Regulation of C4 Gene Expression in Developing Amaranth Leaves.

Wang, Jingliang; Klessig, Daniel F.; Berry, James O.

doi:10.1105/tpc.4.2.173

Cited by 70 publications

(94 citation statements)

References 25 publications

(9 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Using immunofluorescence microscopy and in situ hybridization (Wang et al, 1992), we observed that patterns of RuBPCase gene expression in the apical and basal regions of these leaves were different. In Figures 1A to lD, a series of cross-sections from a typical 7-mm-long leaf were reacted with polyclonal antisera against RuBPCase LSU and SSU, then with R-phycoerythrin-conjugated second antibody.…”

Section: Resultsmentioning

confidence: 99%

“…Leaf samples were fixed, embedded in paraffin, sectioned, and reacted with antisera as previously described (Wang et al, 1992). Briefly, primary antiserum against the RuBPCase LSU or SSU was applied to the sections, followed by the application of R-phycoerythrin-conjugated secondary antibody (Sigma).…”

Section: Lmmunolocallzation Analyslsmentioning

confidence: 99%

“…In the C4 monocot maize, both cell position and light influence the bundle sheath cell-specific expression of RuBPCase genes (Sheen andBogarad, 1985, 1986;Langdale et al, 1988aLangdale et al, , 1988bNelson and Langdale, 1989). Recently, we reported that in the C4 dicot amaranth, the developmental stage of the leaf, rather than light, appears to control bundle sheath cell-specific expression of the RuBPCase LSU and SSU genes (Wang et al, 1992). In very young (5-mm-long) amaranth leaves, the RuBPCase genes were expressed in a pattern similar to that observed in plants that use the C3 photosynthetic pathway, with LSU and SSU proteins and mRNAs present in both bundle sheath and mesophyll cells.…”

Section: Introductionmentioning

confidence: 99%

“…state (Langdale et al, 1988b;Langdale and Nelson, 1991;Wang et al, 1992). Specific signals are then required to suppress the expression of RuBPCase genes in mesophyll cells while allowing their continued expression in bundle sheath cells.…”

Section: Introductionmentioning

confidence: 99%

“…In very young (5-mm-long) amaranth leaves, the RuBPCase genes were expressed in a pattern similar to that observed in plants that use the C3 photosynthetic pathway, with LSU and SSU proteins and mRNAs present in both bundle sheath and mesophyll cells. The RuBPCase proteins and mRNAs became specifically localized to bundle sheath cells in the characteristic C4-type pattern as the leaves expanded to 10 mm in length over the time period of 24 to 36 hr.It is probable that C3-like expression of RuBPCase genes in both photosynthetic cell types represents an initial "default" Langdale et al, 1988b;Langdale and Nelson, 1991;Wang et al, 1992). Specific signals are then required to suppress the expression of RuBPCase genes in mesophyll cells while allowing their continued expression in bundle sheath cells.…”

mentioning

confidence: 99%

See 4 more Smart Citations

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

et al. 1993

Self Cite

View full text Add to dashboard Cite

Plants that use the highly efficient C4 photosynthetic pathway possess two types of specialized leaf cells, the mesophyll and bundle sheath. In mature C4 leaves, the C02 fixation enzyme ribulose-l,5-bisphosphate carboxylase (RuBPCase) is specifically compartmentalized to the bundle sheath cells. However, in very young leaves of amaranth, a dicotyledonous C4 plant, genes encoding the large subunit and small subunit of RuBPCase are initially expressed in both photosynthetic cell types. We show here that the RuBPCase mRNAs and proteins become specifically localized to leaf bundle sheath cells during the developmental transition of the leaf from carbon sink to carbon source. Bundle sheath cell-specific expression of RuBPCase genes and the sink-to-source transition began initially at the leaf apex and progressed rapidly and coordinately toward the leaf base. These findings demonstrated that two developmental transitions, the change in photoassimilate transport status and the establishment of bundle sheath cell-specific RuBPCase gene expression, are tightly coordinated during C4 leaf development. This correlation suggests that processes associated with the accumulation and transport of photosynthetic compounds may influence patterns of photosynthetic gene expression in C4 plants. INTRODUCTIONRibulose-1 5bisphosphate carboxylase (RuBPCase) is located in the chloroplasts of all higher plants and is the principal enzyme in photosynthetic carbon fixation. This enzyme is composed of two subunits, the chloroplast-encoded large subunit (LSU) and the nuclear-encoded small subunit (SSU) (Ellis, 1981; Miziorko and Lorimer, 1983). In plant species that utilize the C3 photosynthetic pathway, RuBPCase is found in all of the photosynthetic cells of the leaf. In mature leaves of plants that utilize the more complex C4 photosynthetic pathway, RuBPCase is specifically localized to one specialized cell type, the bundle sheath cells (Hatch and Slack, 1970;Edwards and Huber, 1981). Bundle sheath cells in C4 leaves occur as one or two rings around each of the leaf veins. Mesophyll cells, the other photosynthetic cell type in C4 plants, surround each ring of bundle sheath cells in one or more layers.The two types of photosynthetic cells compartmentalize the different reactions of the C4 pathway (Hatch and Slack, 1970;Gutierrez et al., 1974;Edwards and Huber, 1981). In C4 plants, the initial fixation of atmospheric COe is accomplished by the enzyme phosphoenolpyruvate carboxylase, which is found only in mesophyll cells. The carboxylation phase of the C4 pathway in mesophyll cells produces C4 acids, which are then transported to neighboring bundle sheath cells. In bundle sheath cells, decarboxylation of the C4 acids releases COn To whom correspondence should be addressed.for refixation by RuBPCase. These reactions cause COn to be concentrated in bundle sheath cells in the vicinity of RuBPCase, thereby increasing photosynthetic efficiency and reducing metabolically wasteful photorespiration caused by the oxygenase activity of this enzyme.The ...

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Lmmunolocallzation Analyslsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

et al. 1993

Self Cite

View full text Add to dashboard Cite

show abstract

EXPRESSION OF THE C₄ PATTERN OF PHOTOSYNTHETIC ENZYME ACCUMULATION DURING LEAF DEVELOPMENT IN ATRIPLEX ROSEA (CHENOPODIACEAE)

Dengler

Donnelly

et al. 1995

American J of Botany

View full text Add to dashboard Cite

Immunolocalization of the bundle sheath‐specific enzyme, ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBPCase), and of the mesophyll‐specific enzyme, phosphoenolpyruvate carboxylase (PEPCase), was used to follow development of the C4 pattern of photosynthetic enzyme expression during leaf growth in Atriplex rosea. The leaf tissue used for this characterization was also used in a parallel ultrastructural study, so that the temporal coordination of developmental changes in enzyme expression and cell structure could be monitored. Bundle sheath‐specific accumulation of RuBPCase occurs early, at the time that bundle sheath tissue is delimited from the ground meristem, and follows the order of vein initiation. PEPCase proteins were detected 2–4 days after the first appearance of RuBPCase. PEPCase accumulation is restricted to ground meristem cells that are in direct contact with bundle sheath tissue and that will become C4 mesophyll; PEPCase was never found in more distant ground tissue. This pattern suggests that, while bundle sheath‐specific accumulation of RuBPCase coincides with formation of the appropriate precursor cells, PEPCase expression is delayed until mesophyll tissue reaches a critical developmental stage. Cell‐specific expression of both photosynthetic enzymes occurs well before the striking anatomical divergence of bundle sheath and mesophyll tissues, suggesting that biochemical compartmentation might serve as a developmental signal for subsequent structural differentiation.

show abstract

Parallelism and diversity in multiple origins of c₄ photosynthesis in the grass family

Sinha

Kellogg

1996

American J of Botany

View full text Add to dashboard Cite

C4 photosynthesis is thought to be an adaptation to warm environments, involving complex changes in the expression of genes governing photosynthesis, intermediary metabolism, and leaf anatomy and histology. Such complexity should be difficult to evolve, yet the pathway has arisen multiple times in the history of the flowering plants and at least four times in the grass family alone. We have used immunolocalization techniques to compare photosynthetic gene expression across all four origins, to determine which genetic changes occur in parallel and which are unique to a particular lineage. The only gene expression patterns common to all origins of the pathway are up‐regulation of PEP carboxylase and down‐regulation of RuBisCO in mesophyll cells. Both NAD‐malic enzyme and NADP‐malic enzyme are expressed in bundle sheaths. Expression patterns of light‐harvesting chlorophyll a/b binding proteins and pyruvate orthophosphate dikinase appear to be lineage specific, and may be localized to bundle sheaths or to mesophyll or expressed throughout the photosynthetic tissue of the leaf. We suggest that future studies of parallel origin of the C4 pathway concentrate on regulation of the two carboxylases, as well as the increased density of vascular tissue, which is the only histological characteristic common to all origins of the pathway.

show abstract

Regulation of C4 Gene Expression in Developing Amaranth Leaves.

Cited by 70 publications

References 25 publications

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

EXPRESSION OF THE C₄ PATTERN OF PHOTOSYNTHETIC ENZYME ACCUMULATION DURING LEAF DEVELOPMENT IN ATRIPLEX ROSEA (CHENOPODIACEAE)

Parallelism and diversity in multiple origins of c₄ photosynthesis in the grass family

Contact Info

Product

Resources

About

Regulation of C4 Gene Expression in Developing Amaranth Leaves.

Cited by 70 publications

References 25 publications

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

EXPRESSION OF THE C4 PATTERN OF PHOTOSYNTHETIC ENZYME ACCUMULATION DURING LEAF DEVELOPMENT IN ATRIPLEX ROSEA (CHENOPODIACEAE)

Parallelism and diversity in multiple origins of c4 photosynthesis in the grass family

Contact Info

Product

Resources

About

EXPRESSION OF THE C₄ PATTERN OF PHOTOSYNTHETIC ENZYME ACCUMULATION DURING LEAF DEVELOPMENT IN ATRIPLEX ROSEA (CHENOPODIACEAE)

Parallelism and diversity in multiple origins of c₄ photosynthesis in the grass family