Comparison of photosynthetic carbon reduction (Kranz) cells having different ontogenetic origins in the C4 NADP – malic enzyme grass Arundinella hirta

1990 ◽  
Vol 68 (6) ◽  
pp. 1222-1232 ◽  
Author(s):  
Nancy G. Dengler ◽  
Ronald E. Dengler ◽  
Douglas J. Grenville

The C4 grass Arundinella hirta is characterized by unusual leaf blade anatomy: photosynthetic carbon reduction takes place both within the chlorenchymatous bundle sheath cells of the longitudinal veins and within longitudinal strands of "distinctive cells" that form part of the leaf mesophyll and are often completely isolated from vascular tissue. Although they are equivalent physiologically, these two cell types have different ontogenetic origins: bundle sheath cells are delimited from procambium early in leaf development, whereas distinctive cells differentiate from ground meristem at a later developmental stage. Although the two cell types share numerous cytological features (large chloroplasts with reduced grana, thick cell walls with a suberin lamella), we also found significant differences in cell lengths, length to width ratios, cell cross-sectional areas, organelle numbers per cell cross section, phenol content of the cell walls, and numbers of pit fields in the longitudinal cell walls. The size and shape of bundle sheath cells are likely a direct consequence of procambial origin. The thicker walls of bundle sheath cells (in major veins) and their greater lignification may reflect the inductive effect of cell differentiation in the proximity of sclerenchyma and vascular tissues. Differences between major and minor vein bundle sheath cells may reflect differences in the timing of initiation of procambial strands. Our analysis of cell wall characteristics has also shown the presence of numerous primary pit fields in the transverse walls between adjacent distinctive cells in a file; plasmodesmata in these pit fields form a pathway for longitudinal symplastic transport not previously known to exist.

1995 ◽  
Vol 22 (4) ◽  
pp. 521 ◽  
Author(s):  
JJ Bruhl ◽  
S Perry

The ultrastructure of photosynthetic organs (leaf blades and culms) was investigated in eight species from four genera of sedges: Fimbristylis (C, fimbristyloid anatomy), Pycreus (C4 chlorocyperoid anatomy), Rhynchospora (C4 rhynchosporoid anatomy) - all NADP-ME (malic enzyme) type, and uninvestigated C3, C4 (eleocharoid anatomy, NAD-ME type) and C3-like C3-C4 intermediate species of Eleocharis. Ultrastructural characteristics previously reported for the former anatomical types are largely confirmed, though some evidence of poorly developed peripheral reticulum in C4 rhynchosporoid sedges is presented. Sedges, regardless of anatomical and biochemical type, possess a suberised lamella in photosynthetic organs which is invariably present in and confined to the mestome sheath cell walls, though it is often incomplete in the radial walls. By contrast with other C4 sedges, NAD-ME Eleocharis species and the C3-like C3-C4 intermediate E. pusilla possess abundant mitochondria and chloroplasts with well-stacked grana in the photosynthetic carbon reduction (PCR) (Kranz)/bundle sheath cells. Peripheral reticulum is well developed in NAD-ME species in both PCR and photosynthetic carbon assimilation (PCA) (C4 mesophyll) chloroplasts, but differs from that seen in chlorocyperoid and fimbristyloid type sedges. The suberised lamella and starch grains (well preserved), and granal stacks (poorly preserved) are identifiable in dried herbarium material (Eleocharis). Prediction of C4 biochemical type of sedges should be possible by combining anatomical, ultrastructural and δ13C value data. The significance of the ultrastructural similarities between the C4 NAD-ME and C3-C4 intermediate Eleocharis species is discussed.


Development ◽  
1998 ◽  
Vol 125 (10) ◽  
pp. 1815-1822 ◽  
Author(s):  
E.A. Kinsman ◽  
K.A. Pyke

Bundle sheath cells form a sheath around the entire vascular tissue in Arabidopsis leaves and constitute a distinct leaf cell type, as defined by their elongate morphology, their position adjacent to the vein and by differences in their chloroplast development compared to mesophyll cells. They constitute about 15% of chloroplast-containing cells in the leaf. In order to identify genes which play a role in the differential development of bundle sheath and mesophyll cell chloroplasts, a screen of reticulate leaf mutants of Arabidopsis was used to identify a new class of mutants termed dov (differential development of vascular-associated cells). The dov1 mutant clearly demonstrates a cell-specific difference in chloroplast development. Mutant leaves are highly reticulate with a green vascular pattern. The underlying bundle sheath cells always contain normal chloroplasts, whereas chloroplasts in mesophyll cells are abnormal, reduced in number per cell and seriously perturbed in morphology at the ultrastructural level. This demonstrates that differential chloroplast development occurs between the bundle sheath and mesophyll cells in the Arabidopsis leaf.


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.


2019 ◽  
Author(s):  
Maria Ermakova ◽  
Patricia E. Lopez-Calcagno ◽  
Christine A. Raines ◽  
Robert T. Furbank ◽  
Susanne von Caemmerer

AbstractC4plants contribute 20% to the global primary productivity despite representing only 4% of higher plant species. Their CO2concentrating mechanism operating between mesophyll and bundle sheath cells increases CO2partial pressure at the site of Rubisco and hence photosynthetic efficiency. Electron transport chains in both cell types supply ATP and NADPH for C4photosynthesis. Since Cytochromeb6fis a key point of control of electron transport in C3plants, we constitutively overexpressed the Rieske FeS subunit inSetaria viridisto study the effects on C4photosynthesis. Rieske FeS overexpression resulted in a higher content of Cytochromeb6fin both mesophyll and bundle sheath cells without marked changes in abundances of other photosynthetic complexes and Rubisco. Plants with higher Cytochromeb6fabundance showed better light conversion efficiency in both Photosystems and could generate higher proton-motive force across the thylakoid membrane. Rieske FeS abundance correlated with CO2assimilation rate and plants with a 10% increase in Rieske FeS content showed a 10% increase in CO2assimilation rate at ambient and saturating CO2and high light. Our results demonstrate that Cytochromeb6fcontrols the rate of electron transport in C4plants and that removing electron transport limitations can increase the rate of C4photosynthesis.


1987 ◽  
Vol 14 (4) ◽  
pp. 403 ◽  
Author(s):  
HDV Prendergast ◽  
PW Hattersley ◽  
NE Stone

Forty-three previously uninvestigated, mainly Australian, grass species (Poaceae) were assayed for activities of C4 acid decarboxylating enzymes (NADP-malic enzyme, NADP-ME; NAD-malic enzyme, NAD-ME; PEP carboxykinase, PCK). Twenty-five species exhibit long-established ('classical') associations between C4 type and structural features of leaf blade vascular bundles. However, Panicum virgatum and Triraphis mollis are NAD-ME species with structure like that of 'classical' PCK species. Seven Enneapogon species and Triodia scariosa are NAD-ME but are structurally intermediate between 'classical' NAD-ME and PCK species. Alloteropsis semialata (R.Br.) Hitch. is PCK, the first recorded non-NADP-ME XyMS - species, and Pheidochloa gracilis S.T. Blake and five Eriachne species are the first known XyMS+ NADP-ME species, with either centripetal or centrifugal/peripheral PCR (photosynthetic carbon reduction, or Kranz) cell chloroplasts. A suberised lamella is absent from the PCR cell walls of all species with an even PCR bundle sheath outline, irrespective of C4 type, as well as from NADP-ME Aristida, Eriachne and Pheidochloa; it is present in all other species with an uneven outline and centrifugal/peripheral chloroplasts. Pheidochloa gracilis and Eriachne spp. have unusually well-developed grana in PCR cell chloroplasts for NADP-ME species. This new-found structural/biochemical diversity is discussed in relation to high [CO2] maintenance in PCR cells.


1974 ◽  
Vol 1 (1) ◽  
pp. 41 ◽  
Author(s):  
CB Osmond

The Hill reaction and photosystem I activity of chloroplasts isolated from mesophyll and bundle sheath cells of Atviplex spongiosa and Sorghum bicolov was measured using narrow-band, high-intensity illumination of 646, 712, and 730 nm. The photosystem I reactions (methylviologen Mehler reaction and diphenylcarbazone reduction) were equally active in 646 and 712 nm light, whereas Hill activity was reduced by 70% in 712 nm light relative to 646 nm. Intact leaves were illuminated with 646 nm light and exposed to a pulse of 14CO2. The pulse was followed by a chase in 646,712, or 730 nm light or in darkness. In A. spongiosa leaves the movement of carbon from C4 acids to carbohydrates during the chase period only occurred to a significant extent in 646 nm light. In S. bicolor leaves, 712 nm light was almost as effective as 646 nm light in inducing the movement of carbon from C4 acids to carbohydrate. Evidently in this species carbon reduction is not entirely dependent on concurrent photosystem I + II activity for the provision of reducing potential. The data are discussed in relation to the deficiency of photosystem II activity in bundle sheath cells of S. bicolor.


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.


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