Functional compartmentation of C4 photosynthesis in the triple layered chlorenchyma of Aristida (Poaceae)

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.

2020 ◽  
Author(s):  
Soni Chowrasia ◽  
Tapan Kumar Mondal

AbstractThe C4 cycle is a complex biochemical pathway that has been evolved in plants to deal with the adverse environmental conditions. Mostly C4 plants grow in arid, water-logged area or poor nutrient habitats. Wild species, Oryza coarctata (genome type KKLL; chromosome number (4x) =48, genome size 665 Mb) belongs to the genus of Oryza which thrives well under high saline as well as submerged conditions. Here, we report for the first time that O. coarctata is a C4 plant by observing the increased biomass growth, morphological features such as vein density, anatomical features including ultrastuctural characteristics as well as expression patterns of C4 related genes. Leaves of O. coarctata have higher vein density and possess Kranz anatomy. The ultrastructural observation showed chloroplast dimorphism i.e. presence of agranal chloroplasts in bundle sheath cells whereas, mesophyll cells contain granal chloroplasts. The cell walls of bundle sheath cells contain tangential suberin lamella. The transcript level of C4 specific genes such as phosphoenolpyruvate carboxylase, pyruvate orthophosphate dikinase, NADP-dependent malic enzyme and malate dehydrogenase was higher in leaves of O. coarctata compare to high yielding rice cultivar (IR-29). These anatomical, ultra structural as well as molecular changes in O. coarctata for C4 photosynthesis adaptation might be might be due to its survival in wide diverse condition from aquatic to saline submerged condition. Being in the genus of Oryza, this plant could be potential donor for production of C4 rice in future through conventional breeding, as successful cross with rice has already been reported.


Weed Science ◽  
1983 ◽  
Vol 31 (1) ◽  
pp. 131-136 ◽  
Author(s):  
C. Dennis Elmore ◽  
Rex N. Paul

Spotted spurge (Euphorbia maculataL.) and prostrate spurge (E. supinaRaf.), both in subgenusChamesyce,were examined by light and electron microscopy using a caffeine - fixation technique to sequester the phenolic pools intercellularly. Both species have typical dicotyledon-type Kranz anatomy. Sequestered phenolic pools were located in vacuoles in epidermal and mesophyll cells. Only in spotted spurge, however, were additional phenolic pools formed in bundle - sheath cells. This study was undertaken because allelopathy has been demonstrated in prostrate spurge and because phenolic compounds have been implicated in allelopathy. These results would indicate that spotted spurge should also be allelopathic.


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.


1984 ◽  
Vol 62 (4) ◽  
pp. 812-817 ◽  
Author(s):  
Maria Emília Estelita-Teixeira ◽  
Walter Handro

Ultrastructural aspects, especially the organization of chloroplasts and their distribution, were studied in leaves of three species of Gomphrena (G. macrocephala, G. prostrata, and G. decipiens) presenting "Kranz anatomy," and in Pfaffia jubata, without that characteristic. In Gomphrena spp. the distribution of chloroplasts according to the complexity of their lamellar system seems to follow a gradient: most of the chloroplasts in the bundle sheath cells have poorly developed grana but some of them, in the cell side opposite to the vascular bundle, may present conspicuous grana. A similar situation occurs in "Kranz mesophyll cells," but in this case grana are more developed. Finally, chloroplasts in "non-Kranz mesophyll cells" have the more developed grana. In P. jubata no differences occur in chloroplast structure, all of them showing well-organized grana. Chloroplasts with well-developed grana were found in vascular parenchyma and in companion cells of Gomphrena spp. and P. jubata.


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.


1974 ◽  
Vol 52 (9) ◽  
pp. 2017-2021 ◽  
Author(s):  
Nels R. Lersten ◽  
Kathryn A. Carvey

Leaves of ocotillo, a shrub of southwestern North America, lack xeromorphic features. After rain, a few leaves at each node expand and function for a short period, then abscise. This cycle may be repeated several times each year. Palisade layers occur interior to both epidermal surfaces, and the spongy mesophyll is reduced. Venation is camptodromous, with many vein endings. In the distal lamina half, sclerified bundle sheath cells ("veinlet elements") become increasingly common in minor veins and vein endings. Near the leaf tip, adjacent mesophyll cells also become sclerified, to such an extent that some areoles appear filled with these cells ("accessory veinlet elements"). Phloem is conspicuous because it stains intensely and occupies more volume than xylem in most bundles. In minor veins and vein endings, sieve tube members become increasingly more slender than associated phloem cells, and xylem frequently changes its position, becoming parallel with, or even abaxial to, the phloem. Phloem mostly ends before, less commonly with, the xylem.


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