Expression of the C4 pattern of photosynthetic enzyme accumulation during leaf development in Atriplex rosea (Chenopodiaceae)

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