scholarly journals Understanding C4 photosynthesis in Setaria by a proteomic and kinetic approach

2021 ◽  
Author(s):  
Paula Calace ◽  
Tomás Tonetti ◽  
Ezequiel Margarit ◽  
Carlos María Figueroa ◽  
Carlos Lobertti ◽  
...  

Plants performing C4 photosynthesis have a higher productivity per crop area related to an optimized use of water and nutrients. This is achieved through a series of anatomical and biochemical features that allow the concentration of CO2 around RuBisCO. In C4 plants the photosynthetic reactions are distributed between two cell types, they initially fix the carbon to C4 acids within the mesophyll cells (M) and then transport these compounds to the bundle sheath cells (BS), where they are decarboxylated so that the resulting CO2 is incorporated into the Calvin cycle (CC). This work is focused on the comparative analysis of the proteins present in M and BS of Setaria viridis, a C4 model close relative of several major feed, fuel, and bioenergy grasses. The integration of kinetic and proteomic approaches agrees that the C4 compound malate is mainly decarboxylated in the chloroplasts of BS cells by NADP-malic enzyme (NADP-ME). Besides, NAD-malic enzyme (NAD-ME) located in the mitochondria could also contribute to the C4 carbon shuttle. We presented evidence of metabolic strategies that involve chloroplastic, mitochondrial and peroxisomal proteins to avoid the leakage of C4 intermediates in order to sustain an efficient photosynthetic performance.

1976 ◽  
Vol 3 (6) ◽  
pp. 863 ◽  
Author(s):  
E Repo ◽  
MD Hatch

Monocotyledonous C4 species classified as NADP-ME-type transfer malate from mesophyll to bundle sheath cells where this acid is decarboxylated via NADP malic enzyme (EC 1.1.1.40) to yield pyruvate and CO2. The dicotyledon G. celosioides is most appropriately classified in thls group on the basis of high leaf activities of NADP malic enzyme and NADP malate dehydrogenase (EC 1.1.1.82). However, this species contains high aspartate aminotransferase (EC 2.6.1.1) and alanine aminotransferase (EC 2.6.1.2) activities and centripetally located bundle sheath chloroplasts, features more typical of other groups of C4 species that cycle aspartate and alanine between mesophyll and bundle sheath cells. During the present study, we found that these aminotransferases and NADP malate dehydrogenase were predominantly located in mesophyll cells, that malate was the major C4 acid labelled when leaves were exposed to 14CO2, and that label was initially lost most rapidly from the C-4 of malate during a chase in 12CO2. These results are consistent with the major route of photosynthetic metabolism being the same as that operative in other NADP-ME-type species, although this may be supplemented by a minor route utilizing aspartate. In contrast to monocotyledonous NADP-ME-type C4 species, isolated bundle sheath cells from G. celosioides were capable of rapid photoreduction of NADP as judged by products formed during assimilation of 14CO2 and their capacity for light-dependent oxygen evolution. This was related to a relatively high frequency of single unstacked granum in the chloroplasts of these cells.


1973 ◽  
Vol 26 (5) ◽  
pp. 1015 ◽  
Author(s):  
CK Pallaghy

Small sections of leaves were floated on distilled water under either light or dark conditions, and were freeze-substituted in a 1 % solution of osmium tetroxide in acetone at -78�C followed by embedding in an epoxy resin. Approximately I-11m-thick sections were cut using a dry diamond knife and examined by scanning transmission electron microscopy. The relative concentrations of potassium and chloride in subcellular compartments were determined using an energy dispersive X-ray analyser. The concentration of sodium in the leaf (1�7 m-equivjkg of wet tissue) was too low to be detected by this method. The spatial resolution of this technique was sufficient to distinguish between concentrations in the chloroplasts, cytoplasm, vacuole, and nuclei. The concentration of chloride in stomata and some other epidermal cells was very much higher than in either mesophyll or bundle sheath cells. The potassium concentration in some vascular cells was at least two- to threefold higher than that in mesophyll or bundle sheath cells. The Cl : K ratio in mesophyll and bundle sheath cells resembled that in the solution (0 �10) used for growing the plants. The concentration of chloride in the "free" cytoplasm of mesophyll cells was always very low. Significant differences were found in the "ion" relations of mesophyll and bundle sheath cells. Whereas the ratio of potassium concentration between the vacuole and chloroplasts of mesophyll cells was high (1 �19) in the light and low (0�65) in the dark, the opposite was true for bundle sheath cells-O� 65 and 0�86 respectively. The ratio of potassium concentration between the vacuo les of mesophyll and those of bundle sheath cells was 1 �48 in the light, but only 0�76 in the dark. These concentration gradients are discussed in relation to a possible transfer of organic acid salts of potassium between these two cell types.


Development ◽  
1994 ◽  
Vol 120 (3) ◽  
pp. 673-681 ◽  
Author(s):  
J. A. Langdale ◽  
C. A. Kidner

Post-primordial differentiation events in developing maize leaves produce two photosynthetic cell types (bundle sheath and mesophyll) that are morphologically and biochemically distinct. We have isolated a mutation that disrupts the differentiation of one of these cell types in light-grown leaves. bundle sheath defective 1-mutable 1 (bsd1-m1) is an unstable allele that was induced by transposon mutagenesis. In the bundle sheath cells of bsd1-m1 leaves, chloroplasts differentiate aberrantly and C4 photosynthetic enzymes are absent. The development of mesophyll cells is unaffected. In dark-grown bsd1-m1 seedlings, morphological differentiation of etioplasts is only disrupted in bundle sheath cells but photosynthetic enzyme accumulation patterns are altered in both cell types. These data suggest that, during normal development, the Bsd1 gene directs the morphological differentiation of chloroplasts in a light-independent and bundle sheath cell-specific fashion. In contrast, Bsd1 gene action on photosynthetic gene expression patterns is cell-type independent in the dark (C3 state) but bundle sheath cell-specific in the light (C4 state). Current models hypothesize that C4 photosynthetic differentiation is achieved through a light-induced interaction between bundle sheath and mesophyll cells (J. A. Langdale and T. Nelson (1991) Trends in Genetics 7, 191–196). Based on the data shown in this paper, we propose that induction of the C4 state restricts Bsd1 gene action to bundle sheath cells.


1995 ◽  
Vol 350 (1331) ◽  
pp. 53-57 ◽  

Mature maize leaves exhibit a series of parallel veins that are surrounded by concentric rings of bundle sheath and mesophyll cells. To identify genes that control cellular differentiation patterns in the leaf, we have isolated a group of mutations that specifically disrupt the differentiation of a single cell-type. In bundle sheath defective ( bsd ) mutant plants, bundle sheath cells fail to differentiate yet mesophyll and all other leaf cell-types develop normally. Morphological and functional characterization of specific bsd mutants ( bsd1, bsd2, bsd3, pg14 and g2 ) reveals that they differ in the degree to which bundle sheath cell differentiation is perturbed. Mutant analysis predicts roles for BSD gene products in normal development.


Measurement of ion concentrations in the vacuoles of different cell types in cereal leaves using a variety of techniques indicates that ions are differentially distributed between different cell types. Thus mesophyll cells are enriched in P but contain relatively little Ca 2+ or Cl - , whereas the reverse is true for epidermal cells. Solutes reach the leaf via the transpiration stream and we consider three possible pathways which they could follow from the xylem to leaf cells. The first is a fully apoplastic mesophyll pathway in which both water and solutes move together through the leaf apoplast passing bundle sheath, mesophyll and epidermis in turn. The second is a partly symplastic mesophyll pathway in which ions and water pass into the symplast at the mestome/bundle sheath cells. Water continues to sites of evaporation via either a transcellular or symplastic pathway, but ions may be secreted back to the mesophyll apoplast and move to the epidermis along an extracellular route. The third is a vein extension pathway which provides a diffusional pathway for ions to the epidermis. A testable hypothesis for the roles of the pathways in supplying solutes to the mesophyll and epidermis is proposed and the implications of each of these pathways for transport systems in individual cell types is discussed.


2021 ◽  
Vol 12 ◽  
Author(s):  
Yue Chen ◽  
Deyi Zhong ◽  
Xiu Yang ◽  
Yonghui Zhao ◽  
Liping Dai ◽  
...  

As important electron carriers, ferredoxin (Fd) proteins play important roles in photosynthesis, and the assimilation of CO2, nitrate, sulfate, and other metabolites. In addition to the well-studied Fds, plant genome encodes two Fd-like protein members named FdC1 and FdC2, which have extension regions at the C-terminus of the 2Fe-2S cluster. Mutation or overexpression of FdC genes caused alterations in photosynthetic electron transfer rate in rice and Arabidopsis. Maize genome contains one copy of each FdC gene. However, the functions of these genes have not been reported. In this study, we identified the ZmFdC2 gene by forward genetics approach. Mutation of this gene causes impaired photosynthetic electron transport and collapsed chloroplasts. The mutant plant is seedling-lethal, indicating the indispensable function of ZmFdC2 gene in maize development. The ZmFdC2 gene is specifically expressed in photosynthetic tissues and induced by light treatment, and the encoded protein is localized on chloroplast, implying its specialized function in photosynthesis. Furthermore, ZmFdC2 expression was detected in both mesophyll cells and bundle sheath cells, the two cell types specialized for C4 and C3 photosynthesis pathways in maize. Epigenomic analyses showed that ZmFdC2 locus was enriched for active histone modifications. Our results demonstrate that ZmFdC2 is a key component of the photosynthesis pathway and is crucial for the development of maize.


1999 ◽  
Vol 12 (7) ◽  
pp. 615-623 ◽  
Author(s):  
Xin Shun Ding ◽  
Stanislaw Flasinski ◽  
Richard S. Nelson

Results from previous cytological studies on barley (Hordeum vulgare) infected with brome mosaic virus (BMV) indicated that this virus can infect and accumulate to high levels in mesophyll and other cell types within the leaves. Through immunocytochemistry and in situ hybridization, we have determined that BMV infection in barley is restricted predominantly to cells within and associated with vasculature when plants are grown at 24/20°C (day/night). This tissue restriction can be fully overcome by growing infected plants at 34°C for 2 h. Our results also indicate that BMV is likely to start systemic infection of young, uninoculated leaves in barley before spreading into all longitudinal veins in inoculated leaves. Possible barrier(s) to BMV movement between vascular bundle sheath cells and mesophyll cells, and the relationship between virus and photoassimilate transport through longitudinal and transverse veins are discussed.


2005 ◽  
Vol 32 (1) ◽  
pp. 67 ◽  
Author(s):  
Elena V. Voznesenskaya ◽  
Simon D. X. Chuong ◽  
Nuria K. Koteyeva ◽  
Gerald E. Edwards ◽  
Vincent R. Franceschi

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.


Genetics ◽  
2001 ◽  
Vol 159 (2) ◽  
pp. 787-797
Author(s):  
Lizzie Cribb ◽  
Lisa N Hall ◽  
Jane A Langdale

Abstract Maize leaf blades differentiate dimorphic photosynthetic cell types, the bundle sheath and mesophyll, between which the reactions of C4 photosynthesis are partitioned. Leaf-like organs of maize such as husk leaves, however, develop a C3 pattern of differentiation whereby ribulose bisphosphate carboxylase (RuBPCase) accumulates in all photosynthetic cell types. The Golden2 (G2) gene has previously been shown to play a role in bundle sheath cell differentiation in C4 leaf blades and to play a less well-defined role in C3 maize tissues. To further analyze G2 gene function in maize, four g2 mutations have been characterized. Three of these mutations were induced by the transposable element Spm. In g2-bsd1-m1 and g2-bsd1-s1, the element is inserted in the second intron and in g2-pg14 the element is inserted in the promoter. In the fourth case, g2-R, four amino acid changes and premature polyadenylation of the G2 transcript are observed. The phenotypes conditioned by these four mutations demonstrate that the primary role of G2 in C4 leaf blades is to promote bundle sheath cell chloroplast development. C4 photosynthetic enzymes can accumulate in both bundle sheath and mesophyll cells in the absence of G2. In C3 tissue, however, G2 influences both chloroplast differentiation and photosynthetic enzyme accumulation patterns. On the basis of the phenotypic data obtained, a model that postulates how G2 acts to facilitate C4 and C3 patterns of tissue development is proposed.


Plants ◽  
2020 ◽  
Vol 10 (1) ◽  
pp. 26
Author(s):  
Ghulam Mustafa ◽  
Muhammad Sarwar Khan

We report here plastid transformation in sugarcane using biolistic transformation and embryogenesis-based regeneration approaches. Somatic embryos were developed from unfurled leaf sections, containing preprogrammed progenitor cells, to recover transformation events on antibiotic-containing regeneration medium. After developing a proficient regeneration system, the FLARE-S (fluorescent antibiotic resistance enzyme, spectinomycin and streptomycin) expression cassette that carries species-specific homologous sequence tails was used to transform plastids and track gene transmission and expression in sugarcane. Plants regenerated from streptomycin-resistant and genetically confirmed shoots were subjected to visual detection of the fluorescent enzyme using a fluorescent stereomicroscope, after genetic confirmation. The resultant heteroplasmic shoots remained to segregate on streptomycin-containing MS medium, referring to the unique pattern of division and sorting of cells in C4 monocotyledonous compared to C3 monocotyledonous and dicotyledonous plants since in sugarcane bundle sheath and mesophyll cells are distinct and sort independently after division. Hence, the transformation of either mesophyll or bundle sheath cells will develop heteroplasmic transgenic plants, suggesting the transformation of both types of cells. Whilst developed transgenic sugarcane plants are heteroplasmic, and selection-based regeneration protocol envisaging the role of division and sorting of cells in the purification of transplastomic demands further improvement, the study has established many parameters that may open up exciting possibilities to express genes of agricultural or pharmaceutical importance in sugarcane.


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