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 ...