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Veronica G Maurino - One of the best experts on this subject based on the ideXlab platform.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cell mitochondria and evolved via association of differentially adapted subunits
The Plant Cell, 2021Co-Authors: Meike Hudig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In plant mitochondria, nicotinamide adenine dinucleotide phosphate (NAD)-malic enzyme (NAD-ME) has a housekeeping function in malate respiration. In different plant lineages, NAD-ME was independently co-opted in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-MEα, NAD-MEβ1, and NAD-MEβ2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 species Tarenaya hassleriana. In Tarenaya hassleriana, the NAD-ME housekeeping function is performed by two heteromers, NAD-MEα/β1 and NAD-MEα/β2, with similar biochemical properties. In both C4 species, this role is restricted to NAD-MEα/β2. In the C4 species, NAD-MEα/β1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-MEα/β1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, NAD-MEβ1 lost its catalytic activity; its contribution to the enzymatic activity results from a stabilizing effect on the associated α-subunit and the adquisition of regulatory properties. We conclude that in Bundle Sheath Cell mitochondria of C4 species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a housekeeping enzyme coexist and are performed by isoforms that combine the same α subunit with differentially adapted β subunits.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cells mitochondria and evolved via association of differentially adapted subunits
bioRxiv, 2021Co-Authors: M Huedig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In different lineages of Cleomaceae, NAD-malic enzyme (NAD-ME) was independently co-opted to participate in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-ME, NAD-ME{beta}1, and NAD-ME{beta}2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 Cleome species Tarenaya hassleriana. In the latter C3 species, the NAD-ME housekeeping function is performed by two heteromers, NAD-ME/{beta}1 and NAD-ME/{beta}2, with similar biochemical properties. In both C4 species analyzed, this role is restricted the NAD-ME/{beta}2 heteromer. In the C4 species, NAD-ME/{beta}1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-ME/{beta}1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, GgNAD-ME{beta}1and CaNAD-ME{beta}1 lost their catalytic activity; their contribution to enzymatic activity results from a stabilizing effect on the associated -subunit. We conclude that in Bundle Sheath Cell mitochondria of C4 Cleome species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a tricarboxylic acid cycle-associated housekeeping enzyme coexist and are performed by isoforms that combine the same subunit with differentially adapted {beta} subunits.
Holger Gohlke - One of the best experts on this subject based on the ideXlab platform.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cell mitochondria and evolved via association of differentially adapted subunits
The Plant Cell, 2021Co-Authors: Meike Hudig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In plant mitochondria, nicotinamide adenine dinucleotide phosphate (NAD)-malic enzyme (NAD-ME) has a housekeeping function in malate respiration. In different plant lineages, NAD-ME was independently co-opted in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-MEα, NAD-MEβ1, and NAD-MEβ2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 species Tarenaya hassleriana. In Tarenaya hassleriana, the NAD-ME housekeeping function is performed by two heteromers, NAD-MEα/β1 and NAD-MEα/β2, with similar biochemical properties. In both C4 species, this role is restricted to NAD-MEα/β2. In the C4 species, NAD-MEα/β1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-MEα/β1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, NAD-MEβ1 lost its catalytic activity; its contribution to the enzymatic activity results from a stabilizing effect on the associated α-subunit and the adquisition of regulatory properties. We conclude that in Bundle Sheath Cell mitochondria of C4 species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a housekeeping enzyme coexist and are performed by isoforms that combine the same α subunit with differentially adapted β subunits.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cells mitochondria and evolved via association of differentially adapted subunits
bioRxiv, 2021Co-Authors: M Huedig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In different lineages of Cleomaceae, NAD-malic enzyme (NAD-ME) was independently co-opted to participate in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-ME, NAD-ME{beta}1, and NAD-ME{beta}2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 Cleome species Tarenaya hassleriana. In the latter C3 species, the NAD-ME housekeeping function is performed by two heteromers, NAD-ME/{beta}1 and NAD-ME/{beta}2, with similar biochemical properties. In both C4 species analyzed, this role is restricted the NAD-ME/{beta}2 heteromer. In the C4 species, NAD-ME/{beta}1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-ME/{beta}1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, GgNAD-ME{beta}1and CaNAD-ME{beta}1 lost their catalytic activity; their contribution to enzymatic activity results from a stabilizing effect on the associated -subunit. We conclude that in Bundle Sheath Cell mitochondria of C4 Cleome species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a tricarboxylic acid cycle-associated housekeeping enzyme coexist and are performed by isoforms that combine the same subunit with differentially adapted {beta} subunits.
Tammy L Sage - One of the best experts on this subject based on the ideXlab platform.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cell mitochondria and evolved via association of differentially adapted subunits
The Plant Cell, 2021Co-Authors: Meike Hudig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In plant mitochondria, nicotinamide adenine dinucleotide phosphate (NAD)-malic enzyme (NAD-ME) has a housekeeping function in malate respiration. In different plant lineages, NAD-ME was independently co-opted in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-MEα, NAD-MEβ1, and NAD-MEβ2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 species Tarenaya hassleriana. In Tarenaya hassleriana, the NAD-ME housekeeping function is performed by two heteromers, NAD-MEα/β1 and NAD-MEα/β2, with similar biochemical properties. In both C4 species, this role is restricted to NAD-MEα/β2. In the C4 species, NAD-MEα/β1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-MEα/β1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, NAD-MEβ1 lost its catalytic activity; its contribution to the enzymatic activity results from a stabilizing effect on the associated α-subunit and the adquisition of regulatory properties. We conclude that in Bundle Sheath Cell mitochondria of C4 species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a housekeeping enzyme coexist and are performed by isoforms that combine the same α subunit with differentially adapted β subunits.
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respiratory and c4 photosynthetic nad malic enzyme coexist in Bundle Sheath Cells mitochondria and evolved via association of differentially adapted subunits
bioRxiv, 2021Co-Authors: M Huedig, Marcos A Tronconi, Juan Pablo Zubimendi, Tammy L Sage, Gereon Poschmann, David Bickel, Holger Gohlke, Veronica G MaurinoAbstract:In different lineages of Cleomaceae, NAD-malic enzyme (NAD-ME) was independently co-opted to participate in C4 photosynthesis. In the C4 Cleome species Gynandropsis gynandra and Cleome angustifolia, all NAD-ME genes (NAD-ME, NAD-ME{beta}1, and NAD-ME{beta}2) were affected by C4 evolution and are expressed at higher levels than their orthologs in the C3 Cleome species Tarenaya hassleriana. In the latter C3 species, the NAD-ME housekeeping function is performed by two heteromers, NAD-ME/{beta}1 and NAD-ME/{beta}2, with similar biochemical properties. In both C4 species analyzed, this role is restricted the NAD-ME/{beta}2 heteromer. In the C4 species, NAD-ME/{beta}1 is exclusively present in the leaves, where it accounts for most of the enzymatic activity. GgNAD-ME/{beta}1 exhibits high catalytic efficiency and is differentially activated by the C4 intermediate aspartate, confirming its role as the C4-decarboxylase. During C4 evolution, GgNAD-ME{beta}1and CaNAD-ME{beta}1 lost their catalytic activity; their contribution to enzymatic activity results from a stabilizing effect on the associated -subunit. We conclude that in Bundle Sheath Cell mitochondria of C4 Cleome species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a tricarboxylic acid cycle-associated housekeeping enzyme coexist and are performed by isoforms that combine the same subunit with differentially adapted {beta} subunits.
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Individual maize chromosomes in the C(3) plant oat can increase Bundle Sheath Cell size and vein density.
Plant physiology, 2012Co-Authors: Ben J. Tolley, Jane A. Langdale, Tammy L Sage, Julian M. HibberdAbstract:C(4) photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, Cell biology, and development of leaves. The characteristic "Kranz" anatomy of most C(4) leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C(4)) chromosomes to be investigated in an oat (Avena sativa; C(3)) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C(4) characteristics into oat and have associated any C(4)-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C(4) biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C(3) oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2'-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger Bundle Sheath Cells with increased Cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C(4) biology could be integrated into leaves of C(3) crops.
Robert T Furbank - One of the best experts on this subject based on the ideXlab platform.
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diffusion of co2 across the mesophyll Bundle Sheath Cell interface in a c4 plant with genetically reduced pep carboxylase activity
Plant Physiology, 2018Co-Authors: Hugo Alonsocantabrana, Susanne Von Caemmerer, Asaph B Cousins, Florence R Danila, Timothy Ryan, Robert E Sharwood, Robert T FurbankAbstract:Phosphoenolpyruvate carboxylase (PEPC), localized to the cytosol of the mesophyll Cell, catalyzes the first carboxylation step of the C4 photosynthetic pathway. Here, we used RNA interference to target the cytosolic photosynthetic PEPC isoform in Setaria viridis and isolated independent transformants with very low PEPC activities. These plants required high ambient CO2 concentrations for growth, consistent with the essential role of PEPC in C4 photosynthesis. The combination of estimating direct CO2 fixation by the Bundle Sheath using gas-exchange measurements and modeling C4 photosynthesis with low PEPC activity allowed the calculation of Bundle Sheath conductance to CO2 diffusion (gbs ) in the progeny of these plants. Measurements made at a range of temperatures suggested no or negligible effect of temperature on gbs depending on the technique used to calculate gbs Anatomical measurements revealed that plants with reduced PEPC activity had reduced Cell wall thickness and increased plasmodesmata (PD) density at the mesophyll-Bundle Sheath (M-BS) Cell interface, whereas we observed little difference in these parameters at the mesophyll-mesophyll Cell interface. The increased PD density at the M-BS interface was largely driven by an increase in the number of PD pit fields (cluster of PDs) rather than an increase in PD per pit field or the size of pit fields. The correlation of gbs with Bundle Sheath surface area per leaf area and PD area per M-BS area showed that these parameters and Cell wall thickness are important determinants of gbs It is intriguing to speculate that PD development is responsive to changes in C4 photosynthetic flux.
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expression of tobacco carbonic anhydrase in the c4 dicot flaveria bidentis leads to increased leakiness of the Bundle Sheath and a defective co2 concentrating mechanism
Plant Physiology, 1998Co-Authors: Martha Ludwig, Susanne Von Caemmerer, Dean G Price, Murray R Badger, Robert T FurbankAbstract:Flaveria bidentis (L.) Kuntze, a C4 dicot, was genetically transformed with a construct encoding the mature form of tobacco (Nicotiana tabacum L.) carbonic anhydrase (CA) under the control of a strong constitutive promoter. Expression of the tobacco CA was detected in transformant whole-leaf and Bundle-Sheath Cell (bsc) extracts by immunoblot analysis. Whole-leaf extracts from two CA-transformed lines demonstrated 10% to 50% more CA activity on a ribulose-1,5-bisphosphate carboxylase/oxygenase-site basis than the extracts from transformed, nonexpressing control plants, whereas 3 to 5 times more activity was measured in CA transformant bsc extracts. This increased CA activity resulted in plants with moderately reduced rates of CO2 assimilation (A) and an appreciable increase in C isotope discrimination compared with the controls. With increasing O2 concentrations up to 40% (v/v), a greater inhibition of A was found for transformants than for wild-type plants; however, the quantum yield of photosystem II did not differ appreciably between these two groups over the O2 levels tested. The quantum yield of photosystem II-to-A ratio suggested that at higher O2 concentrations, the transformants had increased rates of photorespiration. Thus, the expression of active tobacco CA in the cytosol of F. bidentis bsc and mesophyll Cells perturbed the C4 CO2-concentrating mechanism by increasing the permeability of the bsc to inorganic C and, thereby, decreasing the availability of CO2 for photosynthetic assimilation by ribulose-1,5-bisphosphate carboxylase/oxygenase.
Thomas P. Brutnell - One of the best experts on this subject based on the ideXlab platform.
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Review papeR Bundle Sheath suberization in grass leaves: multiple barriers to characterization
2016Co-Authors: Rachel A. Mertz, Thomas P. BrutnellAbstract:High-yielding, stress-tolerant grass crops are essential to meet future food and energy demands. Efforts are under-way to engineer improved varieties of the C3 cereal crop rice by introducing NADP-malic enzyme C4 photosynthesis using maize as a model system. However, several modifications to the rice leaf vasculature are potentially necessary, including the introduction of suberin lamellae into the Bundle Sheath Cell walls. Suberized Cell walls are ubiquitous in the root endodermis of all grasses, and developmental similarities are apparent between endodermis and Bundle Sheath Cell walls. Nonetheless, there is considerable heterogeneity in Sheath Cell development and suberin composi-tion both within and between grass taxa. The effect of this variation on physiological function remains ambiguous over forty years after suberin lamellae were initially proposed to regulate solute and photoassimilate fluxes and C4 gas exchange. Interspecies variation has confounded efforts to ascribe physiological differences specifically to the pres-ence or absence of suberin lamellae. Thus, specific perturbation of suberization within a uniform genetic background is needed, but, until recently, the genetic resources to manipulate suberin composition in the grasses were largely unavailable. The recent dissection of the suberin biosynthesis pathway in model dicots and the identification of sev-eral promising candidate genes in model grasses will facilitate the characterization of the first suberin biosynthesis genes in a monocot. Much remains to be learned about the role of Bundle Sheath suberization in leaf physiology, but the stage is set for significant advances in the near future
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Bundle Sheath suberization in grass leaves multiple barriers to characterization
Journal of Experimental Botany, 2014Co-Authors: Rachel A. Mertz, Thomas P. BrutnellAbstract:High-yielding, stress-tolerant grass crops are essential to meet future food and energy demands. Efforts are underway to engineer improved varieties of the C3 cereal crop rice by introducing NADP-malic enzyme C4 photosynthesis using maize as a model system. However, several modifications to the rice leaf vasculature are potentially necessary, including the introduction of suberin lamellae into the Bundle Sheath Cell walls. Suberized Cell walls are ubiquitous in the root endodermis of all grasses, and developmental similarities are apparent between endodermis and Bundle Sheath Cell walls. Nonetheless, there is considerable heterogeneity in Sheath Cell development and suberin composition both within and between grass taxa. The effect of this variation on physiological function remains ambiguous over forty years after suberin lamellae were initially proposed to regulate solute and photoassimilate fluxes and C4 gas exchange. Interspecies variation has confounded efforts to ascribe physiological differences specifically to the presence or absence of suberin lamellae. Thus, specific perturbation of suberization within a uniform genetic background is needed, but, until recently, the genetic resources to manipulate suberin composition in the grasses were largely unavailable. The recent dissection of the suberin biosynthesis pathway in model dicots and the identification of several promising candidate genes in model grasses will facilitate the characterization of the first suberin biosynthesis genes in a monocot. Much remains to be learned about the role of Bundle Sheath suberization in leaf physiology, but the stage is set for significant advances in the near future.
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Bundle Sheath defective2, a Mutation That Disrupts the Coordinated Development of Bundle Sheath and Mesophyll Cells in the Maize Leaf.
The Plant cell, 1996Co-Authors: Ronelle Roth, Lisa N. Hall, Thomas P. Brutnell, Jane A. LangdaleAbstract:Within the maize leaf primordium, coordinated Cell division and differentiation patterns result in the development of two morphologically and biochemically distinct photosynthetic Cell types, the Bundle Sheath and the mesophyll. The Bundle Sheath defective2-mutablel (bsd2-ml) mutation specifically disrupts C4 differentiation in Bundle Sheath Cells in that the levels of Bundle Sheath Cell-specific photosynthetic enzymes are reduced and the Bundle Sheath chloroplast structure is aberrant. In contrast, mesophyll Cell-specific enzymes accumulate to normal levels, and the mesophyll Cell chloroplast structure is not perturbed. Throughout mutant leaf development, the large and small subunits of ribulose bisphosphate carboxylase are absent; however, both rbcL and RbcS transcripts accumulate. Moreover, chloroplast-encoded rbcL transcripts accumulate ectopically in mesophyll Cells. Although the Bundle Sheath Cell chloroplast structure deteriorates rapidly when plants are exposed to light, this deterioration is most likely a secondary effect resulting from Cell-specific photooxidative damage. Therefore, we propose that the Bsd2 gene plays a direct role in the post-transcriptional control of rbcL transcript accumulation and/or translation, both in Bundle Sheath and mesophyll Cells, and an indirect role in the maintenance of Bundle Sheath Cell chloroplast structure.
