transient gene expression using reporters such as green fluorescent protein is a versatile tool for examining gene functions and intracellular protein trafficking, the establishment of a highly efficient gene manipulation method remains a challenge in many plant species. A reliable transformation protocol has not yet been established for the three single-cell C4 species, despite their potential of serving as model systems for their extraordinary C4 photosynthetic metabolism. We report the first protocol optimized for isolating a large-scale and homogenous population of protoplasts from Chlorenchyma cells of the single-cell C4 species Bienertia sinuspersici. Cytochemical staining confirmed the preservation of the unusual subcellular compartmentation of organelles in Chlorenchyma cells after cell wall digestion. Approximately 84% of isolated protoplasts expressed the reporter fluorescent protein following our optimized polyethylene glycol-mediated transfection procedures. Fluorescent fusion protein tagged with various intracellular sorting signals demonstrated potential use of the transient gene expression system in subcellular protein localization and organelle dynamics studies. Further applications of the current protoplast isolation and transfection techniques in understanding the novel single-cell C4 photosynthetic mechanism are discussed.
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the cytoskeleton maintains organelle partitioning required for single cell c4 photosynthesis in chenopodiaceae species
The Plant Cell, 2006Co-Authors: Simon D X Chuong, Vincent R. Franceschi, Gerald E EdwardsAbstract:Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single Chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm.
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differentiation of cellular and biochemical features of the single cell c4 syndrome during leaf development in bienertia cycloptera chenopodiaceae
American Journal of Botany, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Hossein Akhani, Vincent R. FranceschiAbstract:The terrestrial plant Bienertia cycloptera has been shown to accomplish C4 photosynthesis within individual Chlorenchyma cells by spatially separating the phases of carbon assimilation into distinct peripheral and central compartments. In this study, anatomical, physiological, and biochemical techniques were used to determine how this unique compartmentation develops. Western blots show ribulose-1,5-bisphosphate carboxylase (Rubisco) (chloroplastic) is present in the youngest leaves and increases during development, while levels of C4 enzymes—pyruvate,Pi dikinase (chloroplastic), phosphoenolpyruvate carboxylase (PEPC) (cytosol), and NAD-malic enzyme (mitochondrial)—increase later in development. Immunolocalization confirmed this for Rubisco and PEPC. The youngest Chlorenchyma cells have a central nucleus surrounded by monomorphic granal chloroplasts containing Rubisco. Later stages show progressive development of a central cytoplasmic compartment enriched with chloroplasts and mitochondria and of a peripheral cytoplasm with chloroplasts. A complex reticulum of connections between the compartments also developed and was characterized. d13C isotope analyses show mature leaves have distinct C4-type isotope composition, while the composition in younger leaves is ‘‘C 4like.’’ Based on the results, this form of single-cell C 4 photosynthesis develops from a common pool of organelles through partitioning to separate compartments, and the development of biochemically and ultrastructurally dimorphic chloroplasts.
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functional compartmentation of c4 photosynthesis in the triple layered Chlorenchyma of aristida poaceae
Functional Plant Biology, 2005Co-Authors: Elena V. Voznesenskaya, Simon D X Chuong, Nuria K Koteyeva, Gerald E Edwards, Vincent R. FranceschiAbstract:The genus Aristida (Poaceae), is composed of species that have Kranz anatomy and C4 photosynthesis. Kranz anatomy typically consists of two photosynthetic cell types: a layer of mesophyll cells where atmospheric CO2 is fixed into C4 acids, and an internal, Chlorenchymatous vascular bundle sheath to which C4 acids are transferred and then decarboxylated to donate CO2 to the C3 cycle. The anatomy of Aristida species is unusual as it has three distinct layers of Chlorenchyma cells surrounding the vascular tissue: an inner bundle sheath, an outer bundle sheath and the mesophyll cells. In this study of Aristida purpurea Nutt. var. longiseta, the functions of the three layers of Chlorenchyma cells relative to the C4 photosynthetic mechanism were determined using ultrastructural analysis, western blots, immunolocalisation of photosynthetic enzymes and starch histochemistry. The results indicate that mesophyll cells contain high levels of phosphoenolpyruvate carboxylase (PEPC) and pyruvate Pi dikinase (PPDK), and function to capture CO2 in the C4 cycle. The inner bundle sheath, which is high in Rubisco and contains NADP-malic enzyme and glycine decarboxylase, functions to transfer CO2 to the C3 cycle through decarboxylation of C4 acids and by decarboxylation of glycine in the glycolate pathway. The outer Chlorenchymatous sheath is where ADPG pyrophosphorylase is mainly located, and this cell layer functions as the primary site of starch storage. The outer sheath, which has low levels of Rubisco and PEPC, may also have a role in refixation of any CO2 that leaks from the inner bundle sheath cells.
Ching-i Peng - One of the best experts on this subject based on the ideXlab platform.
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natural foliar variegation without costs the case of begonia
Annals of Botany, 2012Co-Authors: Chiourong Sheue, Peter Chesson, Shang Horng Pao, Lee-feng Chien, Ching-i PengAbstract:†Background and Aims Foliar variegation is recognized as arising from two major mechanisms: leaf structure and pigment-related variegation. Begonia has species with a variety of natural foliar variegation patterns, providing diverse examples of this phenomenon. The aims of this work are to elucidate the mechanisms underlying different foliar variegation patterns in Begonia and to determine their physiological consequences. †Methods Six species and one cultivar of Begonia were investigated. Light and electron microscopy revealed the leaf structure and ultrastructure of chloroplasts in green and light areas of variegated leaves. Maximum quantum yields of photosystem II were measured by chlorophyll fluorescence. Comparison with a cultivar of Ficus revealed key features distinguishing variegation mechanisms. †Key Results Intercellular space above the Chlorenchyma is the mechanism of variegation in these Begonia. This intercellular space can be located (a) below the adaxial epidermis or (b) below the adaxial water storage tissue (the first report for any taxa), creating light areas on a leaf. In addition, Chlorenchyma cell shape and chloroplast distribution within Chlorenchyma cells differ between light and green areas. Chloroplasts from both areas showed dense stacking of grana and stromathylakoid membranes. The maximum quantum yield did not differ significantly between these areas, suggesting minimal loss of function with variegation. However, the absence of chloroplasts in light areas of leaves in the Ficus cultivar led to an extremely low quantum yield. †Conclusions Variegation in these Begonia is structural, where light areas are created by internal reflection between air spaces and cells in a leaf. Two forms of air space structural variegation occur, distinguished by the location of the air spaces. Both forms may have a common origin in development where dermal tissue becomes loosely connected to mesophyll. Photosynthetic functioning is retained in light areas, and these areas do not include primary veins, potentially limiting the costs of variegation.
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Natural foliar variegation without costs? The case of Begonia
Annals of botany, 2012Co-Authors: Chiourong Sheue, Peter Chesson, Shang Horng Pao, Lee-feng Chien, Ching-i PengAbstract:Foliar variegation is recognized as arising from two major mechanisms: leaf structure and pigment-related variegation. Begonia has species with a variety of natural foliar variegation patterns, providing diverse examples of this phenomenon. The aims of this work are to elucidate the mechanisms underlying different foliar variegation patterns in Begonia and to determine their physiological consequences. Six species and one cultivar of Begonia were investigated. Light and electron microscopy revealed the leaf structure and ultrastructure of chloroplasts in green and light areas of variegated leaves. Maximum quantum yields of photosystem II were measured by chlorophyll fluorescence. Comparison with a cultivar of Ficus revealed key features distinguishing variegation mechanisms. Intercellular space above the Chlorenchyma is the mechanism of variegation in these Begonia. This intercellular space can be located (a) below the adaxial epidermis or (b) below the adaxial water storage tissue (the first report for any taxa), creating light areas on a leaf. In addition, Chlorenchyma cell shape and chloroplast distribution within Chlorenchyma cells differ between light and green areas. Chloroplasts from both areas showed dense stacking of grana and stroma thylakoid membranes. The maximum quantum yield did not differ significantly between these areas, suggesting minimal loss of function with variegation. However, the absence of chloroplasts in light areas of leaves in the Ficus cultivar led to an extremely low quantum yield. Variegation in these Begonia is structural, where light areas are created by internal reflection between air spaces and cells in a leaf. Two forms of air space structural variegation occur, distinguished by the location of the air spaces. Both forms may have a common origin in development where dermal tissue becomes loosely connected to mesophyll. Photosynthetic functioning is retained in light areas, and these areas do not include primary veins, potentially limiting the costs of variegation.