Bundle sheath and mesophyll cell differentiation in the C4 dicotyledon Atriplex rosea: quantitative ultrastructure

1994 ◽  
Vol 72 (5) ◽  
pp. 644-657 ◽  
Author(s):  
Youqi Liu ◽  
Nancy G. Dengler

In leaves of most C4 species, both bundle sheath and mesophyll cells are derived from ground meristem, yet at maturity differ in photosynthetic enzyme complement and in cell size, shape, and subcellular ultrastructure. This quantitative ultrastructural study of bundle sheath and mesophyll cell differentiation in Atriplex rosea shows that while developmental pathways of bundle sheath and meosphyll cells are generally coordinated, the timing of developmental divergence differs among individual characteristics. For instance, bundle sheath cells are larger, with more chloroplasts and more and larger mitochondria by 8 days after leaf emergence, while differential growth of mesophyll cell chloroplast peripheral reticulum and increase in thylakoids per granum in bundle sheath chloroplasts do not develop until after 12 days. Multigroup principal components analysis (M-PCA) of the data emphasizes that the greatest source of variation is overall size change as both cell types expand. M-PCA also identifies patterns of allometry within the data; for instance, mesophyll cell vacuoles and chloroplast peripheral reticulum undergo greater relative growth than do bundle sheath microbody area and number. The greater structural specialization of bundle sheath cells is reflected in higher growth rates from the time of divergence, but developmental change in both cell types continues until leaf expansion is complete. Most structural changes occur substantially after the stage of cell-specific expression of C4 enzymes. Key words: bundle sheath, mesophyll, C4 photosynthesis, leaf development, Atriplex rosea, multigroup principal components analysis.


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.



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.



1990 ◽  
Vol 68 (8) ◽  
pp. 1803-1811 ◽  
Author(s):  
InSun Kim ◽  
David G. Fisher

Seven species of Portulaca growing in Hawaii can be divided into two groups based on the morphology, anatomy, and ultrastructure of their leaves. Portulaca oleracea, P. molokiniensis, P. lutea, forming group A, have spatulate to obovate leaves, paradermal minor veins, and mesophyll cells that completely encircle the minor veins. The chloroplasts in their bundle sheath cells are larger than those in the mesophyll cells and have well-developed grana and reduced peripheral reticulum. Bundle sheath mitochondria are larger and more numerous than those in the mesophyll, and chloroplasts in the mesophyll cells have well-developed grana and peripheral reticulum. Portulaca pilosa, P. villosa, P. sclerocarpa, and P. "ulupalakua," forming group B, have lanceolate to oblong–oblanceolate leaves, peripheral minor veins, and incomplete wreaths of mesophyll cells. The choroplasts in their bundle sheath cells are about the same size as those in the mesophyll and have reduced grana and well-developed peripheral reticulum. The bundle sheath mitochondria are about the same in size and number as those in the mesophyll, and the mesophyll chloroplasts have well-developed grana and reduced peripheral reticulum. Groups A and B may be equivalent, respectively, to types ii and i of R. C. Carolin, S. W. L. Jacobs, and M. Vesk (Aust. J. Bot. 26: 683–698, 1978) and to coronary subtypes B and A of E. V. Voznesenskaya and Y. V. Gamalei (Bot. Zh. Leningrad, 71: 1291–1306, 1986), which constitute groupings of Portulaca species studied by those authors.



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.



1996 ◽  
Vol 74 (6) ◽  
pp. 823-837 ◽  
Author(s):  
Nadia C. Bruni ◽  
Nancy G. Dengler ◽  
Jane P. Young

Environmentally induced developmental plasticity is characteristic of many heterophyllous semiaquatic species, including Ranunculus flabellaris. Underwater shoots of this species form leaves with elongate narrow lobes, while aerial shoots form leaves with shorter, broader lobes. In this study, a series of transfer experiments was undertaken to determine the competence of developing leaves to respond to a change in environmental conditions. Plants were transferred from terrestrial to submerged conditions at 8, 16, and 24 days after the approximate time of initiation of leaf 4; these times correspond to the developmental stages before differences in size and shape of aerial and underwater leaves can be detected, the time of divergence, and postdivergence when leaves are about half expanded. Morphological and anatomical traits of mature leaves grown terrestrially, submerged, or after transfer at 8, 16, or 24 days were measured and assessed using analysis of variance and principal components analysis. We found that some traits of leaves (such as lobe number) transferred at 8 days were similar, but not identical, to those of the water control, indicating that some features are determined prior to structural divergence. Leaves transferred at 16 and 24 days were intermediate between the land and water controls in most respects, indicating that traits such as epidermal and mesophyll cell shape are determined gradually during expansion. Other anatomical features, such as development of a palisade layer and extent of intercellular space, did not differ between transfer treatments and the water control, indicating that these features can respond to ambient conditions late in development. Keywords: heterophylly, leaf development, plasticity, Ranunculus, principal components analysis.



1975 ◽  
Vol 2 (2) ◽  
pp. 207 ◽  
Author(s):  
EA Chapman ◽  
JM Bain ◽  
DW Gove

Cytochemical techniques were used to show that all the many large mitochondrion-like bodies present in bundle sheath cells of the aspartate-donor C4 plants, Amaranthus edulis and Atriplex spongiosa, possessed mitochondrial characteristics. The techniques involved the location of cytochrome c oxidase activity with 3,3'-diaminobenzidine and examination of configurational changes in mitochondria after incubation in the inhibitors of oxidative phosphorylation, rotenone and oligomycin, and of substrate phosphorylation, iodoacetate, or the uncouplers of oxidative phosphorylation 2,4-dinitrophenol and carbonyl cyanide p-trifluoromethoxyphenylhydrazone. The peripheral reticulum, which is a prominent feature of C4 mesophyll and bundle sheath chloroplasts and whose internal structure closely resembles that of the bundle sheath mitochondria, was also examined cytochemically. Frequent protrusions or buds from the peripheral reticulum in the bundle sheath chloroplasts strongly suggested that it could give rise to all or some of the mitochondria. Cytochemical investigation with diaminobenzidine, however, demonstrated that the peripheral reticulum does not possess cytochrome c oxidase activity and that the mitochondrial population is homogeneous. Studies of developing leaves of Amaranthus edulis showed that the mitochondria were a prominent feature in the bundle sheath cells before the appearance of the peripheral reticulum. The close proximity of the peripheral reticulum to mitochondria or to peroxisomes and sometimes also to the cell wall plasmodesmata indicates that it may play a role in metabolite transport.



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